The Evolving Battle Between Yellow Rust and Wheat: Implications for Global Food Security

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Mackay, and 1 more This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-557233/v1 This work is licensed under a CC BY 4.0 License Status: Published Journal Publication published 25 Nov, 2021 Read the published version in Theoretical and Applied Genetics → Version 1 posted 4 You are reading this latest preprint version Abstract Wheat ( Triticum aestivum L.) is a global commodity, and its production is a key component underpinning worldwide food security. Yellow rust, also known as stripe rust, is a wheat disease caused by the fungus Puccinia striiformis f. sp. tritici ( Pst ), and results in yield losses in most wheat growing areas. Recently, the rapid global spread of genetically diverse sexually derived Pst races, which have now largely replaced the previous clonally propagated slowly evolving endemic populations, has resulted in further challenges for the protection of global wheat yields. However, advances in the application of genomics approaches, in both the host and pathogen, combined with classical genetic approaches, pathogen and disease monitoring, provide resources to help increase the rate of genetic gain for yellow rust resistance via wheat breeding while reducing the carbon footprint of the crop. Here we review key elements in the evolving battle between the pathogen and host, with a focus on solutions to help protect future wheat production from this globally important disease. Medical Genetics Wheat fungal pathogens disease resistance breeding crop genomics pathogenomics cereal genetics global food security Figures Figure 1 1. Introduction Wheat ( Triticum aestivum L.) is one of the most important staple crops, with global demand predicted to increase to 324 kg/year (per capita) by 2050 (Alexandratos & Bruinsma, 2012). Wheat production faces numerous threats, with 10-16% of global wheat harvests estimated to be lost due to pests and diseases (Oerke, 2006; Strange & Scott, 2005). Yellow rust (YR), also known as stripe rust, is a major disease of wheat caused by the biotrophic fungal pathogen, Puccinia striiformis f. sp. tritici ( Pst ). YR infection is most commonly noted on wheat leaves, where the resulting damage to photosynthetic tissues leads to reduced light interception and radiation use efficiency, thus lowering yields (Figure 1a-b). However, YR infection can also take place on the structures of the wheat ear such as the glumes, lemma and palea, particularly during moderate to severe epidemics, resulting in reduced grain yield and quality (Bouvet et al. 2021a; Cromey, 1989; Wellings, 2003; 2009) (Figure 1c). Recurrent Pst epidemics have occurred in the majority of wheat growing areas over the past 60 years and can cause significant yield losses and reductions in grain quality if not adequately controlled (Wellings, 2011). Notably, the past two decades have seen the rapid global emergence of more aggressive and genetically diverse Pst populations adapted to warmer temperatures (Hovmøller et al. 2016; Hubbard et al. 2015; Milus et al. 2009), with concomitant impact on the YR resistance ratings of many wheat varieties. YR resistance breeding targets have had to adapt to tackle the rapidly changing Pst threat, and sources of genetic resistance for the development of improved wheat varieties are continually being sought. This is now being aided by advances in wheat genomics approaches, as well as detailed characterisation of Pst population pathotypes, genetic diversity, effector characterisation and field monitoring. Ultimately, efficient control of wheat fungal disease will be via approaches that combine agricultural and agronomic practices, disease monitoring, and varietal genetic improvement (Downie et al. 2020). In this review, we summarise current understanding of the Pst lifecycle, modes of dispersal and genetic diversity, and wheat genetic resistance and highlight some of the challenges facing the efforts to maintain adequate protection against wheat YR infection, with a focus on genetic resistance approaches. 2. The Complex Pathogen Lifecycle Pst goes through five different spore stages and requires two plant host species for completion of its lifecycle (Figure 1d). The two broad stages of the Pst lifecycle are classified as: (i) the asexual stage which occurs on wheat (the primary host), and (ii) the sexual stage which we now know occurs on Berberis species (the alternate host). In wheat, YR disease occurs during the asexual stage of the Pst lifecycle and is caused by multiple cycles of dikaryotic (i.e. two nuclei in each cell: n + n) Pst urediniospores re-infecting the primary host via wind dispersal. As it is this Pst lifecycle stage that is detrimental to wheat production, the uredinial infection and colonisation processes have been studied extensively. Early phenotypic studies identified the environmental conditions conducive of infection and colonisation by uredinia: free moisture, a 9-13 °C temperature range for sporulation, and low light levels (reviewed in Line, 2002). During the initial infection stage, urediniospores germinate on the leaf surface and eventually form an appressorium from which hyphae develop and enter the leaf tissue via the stomata. Growing hyphae develop into a dense network extending between and inside host mesophyll cells. Among this network, haustoria infection structures will form and specifically develop in host cell walls to extract nutrients from it (Szabo & Bushnell, 2001). On the leaves of mature susceptible plants, disease symptoms are visible 12-14 days after infection, consisting of yellow to orange coloured urediniospores that erupt from pustules arranged in characteristic stripes that follow the veins down the leaf blade (Chen et al. 2014), which can then lead to successive rounds of secondary infections. On resistant to mildly susceptible varieties, symptoms will range from non-sporulating flecks (a sign of hypersensitivity) to necrotic and chlorotic patches with no to limited sporulation. Towards the end of the wheat growth season, diploid teliospores may be produced by some isolates via karogamy. These readily germinate to produce a promycellim of four cells, with meiosis subsequently resulting in a single haploid nucleus that forms a basidiospore able to infect the alternate host (Chen et al. 2014). Although much less is known about the sexual stage, Berberis species were long speculated to support the lifecycle of Pst (e.g. Mains, 1933; Straib, 1937; Hart & Becker, 1934), as well as the related rust species, Puccinia graminis f. sp. tritici (causal agent of stem rust). Historically this resulted in efforts to eradicate Berberis species in many European and North American countries (Barnes et al. 2020). However, it was not until 2010 that Berberis species were formally confirmed to support development of Pst pycnia and aecia (Jin et al. 2010). Curiously, Berberis species infected with Pst are rarely observed in the wild, with only two accounts from China reported to date (Zhao et al. 2011, 2013). This may be due to the difficulty in finding an environment that simultaneously accommodates germination of teliospores (part of the asexual stage; enclosed in telia that form on wheat leaves towards the end of the infection season and produce basidiospores) and basidiospores (part of the sexual stage; forming on barberry leaves and requiring dew for germination), both of which have short viability (Wang & Chen, 2015). A recent study showed Berberis species do not play a role in YR epidemics in the US Pacific Northwest (Wang & Chen, 2015), and an additional alternate host, Mahonia aquifolium (Oregon grape) has been identified (Wang & Chen, 2013). The main importance of the sexual Pst stage on the alternative host to wheat infection is the generation of novel combinations of standing genetic variation that results in new genetically diverse isolates that can cause widespread epidemics and result in rapid changes in wheat resistance profiles. 3. Pathogens On The Move: Patterns Of Pst Dispersal And The Rise Of Divergent Lineages And Aggressive Races Over the years, monitoring of virulence changes in Pst populations in the major wheat producing regions has revealed notable changes in pathogen movement and adaptation. These studies were based on pathogenicity surveys, which use sets of differential wheat lines carrying known resistance genes, either near isogenic lines or cultivars, for the characterisation of pathotypes at the seedling stage (Wellings et al. 2009). More recently, molecular and genomics techniques have been used to infer Pst population structure and genetic diversity, confirming patterns of adaptation hypothesised in pathotype-based approaches. Here, we summarise key findings and events from the past three decades, specifically focusing on patterns of spore dispersal and Pst evolution and adaptation. Blowing in the wind Pst urediniospores are windborne and can disperse at continental scales. Coupled with the obligate nature of the pathogen (requiring living tissue to survive), this has led to different scenarios for the observed seasonal and geographic patterns of dispersal. One such model is the local extinction and re-colonisation model, illustrated for example in China where regions of the Sichuan and Gansu provinces in which Pst prevails all year round act as a source of inoculum to the more northerly provinces in which wheat is predominantly grown as a winter crop (Brown & Hovmøller, 2002; Zeng & Luo, 2006). In this way, Pst populations re-establish at the beginning of each wheat cropping season in those regions where Pst spores are usually unable to over-winter. A similar pattern of spore movement according to prevailing winds and the seasonality of the cropping seasons has been speculated in North America, with spores migrating from southern central states of USA and Mexico to northern central states of USA and Canada (Chen, 2005). In North Western Europe, Pst spore dispersion appears to follow the continental-island model, first described by Hedrick (1985), and has been the predominant model of Pst spore dispersion in North Western Europe. In this region, urediniospores travel up to 1,700 km with prevailing winds, and migrating between UK, France, Germany and Denmark (Hovmøller et al 2002). Investigations of YR emergence events in countries where it was previously absent provide examples of rapid inter-continental foreign incursion. Australia has been subject to several known incursions, of which two were notably detrimental to the wheat industry due to their rapid spread: (i) the first occurrence of Pst , in 1979 (Wellings et al. 1987), and (ii) the 2002 incursion in Western Australia (Wellings et al. 2003), now known to have originated from the Middle East/East Africa (Ali et al. 2014a) and attributed to a single Pst isolate (Wellings et al. 2003). The more recent arrival of Pst isolates in South Africa in 1996 were related to the Mediterranean and Central Asian populations (Boshoff et al. 2002; Ali et al. 2014a), and was speculated to be due to wind dispersal or human activities (Ali et al. 2014a). In all three cases, human activity, most likely through accidental transport on clothing, has been either demonstrated or strongly speculated, highlighting the increasing role of globalised trade and international travel as a means for Pst urediniospore dispersal. Pathogen evolution and adaptation Prior to 2000, pathogenicity surveys and molecular studies using isolates collected across the main wheat-producing regions in Europe, Australia and America typically reported Pst populations were clonal in nature, and that pathotypes exhibited close-relatedness and low genetic variation - predominantly underpinned by single step-wise mutations (Hovmøller et al. 2002; Enjalbert et al. 2005; Chen, 2005; Steele et al. 2001; Chen et al. 2010; Ali et al. 2014a; Hubbard et al. 2015; Hovmøller et al. 2016). Such clonally-derived Pst mutations have caused several severe YR epidemics, due to the ‘breakdown’ of specific wheat Yr resistance genes present in large acreages across the agricultural landscape. Notable examples include breakdown of Yr17 in Northern Europe (Bayles et al. 2000), Yr27 in Ethiopia (Solh et al. 2012), and Yr9 in America, the Middle East and the Indian sub-continent (Chen et al. 2010; Singh et al. 2004). Before the year 2000, the only exceptions to such patterns of low Pst genetic variation were observed in isolates from the Himalayan (Nepal and Pakistan) and near Himalayan (China) regions, which exhibited high levels of genetic recombination, high ability for sexual reproduction and high genetic diversity (Duan et al. 2010; Mboup et al. 2009; Ali et al. 2014b). These areas were therefore classified the putative centres of Pst origin (Ali et al. 2014b). However, the last two decades have seen the emergence of unusual virulence profiles and aggressive strains across the world. The most noteworthy event was the rise of two strains, PstS1 and PstS2, across the USA (Chen et al. 2002; Markell & Milus, 2008), Europe (Hovmøller & Justesen, 2007) and Australia (Wellings, 2007) in the space of just three years in the early 2000s. A global study of pre- and post-2000 Pst races combining detailed virulence pathotyping and DNA fingerprinting found these while these two strains were genetically similar to each other, they were highly divergent from previous races in their respective geographic regions (Hovmøller et al. 2008). Their rapid spread was thought to be due to their increased aggressiveness (ability to yield more spores and for disease symptoms to occur more quickly) and high temperature adaptation - which was later demonstrated in the detailed study by Milus et al. (2009). In addition to PstS1 and PstS2 , additional atypical occurrences of Pst races have since been reported. Enjalbert et al. (2005) demonstrated high levels of genetic divergence between the Pst population in northern France and a single clone specific to the South. What was atypical was that this single pathotype was maintained for a long time in this region, despite the presence of gene flow between Northern and Southern Pst populations. This isolate was later found to be more closely related to the Central Asian-Mediterranean population (Ali et al. 2014a). Similarly, instances of strong genetic divergence have also been revealed in North Western Europe (Flath & Barthels, 2002; Hovmøller & Justesen 2007a). Two groups of highly divergent pathotypes from the ‘old’ North-Western European population exhibited three to four times higher levels of genetic diversity (Hovmøller et al. 2007). In 2011, two novel Pst races disrupted the European Pst landscape (www.wheatrust.org). Named after the host varieties on which they were first detected, one race was virulent on wheat cv. ‘Warrior’ and the other was virulent on cv. ‘Kranich’. These were later characterised as PstS7 and PstS8 respectively (Ali et al. 2017), and were detected simultaneously across Europe and infected varieties that had exhibited durable adult plant resistance. Both races were distinct from the typical European isolates in that they produced an unusually high number of teliospores (Hubbard et al. 2015; Hovmøller et al. 2016). Additional Pst races have been characterised ( PstS10 also known as ‘Warrior (-)’, PstS4 ‘Triticale aggressive’) and together with the other new genetically diverse Pst races, have come to largely dominate within Europe (Ali et al. 2017; Hovmøller et al. 2016; Hubbard et al. 2015). Collectively, these atypical observations, further supported by genetic diversity studies, have led to speculation of an aerial-induced foreign incursion, which would be the first of its kind in Europe since the establishment of Pst in Europe during the 19 th century. Beyond Europe, rapid invasions and the subsequent Pst population changes have been responsible for a number of YR epidemics in Central Asia, North and East Africa (Ali et al. 2017). 4. Chemical Control Of Yellow Rust Review of global YR epidemics shows most wheat growing regions document recurrent crop losses of 5-10 %, with occasional losses of up to 25 % (Welling, 2011). However, following the global spread of aggressive Pst races since 2000, surveys highlight an increase in both the number of countries being significantly hit by such races, and the extent of the losses incurred (Beddow et al. 2015). Indeed, the financial implications of this change in Pst race structure estimated that a global average of US$ 158 million was lost annually pre 2000s, compared to US$ 979 million post 2000 (Beddow et al. 2015). Wheat growers have two principal options to protect against the effects of YR on yield: (i) protect their crop with agro-chemicals that limit initial infection and progression of pathogen colonisation, and/or (ii) grow wheat varieties with adequate levels of genetic resistance. Systemic fungicides that are absorbed into the plant became commercially available in the 1980s and have since formed an important part of integrated control measures against YR (Chen, 2005). Several products with different modes of action are available for protection against YR (reviewed by Chen & Kang, 2017), with timely application a key aspect of an effective fungicide programme. Such an approach has, for example, prevented significant financial losses in periods of severe epidemics in the USA (Line, 2002). While fungicide control provides an essential tool in combatting sudden yellow rust epidemics and in situations where growing resistant varieties is not an option, over-dependence on their use comes with negative environmental impacts and notable financial cost to growers. For example, in Australia an estimated A$ 359 million per year is spent on fungicides for YR control (Murray & Brennan, 2009). In the mid-to-long term, regular Pst exposure to fungicides also increases the risk that Pst populations develop resistance to frequently used chemistries. Historically, Pst been classified as being at low-risk of developing fungicide resistance. However, of the three classes of fungicides active against Pst (demethylation inhibitors, DMIs; succinate dehydrogenase inhibitors, SDHIs; quinone outside inhibitors, QoIs), Pst resistance has evolved against two. Low levels of DHI resistance have been reported, and while high proportions of isolates carrying resistance associated mutations have been reported in some countries (Cook et al. 2021), DHI resistance has so far had limited agronomic-scale significance (Oliver, 2014). SDHIs active against rusts have only been introduced relatively recently, giving less time for Pst resistance to evolve. Nevertheless, sets of geographically diverse isolates have been identified that carry a mutation homologous to that linked to SDHI resistance in the related rust species P. pachyrhzi (Cook et al. 2021). In the face of additional considerations such as changing regulation surrounding permissible chemistries, such evidence has led to the suggestion that the Pst risk classification should be upgraded (Oliver, 2014), fungicide resistance management practices be considered, and that systematic monitoring for Pst for fungicide resistance should be implemented (Cook et al. 2021). Lastly, the optimisation of fungicide timing, as well as improved fungicide application technologies, represent areas where additional research and development is required (Carmona et al. 2020). 