Potential Threat of Ceratocystis lukuohia on kiwifruit crop

Potential Threat of Ceratocystis lukuohia on kiwifruit crop | Research Square window.SnipcartSettings = { analytics: { enabled: false } }; (function() { var accessVector = localStorage.getItem('access_vector') || ''; window.dataLayer = window.dataLayer || []; if (accessVector) { window.dataLayer.push({ user: { profile: { profileInfo: { snid: accessVector } } } }); } })(); (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],j=d.createElement(s),dl=l!='dataLayer'?'&l='+l:'';j.async=true;j.src='https://www.googletagmanager.com/gtm.js?id='+i+dl;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-K279D39R'); Browse Preprints In Review Journals COVID-19 Preprints AJE Video Bytes Research Tools Research Promotion AJE Professional Editing AJE Rubriq About Preprint Platform In Review Editorial Policies Our Team Advisory Board Help Center Sign In Submit a Preprint Cite Share Download PDF Short Report Potential Threat of Ceratocystis lukuohia on kiwifruit crop Sabrina Angela Cassol, Lisa Keith, Chandan Pal, Acelino Alfenas, and 1 more This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-4164602/v1 This work is licensed under a CC BY 4.0 License Status: Published Journal Publication published 19 Nov, 2024 Read the published version in European Journal of Plant Pathology → Version 1 posted 6 You are reading this latest preprint version Abstract Ceratocystis wilt, caused by Ceratocystis fimbriata , is the most severe disease of the kiwifruit crop in Brazil and represents a threat to other kiwifruit-producing countries where the pathogen has not yet been reported infecting kiwifruit vines. Ceratocystis species have been reported in many countries, some are host specific, while others can infect a wide host range. Given the high impact of the disease on kiwifruit, evaluating whether Ceratocystis isolates from other hosts and countries can also infect kiwifruit is important for implementing biosecurity measures. In the present work, we evaluated if C. lukuohia and C. huliohia , isolated from ohia ( Metrosideros polymorpha ) in Hawaii are pathogenic to kiwifruit cultivars. Inoculations of both species in rooted cuttings of Monty and Gold3 cultivars showed that C. lukuohia can cause wilt in both kiwifruit cultivars evaluated, with high plant mortality. This is the first report that C. lukuohia can infect another host, demonstrating that it is not host-specific and extends its host range. In addition, considering that C. lukuohia is pathogenic and lethal in kiwifruit vines, kiwifruit-producing areas must implement biosecurity measures to prevent the introduction of this species. Actinidia chinensis Actinidia deliciosa Ceratocystis fimbriata Ceratocystis huliohia Ceratocystis wilt Rapid Ohia Death Figures Figure 1 Figure 2 Full Text Kiwifruit ( Actinidia spp.) is native to China but was domesticated and first successfully cultivated commercially in New Zealand (Saquet & Brackmann 1995, Ferguson 2004, Testolin et al. 2016). With the development of new varieties and increased demand for the fruit, the cultivation of kiwifruit became profitable and has spread throughout five continents of the world. With an annual production of approximately 4.5 million metric tons, China, New Zealand, and Italy stand as the largest kiwifruit-producing countries (FAOSTAT, 2022). This increase in world production leads to the emergence of diseases that can cause significant losses in the crop, such as Bacterial canker, caused by Pseudomonas syringae pv. actinidiae (Vannest, 2017) . Additionally, in 2010, Ceratocystis wilt, caused by Ceratocystis fimbriata Ellis & Halst., was reported in kiwifruit orchards in Rio Grande do Sul, state Brazil (Sonego et al. 2010), with symptoms of wilt, dark-brown lesions in the xylem, reduced fruit length, and death of infected vines (Piveta et al., 2016; Ferreira et al., 2017). With the rapid dissemination of the disease to other producing regions in the country and the extensive mortality caused, which can reach up to 30% (Piveta et al., 2016), Ceratocystis wilt emerged as the primary disease affecting kiwifruit cultivation in the country, leading to the abandonment or replacement of many kiwifruit orchards (Piveta et al., 2016). The Ceratocystis fimbriata sensu lato (s.l.) complex is formed by a group of species containing high levels of genetic variation and widely distributed geographically. The intraspecific and interspecific variability in the Ceratocystis species is related to host speciation, aggressiveness variation, and specific interactions with certain cultivars or clones (Cowger et al., 2000; Oliveira et al., 2020). Some species and/or isolates are related to single hosts or geographic regions, while others infect a wide range of hosts (Thorpe et al., 2005; Tyson et al., 2020). Since the first report of Ceratocystis wilt on kiwifruit vines (Sonego et al., 2010), investigation of pathogenicity of Ceratocystis spp. found in other countries, mainly those occurring in kiwifruit-producing countries, has become important for implementing biosecurity measures to prevent the introduction of pathogenic isolates in kiwifruit orchards. Tyson et al. (2020) showed that New Zealand isolates of C. fimbriata from sweet potato (kumara) are not pathogenic to a range of kiwifruit cultivars (Hayward, Gold3, Gold14, Bounty). In addition, the sweet potato isolates were non-pathogenic on mango ( Mangifera indica ), yam ( Dioscoera spp.), cacao ( Theobroma cacao ) and sycamore ( Platanus spp.), which demonstrates a notable host specialization of C. fimbriata isolates from sweet