Breeding for durable resistance in crops: defeated loci may act as Trojan horses compromising the effectiveness of major resistance genes

Breeding for durable resistance in crops: defeated loci may act as Trojan horses compromising the effectiveness of major resistance genes | bioRxiv /* */ /* */ <!-- <!-- /*! * yepnope1.5.4 * (c) WTFPL, GPLv2 */ (function(a,b,c){function d(a){return"[object Function]"==o.call(a)}function e(a){return"string"==typeof a}function f(){}function g(a){return!a||"loaded"==a||"complete"==a||"uninitialized"==a}function h(){var a=p.shift();q=1,a?a.t?m(function(){("c"==a.t?B.injectCss:B.injectJs)(a.s,0,a.a,a.x,a.e,1)},0):(a(),h()):q=0}function i(a,c,d,e,f,i,j){function k(b){if(!o&&g(l.readyState)&&(u.r=o=1,!q&&h(),l.onload=l.onreadystatechange=null,b)){"img"!=a&&m(function(){t.removeChild(l)},50);for(var d in y[c])y[c].hasOwnProperty(d)&&y[c][d].onload()}}var j=j||B.errorTimeout,l=b.createElement(a),o=0,r=0,u={t:d,s:c,e:f,a:i,x:j};1===y[c]&&(r=1,y[c]=[]),"object"==a?l.data=c:(l.src=c,l.type=a),l.width=l.height="0",l.onerror=l.onload=l.onreadystatechange=function(){k.call(this,r)},p.splice(e,0,u),"img"!=a&&(r||2===y[c]?(t.insertBefore(l,s?null:n),m(k,j)):y[c].push(l))}function j(a,b,c,d,f){return q=0,b=b||"j",e(a)?i("c"==b?v:u,a,b,this.i++,c,d,f):(p.splice(this.i++,0,a),1==p.length&&h()),this}function k(){var a=B;return a.loader={load:j,i:0},a}var l=b.documentElement,m=a.setTimeout,n=b.getElementsByTagName("script")[0],o={}.toString,p=[],q=0,r="MozAppearance"in l.style,s=r&&!!b.createRange().compareNode,t=s?l:n.parentNode,l=a.opera&&"[object Opera]"==o.call(a.opera),l=!!b.attachEvent&&!l,u=r?"object":l?"script":"img",v=l?"script":u,w=Array.isArray||function(a){return"[object Array]"==o.call(a)},x=[],y={},z={timeout:function(a,b){return b.length&&(a.timeout=b[0]),a}},A,B;B=function(a){function b(a){var a=a.split("!"),b=x.length,c=a.pop(),d=a.length,c={url:c,origUrl:c,prefixes:a},e,f,g;for(f=0;f<d;f++)g=a[f].split("="),(e=z[g.shift()])&&(c=e(c,g));for(f=0;f<b;f++)c=x[f](c);return c}function g(a,e,f,g,h){var i=b(a),j=i.autoCallback;i.url.split(".").pop().split("?").shift(),i.bypass||(e&&(e=d(e)?e:e[a]||e[g]||e[a.split("/").pop().split("?")[0]]),i.instead?i.instead(a,e,f,g,h):(y[i.url]?i.noexec=!0:y[i.url]=1,f.load(i.url,i.forceCSS||!i.forceJS&&"css"==i.url.split(".").pop().split("?").shift()?"c":c,i.noexec,i.attrs,i.timeout),(d(e)||d(j))&&f.load(function(){k(),e&&e(i.origUrl,h,g),j&&j(i.origUrl,h,g),y[i.url]=2})))}function h(a,b){function c(a,c){if(a){if(e(a))c||(j=function(){var a=[].slice.call(arguments);k.apply(this,a),l()}),g(a,j,b,0,h);else if(Object(a)===a)for(n in m=function(){var b=0,c;for(c in a)a.hasOwnProperty(c)&&b++;return b}(),a)a.hasOwnProperty(n)&&(!c&&!--m&&(d(j)?j=function(){var a=[].slice.call(arguments);k.apply(this,a),l()}:j[n]=function(a){return function(){var b=[].slice.call(arguments);a&&a.apply(this,b),l()}}(k[n])),g(a[n],j,b,n,h))}else!c&&l()}var h=!!a.test,i=a.load||a.both,j=a.callback||f,k=j,l=a.complete||f,m,n;c(h?a.yep:a.nope,!!i),i&&c(i)}var i,j,l=this.yepnope.loader;if(e(a))g(a,0,l,0);else if(w(a))for(i=0;i (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0];var j=d.createElement(s);var dl=l!='dataLayer'?'&l='+l:'';j.src='//www.googletagmanager.com/gtm.js?id='+i+dl;j.type='text/javascript';j.async=true;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-M677548'); Skip to main content Home About Submit ALERTS / RSS Search for this keyword Advanced Search New Results Breeding for durable resistance in crops: defeated loci may act as Trojan horses compromising the effectiveness of major resistance genes View ORCID Profile Tyrone Possamai , View ORCID Profile Sabine Wiedemann-Merdinoglu , Marie-Céline Lacombe , Marie-Annick Dorne , View ORCID Profile Erik Griem , View ORCID Profile René Fuchs , View ORCID Profile Jochen Bogs , View ORCID Profile Raymonde Baltenweck , View ORCID Profile Komlan Avia , View ORCID Profile Didier Merdinoglu , View ORCID Profile Philippe Hugueney doi: https://doi.org/10.1101/2025.04.25.650562 