{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,23]],"date-time":"2026-09-23T09:08:35Z","timestamp":1790154515491,"version":"4.0.1"},"reference-count":70,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2022,11,25]],"date-time":"2022-11-25T00:00:00Z","timestamp":1669334400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Plant Sci."],"abstract":"<jats:p>In recent years, Brown spot disease of rice (BSR) has been observed on leaves and seeds of rice in all rice-growing areas of Burkina Faso. <jats:italic>Bipolaris oryzae<\/jats:italic> and <jats:italic>Exserohilum rostratum<\/jats:italic> are the main fungal species isolated from BSR infected tissues and they are frequently observed in the same field. However, we are lacking information on the genetic diversity and population structure of these fungi in Burkina Faso. The mode of reproduction is also unknown. The genetic diversity of isolates of <jats:italic>B. oryzae<\/jats:italic> (n=61) and <jats:italic>E. rostratum<\/jats:italic> (n=151), collected from major rice-growing areas of Burkina Faso, was estimated using genotyping-by-sequencing (GBS). The mean values for nucleotide diversity (\u03c0) were 1.9 x10<jats:sup>-4<\/jats:sup> for <jats:italic>B. oryzae<\/jats:italic> and 4.8 x10<jats:sup>-4<\/jats:sup> for <jats:italic>E. rostratum<\/jats:italic>. There is no genetic differentiation between the geographical populations of each species. The analysis of molecular variance revealed that 89% and 94% of the genetic variances were within the populations of <jats:italic>B. oryzae<\/jats:italic> and <jats:italic>E. rostratum<\/jats:italic>, respectively. For each species, four genetic clusters were identified by two clustering methods (DAPC and sNMF). The distribution of these genetic groups was independent of the geographical origin of the isolates. Evidence of recombination was detected in the populations of <jats:italic>B. oryzae<\/jats:italic> and <jats:italic>E. rostratum.<\/jats:italic> For <jats:italic>B. oryzae<\/jats:italic> balanced mating type ratios were supporting sexual reproduction. For <jats:italic>E. rostratum<\/jats:italic> overrepresentation of MAT1-2 isolates (79%) suggested a predominant asexual reproduction. This study provides important information on the biology and genetics of the two major fungi causing brown spot disease of rice in Burkina Faso.<\/jats:p>","DOI":"10.3389\/fpls.2022.1022348","type":"journal-article","created":{"date-parts":[[2022,11,25]],"date-time":"2022-11-25T05:53:12Z","timestamp":1669355592000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":14,"title":["Genetic diversity and structure of Bipolaris oryzae and Exserohilum rostratum populations causing brown spot of rice in Burkina Faso based on genotyping-by-sequencing"],"prefix":"10.3389","volume":"13","author":[{"given":"Kouka Hilaire","family":"Kabor\u00e9","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Abalo Itolou","family":"Kassankogno","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Henri","family":"Adreit","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jo\u00eblle","family":"Milazzo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sonia","family":"Guillou","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Laurence","family":"Blondin","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Laurie","family":"Chopin","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"S\u00e9bastien","family":"Ravel","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Florian","family":"Charriat","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mariam","family":"Barro","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Charlottte","family":"Tollenaere","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marc-Henri","family":"Lebrun","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Didier","family":"Tharreau","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2022,11,25]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"181","DOI":"10.1111\/ppa.12714","article-title":"Population structure, genetic diversity, and sexual state of the rice brown spot pathogen Bipolaris oryzae from three Asian countries","volume":"67","author":"Ahmadpour","year":"2018","journal-title":"Plant Pathol."