5. Genetic Control Of Yellow Rust More than 300 wheat genomic regions conferring YR resistance have been reported (Rosewarne et al. 2013; Wang & Chen, 2017). Of these, ~80 are permanently named yellow rust resistance ( Yr ) genes (recently summarised by Jamil et al. 2020). Two main classes of YR resistance ( R ) genes are commonly described. The first is termed ‘all stage resistance’ (or ‘seedling resistance’) and confers qualitative resistance – typically to one or a low number of Pst isolates. The second is termed ‘adult plant resistance’ (APR) and confers quantitative or partial resistance. While these R gene classifications are useful, additional categories are also used, based on criteria such as phenotypic response (infection type, race specificity, resistance levels), temperature sensitivity, durability, the number of genes involved (monogenic versus polygenic) and the size of gene effect (Chen, 2013). One of the issues that comes with defining YR resistance with such a broad range of criteria is the assumptions associated with each of them. For example, APR is typically non-race specific, more durable than seedling resistance and conditioned by genes with minor or partial effect. Nevertheless, some APR genes have been shown to exhibit race specificity, such as Yr11, Yr12, Yr13 and Yr14 (Johnson, 1992; McIntosh et al. 1995). All-stage resistance Initially expressed at the seedling stage, all-stage resistance extends throughout the growth of the wheat plant and is characterised by a hypersensitive response. It is generally effective against some, but not all, Pst races and is therefore also referred to as ‘race-specific resistance’. All-stage resistance is underpinned by the gene-for-gene model, first explored by Flor (1956) in the flax-rust pathosystem, whereby the product of an R gene must be recognised by the protein encoded by its corresponding avirulent ( Avr ) gene in the pathogen, with resistance conferred by an incompatible R-Avr interaction. This results in a qualitative resistance phenotype that can be easily assessed, historically making it a popular selection criterion in breeding programmes, and more recently, for gene cloning. The majority of catalogued YR R genes exhibit this type of phenotype, and many become ineffective against present-day Pst races. This type of resistance has commonly been shown to be a short-term strategy for YR control. Indeed, the deployment of varieties with single or low-numbers of all-stage resistance Yr genes over large acreages inevitably exerts high selective pressure on the pathogen, forcing it to evolve and mutate until host resistance is broken down, and leading to cycles of ‘boom and bust’ (McDonald & Linde, 2002). Adult Plant Resistance Adult plant resistance (APR) is characterised by slow rusting (a long period of latent infection, small lesion size) (Guo et al. 2008) or partial resistance, typically manifests at the adult plant stage, and has long been established as a durable source of YR resistance. Two notable examples are Yr18/Lr34/Sr67/Pm38 , extensively deployed in spring wheat cultivars through the international breeding programme at CIMMYT (Singh et al. 2005) and Yr16 , an APR gene commonly used in early European varieties such as ‘Cappelle Desprez’, a major hub in the European wheat pedigree (Fradgley et al. 2019). While APR is primarily non-race specific, examples of APR specificity to Pst races do exist, such as Yr12 and Yr13 (Johnson, 1992; McIntosh et al. 1995). Such APR race-specificity was initially reported by Johnson (1988) and has recently been observed in Europe following the spread of atypical Pst races (Sørensen et al. 2014). For example, while the APR resistance allele conferred by the founder Claire at the QTL QYr.niab-2D.1 was effective in the UK during the 2015 and 2016 seasons (Bouvet et al. 2021b), it has since broken down (Simon Berry, personal communication). Another example is that of Yr49 , which was initially found to be non-race specific against all Australian Pst isolates, but when tested against Chinese races was found to be virulent and thus showed race-specificity (Ellis et al. 2014). These occurrences undermine the durability of APR and puts into question whether this pathotype criteria should be used to describe this type of resistance. It has been suggested that as some APR genes confer resistance against multiple biotrophic pathogens, this characteristic is a good indicator of durability. Examples include Yr18/Lr34/Sr67/Pm38 (Spielmeyer et al. 2005; Lillemo et al. 2008), Yr29/Lr46/Sr58/Pm39 (Lagudah, 2011), Yr30/Lr27/Sr2 (Mago et al. 2011) and Yr46/Lr67/Sr55/Pm46 (Herrer-Foessel et al. 2014). Interestingly, some of these genes are also associated with traits such as leaf tip necrosis ( Yr18/Lr34/Sr67/Pm38, Singh et al. 1992; Yr29/Lr46/Sr58/Pm39 , Rosewarne et al. 2006; Yr46/Lr67/Sr55/Pm46 , Herrera-Foessel et al. 2014) and pseudo-black chaff ( Yr30/Lr27/Sr2 , Kota et al. 2006). Finally, some APR resistances are more effective at high temperature (usually 25-30 °C), and are termed High Temperature Adult Plant (HTAP) resistance. Yr36 was initially characterised as HTAP (Uauy et al. 2005), with subsequent studies showing resistance was effective over 25 °C at all growth stages (Fu et al. 2009), and that the lower effective temperature range is 18 °C (Bryant et al. 2014). 6. Cloned Yellow Rust Resistance Genes Nucleotide Binding Sequence Leucine Rich Repeat (NBS-LRR) proteins are the most common class of proteins encoded by plant R genes, and act predominantly by recognising the effector molecules that pathogens produce to inhibit host defence responses (Jones et al. 2016). To help fight against potential infecting pathogens, plant NLR gene families have radiated and diversified, for example via localised gene duplication or mutation within their LRR domains that bind pathogen effectors (Sarris et al. 2016). Furthermore, some NBS-LRRs contain additional ‘integrated’ domains, the most common of which are kinase and DNA-binding domains (Andersen et al. 2020; Steuernagel et al. 2020), and are thought to be involved in receptor activation or downstream signalling (Sarris et al. 2016). Of the 18 genes conferring all-stage resistance to wheat rusts (yellow rust, stem rust, leaf rust) that have been cloned, 17 encode NBS-LRRs (Table 1). Furthermore, all but two of these NBS-LRRs contain coiled coil (CC) domains towards their N-termini; the exceptions being Yr7 and the allelic R genes Yr5 / YrSP , each of which contains an N-terminus integrated BED zinc finger domain (Marchal et al. 2018) and Sr60 , which is race-specific but confers a partial resistance phenotype and encodes a protein with two putative kinase domains (Chen et al. 2020). The ongoing changes and rapid spread of Pst populations around the world has led to growing interest in more durable sources of resistance. To date, four adult plant YR resistance genes have been cloned. Yr36 encodes a protein with a kinase and a START lipid-binding domain (WHEAT KINASE START 1 , WKS1; Fu et al. 2009), and is thought to regulate reactive oxygen species (ROS) via phosphorylation of the thylakoid ascorbate peroxidase protein, resulting in increased levels of ROS during immunity (Gou et al. 2015). More recently, WKS1 has been shown to phosphorylate a protein component of photosystem II, sbO, resulting in reduced photosynthesis, leaf chlorosis and Pst resistance (Wang et al. 2019). Yr18 /Lr34 encodes an ABC transporter (Krattinger et al. 2009) involved in the translocation of abscisic acid (Krattinger et al. 2019) while Yr46/Lr67 encodes a hexose transporter (Moore et al. 2015). Finally, the broad-spectrum R gene Yr15 encodes a tandem kinase-pseudokinse protein (Klymiuk et al. 2018) similar to that encoded by the barley stem rust resistance gene Rpg1 (Brueggeman et al .2002), and has recently been shown to be allelic with YrG303/YrH52 (Klymiuk et al. 2020). 7. Designing Yellow Rust Resistant Wheat Pyramiding multiple resistance genes with additive effects into single genetic backgrounds should help prevent dramatic breakdown of wheat Pst field resistance. This first iteration of resistance gene pyramiding was developed using conventional breeding techniques. Indeed, the CIMMYT wheat breeding programme has made extensive use of the ‘ Yr18 complex’ ( Yr18 and at least two closely linked resistance genes), which has provided durable resistance against yellow rust (Singh et al. 2005). Tools to help such approaches are available. These include protocols for the use of diagnostic molecular markers for marker-assisted breeding for many of the cloned resistance genes listed above (https://maswheat.ucdavis.edu/), as well as ‘speed breeding’ methods that include the use of extended day lengths and controlled temperatures to shorten the wheat lifecycle (Watson et al. 2018). However, combining numerous unlinked genes via crossing is time-consuming. For example, a recent crossing scheme for the incorporation of 12 resistance genes int a single recurrent background involved 20 generations (Hafeez et al. 2021). Additionally, sources of YR resistance commonly originate from species related to bread wheat (see Table 1), including diploid wheat (e.g. T. monococcum and Aegilops tauschii ) and wild or cultivated tetraploid wheats ( T. turgidum ssp. dicoccoides and T. turgidum ssp. durum , respectively), resulting in introgression of linked chromosomal regions from the donor progenitor species. Such introgressed regions may have a negative effect on crop performance; for example, while Sr60 has recently been introduced into bread wheat via the introgression of a small T. monococcum segment containing the R gene, it nevertheless contains linked PUROINDOLIN genes which will affect grain texture (Chen et al. 2020). Such considerations mean development of resistance gene cassettes containing multiple R genes could provide a useful breeding tool, providing multiple sources of resistance inherited as a single genetic unit. Assuming their effects will be additive (i.e. show no epistasis), the four cloned APR genes, Yr15, Yr18, Yr36 and Yr46 , possibly combined with one or more ASR genes, represent obvious immediate targets. Indeed, a transgene cassette containing four stem rust ASR genes and one APR gene has recently been shown to confer broad-spectrum field resistance (Luo et al. 2021). However, such approaches do not come without their challenges: genetic modification regulations and consumer acceptance remains an important barrier in many parts of the world, relatively low numbers of Yr genes have been cloned, and further work is needed to determine how specific genes work in combination within the context of inbred lines and F 1 hybrids. Towards tackling some of these issues, proposals to generate an R gene atlas for the major diseases of wheat have been made (Hafeez et al. 2021). Such concepts would be aided by the systematic identification and monitoring of the corresponding Pst effectors and their standing variation across the agricultural environment, and should be extended to identify, characterise and eliminate wheat susceptibility ( S ) genes that act to increase YR susceptibility (e.g. Corredor-Moreno et al. 2021). Underpinning such aims is the availability of new genomic techniques and resources in wheat that complement classical map-based cloning methodologies (recently reviewed by Adamski et al. 2020). For example, candidate gene association mapping using diversity panels of wheat or wheat relatives genotyped via reduced representation sequencing of classes of genes known a priori to be prevalent in disease resistance (such as NBS-LRRs or wall-associated kinases). This method, termed ‘RenSeq’ (Jupe et al. 2013), alongside functional validation via chemical mutagenesis of germplasm containing the functional allele of interest, has been used to identify the wheat stem rust resistance genes Sr46 and SrTA1662 (Arora et al. 2019). Such association mapping approaches can be extended to include more representative coverage across the genome, for example using promotor/exome capture arrays (Gardiner et al. 2019) or whole-genome sequencing at low-coverage combined with imputation of SNPs and haplotypes, aided by the use of reference genome assemblies (e.g. for bread wheat: IWGSC, 2018; Walkowiak et al. 2021). Furthermore, the availability of Pst genome assemblies (e.g. Cantu et al. 2011, 2013; Zheng et al. 2013; Schwessinger et al. 2018, 2020) and mutant populations (Li et al. 2020), as well as gene expression resources and interrogation tools for both species (e.g. Adams et al. 2021) should help identify and characterise pathogen effectors. Detailed knowledge of the specificity of the recognition interactions between wheat R genes and their corresponding Pst effectors could be used, for example, to monitor the functionality of each component of R stacks, and to design synthetic R genes engineered to recognise multiple races (as demonstrated for example by editing of the rice NBS-LRR gene PikP to recognise multiple variants of the effector AvrPik from the rice blast pathogen Magnaporthe oryzae ; De La Concepcion et al. 2019). Similarly, identification of wheat S genes would allow their elimination, via marker assisted approaches, mutation breeding or gene editing. Finally, further understanding of the exact developmental stages at which different adult plant resistance genes become effective, how best to deploy these in the agricultural landscape to best protect the crop from infection throughout the key growth stages, and understand which R genes exhibit the lowest yield cost, will further help protect wheat against the effects of YR. 8. Future Perspectives The wide-ranging spread of new genetically diverse Pst races has meant that YR is likely to become an increasing threat to global wheat production, resulting in lower yields and increased financial and environmental costs. Here, we conclude with a series of recommendations for future research and development in YR management over the next decade: Host genetics Systematic programmes to identify and clone known and novel R genes, particularly those conferring adult plant or non-host resistance. Informed design and development of durable R gene pyramid combinations, via traditional crossing and/or R gene cassettes. Identification and targeted removal of susceptibility ( S ) genes from breeders’ germplasm. Monitoring Regional and international networks to rapidly monitor the emergence and spread of Pst pathotypes. Field networks to monitor R gene effectiveness at regional/international scales. Agronomy Regional monitoring for the emergence and spread of fungicide resistances. Innovation in fungicide application to allow more timely, accurate and efficient fungicide application. The use of variety mixtures, which is becoming increasingly used in some regions. Ultimately, the success of advances in integrated YR management approaches will depend on timely communication of information to wheat growers. Therefore, trusted grower-facing networks and sources of information that can rapidly and succinctly inform and advise farmers of threats and best practice within each growing season will become increasingly critical in realising future ambitions to better protect wheat yields from diseases such as YR. Abbreviations Adult plant resistance APR Demethylation inhibitors DMIs Genome-wide association scan GWAS Marker assisted selection MAS Nucleotide-binding leucine-rich repeat NLR Puccinia striiformis f. sp. tritici Pst Quantitative trait locus QTL Quinone outside inhibitors QoIs Succinate dehydrogenase inhibitors SDHIs Yellow rust YR Declarations Author contributions: LB wrote the manuscript with inputs from JC. All authors edited and critically revised the manuscript. Funding: LB was funded via a Biotechnology and Biological Sciences Research Council (BBSRC) Doctoral Training Partnership PhD award to the University of Cambridge. JC’s time has partly supported by Biotechnology and Biological Research Council grant BB/N00518X/1, funded via the 2 nd call of the ERA-CAPs framework. Acknowledgements: We thank Prof. Julian Hibberd (University of Cambridge) for administrative supervisory input during LB’s PhD. Conflict of interest statement: On behalf of all authors, the corresponding author states that there is no conflict of interest. References Adams TM, Olsson TSG, Ramírez-González RH, Bryant R, Bryson R, et al. (2021). Rust expression browser: an open source database for simultaneous analysis of host pathogen gene expression profiles with expVIP. BMC Genomics, 22: 166. Adamski NH, Borrill P, Brinton J, Harrington SA, Marchal C, et al. (2020). A roadmap for gene functional characterisation in crops with large genomes: lessons from polyploid wheat. eLife, 9: e55646. Alexandratos N, Bruinsma J (2012). World agriculture towards 2030/2050: the 2012 revision: ESA Working Paper No. 12-03 . Rome. Ali S, Gladieux P, Leconte M, Gautier A, Justesen AF, Hovmøller MS, Enjalbert J, de Vallavieille-Pope C (2014a). Origin, migration routes and worldwide population genetic structure of the wheat yellow rust pathogen Puccinia striiformis f.sp. tritici . PLoS Pathogens, 10: e1003903. Ali S, Leconte M, Rahman H, Saqib MS, Gladieux P, Enjalbert J, de Vallavieille-Pope C (2014b). A high virulence and pathotype diversity of Puccinia striiformis f.sp. tritici at its centre of diversity, the Himalayan region of Pakistan. European Journal of Plant Pathology, 140: 275–290. Andersen EJ, Nepal MP, Purintun JM, Nelson D, Mermigka G, Sarris PF (2020). Wheat disease resistance genes and their diversification through integrated domain fusions. Front Genet, 11: 898. Arora S, Steuernagel B, Gaurav K, Chandramohan S, Long Y, et al. (2019). Resistance gene cloning from a wild crop relative by sequence capture and association genetics. Nature Biotechnol, 37: 139-143. Barnes G, Saunders DGO, Williamson T (2020). Banishing barberry: The history of Berberis vulgaris prevalence and wheat stem rust incidence across Britain. Plant Pathology, 69: 1193-1202. Bayles RA, Flath K, Hovmøller MS, de Vallavieille-Pope C (2000). Breakdown of the Yr17 resistance to yellow rust of wheat in northern Europe. Agronomie, 20: 805–811. Beddow JM, Pardey PG, Chai Y, Hurley TM, Kriticos DJ, Braun H-J, Park RF, Cuddy WS, Yonow T (2015). Research investment implications of shifts in the global geography of wheat stripe rust. Nature Plants, 1: 15132. Boshoff WHP, Pretorius ZA, van Niekerk BD (2002). Establishment, distribution, and pathogenicity of Puccinia striiformis f. sp. tritici in South Africa. Plant Disease, 86: 485–492. Bouvet L, Percival-Alwyn L, Berry S, Fenwick P, Mantello CC, Holdgate IJ, Mackay IJ, Cockram J (2021a). Wheat genetic loci conferring resistance to yellow rust in the face of recent epidemics of genetically diverse races of the fungus Puccinia striiformis f. sp. tritici . Research Square, doi: 10.21203/rs.3.rs-459064/v1. Bouvet L, Berry S, Fenwick P, Holdgate IJ, Cockram J (2021b). Genetic resistance to yellow rust infection of the wheat ear is controlled by genes controlling foliar resistance and flowering time. BioRxiv, doi: https://doi.org/10.1101/2021.04.27.44165. Brown JKM, Hovmøller MS (2002). Aerial dispersal of pathogens on the global and continental scales and its impact on plant disease. Science, 297: 537-541. Brueggeman R, Rostoks N, Kudrna D, Kilian A, Han F, et al. (2002). The barley stem rust-resistance gene Rpg1 is a novel disease-resistance gene with homology to receptor kinases. Proc Natl Acad Sci USA, 99: 9328–9333. Bryant RRM, McGrann GRD, Mitchell AR, Schoonbeek H, Boyd LA, Uauy C, Dorling S, Ridout CJ (2014). A change in temperature modulates defence to yellow (stripe) rust in wheat line UC1041 independently of resistance gene Yr36 . BMC Plant Biology, 14: 10. Cantu D, Govindarajulu M, Kozik A, Wang M, Chen X, et al. (2011). Nex generation sequencing provides rapid access to the genome of Puccinia striiformis f. sp. tritici , the causal agent of wheat stripe rust. PLoS One, 6: e24230. Cantu D, Segovia V, MacLearn D, Bayles R, Chen X, Kamoun S, Dubcovsky J, Saunders DGO, Uauy C (2013). Genome analyses of the wheat yellow (stripe) rustpathogen Puccinia striiformis f. sp. tritici reveal polymorphic and haustorial expressed secreted proteins as candidate effectors. BMC Genomics, 14: 270. Carmona M, Saautua F, Pérez-Hérnandez O, Reis EM (2020). Role of fungicide applications on the integreated management of wheat stripe rust. Forntiers in Plant Sciences, 11: 773. Chen XM (2005). Epidemiology and control of stripe rust [ Puccinia striiformis f. sp. tritici ] on wheat. Canadian Journal of Plant Pathology, 27: 314–337. Chen XM (2013). Review Article: High-temperature Adult-Plant Resistance, Key for Sustainable Control of Stripe Rust. American Journal of Plant Sciences, 4:, 608–627. Chen, X., & Kang, Z. (Eds.). (2017). Stripe Rust . Dordrecht: Springer Netherlands. Chen X, Penman L, Wan A, Cheng P (2010). Virulence races of Puccinia striiformis f. sp. tritici in 2006 and 2007 and development of wheat stripe rust and distributions, dynamics, and evolutionary relationships of races from 2000 to 2007 in the United States. Canadian Journal of Plant Pathology, 32: 315–333. Chen S, Rouse MN, Zhang W, Zhang X, Guo Y, Briggs J, et al. (2020). Wheat gene Sr60 encodes a protein with two putative kinase domains that confers resistance to stem rust. New Phytol, 225: 948–959. Chen S, Zhang W, Bolus S, Rouse MN, Dubcovsky J (2018). Identification and characterization of wheat stem rust resistance gene Sr21 effective against the Ug99 race group at high temperature. PLoS Genet, 14: e1007287. Cloutier S, McCallum BD, Loutre C, Banks TW, Wicker T, Feuillet C, Keller B, Jordan MC (2007). Lead rust resistance gene Lr1 , isolated from bread wheat ( Triticum aestivum L.) is a member of the large psr567 gene family. Plant Molecular Biology, 65: 93-106. Cook NM, Chng S, Woodman TL, Warren R, Oliver RP, Saunders DGO (2021). High frequency of fungicide resistance-associated mutations in the wheat yellow rust pathogen Puccinia striiformis f. sp. tritici. Pest Management Science, doi: 10.1002/ps.6380. Corredor-Moreno P, Minter F, Davey PE, Wegel E, Kular B, Brett P, Lewis CM, Morgan YML, Macías Pérez A, Lorolev AV, Hill L, Saunders DGO (2021). The branched-chain amino acid aminotransferase TaBCAT1 modulates amino acid metabolism and positively regulates wheat rust susceptibility. Plant Cell, doi: https://doi.org/10.1093/plcell/koab049. Cromey MG (1989). Infection and control of stripe rust in wheat spikes. New Zealand Journal of Crop and Horticultural Science, 17: 159-164. De la Concepcion JC, Franceschetti M, MacLean D, Terauchi R, Kamoun S, Banfield MJ (2019). Protein engineering expands the effector recognition profile of a rice NLR immune receptor. eLife, 8: e47713. Downie RC, Lin