Tyrone Possamai 1 INRAE, Université de Strasbourg, UMR SVQV , Colmar, France Find this author on Google Scholar Find this author on PubMed Search for this author on this site ORCID record for Tyrone Possamai For correspondence: tyrone.possamai{at}inrae.fr Sabine Wiedemann-Merdinoglu 1 INRAE, Université de Strasbourg, UMR SVQV , Colmar, France Find this author on Google Scholar Find this author on PubMed Search for this author on this site ORCID record for Sabine Wiedemann-Merdinoglu Marie-Céline Lacombe 1 INRAE, Université de Strasbourg, UMR SVQV , Colmar, France Find this author on Google Scholar Find this author on PubMed Search for this author on this site Marie-Annick Dorne 1 INRAE, Université de Strasbourg, UMR SVQV , Colmar, France Find this author on Google Scholar Find this author on PubMed Search for this author on this site Erik Griem 2 State Education and Research Center of Viticulture, Horticulture and Rural Development , Neustadt an der Weinstraße, Germany 3 Heidelberg Institute of Plant Sciences, University of Heidelberg , Heidelberg, Germany Find this author on Google Scholar Find this author on PubMed Search for this author on this site ORCID record for Erik Griem René Fuchs 4 Department of Biology, State Institute of Viticulture and Enology , Freiburg, Germany Find this author on Google Scholar Find this author on PubMed Search for this author on this site ORCID record for René Fuchs Jochen Bogs 2 State Education and Research Center of Viticulture, Horticulture and Rural Development , Neustadt an der Weinstraße, Germany 5 Technische Hochschule Bingen , Bingen am Rhein, Germany Find this author on Google Scholar Find this author on PubMed Search for this author on this site ORCID record for Jochen Bogs Raymonde Baltenweck 1 INRAE, Université de Strasbourg, UMR SVQV , Colmar, France Find this author on Google Scholar Find this author on PubMed Search for this author on this site ORCID record for Raymonde Baltenweck Komlan Avia 1 INRAE, Université de Strasbourg, UMR SVQV , Colmar, France Find this author on Google Scholar Find this author on PubMed Search for this author on this site ORCID record for Komlan Avia Didier Merdinoglu 1 INRAE, Université de Strasbourg, UMR SVQV , Colmar, France Find this author on Google Scholar Find this author on PubMed Search for this author on this site ORCID record for Didier Merdinoglu Philippe Hugueney 1 INRAE, Université de Strasbourg, UMR SVQV , Colmar, France Find this author on Google Scholar Find this author on PubMed Search for this author on this site ORCID record for Philippe Hugueney Abstract Full Text Info/History Metrics Supplementary material Preview PDF Abstract Resistance breeding offers invaluable perspectives for environment-friendly crop protection, but its success may be limited by the breakdown of plant resistance by pathogen strains. This threat is particularly acute for perennial crops, which may be cultivated for several decades. With the increasing use of new varieties carrying multiple major resistance loci, grapevine ( Vitis spp.) represents a distinctive model to investigate the broad agreement that combining several resistance genes (pyramiding) enhances both resistance efficacy and durability. To this end, grapevine progenies segregating for four resistance loci against Plasmopara viticola ( Rpvs ) were used to evaluate the efficiency of single and pyramided major loci when confronted to naive and Rpv -breaking pathogen strains. In the context of polygenic resistance, both undefeated and defeated Rpvs provided significant quantitative effects. However, interactions between pyramided Rpvs were either beneficial, neutral or detrimental to the level of resistance, depending on the loci combination and pathogen strain. In particular, the fact that the presence of defeated resistance loci may compromise the resistance provided by functional major loci has important implications for crops resistance breeding. Thorough phenotypic investigations of pyramiding breeding schemes emerge as a critical