},{"key":"B2","doi-asserted-by":"publisher","first-page":"238","DOI":"10.5897\/AJB2013.12063","article-title":"Genetic diversity and population structure among isolates of the brown spot fungus, bipolaris oryzae, as revealed by inter-simple sequence repeats (ISSR)","volume":"13","author":"Archana","year":"2014","journal-title":"Afr. J. Biotechnol."},{"key":"B3","first-page":"83","article-title":"Study of genomic fingerprints profile of Indian bipolaris oryzae from rice (Oryza sativa) by RAPD-PCR","volume":"3","author":"Archana","year":"2014","journal-title":"Int. J. Life Sci. Biotechnol. Pharma Res."},{"key":"B4","doi-asserted-by":"publisher","first-page":"212","DOI":"10.1094\/PDIS-04-20-0838-PDN","article-title":"First report of brown leaf spot of rice caused by Bipolaris zeicola in Pakistan","volume":"105","author":"Aslam","year":"2021","journal-title":"Plant Dis."},{"key":"B5","doi-asserted-by":"publisher","first-page":"443","DOI":"10.1007\/s10658-013-0195-6","article-title":"A review on crop losses, epidemiology and disease management of rice brown spot to identify research priorities and knowledge gaps","volume":"136","author":"Barnwal","year":"2013","journal-title":"Eur. J. Plant Pathol."},{"key":"B6","doi-asserted-by":"publisher","first-page":"3889","DOI":"10.1094\/PDIS-03-21-0579-RE","article-title":"Spatiotemporal survey of multiple rice diseases in irrigated areas compared to rainfed lowlands in the Western Burkina Faso","volume":"105","author":"Barro","year":"2021","journal-title":"Plant Dis."},{"key":"B7","doi-asserted-by":"publisher","first-page":"103","DOI":"10.33687\/phytopath.007.03.2643","article-title":"Pathogenic variability of Bipolaris oryzae causing leaf spot disease of rice in West Africa","volume":"7","author":"Boka","year":"2018","journal-title":"Int. J. Phytopathol."},{"key":"B8","doi-asserted-by":"publisher","first-page":"415","DOI":"10.1007\/s10658-013-0256-x","article-title":"Genotypic variability and aggressiveness of Bipolaris oryzae in the Philippines","volume":"137","author":"Burgos","year":"2013","journal-title":"Eur. J. Plant Pathol."},{"key":"B9","doi-asserted-by":"publisher","first-page":"226","DOI":"10.1094\/PDIS-91-2-0226C","article-title":"First report of Exserohilum rostratum associated with rice seed in Venezuela","volume":"91","author":"Cardona","year":"2007","journal-title":"Plant Dis."},{"key":"B10","doi-asserted-by":"publisher","first-page":"903","DOI":"10.1111\/j.1365-3059.2011.02581.x","article-title":"Population genetic structure, gene flow and recombination of Cochliobolus miyabeanus on cultivated wildrice (Zizania palustris)","volume":"61","author":"Castell-Miller","year":"2012","journal-title":"Plant Pathol."},{"key":"B11","doi-asserted-by":"publisher","first-page":"31","DOI":"10.1371\/journal.pone.0154122","article-title":"Genome Assembly of the Fungus Cochliobolus miyabeanus, and Transcriptome Analysis during Early Stages of Infection on American Wildrice (Zizania palustris L.)","volume":"11","author":"Castell-Miller","year":"2016","journal-title":"PLoS ONE"},{"key":"B12","doi-asserted-by":"publisher","first-page":"116","DOI":"10.14416\/j.asep.2019.03.004","article-title":"Genetic diversity and aggressiveness of Bipolaris oryzae in north-central Thailand","volume":"12","author":"Chaijuckam","year":"2019","journal-title":"Appl. Sci. Eng. Prog."