M, Borsi B, Ficke A, Lillemo M, Oliver RP, Phan H, Tan K-C, Cockram J (2020). Spetoria nodorum blotch of wheat: disease management and resistance breeding in the face of shifting disease dynamics and a changing environment. Phytopathol doi: https://doi.org/10.1094/PHYTO-07-20-0280-RVW. Duan X, Tellier A, Wan A, Leconte M, de Vallavieille-Pope C, Enjalbert J (2010). Puccinia striiformis f.sp. tritici presents high diversity and recombination in the over-summering zone of Gansu, China. Mycologia, 102: 44–53. Ellis JG, Lagudah ES, Spielmeyer W, Dodds PN (2014). The past, present and future of breeding rust resistant wheat. Frontiers in Plant Science, 5: 641. Enjalbert J, Duan X, Leconte M, Hovmøller MS, Vallavieille-Pope C (2005). Genetic evidence of local adaptation of wheat yellow rust ( Puccinia striiformis f. sp. tritici ) within France. Molecular Ecology, 14: 2065–2073. Feuillet C, Travella S, Stein N, Albar L, Nublat A, Keller B (2003). Map-based isolation of the leaf rust disease resistance gene Lr10 from the hexaploid wheat ( Triticum aestivum L.) genome. Proc Natl Acad Sci U S A, 100: 15253-15258. Flath K, Bartels G (2002). Virulenzsituation in ¨osterreichischen und deutschen Populationen des Weizengelbrostes. Bereicht über die 52. Tagung der Vereinigung der Pflanzenzüchter und Saatgutkaufleute Österreichs, Gumpenstein. Flor HH (1956). The Complementary Genic Systems in Flax and Flax Rust. Advances in Genetics, 8: 29-54. Fradgley N, Gardner KA, Cockram J, Elderfield J, Hickey JA, Howell P, et al. (2019). A large-scale pedigree resource of wheat reveals evidence for adaptation and selection by breeders. PLOS Biol, 17: e3000071. Fu D, Uauy C, Distelfeld A, Bechl A, Epstein L, Chen X, Sela H, Fahima T, Dubcovsky J (2009). A novel kinase-START gene confers temperature-dependent resistance to wheat stripe rust. Science, 322: 1357-1360. Gardiner LJ, Brabbs T, Akhunov A, Jordan K, Budak H, et al. (2019). Integrating genomic resources to present full gene and putative promoter capture probe sets for bread wheat. Gigascience, 8: giz018. Gou J-Y, Li K, Wu K, Wang X, Lin H, Cantu D, Uauy C, Dobon-Alonso A, Midorikawa T, Inoue K, Sánchez J, Fu D, Blechl A, Wallington E, Fahima T, Meeta M, Epstein L, Dubcovsky J (2015). Wheat stripe rust resistance protein WKS1 reduces the ability of the thylakoid-associated ascorbate peroxidase to detoxify reactive oxygen species. The Plant Cell, 27: 1755–1770. Guo Q, Zhang ZJ, Xu YB, Li GH, Feng J, Zhou Y (2008). Quantitative trait loci for high-temperature adult-plant and slow-rusting resistance to Puccinia striiformis f. sp. tritici in wheat cultivars. Phytopathology, 98: 803–809. Hafeez AN, Sanu A, Ghosh S, Gilbert D, Howden RL, Wulff BBH (2021). Creation and judicious application of a wheat resistance gene atlas. Doi: http://doi.org/10.5281/zenodo.4469514. Hedrick PW (1985). Genetics of populations . Boston, USA: Jones and Bartlett Publishers, Inc. Herrera-Foessel SA, Singh RP, Lillemo M, Huerta-Espino J, Bhavani S, Singh S, Lan C, Calvo-Salazar V, Lagudah ES (2014). Lr67 / Yr46 confers adult plant resistance to stem rust and powdery mildew in wheat. Theoretical and Applied Genetics, 127: 781–789. Hovmøller MS, Justesen AF (2007). Appearance of atypical Puccinia striiformis f. sp. tritici phenotypes in north-western Europe. Australian Journal of Agricultural Research, 58: 518–524. Hovmøller MS, Justesen AF, Brown JKM (2002). Clonality and long-distance migration of Puccinia striiformis f.sp. tritici in north-west Europe. Plant Pathology, 51: 24–32. Hovmøller MS, Yahyaoui AH, Milus EA, Justesen AF (2008). Rapid global spread of two aggressive strains of a wheat rust fungus. Molecular Ecology, 17: 3818–3826. Hovmøller MS, Walter S, Bayles RA, Hubbard A, Flath K, Sommerfeldt N, Leconte M, Czembor P, Rodriguez-Algaba J, Thach T, Hansen JG, Lassen P, Justesen AF, Ali S, de Vallavieille-Pope C (2016). Replacement of the European wheat yellow rust population by new races from the centre of diversity in the near-Himalayan region. Plant Pathology, 65:402-411. Huang L, Brooks SA, Li W, Fellers JP, Trick HN, Gill BS (2003). Map-based cloning of leaf rust resistance gene Lr21 from the large and polyploid genome of bread wheat. Genetics, 164: 655–664. Hubbard A, Lewis C, Yoshida K, Ramirez-Gonzalez R, de Vallavieille-Pope C, Thomas J. et al. (2015). Field pathogenomics reveals the emergence of a diverse wheat yellow rust population. Genome Biol 16:23. The International Wheat Genome Sequencing Consortium (IWGSC), Appels R, Eversole K, Stein N, Feuillet C, Keller B, Rogers J Pozniak C, et al. (2018). Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science, 361: eaar7191. Jamil S, Shahzad R, Ahmad S, Fatima R, Zahid R, Anwar M, Iqbal MZ, Wang X (2020). Role of genetics, genomics and breeding approaches to combat stripe rust of wheat. Front Nutr 7:580715. Jin Y, Szabo LJ, Carson M (2010). Century-Old mystery of Puccinia striiformis life history solved with the identification of Berberis as an alternate host. Phytopathology, 100: 432–435. Johnson R (1988). Durable resistance to yellow (stripe) rust in wheat and its implications in plant breeding. In: N.W. Simmonds, S. Rajaram (Eds.) `Breeding Strategies for Resistance to the Rusts of Wheat’. CIMMYT, Mexico D.F. pp 63–75. Johnson R (1992). Past, present and future opportunities in breeding for disease resistance, with examples from wheat. Euphytica , 63: 3–22. Jones JD, Vance RE, Dangl JL (2016). Intracellular innate immune surveillance devices in plants and animals. Science, 354: aaf6395. Jupe F, Witek K, Verweij W, Sliwka J, Pritchard L, et al. (2013). Resistance gene enrichment sequencing (RenSeq) enables reannotation of the NB-LRR gene family from sequenced plant genomes and rapid mapping of resistance loci in segregating populations. Plant Journal, 76: 530–544. Kota R, Spielmeyer W, McIntosh RA, Lagudah ES (2006). Fine genetic mapping fails to dissociate durable stem rust resistance gene Sr2 from pseudo‐black chaff in common wheat. Triticum aestivum L. Theor Appl Genet, 112: 492–499. Klymiuk V, Yaniv E, Huang L, Raats D, Fatiukha A, Chen SS, et al. (2018). Cloning of the wheat Yr15 resistance gene sheds light on the plant tandem kinase-pseudokinase family. Nat. Commun, 9: 3735. Klymiuk V, Fatiukha A, Raats D, Bocharova V, Huang L, Feng L, Jaiwar S, Pozniak Cm Coaker G, Dubcovsky J, Fahima T (2020). Three previously characterized resistances to yellow rust are encoded by a single locus Wtk1 . J Exp Bot, 71: 2561-2572. Krattinger SG, Lagudah ES, Spielmeyer W, Singh RP, Huerta-Espino J, McFadden H, Bossolini E, Selter LL, Keller B (2009). A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. Science, 323: 1360–1363. Krattinger S, Kang J, Bräunlich S, Boni R, Chauhan H, Selter LL, Robinson MD, Schmid MW, Wiederhold E, Hensel G, Kumlehn J, Sucher J, Martinoia E, Keller B (2019). Abscisic acid is a substrate of the ABC transporter encoded by the durable wheat disease resistance gene Lr34 . New Phytologist, 223: 853-866. Lagudah ES (2011). Molecular genetics of race non-specific rust resistance in wheat. Euphytica, 179: 81–91. Li Y, Zia C, Wang M, Yin C, Chen X (2020). Whole-genome sequencing of Puccinia striiformis f. sp. tritici mutant isolates identified avirulence gene candidates. BMC Genomics, 21: 247. Lillemo M, Asalf B, Singh RP, Huerta-Espino J, Chen XM, He ZH, Bjørnstad Å (2008). The adult plant rust resistance loci Lr34 / Yr18 and Lr46 / Yr29 are important determinants of partial resistance to powdery mildew in bread wheat line Saar. Theoretical and Applied Genetics, 116: 1155–1166. Line RF (2002). Stripe rust of wheat and barley in North America: A retrospective historical review. Annual Review of Phytopathology, 40: 75–118. Liu W, Frick M, Huel R, Nykiforuk CL, Wang X, et al. (2014). The stripe rust resistance gene Yr10 encodes an evolutionary-conserved and unique CC-NBS-LRR sequence in wheat. Molecular Plant, 7: 1740-1755. Luo M, Zie L, Chakraborty S, Wang A, Matny O, Jugovich M, et al. (2021). A five-transgene cassette confers broad-spectrum resistance to a fungal rust pathogen in wheat. Nature Biotechnology, doi: https://doi.org/10.1038/s41587-020-00770-x. Mago R, Zhang P, Vautrin S, Šimlová H, Bansal U, et al. (2015). The wheat Sr50 gene reveals rich diversity at a cereal disease resistance locus. Nature Plants, 1: 15186. Marchal C, Zhang J, Zhang P, Fenwick P, Steuernagel B, Adamski NM, Boyd L, McIntosh R, Wulff BBH, Berry S, Lagudah E, Uauy C (2018). BED-domain-containing immune receptors confer diverse resistance spectra to yellow rust. Nature Plants, 4: 662–668. Markell SG, Milus EA (2008). Emergence of a novel population of Puccinia striiformis f. sp. tritici in Eastern United States. Phytopathology, 98: 632–639. Mboup M, Leconte M, Gautier A, Wan AM, Chen W, de Vallavieille-Pope C, Enjalbert J (2009). Evidence of genetic recombination in wheat yellow rust populations of a Chinese oversummering area. Fungal Genetics and Biology, 46: 299–307. McDonald BA, Linde C (2002). Pathogen Population Genetics, Evolutionary Potential, and Durable Resistance. Annual Review of Phytopathology , 40: 349–379. McIntosh RA, Wellings CR, Park RF (1995). Wheat rusts: An atlas of resistance genes . East Melbourne, Australia and Dordrecht and Boston: CSIRO and Kluwer Academic Publishers. Mehmood S, Sajid M, Huang L, Kang Z (2020). Alternate hosts and their impact on genetic diversity of Puccina striiformis f. sp. tritici and disease epidemics. Journal of Plant Interactions, 15: 153-165. Milus EA, Kristensen K, Hovmøller MS (2009). Evidence for increased aggressiveness in a recent widespread strain of Puccina striiformis f. sp. tritici causing stripe rust of wheat. Phytopathology, 99:89-94. Moore JW, Herrera-Foessel S, Lan C, Schnippenkoetter W, Ayliffe M, Huerta-Espino J, Lillemo M, Viccars L, Milne R, Periyannan S, Kong X, Spielmeyer W, Talbot M, Bariana H, Patrick JW, Dodds P, Singh R, Lagudah E (2015). A recently evolved hexose transporter variant confers resistance to multiple pathogens in wheat. Nature Genetics, 47: 1494–1498. Murray G, Brennan J (2009). Estimating disease losses to the Australian wheat industry. Australasian Plant Pathology, 38: 558–570. Oerke EC (2006). Crop losses to pests. The Journal of Agricultural Science, 144: 31. Oliver RP (2014). A reassessment of the risk of rust fungi developing resistance to fungicides. Pest Management Science, 70: 1641–1645. Periyannan S, Moore J, Ayliffe M, Bansal U, Wang X, et al. (2013). The gene Sr33, an ortholog of barley Mla genes, encodes resistance to wheat stem rust race Ug99. Sciece, 341: 786-788. Rodriguez‐Algaba J, Walter S, Sørensen CK, Hovmøller MS, Justesen AF (2014). Sexual structures and recombination of the wheat rust fungus Puccinia striiformis on Berberis vulgaris . Fungal Genetics and Biology 70:77–85. Rosewarne GM, Singh RP, Huerta-Espino J, William HM, Bouchet S, Cloutier S, McFadden H, Lagudah ES (2006). Leaf tip necrosis, molecular markers and β1-proteasome subunits associated with the slow rusting resistance genes Lr46 / Yr29 . Theoretical and Applied Genetics, 112: 500–508. Rosewarne GM, Herrera-Foessel SA, Singh RP, Huerta-Espino J, Lan CX, He ZH (2013). Quantitative trait loci of stripe rust resistance in wheat. Theor Appl Genet 126:2427–2449. Saintenac C, Zhang W, Salcedo A, Rouse MN, Trick HN, Akhunov E, Dubcovsky J (2013). Identification of wheat gene Sr35 that confers resistance to Ug99 stem rust race group. Science, 341: 783-786. Sarris P, Cevik V, Dagadas G, Jones JDG, Krasileva KV (2016). Comparative analysis of plant immune receptor architectures uncovers host proteins likely targeted by pathogens. BMC Biology, 14: 8. Schwessinger B (2016). Fundamental wheat stripe ruest research in the 21 st century. New Phytlogist, 2123: 1625-1631. Schwessinger B, Sperschneider J, Cuddy WS, Garnica DP, Miller ME, et al. (2018). A near-complete haplotype-phased genome of the dikaryotic wheat stripe rust fungus Puccinia striiformis f. sp. tritici reveals high interhaplotype diversity. mBio 9: e02275–e02317. Schwessinger B, Chen Y-J, Tien R, Vogt JK, Sperschneider J, et al. (2020). Distinct life histories impact dikaryotic genome evolution in the rust fungus Puccinia striiformis causing stripe rust in wheat. Genome Biology and Evolution, 12: 597-617. Singh R.P (1992). Association between gene Lr34 for leaf rust resistance and leaf tip necrosis in wheat. Crop Science, 32: 874–878. Singh R, William H, Huerta-Espino J, Rosewarne G (2004). Wheat rust in Asia: meeting the challenges with old and new technologies. Proceedings of the 4th International Crop Science Congress. Brisbane, Australia. Singh RP, Huerta-Espino J, William HM (2005). Genetics and Breeding for Durable Resistance to Leaf and Stripe Rusts in Wheat. Turkish Journal of Agriculture and Forestry, 29: 121–127. Solh M, Nazari K, Tadesse W, Wellings CR (2012). The growing threat of stripe rust worldwide. Borlaug Global Rust Initiative (BGRI) Conference. Beijing, China. Sørensen CK, Hovmøller MS, Leconte M, Dedryver F, de Vallavieille-Pope C (2014). New races of Puccinia striiformis found in Europe reveal race specificity of long-term effective adult plant resistance in wheat. Phytopathology, 104: 1042–1051. Spielmeyer W, McIntosh RA, Kolmer J, Lagudah ES (2005). Powdery mildew resistance and Lr34 / Yr18 genes for durable resistance to leaf and stripe rust cosegregate at a locus on the short arm of chromosome 7D of wheat. Theoretical and Applied Genetics, 111: 731–735. Strange RN, Scott PR (2005). Plant disease: a threat to global food security. Annual Review of Phytopathology, 43: 83–116. Steele KA, Humphreys E, Wellings CR, Dickinson MJ (2001). Support for a stepwise mutation model for pathogen evolution in Australasian Puccinia striiformis f. sp. tritici by use of molecular markers. Plant Pathology, 50: 174–180. Steuernagel B, Periyannan SK, Hernández-Pinzón I, Witek K, Rouse MN, et al. (2016). Rapid cloning of disease-resistance genes in plants using mutagenesis and sequence capture. Nature Biotechnology, 34: 652-655. Steuernagel B, Witek K, Krattinger SG, Ramirez-Gonzalez RH, Schoonbeek J-J, Yu G, Baggs E, Witek AI, Yadav I, Krasileva KV, Jones JDG, Uauy C, Keller B, Ridout CJ, Wulff BBH (2020). The NLR-annotator tool enables annotation of the intracellular immune receptor repertoire. Plant Physiology, 183: 468-482. Szabo LJ, Bushnell WR (2001). Hidden robbers: The role of fungal haustoria in parasitism of plants. Proceedings of the National Academy of Sciences, 98: 7654–7655. Thind AK, Wicker T, Šimková H, Fossati D, Moullet O, Brabant C, Vrána J, Doležel J, Krattinger SG (2017). Rapid cloning of genes in hexaploid wheat using cultivar-specific long-range chromosome assembly. Nature Biotechnology, 35:793-796. Uauy C, Brevis JC, Chen X, Khan I, Jackson L, Chicaiza O, Distelfeld A, Fahima T, Dubcovsky J (2005). High-temperature adult-plant (HTAP) stripe rust resistance gene Yr36 from Triticum turgidum ssp. dicoccoides is closely linked to the grain protein content locus Gpc-B1 . Theoretical and Applied Genetics, 112: 97–105. Walkowiak S, Gao L, Monat C, Haberer G, Kassa MT, et al. (2020). Multiple wheat genomes reveal global variation in modern breeding. Nature, 588: 277–283. Wang MN, Chen XM (2013). First report of Oregon Grape ( Mahonia aquifolium ) as an alternate host for the wheat stripe rust pathogen ( Puccinia striiformis f. sp. tritici ) under artificial inoculation. Plant Disease, 97: 839. Wang MN, Chen XM (2015). Barberry does not function as an alternate gost for Puccinia striiformis f. sp. tritici in the U. S. Pacific Northwest due to teliospore degradation and Barberry phenology. Plant Disease, 99: 1500–1506. Wang M, Chen X (2017). Stripe Rust Resistance. In: Chen X, Kang Z. (eds) Stripe rust. Springer, Dordrecht. Wang S, Li Q-P, Wang J, Yan Y, Zhang G-L, et al. (2019). Yr36/WKS1-mediated phosphorylation of PsbO, an extrinsic member of photosystem II, inhibits photosynthesis and confers stripe rust resistance in wheat. Molecular Plant, 12: 1639-1650. Watson A, Ghosh S, Williams MJ, Cuddy WS, Simmonds J, et al. (2018). Speed breeding is a powerful tool to accelerate crop research and breeding. Nature Plants, 4: 23-29. Wellings CR (2003). Stripe rust head infection. Cereal Rust Report, 1:1–2. Wellings CR (2007). Puccinia striiformis in Australia: A review of the incursion, evolution, and adaptation of stripe rust in the period 1979–2006. Australian Journal of Agricultural Research, 58: 567 . Wellings CR (2009). Late season stripe rust damage: head infection and unpredicted variety responses. Cereal Rust Report, 7: 1–4. Wellings CR (2011). Global status of stripe rust: a review of historical and current threats. Euphytica, 179: 129–141. Wellings CR, McIntosh RA, Walker J (1987). Puccinia striiformis f. sp. tritici in eastern Australia - possible means of entry and implications for plant quarantine. Plant Pathology, 36: 239–241. Wellings CR, Wright D, Keiper F, Loughman R (2003). First detection of wheat stripe rust in Western Australia: Evidence for a foreign incursion. Australasian Plant Pathology, 32: 321–322. Wellings CR, Singh RP, Yahyaoui AH, Nazari K, McIntosh RA (2009). The development and application of near-isogenic lines for monitoring cereal rust pathogens. Proceedings of the Borlaug Global Rust Initiative Technical Workshop, 77–87. Yuan C, Wu J, Yan B, Hao Q, Zhang C, et al. (2018). Remapping of the stripe rust resistance gene Yr10 in common wheat. Theoretical and Applied Genetics, 131: 1253-1262. Zeng S-M, Luo Y (2006). Long-distance spread and interregional epidemics of wheat stripe rust in China. Plant Disease, 90: 980–988. Zhang W, Chen S, Abate Z, Nirmala J, Rouse MN, Dubcovsky J (2017). Identification and characterization of Sr13 , a tetraploid wheat gene that confers resistance to the Ug99 stem rust race group. Proceedings of the National Academy of Sciences U S A, 114: E9483-E9492. Zhang C, Huang L, Zhang H, Hao Q, Yu B, et al. (2019). An ancestral NB-LRR with duplicated 3’UTRs confers stripe rust resistance in wheat and barley. Nature Communications, 10: 4023. Zhao J, Zhang H, Yao J, Huang L, Kang Z (2011). Confirmation of Berberis spp. as alternate hosts of Puccinia striiformis f. sp. tritici on wheat in China. Mygosystema, 30: 895. Zhao J, Wang L, Wang Z, Chen X, Zhang H, Yao J, Zhan G, Chen W, Huang L, Kang Z (2013). Identification of eighteen Berberis species as alternate hosts of Puccinia striiformis f. sp. tritici and virulence variation in the pathogen isolates from natural infection of barberry plants in China. Phytopathology, 103: 927–934. Zheng W, Huang L, Huang J, Wang X, Chen X, et al. (2013). High genome heterozygosity and endemic genetic recombination in the wheat stripe rust fungus. Nature Communications, 4: 2673. Tables Table 1. Cloned wheat rust resistance ( R ) genes. ASR = all-stage resistance. APR = adult plant resistance. Lr = leaf rust, Sr = stem rust, Yr = yellow rust. TKP = tandem kinase-pseudokinase. Chr. = chromosome. † Yr5/YrSP and Yr7 are listed using their RefSeq v1.1 gene model accession numbers. ‡ In bread wheat, the Sr50 locus from rye has been translocated to chromosome 1D. * See also Yuan et al. (2018), who indicate the CC-NBS-LRR gene identified by Liu et al. (2014) may not be the underlying gene. Cloned YR resistance genes Original source Chr. R gene class NCBI protein accession number Gene functional annotation Reference Lr1 T. aestivum 5D ASR ABS29034 CC-NBS-LRR Cloutier et al. 2007 Lr10 T. aestivum 1A ASR AAQ01784 CC-NBS-LRR Feuillet et al. 2003 Lr21 Ae. tauschii 1D ASR ACO53397 NBS-LRR Huang et al. 2003 Lr22a Ae. tauschii 2D ASR ARO38244 CC-NBS-LRR Thind et al. 2017 Sr13 T. turgidum ssp. durum 6A ASR ATE88995 CC-NBS-LRR Zhang et al. 2017 Sr21 T. monococcum 1D ASR AVK42833 CC-NBS-LRR Chen et al. 2018 Sr22 T. monococcum 7A ASR CUM44200 CC-NBS-LRR Steuernagel et al. 2016 Sr33 Ae. tauschii 1D ASR AGQ17384 CC-NBS-LRR Periyannan et al. 2013 Sr35 T. monococcum 3A ASR AGP75918 CC-NBS-LRR Saintenac et al. 2013 Sr45 Ae. tauschii 1D ASR CUM44213 CC-NBS-LRR Steuernagel et al. 2016 Sr46 Ae. tauschii 2D ASR AYV61514 CC-NBS-LRR Arora et al. 2019 Sr50 Secale cereale 1R ‡ ASR ALO61074 CC-NBS-LRR Mago et al. 2015 Sr60 T. monococcum 5A ASR LRRK123 Tandem kinase Chen et al. 2020 SrTA1662 Ae. tauschii 1D ASR Not listed CC-NBS-LRR Arora et al. 2019 Yr5/YrSP T. spelta album 2B ASR TraesCS2B02G488000 † BED-NBS-LRR Marchal et al. 2018 Yr7 T. aestivum 2B ASR TraesCS2B02G488600 † BED-NBS-LRR Marchal et al. 2018 Yr10 * T. aestivum 1B ASR AAG42168 CC-NBS-LRR Liu et al. 2014 Yr15/ YrG303/YrH52 T. turgidum ssp. dicoccoides 1B APR AXC33067 TKP Klymiuk et al. 2018 Yr18/Lr34 T. aestivum 7D APR ACN41354 ABC transporter Krattinger et al. 2009 Yr36 T. turgidum ssp. dicoccoides 6B APR ACF33187 Kinase-START Fu et al. 2009 Yr46/Lr67 T. aestivum 4D APR ALL26331 Hexose transporter Moore et al. 2015 YrAS2388 Ae. tauschii 4D ASR QDW65446 CC-NBS-LRR Zhang et al. 2019 Cite Share Download PDF Status: Published Journal Publication published 25 Nov, 2021 Read the published version in Theoretical and Applied Genetics → Version 1 posted Reviews received at journal 30 May, 2021 Reviewers invited by journal 28 May, 2021 Editor assigned by journal 24 May, 2021 First submitted to journal 24 May, 2021 You are reading this latest preprint version Research Square lets you share your work early, gain feedback from the community, and start making changes to your manuscript prior to peer review in a journal. 