potato (Steimel et al., 2004; Engelbrecht and Harrington, 2005). However, there are numerous species of Ceratocystis spread throughout the world (CAB International, 2023), and if these are pathogenic to kiwifruit, as well as the C. fimbriata isolates present in Brazil, they could pose a potential threat to kiwifruit cultivation in other regions of the world. In 2015, Keith et al. described Ceratocystis wilt causing widespread mortality on ohia ( Metrosideros polymorpha ), the most ecologically and culturally significant native tree in Hawaii, USA. The phenomenon was called rapid ohia death (ROD), and symptoms including wilting of tree canopies and dark-brown lesions in woody xylem were first observed in the Puna district of Hawaii Island (Keith et al., 2015; Hughes et al., 2020). The fungal pathogens causing ROD were described as two new Ceratocystis species, C. lukuohia and C. huliohia (Barnes et al., 2018) . C. lukuohia is the most aggressive, causing rapid wilt and widespread mortality, whereas C. huliohia is associated with less mortality, cankers, and is sometimes associated with wilt of individual limbs (Barnes et al., 2018; Fortini et al., 2019; Hughes et al., 2020). Microsatellite analyses showed two clonal lineages of these species, which were introduced into Hawaii (Barnes et al., 2018). Currently, Ceratocystis wilt caused by C . lukuohia occurs throughout Hawaii Island and Kauai and poses a serious threat to native Hawaiian forests. The Metrosideros forests in other continents and islands like New Zealand may also be in danger (Hughes et al., 2020; Luiz et al., 2021; 2022). Barnes et al. (2018) showed that C. lukuohia and C. huliohia are non-pathogenic to arrowhead vine ( Syngonium podophylum ) , taro ( Colocasia esculenta ), and london planetree ( Platanus × acerifolia ). However, given that certain Ceratocystis spp. can infect a wide range of hosts, and the frequent occurrence of Ceratocystis species introduction into new countries (CAB International, 2023), it is crucial to evaluate the pathogenicity of these two new Ceratocystis species in additional crops, particularly in high-value crops such as kiwifruit, considering the high impact of the disease in this host. Front of this, the present study aimed to evaluate if C. lukuohia and C. huliohia, isolated from infected M. polymorpha in Hawaii, can induce Ceratocystis wilt in kiwifruit cultivars. Firstly, the identity of the Ceratocystis species was confirmed by sequencing ITS and TEF-1 gene regions of DNA and subsequent comparison with other sequences of the respective species in GenBank (Oliveira et al., 2015). For the pathogenicity assay, the Ceratocystis isolates were grown on Potato Dextrose Agar (PDA) at 28 ◦ C with a 12 h photoperiod for twelve days. After incubation, PDA plugs containing the fungus were inoculated on rooted cuttings of ‘Monty’ ( Actinidia deliciosa ) from Brazil and ‘Gold3’ ( Actinidia chinensis var. chinensis 'Zesy002' ) from New Zealand following established protocols (Alfenas and Mafia, 2016). Kiwifruit vines inoculated with the C. fimbriata isolate from infected kiwifruit vines in Brazil and vines that received PDA-only plugs served as positive and negative controls, respectively. A completely randomized design with five replicate plants per treatment and controls was used. The inoculated kiwifruit vines were incubated in the greenhouse (28 ± 5 °C). Forty-five days post-inoculation, vines were evaluated and the number of wilted vines was recorded. Additionally, xylem lesion length (cm) in the inner stem tissue of infected vines was measured and used to evaluate the aggressiveness of the pathogenic isolates on the two kiwifruit cultivars, considering a disease severity of 100% for the wilted vines. Carrot baits prepared with stem samples of inoculated vines were used to confirm the infection was caused by Ceratocystis species, from re-isolation and molecular confirmation by sequencing ITS and TEF-1 gene regions of DNA. The experiment was repeated once in the time. The data analysis was performed considering isolate and cultivar as fixed effects while replicates were considered as random effects. Significance of individual and interaction effects was evaluated at a 5% probability level. All kiwifruit vines inoculated with C. lukuohia and C. fimbriata became infected (Fig. 1C, 2D), resulting in a 60% mortality rate of vines during the incubation period for both isolates. The Ceratocystis infection was confirmed by the presence of pathogen structures (perithecia and ascospores) in carrot baits (Fig. 1E, 1F), and from a subsequent comparison of ITS and TEF-1 gene regions of DNA with other sequences of the respective species in GenBank. None of the vines that were inoculated with C. huliohia (Fig. 1B) or PDA-only plugs showed disease symptoms (Fig. 1A), and no Ceratocystis structures were observed on carrot baits. Therefore, C . huliohia is non-pathogenic in either of the kiwifruit cultivars evaluated. Our data indicate that cultivar and experiment time did not significantly affect (p>0.05) lesion size and disease severity. Only isolate had a significant effect (p<0.05) on these variables. C. fimbriata caused significantly larger lesions and was more aggressive in kiwifruit than C. lukuohia (Fig. 2). However, it is important to consider that there is significant variation in aggressiveness among Ceratocystis isolates, and the C. fimbriata isolate used in the present study (LPF1443) has been identified as a highly aggressive in kiwifruit vines (Oliveira et al., 2020). Given the susceptibility of both kiwifruit cultivars to C. lukuohia , along