},{"key":"B13","first-page":"199","article-title":"Dispersal of airborne pathogenic conidia of Bipolaris oryzae inciting brown spot disease of paddy in West Bengal, India","volume":"58","author":"Chakraborty","year":"2020","journal-title":"J. Trop. Agric."},{"key":"B14","doi-asserted-by":"publisher","first-page":"29","DOI":"10.1371\/journal.pgen.1003233","article-title":"Comparative genome structure, secondary metabolite, and effector coding capacity across Cochliobolus pathogens","volume":"9","author":"Condon","year":"2013","journal-title":"PloS Genet."},{"key":"B15","doi-asserted-by":"publisher","first-page":"116","DOI":"10.1094\/PHYTO-99-1-0116","article-title":"Defective active silicon uptake affects some components of rice resistance to brown spot","volume":"99","author":"Dallagnol","year":"2009","journal-title":"Phytopathology"},{"key":"B16","doi-asserted-by":"publisher","first-page":"2156","DOI":"10.1093\/bioinformatics\/btr330","article-title":"The variant call format and VCFtools","volume":"27","author":"Danecek","year":"2011","journal-title":"Bioinformatics"},{"key":"B17","volume-title":"Observations phytosanitaires sur les riz cultiv\u00e9s en c\u00f4te d\u2019Ivoire et haute Volta pendant la campagne 1962","author":"Davet","year":"1962"},{"key":"B18","author":"Demb\u00e9l\u00e9","year":"2014"},{"key":"B19","doi-asserted-by":"crossref","first-page":"46","DOI":"10.1079\/9781845938123.0046","article-title":"Farmers perceptions of the biophysical constraints to rice production in sub-Saharan Africa, and potential impact of research","volume-title":"Realizing africa\u2019s rice promise","author":"Diagne","year":"2013"},{"key":"B20","first-page":"11","article-title":"A rapid DNA isolation procedure for small quantities of fresh leaf tissue","volume":"19","author":"Doyle","year":"1987","journal-title":"Phytochem. Bull."},{"key":"B21","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0019379","article-title":"A robust, simple genotyping-by-Sequencing (GBS) approach for high diversity species","volume":"6","author":"Elshire","year":"2011","journal-title":"PloS One"},{"key":"B22","doi-asserted-by":"publisher","first-page":"479","DOI":"10.1093\/genetics\/131.2.479","article-title":"Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data","volume":"131","author":"Excoffier","year":"1992","journal-title":"Genetics"},{"key":"B23","doi-asserted-by":"publisher","first-page":"368","DOI":"10.1007\/s11703-007-0062-3","article-title":"Distribution of mating types and genetic diversity induced by sexual recombination in Setosphaeria turcica in northern China","volume":"1","author":"Fan","year":"2007","journal-title":"Front. Agric. China"},{"key":"B24","doi-asserted-by":"publisher","first-page":"973","DOI":"10.1534\/genetics.113.160572","article-title":"Fast and efficient estimation of individual ancestry coefficients","volume":"196","author":"Frichot","year":"2014","journal-title":"Genetics"},{"key":"B25","doi-asserted-by":"publisher","first-page":"184","DOI":"10.1111\/j.1471-8286.2004.00828.x","article-title":"Hierfstat, a package for r to compute and test hierarchical f-statistics","volume":"5","author":"Goudet","year":"2005","journal-title":"Mol. Ecol. Notes"},{"key":"B26","doi-asserted-by":"publisher","first-page":"738","DOI":"10.1094\/PHYTO.2003.93.6.738","article-title":"Analysis of genotypic diversity data for populations of microorganisms","volume":"93","author":"Gr\u00fcnwald","year":"2003","journal-title":"Phytopathology\u00ae"},{"key":"B27","doi-asserted-by":"publisher","first-page":"1134","DOI":"10.1094\/PHYTO-96-1134","article-title":"Hierarchical analysis of diversity, selfing, and genetic differentiation in populations of the oomycete Aphanomyces euteiches","volume":"96","author":"Gr\u00fcnwald","year":"2006","journal-title":"Phytopathology\u00ae"},{"key":"B28","first-page":"285","article-title":"Preinfectional interaction between Helminthosporium oryzae and resistant and susceptible rice plants","volume":"72","author":"Hau","year":"1982","journal-title":"Phytopathology"},{"key":"B29","doi-asserted-by":"publisher","first-page":"254","DOI":"10.1093\/molbev\/msj030","article-title":"Application of phylogenetic networks in evolutionary studies","volume":"23","author":"Huson","year":"2006","journal-title":"Mol. Biol. Evol."