step for the effective and durable management of genetic resistances and plant diseases. Introduction Every year, up to 40 percent of world’s agricultural production is lost due to plant pests and diseases [ 1 ]. Crop protection is therefore essential for the food security chain, but it largely relies on the recurrent use of agrochemicals, which have adverse human health, environmental and socio-economic impacts [ 2 ]. Resistance breeding has been widely used to improve pathogen control while limiting the use of pesticides. However, the breakdown of plant genetic resistance by pathogen strains has become a significant concern for the deployment of plant disease-resistant varieties. The efficient use of genetic resources and resistance durability are particularly important for perennials such as apple ( Malus spp.) [ 3 ], poplar ( Populus spp.) [ 4 ] and grapevine ( Vitis spp.), which are planted for several decades. Indeed, grapevine has benefited from a worldwide breeding effort to control major diseases such as downy mildew caused by the Oomycete Plasmopara viticola [ 5 ]. Resistant grapevine varieties have been developed and planted for over 50 years, and, in many countries, cultivated surfaces are currently expanding to reduce the environmental impact of viticulture [ 5 ]. This wide array of resistant cultivars, which may harbour multiple pyramided resistance loci, provides a unique model to analyse major resistance genes deployment in crops. Over the past two decades, more than 30 resistance loci to P. viticola ( Rpv ) have been identified in Vitis spp. [ 6 ] ( www.vivc.de ). For resistance breeding purposes, some major resistance loci have been successfully introgressed in new cultivars and represent very commonly used genetic resources [ 5 , 7 ]. Nevertheless, the high evolutionary potential of P. viticola has already led to the development of virulent P. viticola strains ( avrRpv- ) that overcome one or more Rpvs [ 8 – 10 ]. The construction of polygenic-based resistance has been widely recognised as a strategy to enhance the efficacy and durability of plant resistance [ 11 ], and the pyramiding of different Rpvs in the same variety is a main objective in grape breeding programs [ 7 ]. However, the interactions between pyramided resistance loci are poorly documented, especially when some of these loci have been defeated. Here, we carried out a comprehensive investigation of the efficacy of grapevine major Rpvs when confronted with naive and Rpv -breaking P. viticola strains. Contrasted impacts of defeated major genes in the context of polygenic resistance defines new implications for resistance breeding in grapevine and other crops. Results An offspring of 165 individuals segregating for four resistance loci, Rpv1, Rpv3 . 1, Rpv10 and Rpv12 , was assessed in laboratory for the resistance to P. viticola , using the standard descriptor OIV452-1 ( Fig 1A ). The contribution of Rpvs to the resistance ( Fig 1B ) and the resistance levels of the 16 Rpv combinations ( Fig 1C ) were assessed with four different P. viticola strain with the following characteristics: one strain was naive, or avirulent, against all the Rpv loci [ 8 ]; one strain was virulent on Rpv3 . 1 , or Rpv3 . 1 -breaking ( avrRpv3 . 1- ) [ 8 ]; one strain was Rpv10 -breaking ( avrRpv10- ); and one was Rpv3 . 1/Rpv12 -breaking ( avr3 . 1-/12- ) [ 9 ]. Download figure Open in new tab Fig 1. Phenotyping results for the evaluation of the Rpv -mediated resistance to P. viticola . (A) Grapevine leaf discs illustrating the range of downy mildew symptoms and the associated scoring according to the OIV452-1 descriptor. (B) Table showing significant contribution of grapevine resistance loci to P. viticola ( Rpv ) to the resistance based on ANOVA results (p-values: < 0.05 = *, < 0.01 = ** and < 0.001 = ***) performed with the OIV452-1 scores and the optimized linear mixed model (LMM) for the four P. viticola strains, naive and virulent ( avr- ) with respect the Rpvs tested (see details in Table A in S1 