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Also discoverable on Platform About Our Team In Review Editorial Policies Advisory Board Help Center Resources Author Services Accessibility API Access RSS feed Manage Cookie Preferences © Research Square 2026 | ISSN 2693-5015 (online) Privacy Policy Terms of Service Do Not Sell My Personal Information {"props":{"pageProps":{"initialData":{"identity":"rs-557233","acceptedTermsAndConditions":true,"allowDirectSubmit":false,"archivedVersions":[],"articleType":"Research Article","associatedPublications":[],"authors":[{"id":30014038,"identity":"c6fde059-50d6-4f92-9b42-d7dd0bd8bb7c","order_by":0,"name":"Laura Bouvet","email":"","orcid":"","institution":"NIAB: National Institute of Agricultural Botany","correspondingAuthor":false,"prefix":"","firstName":"Laura","middleName":"","lastName":"Bouvet","suffix":""},{"id":30014039,"identity":"560971fc-79e6-4bf2-b1fd-2655106b9db7","order_by":1,"name":"Sarah Holdgate","email":"","orcid":"","institution":"NIAB: National Institute of Agricultural Botany","correspondingAuthor":false,"prefix":"","firstName":"Sarah","middleName":"","lastName":"Holdgate","suffix":""},{"id":30014040,"identity":"b5905bdd-f3b7-4470-9798-9ca498af1419","order_by":2,"name":"Lucy James","email":"","orcid":"","institution":"NIAB: National Institute of Agricultural Botany","correspondingAuthor":false,"prefix":"","firstName":"Lucy","middleName":"","lastName":"James","suffix":""},{"id":30014041,"identity":"8301f571-76f6-4f92-89bc-314c7ea27648","order_by":3,"name":"Jane Thomas","email":"","orcid":"","institution":"NIAB: National Institute of Agricultural Botany","correspondingAuthor":false,"prefix":"","firstName":"Jane","middleName":"","lastName":"Thomas","suffix":""},{"id":30014042,"identity":"3c5b01ea-960a-42aa-8268-0e64cb1af304","order_by":4,"name":"Ian J. Mackay","email":"","orcid":"","institution":"NIAB: National Institute of Agricultural Botany","correspondingAuthor":false,"prefix":"","firstName":"Ian","middleName":"J.","lastName":"Mackay","suffix":""},{"id":30014043,"identity":"02c60189-dbb6-4589-b902-5fb0c0d1f71a","order_by":5,"name":"James Cockram","email":"data:image/png;base64,iVBORw0KGgoAAAANSUhEUgAAAZAAAAAyAQMAAABI0h/eAAAABlBMVEX///8AAABVwtN+AAAACXBIWXMAAA7EAAAOxAGVKw4bAAAA7UlEQVRIiWNgGAWjYBAC9gYwZcfAwAOiK4CUBAEtjBAtyVAtZ4jXchCihbENSBDU0n468eEPhgNy/D1nH366Oe+ODP/sBsYPH3PwaOnJ3WzMw3DAWOJsu7F07rZnPBJ3DjBLztyGz2G526QZGA4kbuBnYwBqOczDcCOBjZkXn5b+t9t//oBoYf6dO+cwjzwhLYIzcrcBfX4wcQNvG5t0bsNhHgNCWqQl3m6W5jFINpY4c4zNOufYYR7DOweb8fqFjz9348cfFXbAEEtjvp1Tc9he7nbzwQ8f8WiBAANU/zUQUj8KRsEoGAWjgAAAAB7FT0g0DloUAAAAAElFTkSuQmCC","orcid":"https://orcid.org/0000-0002-1014-6463","institution":"NIAB: National Institute of Agricultural Botany","correspondingAuthor":true,"prefix":"","firstName":"James","middleName":"","lastName":"Cockram","suffix":""}],"badges":[],"createdAt":"2021-05-24 11:04:16","currentVersionCode":1,"declarations":"","doi":"10.21203/rs.3.rs-557233/v1","doiUrl":"https://doi.org/10.21203/rs.3.rs-557233/v1","draftVersion":[],"editorialEvents":[{"content":"https://doi.org/10.1007/s00122-021-03983-z","type":"published","date":"2021-11-25T09:48:25+00:00"}],"editorialNote":"","failedWorkflow":false,"files":[{"id":9992305,"identity":"d701fe00-4689-40c9-b757-0d59c5f5835f","added_by":"auto","created_at":"2021-06-04 16:21:16","extension":"jpg","order_by":1,"title":"Figure 1","display":"","copyAsset":false,"role":"figure","size":90908,"visible":true,"origin":"","legend":"The Puccinia striiformis f. sp. tritici (Pst) lifecycle. Wheat Pst infection at the adult plant stage in wheat, showing (a) yellow, and (b) orange coloured pustules that shed urediniospores. (c) Symptoms of Pst infection of the wheat ear. (d) Diagram illustrating the main features of the Pst lifecycle. Top left: Wheat plants can be infected by, (i) wind-blown single-cell dihaploid dikaryotic urediniospores (containing one haploid genome copy in each of the two nuclei within the cell: n + n′) produced on wheat, or (ii) by aeciospores (n + n′) produced on the alternative host (Berberis spp.). Yellow rust infection is typically observable on the heat upper leaf surface as parallel rows of yellow to orange pustules which release urediniospores, resulting in cycles of re-infection and cross-infection in wheat. Top middle: at ear emergence, yellow rust infection can occur on the florets of the wheat ear. Top right: towards the end of the wheat season, telia may form on the underside of the epidermis, from which diploid doubled haploid (2*n) two-celled teliospores are produced by karyogamy. Teliospores readily germinate to produce haploid basidiospores. Bottom right: Basidiospores germinate and infect leaves of the alternate host. Bottom middle: Basidiospore infection leads to the production of Pycnia, typically on the upper side of the leaves on the alternate host, which release haploid pycniospores. Fusion of pycniospores with the receptive hypha of a mating-type compatible pycnia leads to dikaryozation and the development of aecia on the leaf underside. Bottom left: Aecia release vegetative aeciospores (n + n1) which are only able to infect the primary host species (predominantly wheat). For more information, see Chen et al. (2014), Schwessinger (2016) or Mehmood et al. (2020). ","description":"","filename":"1.jpg","url":"https://assets-eu.researchsquare.com/files/rs-557233/v1/db3dffe9af57dd98ca7f679a.jpg"},{"id":15889136,"identity":"7a1b1012-6af0-4b7b-bd5d-8c8ad25ee997","added_by":"auto","created_at":"2021-11-25 09:48:33","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":442620,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-557233/v1/36347456-e443-4590-8229-afa3ab92ddc2.pdf"}],"financialInterests":"","formattedTitle":"\u003cp\u003eThe Evolving Battle Between Yellow Rust and Wheat: Implications for Global Food Security \u003c/p\u003e","fulltext":[{"header":"1. Introduction ","content":"\u003cp\u003eWheat (\u003cem\u003eTriticum aestivum\u003c/em\u003e L.) is one of the most important staple crops, with global demand predicted to increase to 324 kg/year (per capita) by 2050 (Alexandratos \u0026amp; Bruinsma, 2012). Wheat production faces numerous threats, with 10-16% of global wheat harvests estimated to be lost due to pests and diseases (Oerke, 2006; Strange \u0026amp; Scott, 2005). Yellow rust (YR), also known as stripe rust, is a major disease of wheat caused by the biotrophic fungal pathogen, \u003cem\u003ePuccinia striiformis\u003c/em\u003e f. sp. \u003cem\u003etritici \u003c/em\u003e(\u003cem\u003ePst\u003c/em\u003e). YR infection is most commonly noted on wheat leaves, where the resulting damage to photosynthetic tissues leads to reduced light interception and radiation use efficiency, thus lowering yields (Figure 1a-b). However, YR infection can also take place on the structures of the wheat ear such as the glumes, lemma and palea, particularly during moderate to severe epidemics, resulting in reduced grain yield and quality (Bouvet et al. 2021a; Cromey, 1989; Wellings, 2003; 2009) (Figure 1c). Recurrent \u003cem\u003ePst \u003c/em\u003eepidemics have occurred in the majority of wheat growing areas over the past 60 years and can cause significant yield losses and reductions in grain quality if not adequately controlled (Wellings, 2011). Notably, the past two decades have seen the rapid global emergence of more aggressive and genetically diverse \u003cem\u003ePst \u003c/em\u003epopulations adapted to warmer temperatures (Hovm\u0026oslash;ller et al. 2016; Hubbard et al. 2015; Milus et al. 2009), with concomitant impact on the YR resistance ratings of many wheat varieties. YR resistance breeding targets have had to adapt to tackle the rapidly changing \u003cem\u003ePst \u003c/em\u003ethreat, and sources of genetic resistance for the development of improved wheat varieties are continually being sought. This is now being aided by advances in wheat genomics approaches, as well as detailed characterisation of \u003cem\u003ePst \u003c/em\u003epopulation pathotypes, genetic diversity, effector characterisation and field monitoring. Ultimately, efficient control of wheat fungal disease will be via approaches that combine agricultural and agronomic practices, disease monitoring, and varietal genetic improvement (Downie et al. 2020). In this review, we summarise current understanding of the \u003cem\u003ePst \u003c/em\u003elifecycle, modes of dispersal and genetic diversity, and wheat genetic resistance and highlight some of the challenges facing the efforts to maintain adequate protection against wheat YR infection, with a focus on genetic resistance approaches.\u003c/p\u003e"},{"header":"2. The Complex Pathogen Lifecycle ","content":"\u003cp\u003e\u003cem\u003ePst \u003c/em\u003egoes through five different spore stages and requires two plant host species for completion of its lifecycle (Figure 1d). The two broad stages of the \u003cem\u003ePst \u003c/em\u003elifecycle are classified as: (i) the asexual stage which occurs on wheat (the primary host), and (ii) the sexual stage which we now know occurs on \u003cem\u003eBerberis\u003c/em\u003e species (the alternate host). In wheat, YR disease occurs during the asexual stage of the \u003cem\u003ePst\u003c/em\u003e lifecycle and is caused by multiple cycles of dikaryotic (i.e. two nuclei in each cell: n + n) \u003cem\u003ePst\u003c/em\u003e urediniospores re-infecting the primary host via wind dispersal. As it is this \u003cem\u003ePst \u003c/em\u003elifecycle stage that is detrimental to wheat production, the uredinial infection and colonisation processes have been studied extensively. Early phenotypic studies identified the environmental conditions conducive of infection and colonisation by uredinia: free moisture, a 9-13 \u0026deg;C temperature range for sporulation, and low light levels (reviewed in Line, 2002). During the initial infection stage, urediniospores germinate on the leaf surface and eventually form an appressorium from which hyphae develop and enter the leaf tissue via the stomata. Growing hyphae develop into a dense network extending between and inside host mesophyll cells. Among this network, haustoria infection structures will form and specifically develop in host cell walls to extract nutrients from it (Szabo \u0026amp; Bushnell, 2001). On the leaves of mature susceptible plants, disease symptoms are visible 12-14 days after infection, consisting of yellow to orange coloured urediniospores that erupt from pustules arranged in characteristic stripes that follow the veins down the leaf blade (Chen et al. 2014), which can then lead to successive rounds of secondary infections. On resistant to mildly susceptible varieties, symptoms will range from non-sporulating flecks (a sign of hypersensitivity) to necrotic and chlorotic patches with no to limited sporulation. Towards the end of the wheat growth season, diploid teliospores may be produced by some isolates via karogamy. These readily germinate to produce a promycellim of four cells, with meiosis subsequently resulting in a single haploid nucleus that forms a basidiospore able to infect the alternate host (Chen et al. 2014).\u003c/p\u003e\n\u003cp\u003eAlthough much less is known about the sexual stage, \u003cem\u003eBerberis\u003c/em\u003e species were long speculated to support the lifecycle of \u003cem\u003ePst \u003c/em\u003e(e.g. Mains, 1933; Straib, 1937; Hart \u0026amp; Becker, 1934), as well as the related rust species, \u003cem\u003ePuccinia\u003c/em\u003e\u003cem\u003egraminis\u003c/em\u003e f. sp. \u003cem\u003etritici\u003c/em\u003e (causal agent of stem rust). Historically this resulted in efforts to eradicate \u003cem\u003eBerberis \u003c/em\u003especies in many European and North American countries (Barnes et al. 2020). However, it was not until 2010 that \u003cem\u003eBerberis\u003c/em\u003e species were formally confirmed to support development of \u003cem\u003ePst\u003c/em\u003e pycnia and aecia (Jin et al. 2010). Curiously, \u003cem\u003eBerberis\u003c/em\u003e species infected with \u003cem\u003ePst\u003c/em\u003e are rarely observed in the wild, with only two accounts from China reported to date (Zhao et al. 2011, 2013). This may be due to the difficulty in finding an environment that simultaneously accommodates germination of teliospores (part of the asexual stage; enclosed in telia that form on wheat leaves towards the end of the infection season and produce basidiospores) and basidiospores (part of the sexual stage; forming on barberry leaves and requiring dew for germination), both of which have short viability (Wang \u0026amp; Chen, 2015). A recent study showed \u003cem\u003eBerberis\u003c/em\u003e species do not play a role in YR epidemics in the US Pacific Northwest (Wang \u0026amp; Chen, 2015), and an additional alternate host, \u003cem\u003eMahonia aquifolium\u003c/em\u003e (Oregon grape) has been identified (Wang \u0026amp; Chen, 2013). The main importance of the sexual \u003cem\u003ePst \u003c/em\u003estage on the alternative host to wheat infection is the generation of novel combinations of standing genetic variation that results in new genetically diverse isolates that can cause widespread epidemics and result in rapid changes in wheat resistance profiles.\u003c/p\u003e"},{"header":"3. Pathogens On The Move: Patterns Of Pst Dispersal And The Rise Of Divergent Lineages And Aggressive Races ","content":"\u003cp\u003eOver the years, monitoring of virulence changes in \u003cem\u003ePst\u003c/em\u003e populations in the major wheat producing regions has revealed notable changes in pathogen movement and adaptation. These studies were based on pathogenicity surveys, which use sets of differential wheat lines carrying known resistance genes, either near isogenic lines or cultivars, for the characterisation of pathotypes at the seedling stage (Wellings et al. 2009). More recently, molecular and genomics techniques have been used to infer \u003cem\u003ePst\u003c/em\u003e population structure and genetic diversity, confirming patterns of adaptation hypothesised in pathotype-based approaches. Here, we summarise key findings and events from the past three decades, specifically focusing on patterns of spore dispersal and \u003cem\u003ePst\u003c/em\u003e evolution and adaptation.\u003c/p\u003e\n\u003cp\u003e\u003cem\u003eBlowing in the wind\u003c/em\u003e\u003c/p\u003e\n\u003cp\u003e\u003cem\u003ePst\u003c/em\u003e urediniospores are windborne and can disperse at continental scales. Coupled with the obligate nature of the pathogen (requiring living tissue to survive), this has led to different scenarios for the observed seasonal and geographic patterns of dispersal. One such model is the local extinction and re-colonisation model, illustrated for example in China where regions of the Sichuan and Gansu provinces in which \u003cem\u003ePst\u003c/em\u003e prevails all year round act as a source of inoculum to the more northerly provinces in which wheat is predominantly grown as a winter crop (Brown \u0026amp; Hovm\u0026oslash;ller, 2002; Zeng \u0026amp; Luo, 2006). In this way, \u003cem\u003ePst\u003c/em\u003e populations re-establish at the beginning of each wheat cropping season in those regions where \u003cem\u003ePst\u003c/em\u003e spores are usually unable to over-winter. A similar pattern of spore movement according to prevailing winds and the seasonality of the cropping seasons has been speculated in North America, with spores migrating from southern central states of USA and Mexico to northern central states of USA and Canada (Chen, 2005). In North Western Europe, \u003cem\u003ePst \u003c/em\u003espore dispersion appears to follow the continental-island model, first described by Hedrick (1985), and has been the predominant model of \u003cem\u003ePst\u003c/em\u003e spore dispersion in North Western Europe. In this region, urediniospores travel up to 1,700 km with prevailing winds, and migrating between UK, France, Germany and Denmark (Hovm\u0026oslash;ller et al 2002). Investigations of YR emergence events in countries where it was previously absent provide examples of rapid inter-continental foreign incursion. Australia has been subject to several known incursions, of which two were notably detrimental to the wheat industry due to their rapid spread: (i) the first occurrence of \u003cem\u003ePst\u003c/em\u003e, in 1979 (Wellings et al. 1987), and (ii) the 2002 incursion in Western Australia (Wellings et al. 2003), now known to have originated from the Middle East/East Africa (Ali et al. 2014a) and attributed to a single \u003cem\u003ePst\u003c/em\u003e isolate (Wellings et al. 2003). The more recent arrival of \u003cem\u003ePst\u003c/em\u003e isolates in South Africa in 1996 were related to the Mediterranean and Central Asian populations (Boshoff et al. 2002; Ali et al. 2014a), and was speculated to be due to wind dispersal or human activities (Ali et al. 2014a). In all three cases, human activity, most likely through accidental transport on clothing, has been either demonstrated or strongly speculated, highlighting the increasing role of globalised trade and international travel as a means for \u003cem\u003ePst\u003c/em\u003e urediniospore dispersal.\u003c/p\u003e\n\u003cp\u003e\u003cem\u003ePathogen evolution and adaptation\u003c/em\u003e\u003c/p\u003e\n\u003cp\u003ePrior to 2000, pathogenicity surveys and molecular studies using isolates collected across the main wheat-producing regions in Europe, Australia and America typically reported \u003cem\u003ePst\u003c/em\u003e populations were clonal in nature, and that pathotypes exhibited close-relatedness and low genetic variation - predominantly underpinned by single step-wise mutations (Hovm\u0026oslash;ller et al. 2002; Enjalbert et al. 2005; Chen, 2005; Steele et al. 2001; Chen et al. 2010; Ali et al. 2014a; Hubbard et al. 2015; Hovm\u0026oslash;ller et al. 2016). Such clonally-derived \u003cem\u003ePst \u003c/em\u003emutations have caused several severe YR epidemics, due to the \u0026lsquo;breakdown\u0026rsquo; of specific wheat \u003cem\u003eYr\u003c/em\u003e resistance genes present in large acreages across the agricultural landscape. Notable examples include breakdown of \u003cem\u003eYr17\u003c/em\u003e in Northern Europe (Bayles et al. 2000), \u003cem\u003eYr27\u003c/em\u003e in Ethiopia (Solh et al. 2012), and \u003cem\u003eYr9\u003c/em\u003e in America, the Middle East and the Indian sub-continent (Chen et al. 2010; Singh et al. 2004). Before the year 2000, the only exceptions to such patterns of low \u003cem\u003ePst \u003c/em\u003egenetic variation were observed in isolates from the Himalayan (Nepal and Pakistan) and near Himalayan (China) regions, which exhibited high levels of genetic recombination, high ability for sexual reproduction and high genetic diversity (Duan et al. 2010; Mboup et al. 2009; Ali et al. 2014b). These areas were therefore classified the putative centres of \u003cem\u003ePst \u003c/em\u003eorigin (Ali et al. 2014b). However, the last two decades have seen the emergence of unusual virulence profiles and aggressive strains across the world. The most noteworthy event was the rise of two strains, \u003cem\u003ePstS1\u003c/em\u003e and \u003cem\u003ePstS2,\u003c/em\u003e across the USA (Chen et al. 2002; Markell \u0026amp; Milus, 2008), Europe (Hovm\u0026oslash;ller \u0026amp; Justesen, 2007) and Australia (Wellings, 2007) in the space of just three years in the early 2000s. A global study of pre- and post-2000 \u003cem\u003ePst\u003c/em\u003e races combining detailed virulence pathotyping and DNA fingerprinting found these while these two strains were genetically similar to each other, they were highly divergent from previous races in their respective geographic regions (Hovm\u0026oslash;ller et al. 2008). Their rapid spread was thought to be due to their increased aggressiveness (ability to yield more spores and for disease symptoms to occur more quickly) and high temperature adaptation - which was later demonstrated in the detailed study by Milus et al. (2009). In addition to \u003cem\u003ePstS1\u003c/em\u003e and \u003cem\u003ePstS2\u003c/em\u003e, additional atypical occurrences of \u003cem\u003ePst \u003c/em\u003eraces have since been reported. Enjalbert et al. (2005) demonstrated high levels of genetic divergence between the \u003cem\u003ePst\u003c/em\u003e population in northern France and a single clone specific to the South. What was atypical was that this single pathotype was maintained for a long time in this region, despite the presence of gene flow between Northern and Southern \u003cem\u003ePst\u003c/em\u003e populations. This isolate was later found to be more closely related to the Central Asian-Mediterranean population (Ali et al. 2014a). Similarly, instances of strong genetic divergence have also been revealed in North Western Europe (Flath \u0026amp; Barthels, 2002; Hovm\u0026oslash;ller \u0026amp; Justesen 2007a). Two groups of highly divergent pathotypes from the \u0026lsquo;old\u0026rsquo; North-Western European population exhibited three to four times higher levels of genetic diversity (Hovm\u0026oslash;ller et al. 2007). In 2011, two novel \u003cem\u003ePst\u003c/em\u003e races disrupted the European \u003cem\u003ePst\u003c/em\u003e landscape (www.wheatrust.org). Named after the host varieties on which they were first detected, one race was virulent on wheat cv. \u0026lsquo;Warrior\u0026rsquo; and the other was virulent on cv. \u0026lsquo;Kranich\u0026rsquo;. These were later characterised as \u003cem\u003ePstS7 \u003c/em\u003eand \u003cem\u003ePstS8 \u003c/em\u003erespectively (Ali et al. 2017), and were detected simultaneously across Europe and infected varieties that had exhibited durable adult plant resistance. Both races were distinct from the typical European isolates in that they produced an unusually high number of teliospores (Hubbard et al. 2015; Hovm\u0026oslash;ller et al. 2016). Additional \u003cem\u003ePst \u003c/em\u003eraces have been characterised (\u003cem\u003ePstS10 \u003c/em\u003ealso known as \u0026lsquo;Warrior (-)\u0026rsquo;, \u003cem\u003ePstS4 \u003c/em\u003e\u0026lsquo;Triticale aggressive\u0026rsquo;) and together with the other new genetically diverse \u003cem\u003ePst \u003c/em\u003eraces, have come to largely dominate within Europe (Ali et al. 2017; Hovm\u0026oslash;ller et al. 2016; Hubbard et al. 2015). Collectively, these atypical observations, further supported by genetic diversity studies, have led to speculation of an aerial-induced foreign incursion, which would be the first of its kind in Europe since the establishment of \u003cem\u003ePst\u003c/em\u003e in Europe during the 19\u003csup\u003eth\u003c/sup\u003e century. Beyond Europe, rapid invasions and the subsequent \u003cem\u003ePst \u003c/em\u003epopulation changes have been responsible for a number of YR epidemics in Central Asia, North and East Africa (Ali et al. 2017).