},{"key":"B30","first-page":"2045","article-title":"Helminthosporium rostrata, foliar parasite of rice in Morocco","volume":"19","author":"Imrani","year":"2019","journal-title":"Plant Arch."},{"key":"B31","doi-asserted-by":"publisher","first-page":"1193","DOI":"10.1094\/PD-76-1193","article-title":"Wild rice domestication, fungal brown spot disease, and the future of commercial production in Minnesota","volume":"76","author":"Johnson","year":"1992","journal-title":"Plant Dis."},{"key":"B32","doi-asserted-by":"publisher","first-page":"1403","DOI":"10.1093\/bioinformatics\/btn129","article-title":"Adegenet: a r package for the multivariate analysis of genetic markers","volume":"24","author":"Jombart","year":"2008","journal-title":"Bioinformatics"},{"key":"B33","doi-asserted-by":"publisher","DOI":"10.1186\/1471-2156-11-94","article-title":"Discriminant analysis of principal components: a new method for the analysis of genetically structured populations","volume":"11","author":"Jombart","year":"2010","journal-title":"BMC Genet."},{"key":"B34","volume-title":"Helminthosporiose du riz en afrique de l\u2019Ouest: identification des esp\u00e8ces responsables et diversit\u00e9 g\u00e9n\u00e9tique de bipolaris oryzae et exserohilum rostratum. [Th\u00e8se de doctorat]","author":"Kabor\u00e9","year":"2022"},{"key":"B35","doi-asserted-by":"publisher","first-page":"1747","DOI":"10.1094\/PDIS-03-21-0662-PDN","article-title":"First report of rice brown spot caused by Exserohilum rostratum in Mali","volume":"106","author":"Kabor\u00e9","year":"2022","journal-title":"Plant Dis."},{"key":"B36","doi-asserted-by":"publisher","first-page":"119","DOI":"10.3329\/bjb.v38i2.5135","article-title":"Diversity and pathogenicity of the rice brown spot pathogen, Bipolaris oryzae (Breda de haan) shoem. in Bangladesh assessed by genetic fingerprint analysis","volume":"38","author":"Kamal","year":"2009","journal-title":"Bangladesh J. Bot."},{"key":"B37","doi-asserted-by":"publisher","DOI":"10.7717\/peerj.281","article-title":"Poppr : an r package for genetic analysis of populations with clonal, partially clonal, and\/or sexual reproduction","volume":"2","author":"Kamvar","year":"2014","journal-title":"PeerJ"},{"key":"B38","doi-asserted-by":"publisher","DOI":"10.21203\/rs.3.rs-2027087\/v1","article-title":"Pathogenicity and infection behaviour of Exserohilum rostratum on wheat and associated collateral hosts","author":"Korra","year":"2022","journal-title":"Research Square"},{"key":"B39","doi-asserted-by":"publisher","first-page":"905","DOI":"10.3852\/15-175","article-title":"Morphological and molecular characterization, sexual reproduction, and pathogenicity of Setosphaeria rostrata isolates from rice leaf spot","volume":"108","author":"Kusai","year":"2016","journal-title":"Mycologia"},{"key":"B40","volume-title":"Statistical ecology: A primer on methods and computing","author":"Ludwig","year":"1988"},{"key":"B41","doi-asserted-by":"publisher","first-page":"1456","DOI":"10.1016\/j.csbj.2022.03.016","article-title":"Comparative mitochondrial genome analyses reveal conserved gene arrangement but massive expansion\/contraction in two closely related Exserohilum pathogens","volume":"20","author":"Ma","year":"2022","journal-title":"Comput. Struct. Biotechnol. J."