File). (C) Graph showing the distribution of the data (box plots; Table D in S1 File) and the estimate mean with the standard error (black dots and error bars; Table E in S1 File) of the OIV452-1 scores (x-axis) for the studied Rpv combinations (y-axis) inoculated with the four P. viticola strains (colors). The ANOVA analysis and plots includes all scores from four bioassays and 165 progenies tested (6-12 genotypes/ Rpv combination) for a total of 36-51 discs/ Rpv combination/strain (3 discs/strain/genotype/bioassay). Non-resistant ( Rpv- ) plants exhibited a susceptible phenotype with the naive strain ( Fig 1C ), associated with a dense pathogen sporulation (OIV452-1 scores in the range of 1-3; Fig 1A ). Partial resistances with a less intense sporulation were observed for single Rpv1, Rpv3 . 1 and Rpv10 loci (scores between 4 and 7; Fig 1A ), and loci-mediated resistance was typically enhanced in pyramided combinations (Table B in S1 File), although the 6 to 12 genotypes representing each Rpv combination may exhibit a certain degree of resistance variability ( Fig 1C ). The Rpv12 locus, whether used individually or in pyramiding, exhibited the highest and most consistent resistance ( Fig 1C ), resulting in minimal sporulation of P. viticola (scores around 8 and 9; Fig 1A ). The three Rpv -breaking strains induced susceptible phenotypes in both Rpv- plants and those carrying the corresponding defeated Rpv genes, in the absence of further pyramiding ( Fig 1C ). The linear mixed models (LMMs) and ANOVA confirmed that the Rpvs significantly contributed to the offspring resistance when they were not overcome ( Fig 1B ; see details in Table A in S1 File). However, pyramided Rpvs combining both effective and defeated genes produced contrasting interactions when challenged with the Rpv -breaking strains. Indeed, pairwise comparisons of the Rpv combinations showed significant residual resistance benefits of Rpv10 against the avrRpv10- strain and of Rpv12 against the avrRpv3 . 1-/12- strain ( Fig 2 ; Table C in S1 File), observed in one and two pyramided combinations, respectively. Unexpectedly, Rpv10 also amplified the susceptibility to the Rpv10 -breaking strain when combined solely with Rpv1 . Similarly, Rpv3 . 1 induced detrimental interactions toward the avrRpv3 . 1-/12- strain in two Rpv combinations, undermining the residual effect observed for Rpv12 ( Fig 2 ; Table C in S1 File). Nevertheless, the Rpv3 . 1 locus did not compromise pyramided resistance against the avrRpv3 . 1- strain (Table C in S1 File). Altogether, our results highlight unpredictable interactions between defeated and undefeated resistance loci in pyramided combinations. Download figure Open in new tab Fig 2. Significant pairwise comparisons between Rpv combinations involving defeated loci. Pairwise comparisons of selected Rpv combinations displayed in Fig 1C showing significant benefits (green) or downsides (red) of defeated Rpvs (coloured) in pyramiding (Tukey’s tests for the OIV452-1 LMM-estimated means and standard errors; p-values with Benjamini-Hochberg correction: < 0.05 = *, < 0.01 = ** and < 0.001 = ***). See data and details in S1 File. Discussion Major loci Rpv1, Rpv3 . 1, Rpv10 and Rpv12 have been widely used in grapevine breeding programs [ 5 , 7 ]. The high levels and stability of the resistance to P. viticola obtained by combining three or four Rpv loci confirmed gene pyramiding as an effective strategy to broaden and enhance plant resistance [ 11 ], but infections with Rpv -breaking strains also produced unexpected outcomes. The presence of defeated major loci alone or among pyramided loci was most often described as beneficial or neutral for crop resistance [ 12 – 15 ]. However, our results show that in certain genetic combinations, a defeated locus can compromise the resistance provided by undefeated major loci. Although defeated loci have been associated to lower level of quantitative resistance [ 4 ], their unpredictable interactions with effective major resistance loci raise important