\u003c/p\u003e"},{"header":"4. Chemical Control Of Yellow Rust","content":"\u003cp\u003eReview of global YR epidemics shows most wheat growing regions document recurrent crop losses of 5-10 %, with occasional losses of up to 25 % (Welling, 2011). However, following the global spread of aggressive \u003cem\u003ePst\u003c/em\u003e races since 2000, surveys highlight an increase in both the number of countries being significantly hit by such races, and the extent of the losses incurred (Beddow et al. 2015). Indeed, the financial implications of this change in \u003cem\u003ePst \u003c/em\u003erace structure estimated that a global average of US$ 158 million was lost annually pre 2000s, compared to US$ 979 million post 2000 (Beddow et al. 2015). Wheat growers have two principal options to protect against the effects of YR on yield: (i) protect their crop with agro-chemicals that limit initial infection and progression of pathogen colonisation, and/or (ii) grow wheat varieties with adequate levels of genetic resistance. Systemic fungicides that are absorbed into the plant became commercially available in the 1980s and have since formed an important part of integrated control measures against YR (Chen, 2005). Several products with different modes of action are available for protection against YR (reviewed by Chen \u0026amp; Kang, 2017), with timely application a key aspect of an effective fungicide programme. Such an approach has, for example, prevented significant financial losses in periods of severe epidemics in the USA (Line, 2002). While fungicide control provides an essential tool in combatting sudden yellow rust epidemics and in situations where growing resistant varieties is not an option, over-dependence on their use comes with negative environmental impacts and notable financial cost to growers. For example, in Australia an estimated A$ 359 million per year is spent on fungicides for YR control (Murray \u0026amp; Brennan, 2009). In the mid-to-long term, regular \u003cem\u003ePst \u003c/em\u003eexposure to fungicides also increases the risk that \u003cem\u003ePst \u003c/em\u003epopulations develop resistance to frequently used chemistries. Historically, \u003cem\u003ePst\u003c/em\u003e been classified as being at low-risk of developing fungicide resistance. However, of the three classes of fungicides active against \u003cem\u003ePst\u003c/em\u003e (demethylation inhibitors, DMIs; succinate dehydrogenase inhibitors, SDHIs; quinone outside inhibitors, QoIs), \u003cem\u003ePst \u003c/em\u003eresistance has evolved against two. Low levels of DHI resistance have been reported, and while high proportions of isolates carrying resistance associated mutations have been reported in some countries (Cook et al. 2021), DHI resistance has so far had limited agronomic-scale significance (Oliver, 2014). SDHIs active against rusts have only been introduced relatively recently, giving less time for \u003cem\u003ePst \u003c/em\u003eresistance to evolve. Nevertheless, sets of geographically diverse isolates have been identified that carry a mutation homologous to that linked to SDHI resistance in the related rust species \u003cem\u003eP. pachyrhzi \u003c/em\u003e(Cook et al. 2021). In the face of additional considerations such as changing regulation surrounding permissible chemistries, such evidence has led to the suggestion that the \u003cem\u003ePst\u003c/em\u003e risk classification should be upgraded (Oliver, 2014), fungicide resistance management practices be considered, and that systematic monitoring for \u003cem\u003ePst \u003c/em\u003efor fungicide resistance should be implemented (Cook et al. 2021). Lastly, the optimisation of fungicide timing, as well as improved fungicide application technologies, represent areas where additional research and development is required (Carmona et al. 2020).\u003c/p\u003e"},{"header":"5. Genetic Control Of Yellow Rust","content":"\u003cp\u003eMore than 300 wheat genomic regions conferring YR resistance have been reported (Rosewarne et al. 2013; Wang \u0026amp; Chen, 2017). Of these, ~80 are permanently named yellow rust resistance (\u003cem\u003eYr\u003c/em\u003e) genes (recently summarised by Jamil et al. 2020). Two main classes of YR resistance (\u003cem\u003eR\u003c/em\u003e) genes are commonly described. The first is termed \u0026lsquo;all stage resistance\u0026rsquo; (or \u0026lsquo;seedling resistance\u0026rsquo;) and confers qualitative resistance \u0026ndash; typically to one or a low number of \u003cem\u003ePst \u003c/em\u003eisolates. The second is termed \u0026lsquo;adult plant resistance\u0026rsquo; (APR) and confers quantitative or partial resistance. While these \u003cem\u003eR \u003c/em\u003egene classifications are useful, additional categories are also used, based on criteria such as phenotypic response (infection type, race specificity, resistance levels), temperature sensitivity, durability, the number of genes involved (monogenic versus polygenic) and the size of gene effect (Chen, 2013). One of the issues that comes with defining YR resistance with such a broad range of criteria is the assumptions associated with each of them. For example, APR is typically non-race specific, more durable than seedling resistance and conditioned by genes with minor or partial effect. Nevertheless, some APR genes have been shown to exhibit race specificity, such as \u003cem\u003eYr11, Yr12, Yr13\u003c/em\u003e and \u003cem\u003eYr14\u003c/em\u003e (Johnson, 1992; McIntosh et al. 1995).\u003c/p\u003e\n\u003cp\u003e\u003cem\u003eAll-stage resistance\u003c/em\u003e\u003c/p\u003e\n\u003cp\u003eInitially expressed at the seedling stage, all-stage resistance extends throughout the growth of the wheat plant and is characterised by a hypersensitive response. It is generally effective against some, but not all, \u003cem\u003ePst\u003c/em\u003e races and is therefore also referred to as \u0026lsquo;race-specific resistance\u0026rsquo;. All-stage resistance is underpinned by the gene-for-gene model, first explored by Flor (1956) in the flax-rust pathosystem, whereby the product of an \u003cem\u003eR\u003c/em\u003e gene must be recognised by the protein encoded by its corresponding avirulent (\u003cem\u003eAvr\u003c/em\u003e) gene in the pathogen, with resistance conferred by an incompatible \u003cem\u003eR-Avr\u003c/em\u003e interaction. This results in a qualitative resistance phenotype that can be easily assessed, historically making it a popular selection criterion in breeding programmes, and more recently, for gene cloning. The majority of catalogued YR \u003cem\u003eR\u003c/em\u003e genes exhibit this type of phenotype, and many become ineffective against present-day \u003cem\u003ePst \u003c/em\u003eraces. This type of resistance has commonly been shown to be a short-term strategy for YR control. Indeed, the deployment of varieties with single or low-numbers of all-stage resistance \u003cem\u003eYr\u003c/em\u003e genes over large acreages inevitably exerts high selective pressure on the pathogen, forcing it to evolve and mutate until host resistance is broken down, and leading to cycles of \u0026lsquo;boom and bust\u0026rsquo; (McDonald \u0026amp; Linde, 2002).\u003c/p\u003e\n\u003cp\u003e\u003cem\u003eAdult Plant Resistance\u003c/em\u003e\u003c/p\u003e\n\u003cp\u003eAdult plant resistance (APR) is characterised by slow rusting (a long period of latent infection, small lesion size) (Guo et al. 2008) or partial resistance, typically manifests at the adult plant stage, and has long been established as a durable source of YR resistance. Two notable examples are \u003cem\u003eYr18/Lr34/Sr67/Pm38\u003c/em\u003e, extensively deployed in spring wheat cultivars through the international breeding programme at CIMMYT (Singh et al. 2005) and \u003cem\u003eYr16\u003c/em\u003e, an APR gene commonly used in early European varieties such as \u0026lsquo;Cappelle Desprez\u0026rsquo;, a major hub in the European wheat pedigree (Fradgley et al. 2019). While APR is primarily non-race specific, examples of APR specificity to \u003cem\u003ePst\u003c/em\u003e races do exist, such as \u003cem\u003eYr12\u003c/em\u003e and \u003cem\u003eYr13\u003c/em\u003e (Johnson, 1992; McIntosh et al. 1995). Such APR race-specificity was initially reported by Johnson (1988) and has recently been observed in Europe following the spread of atypical \u003cem\u003ePst \u003c/em\u003eraces (S\u0026oslash;rensen et al. 2014). For example, while the APR resistance allele conferred by the founder Claire at the QTL \u003cem\u003eQYr.niab-2D.1 \u003c/em\u003ewas effective in the UK during the 2015 and 2016 seasons (Bouvet et al. 2021b), it has since broken down (Simon Berry, personal communication). Another example is that of \u003cem\u003eYr49\u003c/em\u003e, which was initially found to be non-race specific against all Australian \u003cem\u003ePst\u003c/em\u003e isolates, but when tested against Chinese races was found to be virulent and thus showed race-specificity (Ellis et al. 2014). These occurrences undermine the durability of APR and puts into question whether this pathotype criteria should be used to describe this type of resistance. It has been suggested that as some APR genes confer resistance against multiple biotrophic pathogens, this characteristic is a good indicator of durability. Examples include \u003cem\u003eYr18/Lr34/Sr67/Pm38\u003c/em\u003e (Spielmeyer et al. 2005; Lillemo et al. 2008), \u003cem\u003eYr29/Lr46/Sr58/Pm39\u003c/em\u003e (Lagudah, 2011), \u003cem\u003eYr30/Lr27/Sr2\u003c/em\u003e (Mago et al. 2011) and \u003cem\u003eYr46/Lr67/Sr55/Pm46\u003c/em\u003e (Herrer-Foessel et al. 2014). Interestingly, some of these genes are also associated with traits such as leaf tip necrosis (\u003cem\u003eYr18/Lr34/Sr67/Pm38,\u003c/em\u003e Singh et al. 1992; \u003cem\u003eYr29/Lr46/Sr58/Pm39\u003c/em\u003e, Rosewarne et al. 2006; \u003cem\u003eYr46/Lr67/Sr55/Pm46\u003c/em\u003e, Herrera-Foessel et al. 2014) and pseudo-black chaff (\u003cem\u003eYr30/Lr27/Sr2\u003c/em\u003e, Kota et al. 2006). Finally, some APR resistances are more effective at high temperature (usually 25-30 \u0026deg;C), and are termed High Temperature Adult Plant (HTAP) resistance. \u003cem\u003eYr36\u003c/em\u003e was initially characterised as HTAP (Uauy et al. 2005), with subsequent studies showing resistance was effective over 25 \u0026deg;C at all growth stages (Fu et al. 2009), and that the lower effective temperature range is 18 \u0026deg;C (Bryant et al. 2014).\u003c/p\u003e"},{"header":"6. Cloned Yellow Rust Resistance Genes","content":"\u003cp\u003eNucleotide Binding Sequence Leucine Rich Repeat (NBS-LRR) proteins are the most common class of proteins encoded by plant \u003cem\u003eR\u003c/em\u003e genes, and act predominantly by recognising the effector molecules that pathogens produce to inhibit host defence responses (Jones et al. 2016). To help fight against potential infecting pathogens, plant NLR gene families have radiated and diversified, for example via localised gene duplication or mutation within their LRR domains that bind pathogen effectors (Sarris et al. 2016). Furthermore, some NBS-LRRs contain additional \u0026lsquo;integrated\u0026rsquo; domains, the most common of which are kinase and DNA-binding domains (Andersen et al. 2020; Steuernagel et al. 2020), and are thought to be involved in receptor activation or downstream signalling (Sarris et al. 2016). Of the 18 genes conferring all-stage resistance to wheat rusts (yellow rust, stem rust, leaf rust) that have been cloned, 17 encode NBS-LRRs (Table 1). Furthermore, all but two of these NBS-LRRs contain coiled coil (CC) domains towards their N-termini; the exceptions being \u003cem\u003eYr7 \u003c/em\u003eand the allelic \u003cem\u003eR \u003c/em\u003egenes \u003cem\u003eYr5\u003c/em\u003e/\u003cem\u003eYrSP\u003c/em\u003e, each of which contains an N-terminus integrated BED zinc finger domain (Marchal et al. 2018) and \u003cem\u003eSr60\u003c/em\u003e, which is race-specific but confers a partial resistance phenotype and encodes a protein with two putative kinase domains (Chen et al. 2020).\u003c/p\u003e\n\u003cp\u003eThe ongoing changes and rapid spread of \u003cem\u003ePst \u003c/em\u003epopulations around the world has led to growing interest in more durable sources of resistance. To date, four adult plant YR resistance genes have been cloned. \u003cem\u003eYr36 \u003c/em\u003eencodes a protein with a kinase and a START lipid-binding domain (WHEAT KINASE START 1\u003cem\u003e, \u003c/em\u003eWKS1; Fu et al. 2009), and is thought to regulate reactive oxygen species (ROS) via phosphorylation of the thylakoid ascorbate peroxidase protein, resulting in increased levels of ROS during immunity (Gou et al. 2015). More recently, WKS1 has been shown to phosphorylate a protein component of photosystem II, sbO, resulting in reduced photosynthesis, leaf chlorosis and \u003cem\u003ePst \u003c/em\u003eresistance (Wang et al. 2019). \u003cem\u003eYr18\u003c/em\u003e\u003cem\u003e/Lr34\u003c/em\u003e encodes an ABC transporter (Krattinger et al. 2009) involved in the translocation of abscisic acid (Krattinger et al. 2019) while \u003cem\u003eYr46/Lr67 \u003c/em\u003eencodes a hexose transporter (Moore et al. 2015). Finally, the broad-spectrum \u003cem\u003eR \u003c/em\u003egene \u003cem\u003eYr15 \u003c/em\u003eencodes a tandem kinase-pseudokinse protein (Klymiuk et al. 2018) similar to that encoded by the barley stem rust resistance gene \u003cem\u003eRpg1 \u003c/em\u003e(Brueggeman et al .2002), and has recently been shown to be allelic with \u003cem\u003eYrG303/YrH52 \u003c/em\u003e(Klymiuk et al. 2020).\u003c/p\u003e"},{"header":"7. Designing Yellow Rust Resistant Wheat","content":"\u003cp\u003ePyramiding multiple resistance genes with additive effects into single genetic backgrounds should help prevent dramatic breakdown of wheat \u003cem\u003ePst \u003c/em\u003efield resistance. This first iteration of resistance gene pyramiding was developed using conventional breeding techniques. Indeed, the CIMMYT wheat breeding programme has made extensive use of the \u0026lsquo;\u003cem\u003eYr18\u003c/em\u003e complex\u0026rsquo; (\u003cem\u003eYr18\u003c/em\u003e and at least two closely linked resistance genes), which has provided durable resistance against yellow rust (Singh et al. 2005). Tools to help such approaches are available. These include protocols for the use of diagnostic molecular markers for marker-assisted breeding for many of the cloned resistance genes listed above (https://maswheat.ucdavis.edu/), as well as \u0026lsquo;speed breeding\u0026rsquo; methods that include the use of extended day lengths and controlled temperatures to shorten the wheat lifecycle (Watson et al. 2018). However, combining numerous unlinked genes via crossing is time-consuming. For example, a recent crossing scheme for the incorporation of 12 resistance genes int a single recurrent background involved 20 generations (Hafeez et al. 2021). Additionally, sources of YR resistance commonly originate from species related to bread wheat (see Table 1), including diploid wheat (e.g. \u003cem\u003eT. monococcum and \u003c/em\u003e\u003cem\u003eAegilops tauschii\u003c/em\u003e) and wild or cultivated tetraploid wheats (\u003cem\u003eT. turgidum \u003c/em\u003essp. \u003cem\u003edicoccoides \u003c/em\u003eand \u003cem\u003eT. turgidum \u003c/em\u003essp. \u003cem\u003edurum\u003c/em\u003e, respectively), resulting in introgression of linked chromosomal regions from the donor progenitor species. Such introgressed regions may have a negative effect on crop performance; for example, while \u003cem\u003eSr60 \u003c/em\u003ehas recently been introduced into bread wheat via the introgression of a small \u003cem\u003eT. monococcum \u003c/em\u003esegment containing the \u003cem\u003eR \u003c/em\u003egene, it nevertheless contains linked \u003cem\u003ePUROINDOLIN \u003c/em\u003egenes which will affect grain texture (Chen et al. 2020). Such considerations mean development of resistance gene cassettes containing multiple \u003cem\u003eR \u003c/em\u003egenes could provide a useful breeding tool, providing multiple sources of resistance inherited as a single genetic unit. Assuming their effects will be additive (i.e. show no epistasis), the four cloned APR genes, \u003cem\u003eYr15, Yr18, Yr36 \u003c/em\u003eand \u003cem\u003eYr46\u003c/em\u003e, possibly combined with one or more ASR genes, represent obvious immediate targets. Indeed, a transgene cassette containing four stem rust ASR genes and one APR gene has recently been shown to confer broad-spectrum field resistance (Luo et al. 2021). However, such approaches do not come without their challenges: genetic modification regulations and consumer acceptance remains an important barrier in many parts of the world, relatively low numbers of \u003cem\u003eYr\u003c/em\u003e genes have been cloned, and further work is needed to determine how specific genes work in combination within the context of inbred lines and F\u003csub\u003e1\u003c/sub\u003e hybrids. Towards tackling some of these issues, proposals to generate an \u003cem\u003eR \u003c/em\u003egene atlas for the major diseases of wheat have been made (Hafeez et al. 2021). Such concepts would be aided by the systematic identification and monitoring of the corresponding \u003cem\u003ePst \u003c/em\u003eeffectors and their standing variation across the agricultural environment, and should be extended to identify, characterise and eliminate wheat susceptibility (\u003cem\u003eS\u003c/em\u003e) genes that act to increase YR susceptibility (e.g. Corredor-Moreno et al. 2021). Underpinning such aims is the availability of new genomic techniques and resources in wheat that complement classical map-based cloning methodologies (recently reviewed by Adamski et al. 2020). For example, candidate gene association mapping using diversity panels of wheat or wheat relatives genotyped via reduced representation sequencing of classes of genes known \u003cem\u003ea priori \u003c/em\u003eto be prevalent in disease resistance (such as NBS-LRRs or wall-associated kinases). This method, termed \u0026lsquo;RenSeq\u0026rsquo; (Jupe et al. 2013), alongside functional validation via chemical mutagenesis of germplasm containing the functional allele of interest, has been used to identify the wheat stem rust resistance genes \u003cem\u003eSr46 \u003c/em\u003eand \u003cem\u003eSrTA1662 \u003c/em\u003e(Arora et al. 2019). Such association mapping approaches can be extended to include more representative coverage across the genome, for example using promotor/exome capture arrays (Gardiner et al. 2019) or whole-genome sequencing at low-coverage combined with imputation of SNPs and haplotypes, aided by the use of reference genome assemblies (e.g. for bread wheat: IWGSC, 2018; Walkowiak et al. 2021). Furthermore, the availability of \u003cem\u003ePst \u003c/em\u003egenome assemblies (e.g. Cantu et al. 2011, 2013; Zheng et al. 2013; Schwessinger et al. 2018, 2020) and mutant populations (Li et al. 2020), as well as gene expression resources and interrogation tools for both species (e.g. Adams et al. 2021) should help identify and characterise pathogen effectors. Detailed knowledge of the specificity of the recognition interactions between wheat \u003cem\u003eR \u003c/em\u003egenes and their corresponding \u003cem\u003ePst \u003c/em\u003eeffectors could be used, for example, to monitor the functionality of each component of \u003cem\u003eR \u003c/em\u003estacks, and to design synthetic \u003cem\u003eR \u003c/em\u003egenes engineered to recognise multiple races (as demonstrated for example by editing of the rice NBS-LRR gene \u003cem\u003ePikP\u003c/em\u003e to recognise multiple variants of the effector AvrPik from the rice blast pathogen \u003cem\u003eMagnaporthe oryzae\u003c/em\u003e; De La Concepcion et al. 2019). Similarly, identification of wheat \u003cem\u003eS \u003c/em\u003egenes would allow their elimination, via marker assisted approaches, mutation breeding or gene editing. Finally, further understanding of the exact developmental stages at which different adult plant resistance genes become effective, how best to deploy these in the agricultural landscape to best protect the crop from infection throughout the key growth stages, and understand which \u003cem\u003eR \u003c/em\u003egenes exhibit the lowest yield cost, will further help protect wheat against the effects of YR.