},{"key":"B42","doi-asserted-by":"publisher","first-page":"2162","DOI":"10.1094\/PDIS-02-16-0220-PDN","article-title":"First report of setosphaeria rostrata causing brown leaf spot of rice in Pakistan","volume":"100","author":"Majeed","year":"2016","journal-title":"Plant Dis."},{"key":"B43","volume-title":"Common laboratory seed health testing methods for detecting fungi","author":"Mathur","year":"2003"},{"key":"B44","doi-asserted-by":"publisher","first-page":"457","DOI":"10.1146\/annurev.phyto.34.1.457","article-title":"Recombination and the multilocus structure of fungal populations","volume":"34","author":"Milgroom","year":"1996","journal-title":"Annu. Rev. Phytopathol."},{"key":"B45","first-page":"638","article-title":"Characterization of new Bipolaris spp.: The causal agent of rice brown spot disease in the north of Iran","volume":"10","author":"Motlagh","year":"2008","journal-title":"Int. J. Agric. Biol."},{"key":"B46","first-page":"497","article-title":"Bipolaris species associated with rice plant: pathogenicity and genetic diversity of Bipolaris oryzae using rep-PCR in mazandaran province of Iran","volume":"4","author":"Nazari","year":"2015","journal-title":"J. Crop Prot."},{"key":"B47","doi-asserted-by":"publisher","DOI":"10.22004\/ag.econ.266026","article-title":"Sub-Saharan Africa Is projected to be the leader in global rice imports","volume":"9","author":"Nigatu","year":"2017"},{"key":"B48","doi-asserted-by":"publisher","first-page":"675","DOI":"10.1002\/jsfa.2415","article-title":"Rice development in sub-Saharan Africa","volume":"86","author":"Nwanze","year":"2006","journal-title":"J. Sci. Food Agric."},{"key":"B49","volume-title":"Rice diseases","author":"Ou","year":"1985"},{"key":"B50","volume-title":"Incidence de l\u2019helminthosporiose du riz au Burkina Faso et caract\u00e9risation des populations de l\u2019agent pathog\u00e8ne [Bipolaris oryzae (Breda de haan) shoemaker]. [Th\u00e8se de doctorat]","author":"Ou\u00e9draogo","year":"2008"},{"key":"B51","first-page":"111","article-title":"Pathogenic, molecular, and genetic diversity among Bipolaris, Drechslera and Exserohilum species on rice","volume":"529","author":"Ou\u00e9draogo","year":"2004","journal-title":"AAES Res. Ser."},{"key":"B52","first-page":"476","article-title":"Survey of fungal seed-borne diseases of rice in Burkina Faso","volume":"5","author":"Ou\u00e9draogo","year":"2016","journal-title":"Int. J. Agric. Innov. Res."},{"key":"B53","doi-asserted-by":"publisher","first-page":"163","DOI":"10.1023\/A:1020654319130","article-title":"Pyricularia grisea and Bipolaris oryzae: a preliminary study on the occurrence of airborne spores in a rice field","volume":"18","author":"Picco","year":"2002","journal-title":"Aerobiologia"},{"key":"B54","volume-title":"Ecological diversity","author":"Pielou","year":"1975"},{"key":"B55","doi-asserted-by":"publisher","first-page":"263","DOI":"10.1016\/j.fcr.2004.07.017","article-title":"Multiple effects of two drivers of agricultural change, labour shortage and water scarcity, on rice pest profiles in tropical Asia","volume":"91","author":"Savary","year":"2005","journal-title":"Field Crops Res."},{"key":"B56","doi-asserted-by":"publisher","first-page":"357","DOI":"10.1094\/PDIS.2000.84.3.357","article-title":"Rice pest constraints in tropical Asia: Quantification of yield losses due to rice pests in a range of production situations","volume":"84","author":"Savary","year":"2000","journal-title":"Plant Dis."},{"key":"B57","doi-asserted-by":"publisher","first-page":"430","DOI":"10.1038\/s41559-018-0793-y","article-title":"The global burden of pathogens and pests on major food crops","volume":"3","author":"Savary","year":"2019","journal-title":"Nat. Ecol. Evol."},{"key":"B58","doi-asserted-by":"publisher","first-page":"623","DOI":"10.1002\/j.1538-7305.1948.tb00917.x","article-title":"A mathematical theory of communication","volume":"27","author":"Shannon","year":"1948","journal-title":"Bell Syst. Tech. J."