questions about the management of genetic resistance for effective and durable control of fungal diseases. In the context of crop breeding, this suggests that defeated resistance may still be of interest as minor loci to improve and protect effective major loci. However, the potential benefits needs to be confirmed with multiple pathogen strains [ 4 ] and through long-term field trials [ 3 , 16 ]. On the other hand, the adverse effects of defeated loci could exacerbate plant susceptibility, thereby compromising the performance and the durability of undefeated major loci. Genetic resistances represent an invaluable natural capital, and it is therefore essential to ensure their sustainable use, even more considering the unpredictable consequences of resistance breakdown. Hence, an integrated approach that combines plant resistance diversity, agronomic practices and agrochemicals remains crucial for optimal pathogen control [ 17 ]. For instance, the judicious use of agrochemicals can protect resistant varieties from the emergence of resistance-breaking pathogen strains [ 18 , 19 ], especially in perennials, where pyramiding remains the most viable strategy for the deployment of resistance diversity [ 17 , 18 , 20 ]. In the context of crop protection, our findings underline that interactions between resistance loci are inherently unpredictable, highlighting the need for comprehensive phenotypic investigations of pyramiding breeding schemes to ensure durable management of genetic resistances and plant diseases. Materials and Methods The biparental grapevine offspring was generated and screened using molecular markers as described in Blasi et al. [ 21 ] at INRAE -UMR 1131 SVQV (Colmar, France) in 2023 and 2024. The choice of the parental plants among two advanced breeding lines and the population full sib structure allowed to limit the effect of the genetic background on Rpv -mediated resistance. The plants were grown as own rotted plants in 2 l pots in greenhouse, receiving optimal growth conditions (light, temperature and fertilization), regular pruning and the application of sprays for the control of Erysiphe necator , the causal agent of grape powdery mildew. The phenotyping of progenies resistance to P. viticola took place under laboratory conditions as described in Wiedemann-Merdinoglu et al. (2022). For the bioassays, the fourth, fifth and sixth leaves from the apex of actively growing shoots were collected and used to produce 2 cm leaf discs. Four P. viticola strains were tested with parallel spray inoculations (50,000 sporangia/ml). Leaf discs were visually scored at 6 days-post inoculation (dpi) for the OIV452-1 descriptor [ 23 ] as described in Macia et al. [ 24 ] but using a nine-classes rating scale (1 = discs completely covered by a dense sporulation – very susceptible to 9 = absence of sporulation – totally resistant). P. viticola strains were considered as virulent and the Rpv as defeated when the single Rpv -strain interaction produced susceptible-like phenotypes as described in Paineau et al. [ 10 ]. Four phenotyping bioassays were carried out (two in 2023 and two in 2024) testing 3 discs/strain/genotype/bioassay (most of the genotypes were tested twice) for a final amount of 36-51 discs/ Rpv combination/strain and 699 discs/strain (Table D in S1 File). A randomisation scheme for the genotypes discs was replicated for each strain and experiment. Two sets of common genotypes (one in 2023 and one in 2024) were used to verify the replicability of the bioassays by t-tests. A linear mixed effect models for each P. viticola strain was fitted (‘lmer’ function) and optimised (‘step’ function) by using the ‘lme4’ package [ 25 ] in R software [ 26 ]. The initial models included the OIV452-1 observations as dependent variable, the Rpv1, Rpv3 . 