\u003c/p\u003e"},{"header":"8. Future Perspectives","content":"\u003cp\u003eThe wide-ranging spread of new genetically diverse \u003cem\u003ePst \u003c/em\u003eraces has meant that YR is likely to become an increasing threat to global wheat production, resulting in lower yields and increased financial and environmental costs. Here, we conclude with a series of recommendations for future research and development in YR management over the next decade:\u003c/p\u003e\n\u003cp\u003e\u003cem\u003eHost genetics\u003c/em\u003e\u003c/p\u003e\n\u003col\u003e\n\u003cli\u003eSystematic programmes to identify and clone known and novel \u003cem\u003eR \u003c/em\u003egenes, particularly those conferring adult plant or non-host resistance.\u003c/li\u003e\n\u003cli\u003eInformed design and development of durable \u003cem\u003eR \u003c/em\u003egene pyramid combinations, via traditional crossing and/or \u003cem\u003eR \u003c/em\u003egene cassettes.\u003c/li\u003e\n\u003cli\u003eIdentification and targeted removal of susceptibility (\u003cem\u003eS\u003c/em\u003e) genes from breeders\u0026rsquo; germplasm.\u003c/li\u003e\n\u003c/ol\u003e\n\u003cp\u003e\u003cem\u003eMonitoring \u003c/em\u003e\u003c/p\u003e\n\u003col\u003e\n\u003cli\u003eRegional and international networks to rapidly monitor the emergence and spread of \u003cem\u003ePst \u003c/em\u003epathotypes.\u003c/li\u003e\n\u003cli\u003eField networks to monitor \u003cem\u003eR \u003c/em\u003egene effectiveness at regional/international scales.\u003c/li\u003e\n\u003c/ol\u003e\n\u003cp\u003e\u003cem\u003eAgronomy \u003c/em\u003e\u003c/p\u003e\n\u003col\u003e\n\u003cli\u003eRegional monitoring for the emergence and spread of fungicide resistances.\u003c/li\u003e\n\u003cli\u003eInnovation in fungicide application to allow more timely, accurate and efficient fungicide application.\u003c/li\u003e\n\u003cli\u003eThe use of variety mixtures, which is becoming increasingly used in some regions.\u003c/li\u003e\n\u003c/ol\u003e\n\u003cp\u003eUltimately, the success of advances in integrated YR management approaches will depend on timely communication of information to wheat growers. Therefore, trusted grower-facing networks and sources of information that can rapidly and succinctly inform and advise farmers of threats and best practice within each growing season will become increasingly critical in realising future ambitions to better protect wheat yields from diseases such as YR.\u003c/p\u003e"},{"header":"Abbreviations","content":"\u003cp\u003eAdult plant resistance APR\u003c/p\u003e\n\u003cp\u003eDemethylation inhibitors DMIs\u003c/p\u003e\n\u003cp\u003eGenome-wide association scan GWAS\u003c/p\u003e\n\u003cp\u003eMarker assisted selection MAS\u003c/p\u003e\n\u003cp\u003eNucleotide-binding leucine-rich repeat NLR\u003c/p\u003e\n\u003cp\u003e\u003cem\u003ePuccinia striiformis\u003c/em\u003e f. sp. \u003cem\u003etritici Pst\u003c/em\u003e\u003c/p\u003e\n\u003cp\u003eQuantitative trait locus QTL\u003c/p\u003e\n\u003cp\u003eQuinone outside inhibitors QoIs\u003c/p\u003e\n\u003cp\u003eSuccinate dehydrogenase inhibitors SDHIs\u003c/p\u003e\n\u003cp\u003eYellow rust YR\u003c/p\u003e"},{"header":"Declarations","content":"\u003cp\u003e\u003cstrong\u003eAuthor contributions: \u003c/strong\u003eLB wrote the manuscript with inputs from JC. All authors edited and critically revised the manuscript.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eFunding: \u003c/strong\u003eLB was funded via a Biotechnology and Biological Sciences Research Council (BBSRC) Doctoral Training Partnership PhD award to the University of Cambridge. JC\u0026rsquo;s time has partly supported by Biotechnology and Biological Research Council grant BB/N00518X/1, funded via the 2\u003csup\u003end\u003c/sup\u003e call of the ERA-CAPs framework.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eAcknowledgements: \u003c/strong\u003eWe thank Prof. Julian Hibberd (University of Cambridge) for administrative supervisory input during LB\u0026rsquo;s PhD.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eConflict of interest statement: \u003c/strong\u003eOn behalf of all authors, the corresponding author states that there is no conflict of interest.\u003cstrong\u003e\u003cbr /\u003e\u003c/strong\u003e\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\n\u003cli\u003eAdams TM, Olsson TSG, Ram\u0026iacute;rez-Gonz\u0026aacute;lez RH, Bryant R, Bryson R, et al. (2021). Rust expression browser: an open source database for simultaneous analysis of host pathogen gene expression profiles with expVIP. BMC Genomics, 22: 166.\u003c/li\u003e\n\u003cli\u003eAdamski NH, Borrill P, Brinton J, Harrington SA, Marchal C, et al. (2020). A roadmap for gene functional characterisation in crops with large genomes: lessons from polyploid wheat. eLife, 9: e55646.\u003c/li\u003e\n\u003cli\u003eAlexandratos N, Bruinsma J (2012). \u003cem\u003eWorld agriculture towards 2030/2050: the 2012 revision: ESA Working Paper No. 12-03\u003c/em\u003e. Rome.\u003c/li\u003e\n\u003cli\u003eAli S, Gladieux P, Leconte M, Gautier A, Justesen AF, Hovm\u0026oslash;ller MS, Enjalbert J, de Vallavieille-Pope C (2014a). Origin, migration routes and worldwide population genetic structure of the wheat yellow rust pathogen \u003cem\u003ePuccinia\u003c/em\u003e\u003cem\u003estriiformis\u003c/em\u003e f.sp. \u003cem\u003etritici\u003c/em\u003e. PLoS Pathogens, 10: e1003903.\u003c/li\u003e\n\u003cli\u003eAli S, Leconte M, Rahman H, Saqib MS, Gladieux P, Enjalbert J, de Vallavieille-Pope C (2014b). A high virulence and pathotype diversity of \u003cem\u003ePuccinia\u003c/em\u003e\u003cem\u003estriiformis\u003c/em\u003e f.sp. \u003cem\u003etritici\u003c/em\u003e at its centre of diversity, the Himalayan region of Pakistan. European Journal of Plant Pathology, 140: 275\u0026ndash;290.\u003c/li\u003e\n\u003cli\u003eAndersen EJ, Nepal MP, Purintun JM, Nelson D, Mermigka G, Sarris PF (2020). Wheat disease resistance genes and their diversification through integrated domain fusions. Front Genet, 11: 898.\u003c/li\u003e\n\u003cli\u003eArora S, Steuernagel B, Gaurav K, Chandramohan S, Long Y, et al. (2019). Resistance gene cloning from a wild crop relative by sequence capture and association genetics. Nature Biotechnol, 37: 139-143.\u003c/li\u003e\n\u003cli\u003eBarnes G, Saunders DGO, Williamson T (2020). Banishing barberry: The history of \u003cem\u003eBerberis vulgaris \u003c/em\u003eprevalence and wheat stem rust incidence across Britain. Plant Pathology, 69: 1193-1202.\u003c/li\u003e\n\u003cli\u003eBayles RA, Flath K, Hovm\u0026oslash;ller MS, de Vallavieille-Pope C (2000). Breakdown of the \u003cem\u003eYr17\u003c/em\u003e resistance to yellow rust of wheat in northern Europe. Agronomie, 20: 805\u0026ndash;811.\u003c/li\u003e\n\u003cli\u003eBeddow JM, Pardey PG, Chai Y, Hurley TM, Kriticos DJ, Braun H-J, Park RF, Cuddy WS, Yonow T (2015). Research investment implications of shifts in the global geography of wheat stripe rust. Nature Plants, 1: 15132.\u003c/li\u003e\n\u003cli\u003eBoshoff WHP, Pretorius ZA, van Niekerk BD (2002). Establishment, distribution, and pathogenicity of \u003cem\u003ePuccinia striiformis\u003c/em\u003e f. sp. \u003cem\u003etritici\u003c/em\u003e in South Africa. Plant Disease, 86: 485\u0026ndash;492.\u003c/li\u003e\n\u003cli\u003eBouvet L, Percival-Alwyn L, Berry S, Fenwick P, Mantello CC, Holdgate IJ, Mackay IJ, Cockram J (2021a). Wheat genetic loci conferring resistance to yellow rust in the face of recent epidemics of genetically diverse races of the fungus \u003cem\u003ePuccinia striiformis\u003c/em\u003e f. sp. \u003cem\u003etritici\u003c/em\u003e. Research Square, doi: 10.21203/rs.3.rs-459064/v1.\u003c/li\u003e\n\u003cli\u003eBouvet L, Berry S, Fenwick P, Holdgate IJ, Cockram J (2021b). Genetic resistance to yellow rust infection of the wheat ear is controlled by genes controlling foliar resistance and flowering time. BioRxiv, doi: https://doi.org/10.1101/2021.04.27.44165.\u003c/li\u003e\n\u003cli\u003eBrown JKM, Hovm\u0026oslash;ller MS (2002). Aerial dispersal of pathogens on the global and continental scales and its impact on plant disease. Science, 297: 537-541.\u003c/li\u003e\n\u003cli\u003eBrueggeman R, Rostoks N, Kudrna D, Kilian A, Han F, et al. (2002). The barley stem rust-resistance gene \u003cem\u003eRpg1\u003c/em\u003e is a novel disease-resistance gene with homology to receptor kinases. Proc Natl Acad Sci USA, 99: 9328\u0026ndash;9333.\u003c/li\u003e\n\u003cli\u003eBryant RRM, McGrann GRD, Mitchell AR, Schoonbeek H, Boyd LA, Uauy C, Dorling S, Ridout CJ (2014). A change in temperature modulates defence to yellow (stripe) rust in wheat line UC1041 independently of resistance gene \u003cem\u003eYr36\u003c/em\u003e. BMC Plant Biology, 14: 10.\u003c/li\u003e\n\u003cli\u003eCantu D, Govindarajulu M, Kozik A, Wang M, Chen X, et al. (2011). Nex generation sequencing provides rapid access to the genome of \u003cem\u003ePuccinia striiformis\u003c/em\u003e f. sp. \u003cem\u003etritici\u003c/em\u003e, the causal agent of wheat stripe rust. PLoS One, 6: e24230.\u003c/li\u003e\n\u003cli\u003eCantu D, Segovia V, MacLearn D, Bayles R, Chen X, Kamoun S, Dubcovsky J, Saunders DGO, Uauy C (2013). Genome analyses of the wheat yellow (stripe) rustpathogen \u003cem\u003ePuccinia\u003c/em\u003e\u003cem\u003estriiformis\u003c/em\u003e f. sp. \u003cem\u003etritici\u003c/em\u003e reveal polymorphic and haustorial expressed secreted proteins as candidate effectors. BMC Genomics, 14: 270.\u003c/li\u003e\n\u003cli\u003eCarmona M, Saautua F, P\u0026eacute;rez-H\u0026eacute;rnandez O, Reis EM (2020). Role of fungicide applications on the integreated management of wheat stripe rust. Forntiers in Plant Sciences, 11: 773.\u003c/li\u003e\n\u003cli\u003eChen XM (2005). Epidemiology and control of stripe rust [\u003cem\u003ePuccinia\u003c/em\u003e\u003cem\u003estriiformis\u003c/em\u003e f. sp. \u003cem\u003etritici\u003c/em\u003e] on wheat. Canadian Journal of Plant Pathology, 27: 314\u0026ndash;337.\u003c/li\u003e\n\u003cli\u003eChen XM (2013). Review Article: High-temperature Adult-Plant Resistance, Key for Sustainable Control of Stripe Rust. American Journal of Plant Sciences, 4:, 608\u0026ndash;627.\u003c/li\u003e\n\u003cli\u003eChen, X., \u0026amp; Kang, Z. (Eds.). (2017). \u003cem\u003eStripe Rust\u003c/em\u003e. Dordrecht: Springer Netherlands.\u003c/li\u003e\n\u003cli\u003eChen X, Penman L, Wan A, Cheng P (2010). Virulence races of \u003cem\u003ePuccinia striiformis\u003c/em\u003e f. sp. \u003cem\u003etritici\u003c/em\u003e in 2006 and 2007 and development of wheat stripe rust and distributions, dynamics, and evolutionary relationships of races from 2000 to 2007 in the United States. Canadian Journal of Plant Pathology, 32: 315\u0026ndash;333.\u003c/li\u003e\n\u003cli\u003eChen S, Rouse MN, Zhang W, Zhang X, Guo Y, Briggs J, et al. (2020). Wheat gene \u003cem\u003eSr60\u003c/em\u003e encodes a protein with two putative kinase domains that confers resistance to stem rust. New Phytol, 225: 948\u0026ndash;959.\u003c/li\u003e\n\u003cli\u003eChen S, Zhang W, Bolus S, Rouse MN, Dubcovsky J (2018). Identification and characterization of wheat stem rust resistance gene \u003cem\u003eSr21\u003c/em\u003e effective against the Ug99 race group at high temperature. PLoS Genet, 14: e1007287.\u003c/li\u003e\n\u003cli\u003eCloutier S, McCallum BD, Loutre C, Banks TW, Wicker T, Feuillet C, Keller B, Jordan MC (2007). Lead rust resistance gene \u003cem\u003eLr1\u003c/em\u003e, isolated from bread wheat (\u003cem\u003eTriticum aestivum \u003c/em\u003eL.) is a member of the large \u003cem\u003epsr567 \u003c/em\u003egene family. Plant Molecular Biology, 65: 93-106.\u003c/li\u003e\n\u003cli\u003eCook NM, Chng S, Woodman TL, Warren R, Oliver RP, Saunders DGO (2021). High frequency of fungicide resistance-associated mutations in the wheat yellow rust pathogen \u003cem\u003ePuccinia striiformis \u003c/em\u003ef. sp. \u003cem\u003etritici. \u003c/em\u003ePest Management Science, doi: 10.1002/ps.6380.\u003c/li\u003e\n\u003cli\u003eCorredor-Moreno P, Minter F, Davey PE, Wegel E, Kular B, Brett P, Lewis CM, Morgan YML, Mac\u0026iacute;as P\u0026eacute;rez A, Lorolev AV, Hill L, Saunders DGO (2021). The branched-chain amino acid aminotransferase TaBCAT1 modulates amino acid metabolism and positively regulates wheat rust susceptibility. Plant Cell, doi: https://doi.org/10.1093/plcell/koab049.\u003c/li\u003e\n\u003cli\u003eCromey MG (1989). Infection and control of stripe rust in wheat spikes. New Zealand Journal of Crop and Horticultural Science, 17: 159-164.\u003c/li\u003e\n\u003cli\u003eDe la Concepcion JC, Franceschetti M, MacLean D, Terauchi R, Kamoun S, Banfield MJ (2019). Protein engineering expands the effector recognition profile of a rice NLR immune receptor. eLife, 8: e47713.\u003c/li\u003e\n\u003cli\u003eDownie RC, Lin M, Borsi B, Ficke A, Lillemo M, Oliver RP, Phan H, Tan K-C, Cockram J (2020). Spetoria nodorum blotch of wheat: disease management and resistance breeding in the face of shifting disease dynamics and a changing environment. Phytopathol doi: https://doi.org/10.1094/PHYTO-07-20-0280-RVW.\u003c/li\u003e\n\u003cli\u003eDuan X, Tellier A, Wan A, Leconte M, de Vallavieille-Pope C, Enjalbert J (2010). \u003cem\u003ePuccinia\u003c/em\u003e\u003cem\u003estriiformis\u003c/em\u003e f.sp. \u003cem\u003etritici\u003c/em\u003e presents high diversity and recombination in the over-summering zone of Gansu, China. Mycologia, 102: 44\u0026ndash;53.\u003c/li\u003e\n\u003cli\u003eEllis JG, Lagudah ES, Spielmeyer W, Dodds PN (2014). The past, present and future of breeding rust resistant wheat. Frontiers in Plant Science, 5: 641.\u003c/li\u003e\n\u003cli\u003eEnjalbert J, Duan X, Leconte M, Hovm\u0026oslash;ller MS, Vallavieille-Pope C (2005). Genetic evidence of local adaptation of wheat yellow rust (\u003cem\u003ePuccinia striiformis\u003c/em\u003e f. sp. \u003cem\u003etritici\u003c/em\u003e) within France. Molecular Ecology, 14: 2065\u0026ndash;2073.\u003c/li\u003e\n\u003cli\u003eFeuillet C, Travella S, Stein N, Albar L, Nublat A, Keller B (2003). Map-based isolation of the leaf rust disease resistance gene \u003cem\u003eLr10 \u003c/em\u003efrom the hexaploid wheat (\u003cem\u003eTriticum aestivum \u003c/em\u003eL.) genome. Proc Natl Acad Sci U S A, 100: 15253-15258.\u003c/li\u003e\n\u003cli\u003eFlath K, Bartels G (2002). Virulenzsituation in \u0026uml;osterreichischen und deutschen Populationen des Weizengelbrostes. Bereicht \u0026uuml;ber die 52. Tagung der Vereinigung der Pflanzenz\u0026uuml;chter und Saatgutkaufleute \u0026Ouml;sterreichs, Gumpenstein.\u003c/li\u003e\n\u003cli\u003eFlor HH (1956). The Complementary Genic Systems in Flax and Flax Rust. Advances in Genetics, 8: 29-54.\u003c/li\u003e\n\u003cli\u003eFradgley N, Gardner KA, Cockram J, Elderfield J, Hickey JA, Howell P, et al. (2019). A large-scale pedigree resource of wheat reveals evidence for adaptation and selection by breeders. PLOS Biol, 17: e3000071.\u003c/li\u003e\n\u003cli\u003eFu D, Uauy C, Distelfeld A, Bechl A, Epstein L, Chen X, Sela H, Fahima T, Dubcovsky J (2009). A novel kinase-START gene confers temperature-dependent resistance to wheat stripe rust. Science, 322: 1357-1360.\u003c/li\u003e\n\u003cli\u003eGardiner LJ, Brabbs T, Akhunov A, Jordan K, Budak H, et al. (2019). Integrating genomic resources to present full gene and putative promoter capture probe sets for bread wheat. Gigascience, 8: giz018.\u003c/li\u003e\n\u003cli\u003eGou J-Y, Li K, Wu K, Wang X, Lin H, Cantu D, Uauy C, Dobon-Alonso A, Midorikawa T, Inoue K, S\u0026aacute;nchez J, Fu D, Blechl A, Wallington E, Fahima T, Meeta M, Epstein L, Dubcovsky J (2015). Wheat stripe rust resistance protein WKS1 reduces the ability of the thylakoid-associated ascorbate peroxidase to detoxify reactive oxygen species. The Plant Cell, 27: 1755\u0026ndash;1770.\u003c/li\u003e\n\u003cli\u003eGuo Q, Zhang ZJ, Xu YB, Li GH, Feng J, Zhou Y (2008). Quantitative trait loci for high-temperature adult-plant and slow-rusting resistance to \u003cem\u003ePuccinia\u003c/em\u003e\u003cem\u003estriiformis\u003c/em\u003e f. sp. \u003cem\u003etritici\u003c/em\u003e in wheat cultivars. Phytopathology, 98: 803\u0026ndash;809.\u003c/li\u003e\n\u003cli\u003eHafeez AN, Sanu A, Ghosh S, Gilbert D, Howden RL, Wulff BBH (2021). Creation and judicious application of a wheat resistance gene atlas. Doi: http://doi.org/10.5281/zenodo.4469514.\u003c/li\u003e\n\u003cli\u003eHedrick PW (1985). \u003cem\u003eGenetics of populations\u003c/em\u003e. Boston, USA: Jones and Bartlett Publishers, Inc.\u003c/li\u003e\n\u003cli\u003eHerrera-Foessel SA, Singh RP, Lillemo M, Huerta-Espino J, Bhavani S, Singh S, Lan C, Calvo-Salazar V, Lagudah ES (2014). \u003cem\u003eLr67\u003c/em\u003e/\u003cem\u003eYr46\u003c/em\u003e confers adult plant resistance to stem rust and powdery mildew in wheat. Theoretical and Applied Genetics, 127: 781\u0026ndash;789.\u003c/li\u003e\n\u003cli\u003eHovm\u0026oslash;ller MS, Justesen AF (2007). Appearance of atypical \u003cem\u003ePuccinia striiformis\u003c/em\u003e f. sp. \u003cem\u003etritici\u003c/em\u003e phenotypes in north-western Europe. Australian Journal of Agricultural Research, 58: 518\u0026ndash;524.\u003c/li\u003e\n\u003cli\u003eHovm\u0026oslash;ller MS, Justesen AF, Brown JKM (2002). Clonality and long-distance migration of \u003cem\u003ePuccinia striiformis\u003c/em\u003e f.sp. \u003cem\u003etritici\u003c/em\u003e in north-west Europe. Plant Pathology, 51: 24\u0026ndash;32.\u003c/li\u003e\n\u003cli\u003eHovm\u0026oslash;ller MS, Yahyaoui AH, Milus EA, Justesen AF (2008). Rapid global spread of two aggressive strains of a wheat rust fungus. Molecular Ecology, 17: 3818\u0026ndash;3826.\u003c/li\u003e\n\u003cli\u003eHovm\u0026oslash;ller MS, Walter S, Bayles RA, Hubbard A, Flath K, Sommerfeldt N, Leconte M, Czembor P, Rodriguez-Algaba J, Thach T, Hansen JG, Lassen P, Justesen AF, Ali S, de Vallavieille-Pope C (2016). Replacement of the European wheat yellow rust population by new races from the centre of diversity in the near-Himalayan region. Plant Pathology, 65:402-411.\u003c/li\u003e\n\u003cli\u003eHuang L, Brooks SA, Li W, Fellers JP, Trick HN, Gill BS (2003). Map-based cloning of leaf rust resistance gene \u003cem\u003eLr21\u003c/em\u003e from the large and polyploid genome of bread wheat. Genetics, 164: 655\u0026ndash;664.\u003c/li\u003e\n\u003cli\u003eHubbard A, Lewis C, Yoshida K, Ramirez-Gonzalez R, de Vallavieille-Pope C, Thomas J. et al. (2015). Field pathogenomics reveals the emergence of a diverse wheat yellow rust population. Genome Biol 16:23.\u003c/li\u003e\n\u003cli\u003eThe International Wheat Genome Sequencing Consortium (IWGSC), Appels R, Eversole K, Stein N, Feuillet C, Keller B, Rogers J Pozniak C, et al. (2018). Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science, 361: eaar7191.\u003c/li\u003e\n\u003cli\u003eJamil S, Shahzad R, Ahmad S, Fatima R, Zahid R, Anwar M, Iqbal MZ, Wang X (2020). Role of genetics, genomics and breeding approaches to combat stripe rust of wheat. Front Nutr 7:580715.\u003c/li\u003e\n\u003cli\u003eJin Y, Szabo LJ, Carson M (2010). Century-Old mystery of \u003cem\u003ePuccinia striiformis\u003c/em\u003e life history solved with the identification of \u003cem\u003eBerberis\u003c/em\u003e as an alternate host. Phytopathology, 100: 432\u0026ndash;435.\u003c/li\u003e\n\u003cli\u003eJohnson R (1988). Durable resistance to yellow (stripe) rust in wheat and its implications in plant breeding. In: N.W. Simmonds, S. Rajaram (Eds.) `Breeding Strategies for Resistance to the Rusts of Wheat\u0026rsquo;. CIMMYT, Mexico D.F. pp 63\u0026ndash;75.\u003c/li\u003e\n\u003cli\u003eJohnson R (1992). Past, present and future opportunities in breeding for disease resistance, with examples from wheat. Euphytica\u003cem\u003e, \u003c/em\u003e63: 3\u0026ndash;22.