with high plant mortality rates, there is a potential threat that this pathogen may pose not only to kiwifruit-producing areas in Hawaii but also to other countries with kiwifruit cultivation, such as New Zealand and Italy. Although C. lukuohia and C. huliohia are associated with ROD, only C. lukuohia is considered a systemic vascular wilt pathogen on M. polymorpha (Hughes et al., 2020). Similarly, we showed that of the two ROD pathogens, only C. lukuohia causes wilt on kiwifruit vines, with high aggressiveness and mortality. This corroborates other studies that suggest that C. lukuohia causes Ceratocystis wilt on M. polymorpha , and this species is the main cause of the high mortality caused by ROD, and that the distinct symptoms caused by C. huliohia seem to be less important (Keith et al., 2015; Hughes et al., 2020). This is the first report indicating that C. lukuohia is not host-specific, which suggests that it poses a threat to other agricultural and forestry crops growing in Hawaii and the Pacific Basin. Implementation of biosecurity measures, including rapid detection and eradication strategies of the pathogen are imperative to prevent local and long-distance spread. Furthermore, knowing that C. lukuohia can cause Ceratocystis wilt on kiwifruit vines, it is essential to avoid the introduction of this pathogen to kiwifruit-producing countries, especially where native Metrosideros spp. co-exist. Declarations ACKNOWLEDGMENTS The authors are grateful to Zespri Group Limited for the financial support of this work, to Clonar Resistência a Doenças Florestais for providing the greenhouse facilities for plant growth and inoculations, to Department of Agriculture, Livestock and Food Supply (MAPA) for the import and inoculation guidelines, and Carolina Pessanha Alonso for help with the experiments. FUNDING This work was supported by: ‘Conselho Nacional de Desenvolvimento Científico e Tecnológico’ (CNPq); ‘Coordenação de Aperfeiçoamento de Pessoal de Nível Superior’ (CAPES); and ‘Fundação de Amparo à Pesquisa do Estado de Minas Gerais’ (FAPEMIG). AUTHOR CONTRIBUTIONS STATEMENT Investigation and methodology were performed by Sabrina Angela Cassol. The data curation and formal analysis were performed by Sabrina Angela Cassol. The funding acquisition and supervision by Acelino Couto Alfenas, Chandan Pal, and Rafael Ferreira Alfenas. The original draft was written by Sabrina Angela Cassol and all authors reviewed and edited previous versions of the manuscript. All authors read and approved the final manuscript. DATA AVAILABILITY The data will be made available upon request from the corresponding author of the article. CONFLICT OF INTEREST Chandan Pal is employed by Zespri International Limited. All other authors have no competing interests. References Alfenas, A.C., Mafia, R.G. (2016). Métodos em Fitopatologia. 2ª Ed. Editora UFV, Viçosa, MG. 516p. Barnes, I., Fourie, A., Wingfield, M.J., Harrington, T.C., McNew, D.L., Sugiyama, L.S., Luiz, B.C., Heller, W.P., Keith, L.M. (2018). New Ceratocystis species associated with rapid death of Metrosideros polymorpha in Hawaii. Persoonia, 40, 154-181. 10.3767/persoonia.2018.40.07 CAB International. (2023). https://www.cabi.org/. Accessed 14 October 2023. Cowger, C., Hoffer, M.E., Mundt, C.C. (2000). Specific adaptation by Mycosphaerella graminicola to a resistant wheat cultivar. Plant Pathology, 49, 445–451. https://doi.org/10.1046/j.1365-3059.2000.00472.x Engelbrecht, C.J.B. and Harrington, T.C. (2005). Intersterility, morphology and taxonomy of Ceratocystis fimbriata on sweet potato, cacao and sycamore. Mycologia, 97, 57-69. 10.3852/mycologia.97.1.57 FAOSTAT. 2022. Food and Agriculture Organization of the United Nations. https://www.fao.org/faostat/en/#home. Accessed 5 March 2024. Ferreira, M.A., Harrington, T.C., Piveta, G., Alfenas, A.C. (2017). Genetic variability suggests that three populations of Ceratocystis fimbriata are responsible for the Ceratocystis wilt epidemic on kiwifruit in Brazil. Tropical Plant Pathology , 42, 86–95. https://doi.org/10.1007/s40858-017-0131-y Fortini, L.B., Kaiser, L.R., Keith, L.M., Price, J., Hughes, R.F., Jacobi, J.D., Friday, J.B. (2019). The evolving threat of Rapid ‘Ōhi‘a Death (ROD) to Hawai‘i’s native ecosystems and rare plant species. Forest Ecology and Management, 448, 376-385. https://doi.org/10.1016/j.foreco.2019.06.025 Harrington, T.C. (2013). Ceratocystis diseases. In: Infectious Forest Diseases , ed. by P. Gonthier and G. Nicolotti, pp. 230-255. CABI, Oxfordshire, United Kingdom. Harrington, T.C., Kazmi M., Al-Sadi, A., Ismail, I. (2014). Intraspecific and intragenomic variability of ITS rDNA sequences reveals taxonomic problems in Ceratocystis fimbriata sensu stricto. Mycologia , 106, 224–242. 10.3852/106.2.224 Hughes, M.A., Juzwik, J., Harrington, T.C., Keith, L.M. (2020). Pathogenicity, symptom development, and colonization of Metrosideros polymorpha by Ceratocystis lukuohia . Plant Disease, 104, 2233-2241. https://doi.org/10.1094/PDIS-09-19-1905-RE Keith, L.M., Hughes, R.F., Sugiyama, L.S., Heller, W.P., Bushe, B.C., Friday, J.B. (2015). First report of Ceratocystis wilt on Ohia ( Metrosideros polymorpha ). Plant Disease 99(9), 1276. https://doi.org/10.1094/PDIS-12-14-1293-PDN Luiz, B., McNeill, M. R., Bodley, E., Keith, L. M. (2022). Assessing susceptibility of Metrosideros excelsa (pōhutukawa) to the vascular wilt pathogen, Ceratocystis lukuohia , causing Rapid ‘Ōhi‘a death. Australasian Plant Pathology, 51, 327–331. 