1, Rpv10, Rpv12 and the Year as fixed factors with completes cross-interactions, and the experiment-genotype variability as a random factor for the intercept value (Table A in S1 File). Homoscedasticity and normality of the residuals were visually checked in the final models, while ANOVA was used to test the significance of the retained factors and interactions. Estimated marginal means and standard errors of the Rpv combinations (Table E in S1 File) were calculated from the optimised models by using the ‘emmeans’ package [ 27 ] and used to compare the Rpv combinations with Tukey’s tests averaging the data at the year level (p-value with the Benjamini-Hochberg correction; Table B and C in S1 File). All data of the study are included in the article and its supporting information. Funding This work was supported by the FUNDUR project (ANR-22-CE92-0005; DFG project n° 504993256). Author Contributions PH, JB and DM write the research project and acquired the financial support; PH and SW supervised the research work; TP, SW, MCL, MAD and EG performed the phenotyping bioassays; KA conceived the generation of the offspring; RF isolated the P. viticola strains virulent on Rpv10 ( avrRpv10- ); TP produced the statistical analysis and the visualizations; TP, SW, RB, RF, JB, KA, DM and PH were involved in data and results interpretation; TP and PH drafted the manuscript with input from all authors. The final version of the manuscript has been reviewed, edited and approved by all authors. Declaration of interests The authors declare no competing interests. Acknowledgments We thank Christine Onimus (INRAE UMR1131 SVQV, Colmar, France) for generating the grapevine population; the staff of Unité Expérimentale Agronomique et Viticole (INRAE UE0871, Colmar, France) for maintenance of plant material; and the VEGOIA phenotyping platform (INRAE-Centre Grand Est, Colmar, France), part of the Strasbourg’s University network ‘Cortecs’ ( https://cortecs.unistra.fr ). Funder Information Declared Agence Nationale de la RechercheAgence Nationale de la Recherche, https://ror.org/00rbzpz17 , ANR-22-CE92-0005 Deutsche ForschungsgemeinschaftDeutsche Forschungsgemeinschaft, , 504993256 References 1. ↵ FAO’s Plant Production and Protection Division . FAO ; 2022 . doi: 10.4060/cc2447en OpenUrl CrossRef 2. ↵ European Parliament. Directorate General for Parliamentary Research Services. The future of crop protection in Europe . LU: Publications Office ; 2021 . 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Share Breeding for durable resistance in crops: defeated loci may act as Trojan horses compromising the effectiveness of major resistance genes Tyrone Possamai , Sabine Wiedemann-Merdinoglu , Marie-Céline Lacombe , Marie-Annick Dorne , Erik Griem , René Fuchs , Jochen Bogs , Raymonde Baltenweck , Komlan Avia , Didier Merdinoglu , Philippe Hugueney bioRxiv 2025.04.25.650562; doi: https://doi.org/10.1101/2025.04.25.650562 Share This Article: Copy Citation Tools Breeding for durable resistance in crops: defeated loci may act as Trojan horses compromising the effectiveness of major resistance genes Tyrone Possamai , Sabine Wiedemann-Merdinoglu , Marie-Céline Lacombe , Marie-Annick Dorne , Erik Griem , René Fuchs , Jochen Bogs , Raymonde Baltenweck , Komlan Avia , Didier Merdinoglu , Philippe Hugueney bioRxiv 2025.04.25.650562; doi: https://doi.org/10.1101/2025.04.25.650562 Citation Manager Formats BibTeX Bookends EasyBib EndNote (tagged) EndNote 8 (xml) Medlars Mendeley Papers RefWorks Tagged Ref Manager RIS Zotero Tweet Widget Facebook Like Google Plus One Subject Area Plant Biology Subject Areas All Articles Animal Behavior and Cognition (7636) Biochemistry (17704) Bioengineering (13898) Bioinformatics (41967) Biophysics (21460) Cancer Biology (18599) Cell Biology (25525) Clinical Trials (138) Developmental Biology (13384) Ecology (19909) Epidemiology (2067) Evolutionary Biology (24326) Genetics (15613) Genomics (22512) Immunology (17740) Microbiology (40423) Molecular Biology (17191) Neuroscience (88645) Paleontology (667) Pathology (2835) Pharmacology and Toxicology (4825) Physiology (7646) Plant Biology (15158) Scientific Communication and Education (2046) Synthetic Biology (4302) Systems Biology (9825) Zoology (2271)