\u003c/li\u003e\n\u003cli\u003eJones JD, Vance RE, Dangl JL (2016). Intracellular innate immune surveillance devices in plants and animals. Science, 354: aaf6395.\u003c/li\u003e\n\u003cli\u003eJupe F, Witek K, Verweij W, Sliwka J, Pritchard L, et al. (2013). Resistance gene enrichment sequencing (RenSeq) enables reannotation of the NB-LRR gene family from sequenced plant genomes and rapid mapping of resistance loci in segregating populations.\u003cem\u003e Plant Journal,\u003c/em\u003e 76: 530\u0026ndash;544.\u003c/li\u003e\n\u003cli\u003eKota R,\u0026nbsp;Spielmeyer W,\u0026nbsp;McIntosh RA,\u0026nbsp;Lagudah ES\u0026nbsp;(2006).\u0026nbsp;Fine genetic mapping fails to dissociate durable stem rust resistance gene\u0026nbsp;\u003cem\u003eSr2\u003c/em\u003e\u0026nbsp;from pseudo‐black chaff in common wheat.\u0026nbsp;\u003cem\u003eTriticum aestivum\u003c/em\u003e\u0026nbsp;L.\u0026nbsp;Theor Appl Genet,\u0026nbsp;112: 492\u0026ndash;499.\u003c/li\u003e\n\u003cli\u003eKlymiuk V, Yaniv E, Huang L, Raats D, Fatiukha A, Chen SS, et al. (2018). Cloning of the wheat \u003cem\u003eYr15\u003c/em\u003e resistance gene sheds light on the plant tandem kinase-pseudokinase family. Nat. Commun, 9: 3735.\u003c/li\u003e\n\u003cli\u003eKlymiuk V, Fatiukha A, Raats D, Bocharova V, Huang L, Feng L, Jaiwar S, Pozniak Cm Coaker G, Dubcovsky J, Fahima T (2020). Three previously characterized resistances to yellow rust are encoded by a single locus \u003cem\u003eWtk1\u003c/em\u003e. J Exp Bot, 71: 2561-2572.\u003c/li\u003e\n\u003cli\u003eKrattinger SG, Lagudah ES, Spielmeyer W, Singh RP, Huerta-Espino J, McFadden H, Bossolini E, Selter LL, Keller B (2009). A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. Science, 323: 1360\u0026ndash;1363.\u003c/li\u003e\n\u003cli\u003eKrattinger S, Kang J, Br\u0026auml;unlich S, Boni R, Chauhan H, Selter LL, Robinson MD, Schmid MW, Wiederhold E, Hensel G, Kumlehn J, Sucher J, Martinoia E, Keller B (2019). Abscisic acid is a substrate of the ABC transporter encoded by the durable wheat disease resistance gene \u003cem\u003eLr34\u003c/em\u003e. New Phytologist, 223: 853-866.\u003c/li\u003e\n\u003cli\u003eLagudah ES (2011). Molecular genetics of race non-specific rust resistance in wheat. Euphytica, 179: 81\u0026ndash;91.\u003c/li\u003e\n\u003cli\u003eLi Y, Zia C, Wang M, Yin C, Chen X (2020). Whole-genome sequencing of \u003cem\u003ePuccinia striiformis\u003c/em\u003e f. sp. \u003cem\u003etritici \u003c/em\u003emutant isolates identified avirulence gene candidates. BMC Genomics, 21: 247.\u003c/li\u003e\n\u003cli\u003eLillemo M, Asalf B, Singh RP, Huerta-Espino J, Chen XM, He ZH, Bj\u0026oslash;rnstad \u0026Aring; (2008). The adult plant rust resistance loci \u003cem\u003eLr34\u003c/em\u003e/\u003cem\u003eYr18\u003c/em\u003e and \u003cem\u003eLr46\u003c/em\u003e/\u003cem\u003eYr29\u003c/em\u003e are important determinants of partial resistance to powdery mildew in bread wheat line Saar. Theoretical and Applied Genetics, 116: 1155\u0026ndash;1166.\u003c/li\u003e\n\u003cli\u003eLine RF (2002). Stripe rust of wheat and barley in North America: A retrospective historical review. Annual Review of Phytopathology, 40: 75\u0026ndash;118.\u003c/li\u003e\n\u003cli\u003eLiu W, Frick M, Huel R, Nykiforuk CL, Wang X, et al. (2014). The stripe rust resistance gene \u003cem\u003eYr10 \u003c/em\u003eencodes an evolutionary-conserved and unique CC-NBS-LRR sequence in wheat. Molecular Plant, 7: 1740-1755.\u003c/li\u003e\n\u003cli\u003eLuo M, Zie L, Chakraborty S, Wang A, Matny O, Jugovich M, et al. (2021). A five-transgene cassette confers broad-spectrum resistance to a fungal rust pathogen in wheat. Nature Biotechnology, doi: https://doi.org/10.1038/s41587-020-00770-x.\u003c/li\u003e\n\u003cli\u003eMago R, Zhang P, Vautrin S, \u0026Scaron;imlov\u0026aacute; H, Bansal U, et al. (2015). The wheat \u003cem\u003eSr50 \u003c/em\u003egene reveals rich diversity at a cereal disease resistance locus. Nature Plants, 1: 15186.\u003c/li\u003e\n\u003cli\u003eMarchal C, Zhang J, Zhang P, Fenwick P, Steuernagel B, Adamski NM, Boyd L, McIntosh R, Wulff BBH, Berry S, Lagudah E, Uauy C (2018). BED-domain-containing immune receptors confer diverse resistance spectra to yellow rust. Nature Plants, 4: 662\u0026ndash;668.\u003c/li\u003e\n\u003cli\u003eMarkell SG, Milus EA (2008). Emergence of a novel population of \u003cem\u003ePuccinia striiformis\u003c/em\u003e f. sp. \u003cem\u003etritici\u003c/em\u003e in Eastern United States. Phytopathology, 98: 632\u0026ndash;639.\u003c/li\u003e\n\u003cli\u003eMboup M, Leconte M, Gautier A, Wan AM, Chen W, de Vallavieille-Pope C, Enjalbert J (2009). Evidence of genetic recombination in wheat yellow rust populations of a Chinese oversummering area. Fungal Genetics and Biology, 46: 299\u0026ndash;307.\u003c/li\u003e\n\u003cli\u003eMcDonald BA, Linde C (2002). Pathogen Population Genetics, Evolutionary Potential, and Durable Resistance. Annual Review of Phytopathology\u003cem\u003e,\u003c/em\u003e 40: 349\u0026ndash;379.\u003c/li\u003e\n\u003cli\u003eMcIntosh RA, Wellings CR, Park RF (1995). \u003cem\u003eWheat rusts: An atlas of resistance genes\u003c/em\u003e. East Melbourne, Australia and Dordrecht and Boston: CSIRO and Kluwer Academic Publishers.\u003c/li\u003e\n\u003cli\u003eMehmood S, Sajid M, Huang L, Kang Z (2020). Alternate hosts and their impact on genetic diversity of \u003cem\u003ePuccina striiformis \u003c/em\u003ef. sp. \u003cem\u003etritici \u003c/em\u003eand disease epidemics. Journal of Plant Interactions, 15: 153-165.\u003c/li\u003e\n\u003cli\u003eMilus EA, Kristensen K, Hovm\u0026oslash;ller MS (2009). Evidence for increased aggressiveness in a recent widespread strain of \u003cem\u003ePuccina striiformis \u003c/em\u003ef. sp. \u003cem\u003etritici \u003c/em\u003ecausing stripe rust of wheat. Phytopathology, 99:89-94.\u003c/li\u003e\n\u003cli\u003eMoore JW, Herrera-Foessel S, Lan C, Schnippenkoetter W, Ayliffe M, Huerta-Espino J, Lillemo M, Viccars L, Milne R, Periyannan S, Kong X, Spielmeyer W, Talbot M, Bariana H, Patrick JW, Dodds P, Singh R, Lagudah E (2015). A recently evolved hexose transporter variant confers resistance to multiple pathogens in wheat. Nature Genetics, 47: 1494\u0026ndash;1498.\u003c/li\u003e\n\u003cli\u003eMurray G, Brennan J (2009). Estimating disease losses to the Australian wheat industry. Australasian Plant Pathology, 38: 558\u0026ndash;570.\u003c/li\u003e\n\u003cli\u003eOerke EC (2006). Crop losses to pests. The Journal of Agricultural Science, 144: 31.\u003c/li\u003e\n\u003cli\u003eOliver RP (2014). A reassessment of the risk of rust fungi developing resistance to fungicides. Pest Management Science, 70: 1641\u0026ndash;1645.\u003c/li\u003e\n\u003cli\u003ePeriyannan S, Moore J, Ayliffe M, Bansal U, Wang X, et al. (2013). The gene \u003cem\u003eSr33, \u003c/em\u003ean ortholog of barley \u003cem\u003eMla \u003c/em\u003egenes, encodes resistance to wheat stem rust race Ug99. Sciece, 341: 786-788.\u003c/li\u003e\n\u003cli\u003eRodriguez‐Algaba J, Walter S, S\u0026oslash;rensen CK, Hovm\u0026oslash;ller MS, Justesen AF (2014). Sexual structures and recombination of the wheat rust fungus \u003cem\u003ePuccinia striiformis\u003c/em\u003e on \u003cem\u003eBerberis\u003c/em\u003e\u003cem\u003evulgaris\u003c/em\u003e. Fungal Genetics and Biology 70:77\u0026ndash;85.\u003c/li\u003e\n\u003cli\u003eRosewarne GM, Singh RP, Huerta-Espino J, William HM, Bouchet S, Cloutier S, McFadden H, Lagudah ES (2006). Leaf tip necrosis, molecular markers and \u0026beta;1-proteasome subunits associated with the slow rusting resistance genes \u003cem\u003eLr46\u003c/em\u003e/\u003cem\u003eYr29\u003c/em\u003e. Theoretical and Applied Genetics, 112: 500\u0026ndash;508.\u003c/li\u003e\n\u003cli\u003eRosewarne GM, Herrera-Foessel SA, Singh RP, Huerta-Espino J, Lan CX, He ZH (2013). Quantitative trait loci of stripe rust resistance in wheat. Theor Appl Genet 126:2427\u0026ndash;2449.\u003c/li\u003e\n\u003cli\u003eSaintenac C, Zhang W, Salcedo A, Rouse MN, Trick HN, Akhunov E, Dubcovsky J (2013). Identification of wheat gene \u003cem\u003eSr35 \u003c/em\u003ethat confers resistance to Ug99 stem rust race group. Science, 341: 783-786.\u003c/li\u003e\n\u003cli\u003eSarris P, Cevik V, Dagadas G, Jones JDG, Krasileva KV (2016). Comparative analysis of plant immune receptor architectures uncovers host proteins likely targeted by pathogens. BMC Biology, 14: 8.\u003c/li\u003e\n\u003cli\u003eSchwessinger B (2016). Fundamental wheat stripe ruest research in the 21\u003csup\u003est\u003c/sup\u003e century. New Phytlogist, 2123: 1625-1631.\u003c/li\u003e\n\u003cli\u003eSchwessinger B, Sperschneider J, Cuddy WS, Garnica DP, Miller ME, et al. (2018). A near-complete haplotype-phased genome of the dikaryotic wheat stripe rust fungus \u003cem\u003ePuccinia\u003c/em\u003e\u003cem\u003estriiformis\u003c/em\u003e f. sp. \u003cem\u003etritici\u003c/em\u003e reveals high interhaplotype diversity. mBio 9: e02275\u0026ndash;e02317.\u003c/li\u003e\n\u003cli\u003eSchwessinger B, Chen Y-J, Tien R, Vogt JK, Sperschneider J, et al. (2020). Distinct life histories impact dikaryotic genome evolution in the rust fungus \u003cem\u003ePuccinia striiformis \u003c/em\u003ecausing stripe rust in wheat. Genome Biology and Evolution, 12: 597-617.\u003c/li\u003e\n\u003cli\u003eSingh R.P (1992). Association between gene \u003cem\u003eLr34\u003c/em\u003e for leaf rust resistance and leaf tip necrosis in wheat. Crop Science, 32: 874\u0026ndash;878.\u003c/li\u003e\n\u003cli\u003eSingh R, William H, Huerta-Espino J, Rosewarne G (2004). Wheat rust in Asia: meeting the challenges with old and new technologies. Proceedings of the 4th International Crop Science Congress. Brisbane, Australia.\u003c/li\u003e\n\u003cli\u003eSingh RP, Huerta-Espino J, William HM (2005). Genetics and Breeding for Durable Resistance to Leaf and Stripe Rusts in Wheat. Turkish Journal of Agriculture and Forestry, 29: 121\u0026ndash;127.\u003c/li\u003e\n\u003cli\u003eSolh M, Nazari K, Tadesse W, Wellings CR (2012). The growing threat of stripe rust worldwide. Borlaug Global Rust Initiative (BGRI) Conference. Beijing, China.\u003c/li\u003e\n\u003cli\u003eS\u0026oslash;rensen CK, Hovm\u0026oslash;ller MS, Leconte M, Dedryver F, de Vallavieille-Pope C (2014). New races of \u003cem\u003ePuccinia striiformis\u003c/em\u003e found in Europe reveal race specificity of long-term effective adult plant resistance in wheat. Phytopathology, 104: 1042\u0026ndash;1051.\u003c/li\u003e\n\u003cli\u003eSpielmeyer W, McIntosh RA, Kolmer J, Lagudah ES (2005). Powdery mildew resistance and \u003cem\u003eLr34\u003c/em\u003e/\u003cem\u003eYr18\u003c/em\u003e genes for durable resistance to leaf and stripe rust cosegregate at a locus on the short arm of chromosome 7D of wheat. Theoretical and Applied Genetics, 111: 731\u0026ndash;735.\u003c/li\u003e\n\u003cli\u003eStrange RN, Scott PR (2005). Plant disease: a threat to global food security. Annual Review of Phytopathology, 43: 83\u0026ndash;116.\u003c/li\u003e\n\u003cli\u003eSteele KA, Humphreys E, Wellings CR, Dickinson MJ (2001). Support for a stepwise mutation model for pathogen evolution in Australasian \u003cem\u003ePuccinia\u003c/em\u003e\u003cem\u003estriiformis\u003c/em\u003e f. sp. \u003cem\u003etritici\u003c/em\u003e by use of molecular markers. Plant Pathology, 50: 174\u0026ndash;180.\u003c/li\u003e\n\u003cli\u003eSteuernagel B, Periyannan SK, Hern\u0026aacute;ndez-Pinz\u0026oacute;n I, Witek K, Rouse MN, et al. (2016). Rapid cloning of disease-resistance genes in plants using mutagenesis and sequence capture. Nature Biotechnology, 34: 652-655.\u003c/li\u003e\n\u003cli\u003eSteuernagel B, Witek K, Krattinger SG, Ramirez-Gonzalez RH, Schoonbeek J-J, Yu G, Baggs E, Witek AI, Yadav I, Krasileva KV, Jones JDG, Uauy C, Keller B, Ridout CJ, Wulff BBH (2020). The NLR-annotator tool enables annotation of the intracellular immune receptor repertoire. Plant Physiology, 183: 468-482.\u003c/li\u003e\n\u003cli\u003eSzabo LJ, Bushnell WR (2001). Hidden robbers: The role of fungal haustoria in parasitism of plants. Proceedings of the National Academy of Sciences, 98: 7654\u0026ndash;7655.\u003c/li\u003e\n\u003cli\u003eThind AK, Wicker T, \u0026Scaron;imkov\u0026aacute; H, Fossati D, Moullet O, Brabant C, Vr\u0026aacute;na J, Doležel J, Krattinger SG (2017). Rapid cloning of genes in hexaploid wheat using cultivar-specific long-range chromosome assembly. Nature Biotechnology, 35:793-796.\u003c/li\u003e\n\u003cli\u003eUauy C, Brevis JC, Chen X, Khan I, Jackson L, Chicaiza O, Distelfeld A, Fahima T, Dubcovsky J (2005). High-temperature adult-plant (HTAP) stripe rust resistance gene \u003cem\u003eYr36\u003c/em\u003e from \u003cem\u003eTriticum\u003c/em\u003e\u003cem\u003eturgidum\u003c/em\u003e ssp. \u003cem\u003edicoccoides\u003c/em\u003e is closely linked to the grain protein content locus \u003cem\u003eGpc-B1\u003c/em\u003e. Theoretical and Applied Genetics, 112: 97\u0026ndash;105.\u003c/li\u003e\n\u003cli\u003eWalkowiak S, Gao L, Monat C, Haberer G, Kassa MT, et al. (2020). Multiple wheat genomes reveal global variation in modern breeding. Nature, 588: 277\u0026ndash;283.\u003c/li\u003e\n\u003cli\u003eWang MN, Chen XM (2013). First report of Oregon Grape (\u003cem\u003eMahonia aquifolium\u003c/em\u003e) as an alternate host for the wheat stripe rust pathogen (\u003cem\u003ePuccinia striiformis\u003c/em\u003e f. sp. \u003cem\u003etritici\u003c/em\u003e) under artificial inoculation. Plant Disease, 97: 839.\u003c/li\u003e\n\u003cli\u003eWang MN, Chen XM (2015). Barberry does not function as an alternate gost for \u003cem\u003ePuccinia\u003c/em\u003e\u003cem\u003estriiformis\u003c/em\u003e f. sp. \u003cem\u003etritici\u003c/em\u003e in the U. S. Pacific Northwest due to teliospore degradation and Barberry phenology. Plant Disease, 99: 1500\u0026ndash;1506.\u003c/li\u003e\n\u003cli\u003eWang M, Chen X (2017). Stripe Rust Resistance. In: Chen X, Kang Z. (eds) Stripe rust. Springer, Dordrecht.\u003c/li\u003e\n\u003cli\u003eWang S, Li Q-P, Wang J, Yan Y, Zhang G-L, et al. (2019). Yr36/WKS1-mediated phosphorylation of PsbO, an extrinsic member of photosystem II, inhibits photosynthesis and confers stripe rust resistance in wheat. Molecular Plant, 12: 1639-1650.\u003c/li\u003e\n\u003cli\u003eWatson A, Ghosh S, Williams MJ, Cuddy WS, Simmonds J, et al. (2018). Speed breeding is a powerful tool to accelerate crop research and breeding. Nature Plants, 4: 23-29.\u003c/li\u003e\n\u003cli\u003eWellings CR (2003). Stripe rust head infection. Cereal Rust Report, 1:1\u0026ndash;2.\u003c/li\u003e\n\u003cli\u003eWellings CR (2007). \u003cem\u003ePuccinia\u003c/em\u003e\u003cem\u003estriiformis\u003c/em\u003e in Australia: A review of the incursion, evolution, and adaptation of stripe rust in the period 1979\u0026ndash;2006. Australian Journal of Agricultural Research, 58: 567\u003cem\u003e.\u003c/em\u003e\u003c/li\u003e\n\u003cli\u003eWellings CR (2009). Late season stripe rust damage: head infection and unpredicted variety responses. Cereal Rust Report, 7: 1\u0026ndash;4.\u003c/li\u003e\n\u003cli\u003eWellings CR (2011). Global status of stripe rust: a review of historical and current threats. Euphytica, 179: 129\u0026ndash;141.\u003c/li\u003e\n\u003cli\u003eWellings CR, McIntosh RA, Walker J (1987). \u003cem\u003ePuccinia striiformis\u003c/em\u003e f. sp. \u003cem\u003etritici\u003c/em\u003e in eastern Australia - possible means of entry and implications for plant quarantine. Plant Pathology, 36: 239\u0026ndash;241.\u003c/li\u003e\n\u003cli\u003eWellings CR, Wright D, Keiper F, Loughman R (2003). First detection of wheat stripe rust in Western Australia: Evidence for a foreign incursion. Australasian Plant Pathology, 32: 321\u0026ndash;322.\u003c/li\u003e\n\u003cli\u003eWellings CR, Singh RP, Yahyaoui AH, Nazari K, McIntosh RA (2009). The development and application of near-isogenic lines for monitoring cereal rust pathogens. Proceedings of the Borlaug Global Rust Initiative Technical Workshop, 77\u0026ndash;87.\u003c/li\u003e\n\u003cli\u003eYuan C, Wu J, Yan B, Hao Q, Zhang C, et al. (2018). Remapping of the stripe rust resistance gene \u003cem\u003eYr10 \u003c/em\u003ein common wheat. Theoretical and Applied Genetics, 131: 1253-1262.\u003c/li\u003e\n\u003cli\u003eZeng S-M, Luo Y (2006). Long-distance spread and interregional epidemics of wheat stripe rust in China. Plant Disease, 90: 980\u0026ndash;988.\u003c/li\u003e\n\u003cli\u003eZhang W, Chen S, Abate Z, Nirmala J, Rouse MN, Dubcovsky J (2017). Identification and characterization of \u003cem\u003eSr13\u003c/em\u003e, a tetraploid wheat gene that confers resistance to the Ug99 stem rust race group. Proceedings of the National Academy of Sciences U S A, 114: E9483-E9492.\u003c/li\u003e\n\u003cli\u003eZhang C, Huang L, Zhang H, Hao Q, Yu B, et al. (2019). An ancestral NB-LRR with duplicated 3\u0026rsquo;UTRs confers stripe rust resistance in wheat and barley. Nature Communications, 10: 4023.\u003c/li\u003e\n\u003cli\u003eZhao J, Zhang H, Yao J, Huang L, Kang Z (2011). Confirmation of \u003cem\u003eBerberis\u003c/em\u003e spp. as alternate hosts of \u003cem\u003ePuccinia striiformis\u003c/em\u003e f. sp. \u003cem\u003etritici\u003c/em\u003e on wheat in China. Mygosystema, 30: 895.\u003c/li\u003e\n\u003cli\u003eZhao J, Wang L, Wang Z, Chen X, Zhang H, Yao J, Zhan G, Chen W, Huang L, Kang Z (2013). Identification of eighteen Berberis species as alternate hosts of \u003cem\u003ePuccinia striiformis\u003c/em\u003e f. sp. \u003cem\u003etritici\u003c/em\u003e and virulence variation in the pathogen isolates from natural infection of barberry plants in China. Phytopathology, 103: 927\u0026ndash;934.\u003c/li\u003e\n\u003cli\u003eZheng W, Huang L, Huang J, Wang X, Chen X, et al. (2013). High genome heterozygosity and endemic genetic recombination in the wheat stripe rust fungus. Nature Communications, 4: 2673.\u003cstrong\u003e\u003cbr /\u003e\u003c/strong\u003e\u003c/li\u003e\n\u003c/ol\u003e"},{"header":"Tables","content":"\u003cp\u003e\u003cstrong\u003eTable 1. \u003c/strong\u003eCloned wheat rust resistance (\u003cem\u003eR\u003c/em\u003e) genes. ASR = all-stage resistance. APR = adult plant resistance. \u003cem\u003eLr \u003c/em\u003e= leaf rust, \u003cem\u003eSr \u003c/em\u003e= stem rust, \u003cem\u003eYr \u003c/em\u003e= yellow rust. TKP = tandem kinase-pseudokinase. Chr. = chromosome. \u003csup\u003e\u0026dagger;\u003c/sup\u003e\u003cem\u003eYr5/YrSP \u003c/em\u003eand \u003cem\u003eYr7 \u003c/em\u003eare listed using their RefSeq v1.1 gene model accession numbers. \u003csup\u003e\u0026Dagger;\u003c/sup\u003eIn bread wheat, the \u003cem\u003eSr50 \u003c/em\u003elocus from rye has been translocated to chromosome 1D. \u003csup\u003e*\u003c/sup\u003eSee also Yuan et al. (2018), who indicate the CC-NBS-LRR gene identified by Liu et al. (2014) may not be the underlying gene.\u003c/p\u003e\n\u003ctable border=\"1\" width=\"0\"\u003e\n\u003ctbody\u003e\n\u003ctr style=\"height: 61px;\"\u003e\n\u003ctd style=\"height: 61px;\" width=\"151\"\u003e\u003cbr /\u003e\n\u003cp\u003e\u003cstrong\u003eCloned YR resistance genes \u003c/strong\u003e\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 61px;\" width=\"198\"\u003e\n\u003cp\u003e\u003cstrong\u003eOriginal source\u003c/strong\u003e\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 61px;\" width=\"47\"\u003e\n\u003cp\u003e\u003cstrong\u003eChr.