},{"key":"B59","doi-asserted-by":"publisher","first-page":"2531","DOI":"10.1094\/PDIS-05-16-0709-PDN","article-title":"First report on Exserohilum rostratum pathogenicity causing brown spot to rice in Brazil","volume":"100","author":"Silva","year":"2016","journal-title":"Plant Dis."},{"key":"B60","doi-asserted-by":"publisher","first-page":"688","DOI":"10.1038\/163688a0","article-title":"Measurement of diversity","volume":"163","author":"Simpson","year":"1949","journal-title":"Nature"},{"key":"B61","doi-asserted-by":"publisher","first-page":"1312","DOI":"10.1093\/bioinformatics\/btu033","article-title":"RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies","volume":"30","author":"Stamatakis","year":"2014","journal-title":"Bioinformatics"},{"key":"B62","first-page":"201","article-title":"Brown spot of rice: An overview","volume":"67","author":"Sunder","year":"2014","journal-title":"Indian Phytopathol."},{"key":"B63","doi-asserted-by":"publisher","first-page":"226","DOI":"10.1094\/PDIS-03-15-0276-PDN","article-title":"First report of Exserohilum rostratum as pathogen of rice brown spot in Malaysia","volume":"100","author":"Toher","year":"2016","journal-title":"Plant Dis."},{"key":"B64","doi-asserted-by":"publisher","first-page":"7","DOI":"10.3186\/jjphytopath.42.7","article-title":"Distribution of two mating types of Cochliobolus miyabeanus in field and a laboratory attempt to produce hybrids between isolates of Helminthosporium oryzae from the USA and Japan","volume":"42","author":"Tsuda","year":"1976","journal-title":"Ann. Phytopath. Soc. Jpn."},{"key":"B65","first-page":"81","article-title":"Histological studies of rice leaves infected with helminthosporium oryzae","volume":"50","author":"Tullis","year":"1935","journal-title":"J. Agric. Res."},{"key":"B66","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3186\/jjphytopath.42.1","article-title":"Mating type and sexuality of Cochliobolus miyabeanus, the perfect state of Helminthosporium oryzae","volume":"42","author":"Ueyama","year":"1976","journal-title":"Ann. Phytopathol. Soc Jpn."},{"key":"B67","doi-asserted-by":"publisher","first-page":"55","DOI":"10.1016\/j.fcr.2018.01.016","article-title":"Mapping abiotic stresses for rice in Africa: Drought, cold, iron toxicity, salinity and sodicity","volume":"219","author":"van Oort","year":"2018","journal-title":"Field Crops Res."},{"key":"B68","doi-asserted-by":"publisher","first-page":"1358","DOI":"10.2307\/2408641","article-title":"Estimating f-statistics for the analysis of population structure","volume":"38","author":"Weir","year":"1984","journal-title":"Evolution"},{"key":"B69","first-page":"765","article-title":"The role of epidemiology in modern phytopathology","volume":"64","author":"Zadoks","year":"1974","journal-title":"Phytopathology"},{"key":"B70","doi-asserted-by":"publisher","first-page":"1786","DOI":"10.1093\/bioinformatics\/bty875","article-title":"PopLDdecay: A fast and effective tool for linkage disequilibrium decay analysis based on variant call format files","volume":"35","author":"Zhang","year":"2019","journal-title":"Bioinformatics"}],"container-title":["Frontiers in Plant Science"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fpls.2022.1022348\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,11,25]],"date-time":"2022-11-25T05:53:29Z","timestamp":1669355609000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fpls.2022.1022348\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,11,25]]},"references-count":70,"alternative-id":["10.3389\/fpls.2022.1022348"],"URL":"https:\/\/doi.org\/10.3389\/fpls.2022.1022348","relation":{},"ISSN":["1664-462X"],"issn-type":[{"value":"1664-462X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,11,25]]},"article-number":"1022348"}}