10.1007/s13313-022-00858-9 Luiz, B., Stacey, E. A., Keith, L. M. (2021). Screening of Metrosideros polymorpha (‘ōhi‘a) varieties for resistance to Ceratocystis lukuohia . Forest Pathology, 51, 1-9. https://doi.org/10.1111/efp.12656 Oliveira, L.S.S., Damacena, M.B., Guimarães, L.M.S., Siqueira, D.L., Alfenas, A.C. (2016). Ceratocystis fimbriata isolates on Mangifera indica have different levels of aggressiveness. European Journal of Plant Pathology, 145, 847–856. https://doi.org/10.1007/s10658-016-0873-2 Oliveira, L.S.S., Harrington, T.C., Ferreira, M.A., Damacena, M.B., Al-Sadi, A.M., Al Mahmooli, I.H.S., Alfenas, A.C. (2015). Species or genotypes? Reassessment of four recently described species of the Ceratocystis wilt pathogen, C. fimbriata , on Mangifera indica . Phytopathology, 105(9), 1229–1244. 10.1094/PHYTO-03-15-0065-R Oliveira, L.S.S., Pimenta, L.V.A., Guimarães, L.M.S. de Souza, P.V.D., Bhering, L.L., Alfenas, A.C. (2020). Resistance of kiwifruit cultivars to Ceratocystis wilt: an approach considering the genetic diversity and variation in aggressiveness of the pathogen. Plant Pathology, 70, 349-357. https://doi.org/10.1111/ppa.13305 Piveta, G., Ferreira, M.A., Muniz, M.F.B., Valdetaro, D., Valdebenito-Sanhueza, R., Harrington, T.C., Alfenas, A.C. (2016). Ceratocystis fimbriata on kiwifruit ( Actinidia spp.) in Brazil. New Zealand Journal of Crop and Horticultural Science, 44, 31-24. https://doi.org/10.1080/01140671.2016.1143020 Sonego, O.R., Ferreira, M.A., Sanhueza, R.M., Gava, R., Garrido, L.R., Alfenas, A.C. (2010). Primeiro relato da murcha-de-ceratocystis em kiwifruit. Tropical Plant Pathology, 35, S233. Steimel, J., Engelbrecht, C.J.B., Harrington, T.C. (2004). Development and characterization of microsatellite markers for the fungus Ceratocystis fimbriata . Molecular Ecology Resources, 4, 215–218. https://doi.org/10.1111/j.1471-8286.2004.00621.x Vanneste, J.L. (2017). The scientific, economic, and social impacts of the New Zealand outbreak of bacterial canker of kiwifruit ( Pseudomonas syringae pv. actinidiae ). Annu. Rev. Phytopathol. 55 , 377–399. https://doi.org/10.1146/annurev-phyto-080516-035530 Thorpe, D.J., Harrinton, T.C., Uchida, J.Y. (2005). Pathogenicity, internal transcribed spacer-rDNA variation, and human dispersal of Ceratocystis fimbriata on the Family Araceae. Phytopathology, 95, 316-323. 10.1094/PHYTO-95-0316 Tyson, J.L., Manning, M.A., Wright, P.J. (2020). Pathogenicity of Ceratocystis fimbriata from New Zealand kūmara on kiwifruit cultivars. New Zealand Plant Protection, 73, 6-12. https://doi.org/10.30843/nzpp.2020.73.11717 Cite Share Download PDF Status: Published Journal Publication published 19 Nov, 2024 Read the published version in European Journal of Plant Pathology → Version 1 posted Editorial decision: Major revisions 29 Apr, 2024 Reviewers agreed at journal 02 Apr, 2024 Reviewers invited by journal 28 Mar, 2024 Editor invited by journal 28 Mar, 2024 Editor assigned by journal 26 Mar, 2024 First submitted to journal 25 Mar, 2024 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. As a division of Research Square Company, we’re committed to making research communication faster, fairer, and more useful. We do this by developing innovative software and high quality services for the global research community. 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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-4164602","acceptedTermsAndConditions":true,"allowDirectSubmit":false,"archivedVersions":[],"articleType":"Short Report","associatedPublications":[],"authors":[{"id":285161010,"identity":"bace1087-b35c-45fb-a9b3-5e86a4a61d0d","order_by":0,"name":"Sabrina Angela Cassol","email":"","orcid":"","institution":"Universidade Federal de Vicosa Departamento de Fitopatologia","correspondingAuthor":false,"prefix":"","firstName":"Sabrina","middleName":"Angela","lastName":"Cassol","suffix":""},{"id":285161011,"identity":"fa7c3343-67a2-4bc8-bb1c-bc99df3d296b","order_by":1,"name":"Lisa Keith","email":"","orcid":"","institution":"USDA ARS: USDA 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\u003cstrong\u003eD\u003c/strong\u003e Inoculated with \u003cem\u003eC. fimbriata\u003c/em\u003e from kiwifruit vine. \u003cstrong\u003eE\u003c/strong\u003eCarrot baits prepared with stem samples of kiwifruit vines inoculated with \u003cem\u003eC. \u003c/em\u003elukuohia\u003cem\u003e \u003c/em\u003e\u003cstrong\u003eF –\u003c/strong\u003e \u003cem\u003eC. lukuohia\u003c/em\u003estructures detected in carrot baits.\u003c/p\u003e","description":"","filename":"1.png","url":"https://assets-eu.researchsquare.com/files/rs-4164602/v1/ebd0480cd39ee198f0bf35be.png"},{"id":53949242,"identity":"bb1f9d45-f700-4304-93be-a35c56147064","added_by":"auto","created_at":"2024-04-02 15:25:25","extension":"png","order_by":2,"title":"Figure 2","display":"","copyAsset":false,"role":"figure","size":60583,"visible":true,"origin":"","legend":"\u003cp\u003eLesion size and disease severity of kiwifruit vines inoculated with \u003cem\u003eCeratocystis fimbriata\u003c/em\u003e and \u003cem\u003eC. lukuohia\u003c/em\u003e, after 45 days of incubation. \u003cstrong\u003eA \u003c/strong\u003eAverage lesion size (cm) and \u003cstrong\u003eB\u003c/strong\u003e Average disease severity (%)\u003c/p\u003e","description":"","filename":"2.png","url":"https://assets-eu.researchsquare.com/files/rs-4164602/v1/2af442fdf50588e9eea7c013.png"},{"id":69834791,"identity":"860699eb-0c81-45b9-bff4-6db46a3f03d1","added_by":"auto","created_at":"2024-11-25 16:08:51","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":1207194,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-4164602/v1/d79c7b7c-6165-47b6-84c3-338b18d3afb8.pdf"}],"financialInterests":"","formattedTitle":"Potential Threat of Ceratocystis lukuohia on kiwifruit crop","fulltext":[{"header":"Full Text","content":"\u003cp\u003eKiwifruit (\u003cem\u003eActinidia\u003c/em\u003e spp.) is native to China but was domesticated and first successfully cultivated commercially in New Zealand (Saquet \u0026amp; Brackmann 1995, Ferguson 2004, Testolin et al. 2016). With the development of new varieties and increased demand for the fruit, the cultivation of kiwifruit became profitable and has spread throughout five continents of the world. With an annual production of approximately 4.5 million metric tons, China, New Zealand, and Italy stand as the largest kiwifruit-producing countries (FAOSTAT, 2022).