\u003c/strong\u003e\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 61px;\" width=\"66\"\u003e\n\u003cp\u003e\u003cstrong\u003e\u003cem\u003eR \u003c/em\u003e\u003c/strong\u003e\u003cstrong\u003egene class\u003c/strong\u003e\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 61px;\" width=\"170\"\u003e\n\u003cp\u003e\u003cstrong\u003eNCBI protein accession number \u003c/strong\u003e\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 61px;\" width=\"151\"\u003e\n\u003cp\u003e\u003cstrong\u003eGene functional annotation \u003c/strong\u003e\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 61px;\" width=\"161\"\u003e\n\u003cp\u003e\u003cstrong\u003eReference \u003c/strong\u003e\u003c/p\u003e\n\u003c/td\u003e\n\u003c/tr\u003e\n\u003ctr style=\"height: 35px;\"\u003e\n\u003ctd style=\"height: 35px;\" width=\"151\"\u003e\n\u003cp\u003e\u003cem\u003eLr1 \u003c/em\u003e\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"198\"\u003e\n\u003cp\u003e\u003cem\u003eT. aestivum\u003c/em\u003e\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"47\"\u003e\n\u003cp\u003e5D\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"66\"\u003e\n\u003cp\u003eASR\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"170\"\u003e\n\u003cp\u003eABS29034\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"151\"\u003e\n\u003cp\u003eCC-NBS-LRR\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"161\"\u003e\n\u003cp\u003eCloutier et al. 2007\u003c/p\u003e\n\u003c/td\u003e\n\u003c/tr\u003e\n\u003ctr style=\"height: 35px;\"\u003e\n\u003ctd style=\"height: 35px;\" width=\"151\"\u003e\n\u003cp\u003e\u003cem\u003eLr10 \u003c/em\u003e\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"198\"\u003e\n\u003cp\u003e\u003cem\u003eT. aestivum\u003c/em\u003e\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"47\"\u003e\n\u003cp\u003e1A\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"66\"\u003e\n\u003cp\u003eASR\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"170\"\u003e\n\u003cp\u003eAAQ01784\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"151\"\u003e\n\u003cp\u003eCC-NBS-LRR\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"161\"\u003e\n\u003cp\u003eFeuillet et al. 2003\u003c/p\u003e\n\u003c/td\u003e\n\u003c/tr\u003e\n\u003ctr style=\"height: 35px;\"\u003e\n\u003ctd style=\"height: 35px;\" width=\"151\"\u003e\n\u003cp\u003e\u003cem\u003eLr21 \u003c/em\u003e\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"198\"\u003e\n\u003cp\u003e\u003cem\u003eAe. tauschii\u003c/em\u003e\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"47\"\u003e\n\u003cp\u003e1D\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"66\"\u003e\n\u003cp\u003eASR\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"170\"\u003e\n\u003cp\u003eACO53397\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"151\"\u003e\n\u003cp\u003eNBS-LRR\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"161\"\u003e\n\u003cp\u003eHuang et al. 2003\u003c/p\u003e\n\u003c/td\u003e\n\u003c/tr\u003e\n\u003ctr style=\"height: 35px;\"\u003e\n\u003ctd style=\"height: 35px;\" width=\"151\"\u003e\n\u003cp\u003e\u003cem\u003eLr22a\u003c/em\u003e\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"198\"\u003e\n\u003cp\u003e\u003cem\u003eAe. tauschii\u003c/em\u003e\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"47\"\u003e\n\u003cp\u003e2D\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"66\"\u003e\n\u003cp\u003eASR\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"170\"\u003e\n\u003cp\u003eARO38244\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"151\"\u003e\n\u003cp\u003eCC-NBS-LRR\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"161\"\u003e\n\u003cp\u003eThind et al. 2017\u003c/p\u003e\n\u003c/td\u003e\n\u003c/tr\u003e\n\u003ctr style=\"height: 35px;\"\u003e\n\u003ctd style=\"height: 35px;\" width=\"151\"\u003e\n\u003cp\u003e\u003cem\u003eSr13\u003c/em\u003e\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"198\"\u003e\n\u003cp\u003e\u003cem\u003eT. turgidum \u003c/em\u003essp. \u003cem\u003edurum\u003c/em\u003e\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"47\"\u003e\n\u003cp\u003e6A\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"66\"\u003e\n\u003cp\u003eASR\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"170\"\u003eATE88995\u0026nbsp;\u0026nbsp;\u0026nbsp;\u0026nbsp;\u0026nbsp;\u0026nbsp;\u0026nbsp;\u0026nbsp;\u0026nbsp;\u0026nbsp;\u0026nbsp;\u0026nbsp;\u0026nbsp;\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"151\"\u003e\n\u003cp\u003eCC-NBS-LRR\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"161\"\u003e\n\u003cp\u003eZhang et al. 2017\u003c/p\u003e\n\u003c/td\u003e\n\u003c/tr\u003e\n\u003ctr style=\"height: 35px;\"\u003e\n\u003ctd style=\"height: 35px;\" width=\"151\"\u003e\n\u003cp\u003e\u003cem\u003eSr21\u003c/em\u003e\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"198\"\u003e\n\u003cp\u003e\u003cem\u003eT. monococcum\u003c/em\u003e\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"47\"\u003e\n\u003cp\u003e1D\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"66\"\u003e\n\u003cp\u003eASR\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"170\"\u003e\n\u003cp\u003eAVK42833\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"151\"\u003e\n\u003cp\u003eCC-NBS-LRR\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"161\"\u003e\n\u003cp\u003eChen et al. 2018\u003c/p\u003e\n\u003c/td\u003e\n\u003c/tr\u003e\n\u003ctr style=\"height: 35px;\"\u003e\n\u003ctd style=\"height: 35px;\" width=\"151\"\u003e\n\u003cp\u003e\u003cem\u003eSr22 \u003c/em\u003e\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"198\"\u003e\n\u003cp\u003e\u003cem\u003eT. monococcum\u003c/em\u003e\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"47\"\u003e\n\u003cp\u003e7A\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"66\"\u003e\n\u003cp\u003eASR\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"170\"\u003e\n\u003cp\u003eCUM44200\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"151\"\u003e\n\u003cp\u003eCC-NBS-LRR\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"161\"\u003e\n\u003cp\u003eSteuernagel et al. 2016\u003c/p\u003e\n\u003c/td\u003e\n\u003c/tr\u003e\n\u003ctr style=\"height: 35px;\"\u003e\n\u003ctd style=\"height: 35px;\" width=\"151\"\u003e\n\u003cp\u003e\u003cem\u003eSr33 \u003c/em\u003e\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"198\"\u003e\n\u003cp\u003e\u003cem\u003eAe. tauschii\u003c/em\u003e\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"47\"\u003e\n\u003cp\u003e1D\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"66\"\u003e\n\u003cp\u003eASR\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"170\"\u003e\n\u003cp\u003eAGQ17384\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"151\"\u003e\n\u003cp\u003eCC-NBS-LRR\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"161\"\u003e\n\u003cp\u003ePeriyannan et al. 2013\u003c/p\u003e\n\u003c/td\u003e\n\u003c/tr\u003e\n\u003ctr style=\"height: 35px;\"\u003e\n\u003ctd style=\"height: 35px;\" width=\"151\"\u003e\n\u003cp\u003e\u003cem\u003eSr35 \u003c/em\u003e\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"198\"\u003e\n\u003cp\u003e\u003cem\u003eT. monococcum\u003c/em\u003e\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"47\"\u003e\n\u003cp\u003e3A\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"66\"\u003e\n\u003cp\u003eASR\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"170\"\u003e\n\u003cp\u003eAGP75918\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"151\"\u003e\n\u003cp\u003eCC-NBS-LRR\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"161\"\u003e\n\u003cp\u003eSaintenac et al. 2013\u003c/p\u003e\n\u003c/td\u003e\n\u003c/tr\u003e\n\u003ctr style=\"height: 35px;\"\u003e\n\u003ctd style=\"height: 35px;\" width=\"151\"\u003e\n\u003cp\u003e\u003cem\u003eSr45 \u003c/em\u003e\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"198\"\u003e\n\u003cp\u003e\u003cem\u003eAe. tauschii\u003c/em\u003e\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"47\"\u003e\n\u003cp\u003e1D\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"66\"\u003e\n\u003cp\u003eASR\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"170\"\u003e\n\u003cp\u003eCUM44213\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"151\"\u003e\n\u003cp\u003eCC-NBS-LRR\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"161\"\u003e\n\u003cp\u003eSteuernagel et al. 2016\u003c/p\u003e\n\u003c/td\u003e\n\u003c/tr\u003e\n\u003ctr style=\"height: 35px;\"\u003e\n\u003ctd style=\"height: 35px;\" width=\"151\"\u003e\n\u003cp\u003e\u003cem\u003eSr46\u003c/em\u003e\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"198\"\u003e\n\u003cp\u003e\u003cem\u003eAe. tauschii\u003c/em\u003e\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"47\"\u003e\n\u003cp\u003e2D\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"66\"\u003e\n\u003cp\u003eASR\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"170\"\u003e\n\u003cp\u003eAYV61514\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"151\"\u003e\n\u003cp\u003eCC-NBS-LRR\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"161\"\u003e\n\u003cp\u003eArora et al. 2019\u003c/p\u003e\n\u003c/td\u003e\n\u003c/tr\u003e\n\u003ctr style=\"height: 37px;\"\u003e\n\u003ctd style=\"height: 37px;\" width=\"151\"\u003e\n\u003cp\u003e\u003cem\u003eSr50 \u003c/em\u003e\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 37px;\" width=\"198\"\u003e\n\u003cp\u003e\u003cem\u003eSecale cereale\u003c/em\u003e\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 37px;\" width=\"47\"\u003e\n\u003cp\u003e1R\u003csup\u003e\u0026Dagger;\u003c/sup\u003e\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 37px;\" width=\"66\"\u003e\n\u003cp\u003eASR\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 37px;\" width=\"170\"\u003e\n\u003cp\u003eALO61074\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 37px;\" width=\"151\"\u003e\n\u003cp\u003eCC-NBS-LRR\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 37px;\" width=\"161\"\u003e\n\u003cp\u003eMago et al. 2015\u003c/p\u003e\n\u003c/td\u003e\n\u003c/tr\u003e\n\u003ctr style=\"height: 35px;\"\u003e\n\u003ctd style=\"height: 35px;\" width=\"151\"\u003e\n\u003cp\u003e\u003cem\u003eSr60\u003c/em\u003e\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"198\"\u003e\n\u003cp\u003e\u003cem\u003eT. monococcum\u003c/em\u003e\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"47\"\u003e\n\u003cp\u003e5A\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"66\"\u003e\n\u003cp\u003eASR\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"170\"\u003e\n\u003cp\u003eLRRK123\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"151\"\u003e\n\u003cp\u003eTandem kinase\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"161\"\u003e\n\u003cp\u003eChen et al. 2020\u003c/p\u003e\n\u003c/td\u003e\n\u003c/tr\u003e\n\u003ctr style=\"height: 35px;\"\u003e\n\u003ctd style=\"height: 35px;\" width=\"151\"\u003e\n\u003cp\u003e\u003cem\u003eSrTA1662\u003c/em\u003e\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"198\"\u003e\n\u003cp\u003e\u003cem\u003eAe. tauschii\u003c/em\u003e\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"47\"\u003e\n\u003cp\u003e1D\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"66\"\u003e\n\u003cp\u003eASR\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"170\"\u003e\n\u003cp\u003e\u003cem\u003eNot listed\u003c/em\u003e\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"151\"\u003e\n\u003cp\u003eCC-NBS-LRR\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"161\"\u003e\n\u003cp\u003eArora et al. 2019\u003c/p\u003e\n\u003c/td\u003e\n\u003c/tr\u003e\n\u003ctr style=\"height: 37px;\"\u003e\n\u003ctd style=\"height: 37px;\" width=\"151\"\u003e\n\u003cp\u003e\u003cem\u003eYr5/YrSP\u003c/em\u003e\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 37px;\" width=\"198\"\u003e\n\u003cp\u003e\u003cem\u003eT. spelta album\u003c/em\u003e\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 37px;\" width=\"47\"\u003e\n\u003cp\u003e2B\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 37px;\" width=\"66\"\u003e\n\u003cp\u003eASR\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 37px;\" width=\"170\"\u003e\n\u003cp\u003e\u003cem\u003eTraesCS2B02G488000\u003c/em\u003e\u003csup\u003e\u0026dagger;\u003c/sup\u003e\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 37px;\" width=\"151\"\u003e\n\u003cp\u003eBED-NBS-LRR\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 37px;\" width=\"161\"\u003e\n\u003cp\u003eMarchal et al. 2018\u003c/p\u003e\n\u003c/td\u003e\n\u003c/tr\u003e\n\u003ctr style=\"height: 37px;\"\u003e\n\u003ctd style=\"height: 37px;\" width=\"151\"\u003e\n\u003cp\u003e\u003cem\u003eYr7\u003c/em\u003e\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 37px;\" width=\"198\"\u003e\n\u003cp\u003e\u003cem\u003eT. aestivum\u003c/em\u003e\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 37px;\" width=\"47\"\u003e\n\u003cp\u003e2B\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 37px;\" width=\"66\"\u003e\n\u003cp\u003eASR\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 37px;\" width=\"170\"\u003e\n\u003cp\u003e\u003cem\u003eTraesCS2B02G488600\u003c/em\u003e\u003csup\u003e\u0026dagger;\u003c/sup\u003e\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 37px;\" width=\"151\"\u003e\n\u003cp\u003eBED-NBS-LRR\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 37px;\" width=\"161\"\u003e\n\u003cp\u003eMarchal et al. 2018\u003c/p\u003e\n\u003c/td\u003e\n\u003c/tr\u003e\n\u003ctr style=\"height: 37px;\"\u003e\n\u003ctd style=\"height: 37px;\" width=\"151\"\u003e\n\u003cp\u003e\u003cem\u003eYr10\u003c/em\u003e\u003csup\u003e*\u003c/sup\u003e\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 37px;\" width=\"198\"\u003e\n\u003cp\u003e\u003cem\u003eT. aestivum\u003c/em\u003e\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 37px;\" width=\"47\"\u003e\n\u003cp\u003e1B\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 37px;\" width=\"66\"\u003e\n\u003cp\u003eASR\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 37px;\" width=\"170\"\u003e\n\u003cp\u003eAAG42168\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 37px;\" width=\"151\"\u003e\n\u003cp\u003eCC-NBS-LRR\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 37px;\" width=\"161\"\u003e\n\u003cp\u003eLiu et al. 2014\u003c/p\u003e\n\u003c/td\u003e\n\u003c/tr\u003e\n\u003ctr style=\"height: 35px;\"\u003e\n\u003ctd style=\"height: 35px;\" width=\"151\"\u003e\n\u003cp\u003e\u003cem\u003eYr15/\u003c/em\u003e\u003cem\u003eYrG303/YrH52\u003c/em\u003e\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"198\"\u003e\n\u003cp\u003e\u003cem\u003eT. turgidum \u003c/em\u003essp. \u003cem\u003edicoccoides\u003c/em\u003e\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"47\"\u003e\n\u003cp\u003e1B\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"66\"\u003e\n\u003cp\u003eAPR\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"170\"\u003e\n\u003cp\u003eAXC33067\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"151\"\u003e\n\u003cp\u003eTKP\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"161\"\u003e\n\u003cp\u003eKlymiuk et al. 2018\u003c/p\u003e\n\u003c/td\u003e\n\u003c/tr\u003e\n\u003ctr style=\"height: 35px;\"\u003e\n\u003ctd style=\"height: 35px;\" width=\"151\"\u003e\n\u003cp\u003e\u003cem\u003eYr18/Lr34 \u003c/em\u003e\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"198\"\u003e\n\u003cp\u003e\u003cem\u003eT. aestivum\u003c/em\u003e\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"47\"\u003e\n\u003cp\u003e7D\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"66\"\u003e\n\u003cp\u003eAPR\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"170\"\u003e\n\u003cp\u003eACN41354\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"151\"\u003e\n\u003cp\u003eABC transporter\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"161\"\u003e\n\u003cp\u003eKrattinger et al. 2009\u003c/p\u003e\n\u003c/td\u003e\n\u003c/tr\u003e\n\u003ctr style=\"height: 35px;\"\u003e\n\u003ctd style=\"height: 35px;\" width=\"151\"\u003e\n\u003cp\u003e\u003cem\u003eYr36 \u003c/em\u003e\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"198\"\u003e\n\u003cp\u003e\u003cem\u003eT. turgidum \u003c/em\u003essp. \u003cem\u003edicoccoides\u003c/em\u003e\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"47\"\u003e\n\u003cp\u003e6B\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"66\"\u003e\n\u003cp\u003eAPR\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"170\"\u003e\n\u003cp\u003eACF33187\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"151\"\u003e\n\u003cp\u003eKinase-START\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"161\"\u003e\n\u003cp\u003eFu et al. 2009\u003c/p\u003e\n\u003c/td\u003e\n\u003c/tr\u003e\n\u003ctr style=\"height: 35px;\"\u003e\n\u003ctd style=\"height: 35px;\" width=\"151\"\u003e\n\u003cp\u003e\u003cem\u003eYr46/Lr67 \u003c/em\u003e\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"198\"\u003e\n\u003cp\u003e\u003cem\u003eT. aestivum\u003c/em\u003e\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"47\"\u003e\n\u003cp\u003e4D\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"66\"\u003e\n\u003cp\u003eAPR\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"170\"\u003e\n\u003cp\u003eALL26331\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"151\"\u003e\n\u003cp\u003eHexose transporter\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"161\"\u003e\n\u003cp\u003eMoore et al. 2015\u003c/p\u003e\n\u003c/td\u003e\n\u003c/tr\u003e\n\u003ctr style=\"height: 35px;\"\u003e\n\u003ctd style=\"height: 35px;\" width=\"151\"\u003e\n\u003cp\u003e\u003cem\u003eYrAS2388\u003c/em\u003e\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"198\"\u003e\n\u003cp\u003e\u003cem\u003eAe. tauschii\u003c/em\u003e\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"47\"\u003e\n\u003cp\u003e4D\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"66\"\u003e\n\u003cp\u003eASR\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"170\"\u003eQDW65446\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"151\"\u003e\n\u003cp\u003eCC-NBS-LRR\u003c/p\u003e\n\u003c/td\u003e\n\u003ctd style=\"height: 35px;\" width=\"161\"\u003e\n\u003cp\u003eZhang et al. 2019\u003c/p\u003e\n\u003c/td\u003e\n\u003c/tr\u003e\n\u003c/tbody\u003e\n\u003c/table\u003e\n\u003cp\u003e\u0026nbsp;\u003c/p\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":false,"highlight":"","institution":"","isAcceptedByJournal":true,"isAuthorSuppliedPdf":false,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":true,"isPdf":false,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"theoretical-and-applied-genetics","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"taag","sideBox":"Learn more about [Theoretical and Applied Genetics](https://www.springer.com/journal/122)","snPcode":"122","submissionUrl":"https://submission.nature.com/new-submission/122/3","title":"Theoretical and Applied Genetics","twitterHandle":"","acdcEnabled":true,"dfaEnabled":true,"editorialSystem":"em","reportingPortfolio":"Springer Hybrid","inReviewEnabled":true,"inReviewRevisionsEnabled":false},"keywords":"Wheat fungal pathogens, disease resistance breeding, crop genomics, pathogenomics, cereal genetics, global food security","lastPublishedDoi":"10.21203/rs.3.rs-557233/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-557233/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003cp\u003eWheat (\u003cem\u003eTriticum aestivum \u003c/em\u003eL.) is a global commodity, and its production is a key component underpinning worldwide food security. Yellow rust, also known as stripe rust, is a wheat disease caused by the fungus \u003cem\u003ePuccinia striiformis\u003c/em\u003e f. sp. \u003cem\u003etritici \u003c/em\u003e(\u003cem\u003ePst\u003c/em\u003e), and results in yield losses in most wheat growing areas. Recently, the rapid global spread of genetically diverse sexually derived \u003cem\u003ePst \u003c/em\u003eraces, which have now largely replaced the previous clonally propagated slowly evolving endemic populations, has resulted in further challenges for the protection of global wheat yields. However, advances in the application of genomics approaches, in both the host and pathogen, combined with classical genetic approaches, pathogen and disease monitoring, provide resources to help increase the rate of genetic gain for yellow rust resistance via wheat breeding while reducing the carbon footprint of the crop. Here we review key elements in the evolving battle between the pathogen and host, with a focus on solutions to help protect future wheat production from this globally important disease.\u0026nbsp;\u003c/p\u003e","manuscriptTitle":"The Evolving Battle Between Yellow Rust and Wheat: Implications for Global Food Security","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2021-06-04 16:21:14","doi":"10.21203/rs.3.rs-557233/v1","editorialEvents":[{"type":"communityComments","content":0},{"type":"editorInvitedReview","content":"","date":"2021-05-31T00:57:00+00:00","index":0,"fulltext":""},{"type":"reviewersInvited","content":"","date":"2021-05-28T07:53:00+00:00","index":"","fulltext":""},{"type":"editorAssigned","content":"","date":"2021-05-24T23:35:00+00:00","index":"","fulltext":""},{"type":"submitted","content":"Theoretical and Applied Genetics","date":"2021-05-24T06:35:25+00:00","index":"","fulltext":""}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"theoretical-and-applied-genetics","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"taag","sideBox":"Learn more about [Theoretical and Applied Genetics](https://www.springer.com/journal/122)","snPcode":"122","submissionUrl":"https://submission.nature.com/new-submission/122/3","title":"Theoretical and Applied Genetics","twitterHandle":"","acdcEnabled":true,"dfaEnabled":true,"editorialSystem":"em","reportingPortfolio":"Springer Hybrid","inReviewEnabled":true,"inReviewRevisionsEnabled":false}}],"origin":"","ownerIdentity":"56b7c838-1f6c-406c-ab28-213cbceb2e2d","owner":[],"postedDate":"June 4th, 2021","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"published-in-journal","subjectAreas":[{"id":4753502,"name":"Medical Genetics"}],"tags":[],"updatedAt":"2021-11-25T09:48:25+00:00","versionOfRecord":{"articleIdentity":"rs-557233","link":"https://doi.org/10.1007/s00122-021-03983-z","journal":{"identity":"theoretical-and-applied-genetics","isVorOnly":false,"title":"Theoretical and Applied Genetics"},"publishedOn":"2021-11-25 09:48:25","publishedOnDateReadable":"November 25th, 2021"},"versionCreatedAt":"2021-06-04 16:21:14","video":"","vorDoi":"10.1007/s00122-021-03983-z","vorDoiUrl":"https://doi.org/10.1007/s00122-021-03983-z","workflowStages":[]},"version":"v1","identity":"rs-557233","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-557233","identity":"rs-557233","version":["v1"]},"buildId":"2u56kwukJI3zHK-uzyFNs","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}