\u0026nbsp;\u003c/p\u003e\n\u003cp\u003eThis increase in world production leads to the emergence of diseases that can cause significant losses in the crop, such as Bacterial canker, caused by \u003cem\u003ePseudomonas syringae\u003c/em\u003e pv. \u003cem\u003eactinidiae\u0026nbsp;\u003c/em\u003e(Vannest, 2017)\u003cem\u003e.\u003c/em\u003e Additionally, in 2010, Ceratocystis wilt, caused by \u003cem\u003eCeratocystis fimbriata\u0026nbsp;\u003c/em\u003eEllis \u0026amp; Halst., was reported in kiwifruit orchards in Rio Grande do Sul, state Brazil (Sonego et al. 2010), with symptoms of wilt, dark-brown lesions in the xylem, reduced fruit length, and death of infected vines (Piveta et al., 2016; Ferreira et al., 2017). With the rapid dissemination of the disease to other producing regions in the country and the extensive mortality caused, which can reach up to 30% (Piveta et al., 2016), Ceratocystis wilt emerged as the primary disease affecting kiwifruit cultivation in the country, leading to the abandonment or replacement of many kiwifruit orchards (Piveta et al., 2016).\u003c/p\u003e\n\u003cp\u003eThe \u003cem\u003eCeratocystis fimbriata\u003c/em\u003e sensu lato (s.l.) complex is formed by a group of species containing high levels of genetic variation and widely distributed geographically. The intraspecific and interspecific variability in the \u003cem\u003eCeratocystis\u0026nbsp;\u003c/em\u003especies is related to host speciation, aggressiveness variation, and specific interactions with certain cultivars or clones (Cowger et al., 2000; Oliveira et al., 2020).\u0026nbsp;Some species and/or isolates are related to single hosts or geographic regions, while others infect a wide range of hosts (Thorpe et al., 2005; Tyson et al., 2020). Since the first report of Ceratocystis wilt on kiwifruit vines (Sonego et al., 2010), investigation of pathogenicity of \u003cem\u003eCeratocystis\u003c/em\u003e spp. found in other countries, mainly those occurring in kiwifruit-producing countries, has become important for implementing biosecurity measures to prevent the introduction of pathogenic isolates in kiwifruit orchards. Tyson et al. (2020) showed that New Zealand isolates of \u003cem\u003eC. fimbriata\u003c/em\u003e from sweet potato (kumara) are not pathogenic to a range of kiwifruit cultivars (Hayward, Gold3, Gold14, Bounty). In addition, the sweet potato isolates were non-pathogenic on mango (\u003cem\u003eMangifera indica\u003c/em\u003e), yam (\u003cem\u003eDioscoera\u003c/em\u003e spp.), cacao (\u003cem\u003eTheobroma cacao\u003c/em\u003e) and sycamore (\u003cem\u003ePlatanus\u003c/em\u003e spp.), which demonstrates a notable host specialization of\u0026nbsp;\u003cem\u003eC. fimbriata\u003c/em\u003e isolates from sweet potato (Steimel et al., 2004; Engelbrecht and Harrington, 2005).\u0026nbsp;However, there are numerous species of \u003cem\u003eCeratocystis\u0026nbsp;\u003c/em\u003espread throughout the world (CAB International, 2023), and if these are pathogenic to kiwifruit, as well as the \u003cem\u003eC. fimbriata\u003c/em\u003e isolates present in Brazil, they could pose a potential threat to kiwifruit cultivation in other regions of the world.\u003c/p\u003e\n\u003cp\u003eIn 2015, Keith et al. described Ceratocystis wilt causing widespread mortality on ohia (\u003cem\u003eMetrosideros polymorpha\u003c/em\u003e), the most ecologically and culturally significant native tree in Hawaii, USA. The phenomenon was called rapid ohia death (ROD), and symptoms including wilting of tree canopies and\u0026nbsp;dark-brown lesions in woody xylem were first observed in the Puna district of Hawaii Island (Keith et al., 2015; Hughes et al., 2020). The fungal pathogens causing ROD were described as two new \u003cem\u003eCeratocystis\u003c/em\u003e species, \u003cem\u003eC. lukuohia\u003c/em\u003e and \u003cem\u003eC. huliohia\u003c/em\u003e (Barnes et al., 2018)\u003cem\u003e. C. lukuohia\u003c/em\u003e is the most aggressive, causing rapid wilt and widespread mortality, whereas \u003cem\u003eC. huliohia\u0026nbsp;\u003c/em\u003eis associated with less mortality, cankers, and is sometimes associated with wilt of individual limbs (Barnes et al., 2018; Fortini et al., 2019; Hughes et al., 2020). Microsatellite analyses showed two clonal lineages of these species, which were introduced into Hawaii (Barnes et al., 2018). Currently, Ceratocystis wilt caused by \u003cem\u003eC\u003c/em\u003e. \u003cem\u003elukuohia\u003c/em\u003e occurs throughout Hawaii Island and Kauai and poses a serious threat to native Hawaiian forests. The \u003cem\u003eMetrosideros\u003c/em\u003e forests in other continents and islands like New Zealand may also be in danger (Hughes et al., 2020; Luiz et al., 2021; 2022). Barnes et al. (2018) showed that \u003cem\u003eC. lukuohia\u003c/em\u003e and \u003cem\u003eC. huliohia\u003c/em\u003e are non-pathogenic to arrowhead vine (\u003cem\u003eSyngonium podophylum\u003c/em\u003e)\u003cem\u003e,\u0026nbsp;\u003c/em\u003etaro\u003cem\u003e\u0026nbsp;\u003c/em\u003e(\u003cem\u003eColocasia esculenta\u003c/em\u003e),\u0026nbsp;and london planetree (\u003cem\u003ePlatanus \u0026times; acerifolia\u003c/em\u003e).\u0026nbsp;However, given that certain \u003cem\u003eCeratocystis\u003c/em\u003e spp. can infect a wide range of hosts, and the frequent occurrence of \u003cem\u003eCeratocystis\u003c/em\u003e species introduction into new countries (CAB International, 2023), it is crucial to evaluate the pathogenicity of these two new \u003cem\u003eCeratocystis\u003c/em\u003e species in additional crops, particularly in high-value crops such as kiwifruit, considering the high impact of the disease in this host.\u0026nbsp;\u003c/p\u003e\n\u003cp\u003eFront of this, the present study aimed to evaluate if \u003cem\u003eC. lukuohia\u003c/em\u003e and \u003cem\u003eC. huliohia,\u003c/em\u003e isolated from infected \u003cem\u003eM. polymorpha\u003c/em\u003e in Hawaii, can induce Ceratocystis wilt in kiwifruit cultivars. Firstly, the identity of the \u003cem\u003eCeratocystis\u003c/em\u003e species was confirmed by sequencing ITS and TEF-1 gene regions of DNA and subsequent comparison with other sequences of the respective species in GenBank (Oliveira et al., 2015). For the pathogenicity assay, the \u003cem\u003eCeratocystis\u003c/em\u003e isolates were grown on Potato Dextrose Agar (PDA) at 28\u003csup\u003e◦\u003c/sup\u003eC with a 12 h photoperiod for twelve days. After incubation, PDA plugs containing the fungus were inoculated on rooted cuttings of \u0026lsquo;Monty\u0026rsquo; (\u003cem\u003eActinidia deliciosa\u003c/em\u003e) from Brazil and \u0026lsquo;Gold3\u0026rsquo; (\u003cem\u003eActinidia chinensis var. chinensis \u0026apos;Zesy002\u0026apos;\u003c/em\u003e) from New Zealand following established protocols (Alfenas and Mafia, 2016). Kiwifruit vines inoculated with the \u003cem\u003eC. fimbriata\u0026nbsp;\u003c/em\u003eisolate from infected kiwifruit vines in Brazil and vines that received PDA-only plugs served as positive and negative controls, respectively. A completely randomized design with five replicate plants per treatment and controls was used. The inoculated kiwifruit vines were incubated in the greenhouse (28 \u0026plusmn; 5 \u0026deg;C). Forty-five days post-inoculation, vines were evaluated and the number of wilted vines was recorded. Additionally, xylem lesion length (cm) in the inner stem tissue of infected vines was measured and used to evaluate the aggressiveness of the pathogenic isolates on the two kiwifruit cultivars, considering a disease severity of 100% for the wilted vines. Carrot baits prepared with stem samples of inoculated vines were used to confirm the infection was caused by \u003cem\u003eCeratocystis\u0026nbsp;\u003c/em\u003especies, from re-isolation and molecular confirmation by sequencing ITS and TEF-1 gene regions of DNA. The experiment was repeated once in the time. The data analysis was performed considering isolate and cultivar as fixed effects while replicates were considered as random effects. Significance of individual and interaction effects was evaluated at a 5% probability level.\u0026nbsp;\u003c/p\u003e\n\u003cp\u003eAll kiwifruit vines inoculated with \u003cem\u003eC. lukuohia\u0026nbsp;\u003c/em\u003eand \u003cem\u003eC. fimbriata\u0026nbsp;\u003c/em\u003ebecame infected (Fig. 1C, 2D), resulting in a 60% mortality rate of vines during the incubation period for both isolates. The \u003cem\u003eCeratocystis\u003c/em\u003e infection was confirmed by the presence of pathogen structures (perithecia and ascospores) in carrot baits (Fig. 1E, 1F), and from a subsequent comparison of ITS and TEF-1 gene regions of DNA with other sequences of the respective species in GenBank. None of the vines that were inoculated with \u003cem\u003eC. huliohia\u003c/em\u003e (Fig. 1B) or PDA-only plugs showed disease symptoms (Fig. 1A), and no \u003cem\u003eCeratocystis\u003c/em\u003e structures were observed on carrot baits. Therefore, \u003cem\u003eC\u003c/em\u003e. \u003cem\u003ehuliohia\u003c/em\u003e is non-pathogenic in either of the kiwifruit cultivars evaluated.\u0026nbsp;\u003c/p\u003e\n\u003cp\u003eOur data indicate that cultivar and experiment time did not significantly affect (p\u0026gt;0.05) lesion size and disease severity. Only isolate had a significant effect (p\u0026lt;0.05) on these variables. \u003cem\u003eC. fimbriata\u003c/em\u003e caused significantly larger lesions and was more aggressive in kiwifruit than \u003cem\u003eC. lukuohia\u003c/em\u003e (Fig. 2). However, it is important to consider that there is significant variation in aggressiveness among \u003cem\u003eCeratocystis\u003c/em\u003e isolates, and the \u003cem\u003eC. fimbriata\u003c/em\u003e isolate used in the present study (LPF1443) has been identified as a highly aggressive in kiwifruit vines (Oliveira et al., 2020). Given the susceptibility of both kiwifruit cultivars to \u003cem\u003eC. lukuohia\u003c/em\u003e, along with high plant mortality rates, there is a potential threat that this pathogen may pose not only to kiwifruit-producing areas in Hawaii but also to other countries with kiwifruit cultivation, such as New Zealand and Italy.\u003c/p\u003e\n\u003cp\u003eAlthough \u003cem\u003eC. lukuohia\u0026nbsp;\u003c/em\u003eand\u003cem\u003e\u0026nbsp;C. huliohia\u0026nbsp;\u003c/em\u003eare associated with ROD, only \u003cem\u003eC. lukuohia\u003c/em\u003e is considered a systemic vascular wilt pathogen on \u003cem\u003eM. polymorpha\u003c/em\u003e (Hughes et al., 2020). Similarly, we showed that of the two ROD pathogens, only \u003cem\u003eC. lukuohia\u003c/em\u003e causes wilt on kiwifruit vines,\u0026nbsp;with high aggressiveness and mortality. This corroborates other studies that suggest that \u003cem\u003eC. lukuohia\u0026nbsp;\u003c/em\u003ecauses Ceratocystis wilt on \u003cem\u003eM. polymorpha\u003c/em\u003e, and this species is the main cause of the high mortality caused by ROD, and that the distinct symptoms caused by \u003cem\u003eC. huliohia\u003c/em\u003e seem to be less important (Keith et al., 2015; Hughes et al., 2020).\u0026nbsp;\u003c/p\u003e\n\u003cp\u003eThis is the first report indicating that \u003cem\u003eC. lukuohia\u003c/em\u003e is not host-specific, which suggests that it poses a threat to other agricultural and forestry crops growing in Hawaii and the Pacific Basin. Implementation of biosecurity measures, including rapid detection and eradication strategies of the pathogen are imperative to prevent local and long-distance spread. Furthermore, knowing that \u003cem\u003eC. lukuohia\u003c/em\u003e can cause Ceratocystis wilt on kiwifruit vines, it is essential to avoid the introduction of this pathogen to kiwifruit-producing countries, especially where native \u003cem\u003eMetrosideros\u003c/em\u003e spp. co-exist.\u003c/p\u003e"},{"header":"Declarations","content":"\u003cp\u003e\u003cstrong\u003eACKNOWLEDGMENTS\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe authors are grateful to Zespri Group Limited for the financial support of this work, to Clonar Resist\u0026ecirc;ncia a Doen\u0026ccedil;as Florestais for providing the greenhouse facilities for plant growth and inoculations, to Department of Agriculture, Livestock and Food Supply (MAPA) for the import and inoculation guidelines, and Carolina Pessanha Alonso for help with the experiments.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eFUNDING\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThis work was supported by: \u0026lsquo;Conselho Nacional de Desenvolvimento Cient\u0026iacute;fico e Tecnol\u0026oacute;gico\u0026rsquo; (CNPq); \u0026lsquo;Coordena\u0026ccedil;\u0026atilde;o de Aperfei\u0026ccedil;oamento de Pessoal de N\u0026iacute;vel Superior\u0026rsquo; (CAPES); and \u0026lsquo;Funda\u0026ccedil;\u0026atilde;o de Amparo \u0026agrave; Pesquisa do Estado de Minas Gerais\u0026rsquo; (FAPEMIG). \u0026nbsp;\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eAUTHOR CONTRIBUTIONS STATEMENT\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eInvestigation and methodology were performed by Sabrina Angela Cassol. The data curation and formal analysis were performed by Sabrina Angela Cassol. The funding acquisition and supervision by Acelino Couto Alfenas, Chandan Pal, and Rafael Ferreira Alfenas. The original draft was written by Sabrina Angela Cassol and all authors reviewed and edited previous versions of the manuscript. All authors read and approved the final manuscript.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eDATA AVAILABILITY\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe data will be made available upon request from the corresponding author of the article.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eCONFLICT OF INTEREST\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eChandan Pal is employed by Zespri International Limited. All other authors have no competing interests.\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\n\u003cli\u003eAlfenas, A.C., Mafia, R.G. (2016). M\u0026eacute;todos em Fitopatologia. 2\u0026ordf; Ed. 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Species or genotypes? Reassessment of four recently described species of the Ceratocystis wilt pathogen, \u003cem\u003eC. fimbriata\u003c/em\u003e, on \u003cem\u003eMangifera indica\u003c/em\u003e. \u003cem\u003ePhytopathology,\u003c/em\u003e 105(9), 1229\u0026ndash;1244. 10.1094/PHYTO-03-15-0065-R\u003c/li\u003e\n\u003cli\u003eOliveira, L.S.S., Pimenta, L.V.A., Guimar\u0026atilde;es, L.M.S. de Souza, P.V.D., Bhering, L.L., Alfenas, A.C. (2020). Resistance of kiwifruit cultivars to Ceratocystis wilt: an approach considering the genetic diversity and variation in aggressiveness of the pathogen. \u003cem\u003ePlant\u003c/em\u003e \u003cem\u003ePathology,\u003c/em\u003e 70, 349-357. https://doi.org/10.1111/ppa.13305\u003c/li\u003e\n\u003cli\u003ePiveta, G., Ferreira, M.A., Muniz, M.F.B., Valdetaro, D., Valdebenito-Sanhueza, R., Harrington, T.C., Alfenas, A.C. (2016). \u003cem\u003eCeratocystis fimbriata \u003c/em\u003eon kiwifruit (\u003cem\u003eActinidia \u003c/em\u003espp.) in Brazil. \u003cem\u003eNew Zealand Journal of Crop and Horticultural Science,\u003c/em\u003e 44, 31-24. https://doi.org/10.1080/01140671.2016.1143020\u003c/li\u003e\n\u003cli\u003eSonego, O.R., Ferreira, M.A., Sanhueza, R.M., Gava, R., Garrido, L.R., Alfenas, A.C. (2010). Primeiro relato da murcha-de-ceratocystis em kiwifruit. \u003cem\u003eTropical Plant Pathology,\u003c/em\u003e 35, S233.\u003c/li\u003e\n\u003cli\u003eSteimel, J., Engelbrecht, C.J.B., Harrington, T.C. (2004). Development and characterization of microsatellite markers for the fungus \u003cem\u003eCeratocystis fimbriata\u003c/em\u003e. \u003cem\u003eMolecular Ecology Resources,\u003c/em\u003e 4, 215\u0026ndash;218. https://doi.org/10.1111/j.1471-8286.2004.00621.x\u003c/li\u003e\n\u003cli\u003eVanneste, J.L. (2017). The scientific, economic, and social impacts of the New Zealand outbreak of bacterial canker of kiwifruit (\u003cem\u003ePseudomonas syringae\u003c/em\u003e pv. \u003cem\u003eactinidiae\u003c/em\u003e). \u003cem\u003eAnnu. Rev. Phytopathol.\u003c/em\u003e \u003cem\u003e55\u003c/em\u003e, 377\u0026ndash;399. https://doi.org/10.1146/annurev-phyto-080516-035530\u003c/li\u003e\n\u003cli\u003eThorpe, D.J., Harrinton, T.C., Uchida, J.Y. (2005). Pathogenicity, internal transcribed spacer-rDNA variation, and human dispersal of \u003cem\u003eCeratocystis fimbriata\u003c/em\u003e on the Family Araceae. \u003cem\u003ePhytopathology,\u003c/em\u003e 95, 316-323. 10.1094/PHYTO-95-0316\u003c/li\u003e\n\u003cli\u003eTyson, J.L., Manning, M.A., Wright, P.J. (2020). Pathogenicity of \u003cem\u003eCeratocystis fimbriata\u003c/em\u003e from New Zealand kūmara on kiwifruit cultivars. \u003cem\u003eNew Zealand Plant Protection,\u003c/em\u003e 73, 6-12. https://doi.org/10.30843/nzpp.2020.73.11717\u003c/li\u003e\n\u003c/ol\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":"european-journal-of-plant-pathology","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"ejpp","sideBox":"Learn more about [European Journal of Plant Pathology](http://link.springer.com/journal/10658)","snPcode":"10658","submissionUrl":"https://www.editorialmanager.com/ejpp/default2.aspx","title":"European Journal of Plant Pathology","twitterHandle":"","acdcEnabled":true,"dfaEnabled":true,"editorialSystem":"em","reportingPortfolio":"Springer Hybrid","inReviewEnabled":true,"inReviewRevisionsEnabled":false},"keywords":"Actinidia chinensis, Actinidia deliciosa, Ceratocystis fimbriata, Ceratocystis huliohia, Ceratocystis wilt, Rapid Ohia Death","lastPublishedDoi":"10.21203/rs.3.rs-4164602/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-4164602/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003cp\u003eCeratocystis wilt, caused by \u003cem\u003eCeratocystis fimbriata\u003c/em\u003e, is the most severe disease of the kiwifruit crop in Brazil and represents a threat to other kiwifruit-producing countries where the pathogen has not yet been reported infecting kiwifruit vines. \u003cem\u003eCeratocystis\u003c/em\u003e species have been reported in many countries, some are host specific, while others can infect a wide host range. Given the high impact of the disease on kiwifruit, evaluating whether \u003cem\u003eCeratocystis\u003c/em\u003e isolates from other hosts and countries can also infect kiwifruit is important for implementing biosecurity measures. In the present work, we evaluated if \u003cem\u003eC. lukuohia\u003c/em\u003e and \u003cem\u003eC. huliohia\u003c/em\u003e, isolated from ohia (\u003cem\u003eMetrosideros polymorpha\u003c/em\u003e) in Hawaii are pathogenic to kiwifruit cultivars. Inoculations of both species in rooted cuttings of Monty and Gold3 cultivars showed that \u003cem\u003eC. lukuohia\u003c/em\u003e can cause wilt in both kiwifruit cultivars evaluated, with high plant mortality. This is the first report that \u003cem\u003eC. lukuohia\u003c/em\u003e can infect another host, demonstrating that it is not host-specific and extends its host range. In addition, considering that \u003cem\u003eC. lukuohia\u003c/em\u003e is pathogenic and lethal in kiwifruit vines, kiwifruit-producing areas must implement biosecurity measures to prevent the introduction of this species.\u003c/p\u003e","manuscriptTitle":"Potential Threat of Ceratocystis lukuohia on kiwifruit crop","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2024-04-02 15:25:20","doi":"10.21203/rs.3.rs-4164602/v1","editorialEvents":[{"type":"communityComments","content":0},{"type":"decision","content":"Major revisions","date":"2024-04-29T07:40:05+00:00","index":"","fulltext":""},{"type":"reviewerAgreed","content":"","date":"2024-04-02T05:20:23+00:00","index":0,"fulltext":""},{"type":"reviewersInvited","content":"","date":"2024-03-28T22:29:10+00:00","index":"","fulltext":""},{"type":"editorInvited","content":"European Journal of Plant Pathology","date":"2024-03-28T08:47:11+00:00","index":"","fulltext":""},{"type":"editorAssigned","content":"","date":"2024-03-27T03:31:44+00:00","index":"","fulltext":""},{"type":"submitted","content":"European Journal of Plant Pathology","date":"2024-03-25T12:09:21+00:00","index":"","fulltext":""}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"european-journal-of-plant-pathology","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"ejpp","sideBox":"Learn more about [European Journal of Plant Pathology](http://link.springer.com/journal/10658)","snPcode":"10658","submissionUrl":"https://www.editorialmanager.com/ejpp/default2.aspx","title":"European Journal of Plant Pathology","twitterHandle":"","acdcEnabled":true,"dfaEnabled":true,"editorialSystem":"em","reportingPortfolio":"Springer Hybrid","inReviewEnabled":true,"inReviewRevisionsEnabled":false}}],"origin":"","ownerIdentity":"fd94fb0d-bbf9-4ea5-b095-f436ecc79151","owner":[],"postedDate":"April 2nd, 2024","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"published-in-journal","subjectAreas":[],"tags":[],"updatedAt":"2024-11-25T16:00:09+00:00","versionOfRecord":{"articleIdentity":"rs-4164602","link":"https://doi.org/10.1007/s10658-024-02980-4","journal":{"identity":"european-journal-of-plant-pathology","isVorOnly":false,"title":"European Journal of Plant Pathology"},"publishedOn":"2024-11-19 15:57:09","publishedOnDateReadable":"November 19th, 2024"},"versionCreatedAt":"2024-04-02 15:25:20","video":"","vorDoi":"10.1007/s10658-024-02980-4","vorDoiUrl":"https://doi.org/10.1007/s10658-024-02980-4","workflowStages":[]},"version":"v1","identity":"rs-4164602","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-4164602","identity":"rs-4164602","version":["v1"]},"buildId":"qtupq5eGEP_6zYnWcrvyt","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}