Population genomics provide insights into the global genetic structure of Colletotrichum graminicola, the causal agent of maize anthracnose.

Detalhes bibliográficos
Autor(a) principal: ROGÉRIO, F.
Data de Publicação: 2022
Outros Autores: BARONCELLI, R., CUEVAS-FERNÁNDEZ, F. B., BECERRA, S., CROUCH, J., BETTIOL, W., AZCÁRATE-PERIL, M. A., MALAPI-WIGHT, M., ORTEGA, V., BETRAN, J., TENUTA, A., DAMBOLENA, J. S., ESKER, P. D., REVILLA, P., JACKSON-ZIEMS, HILTBRUNNER, J., MUNKVOLD, G., BUHINICEK, I., VICENTE-VILLARDÓN, J. L.'''', SUKNO, S. A., THON, M. R.
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Institucional da EMBRAPA (Repository Open Access to Scientific Information from EMBRAPA - Alice)
Texto Completo: http://www.alice.cnptia.embrapa.br/alice/handle/doc/1151733
https://doi.org/10.1128/mbio.02878-22
Resumo: Abstract: Understanding the genetic diversity and mechanisms underlying genetic variation in pathogen populations is crucial to the development of effective control strategies. We investigated the genetic diversity and reproductive biology of Colletotrichum graminicola isolates which infect maize by sequencing the genomes of 108 isolates collected from 14 countries using restriction site-associated DNA sequencing (RAD-seq) and whole-genome sequencing (WGS). Clustering analyses based on single-nucleotide polymorphisms revealed three genetic groups delimited by continental origin, compatible with short-dispersal of the pathogen and geographic subdivision. Intra- and intercontinental migration was observed between Europe and South America, likely associated with the movement of contaminated germplasm. Low clonality, evidence of genetic recombination, and high phenotypic diversity were detected. We show evidence that, although it is rare (possibly due to losses of sexual reproduction- and meiosis-associated genes) C. graminicola can undergo sexual recombination. Our results support the hypotheses that intra- and intercontinental pathogen migration and genetic recombination have great impacts on the C. graminicola population structure. Importance: Plant pathogens cause significant reductions in yield and crop quality and cause enormous economic losses worldwide. Reducing these losses provides an obvious strategy to increase food production without further degrading natural ecosystems; however, this requires knowledge of the biology and evolution of the pathogens in agroecosystems. We employed a population genomics approach to investigate the genetic diversity and reproductive biology of the maize anthracnose pathogen (Colletotrichum graminicola) in 14 countries. We found that the populations are correlated with their geographical origin and that migration between countries is ongoing, possibly caused by the movement of infected plant material. This result has direct implications for disease management because migration can cause the movement of more virulent and/or fungicide-resistant genotypes. We conclude that genetic recombination is frequent (in contrast to the traditional view of C. graminicola being mainly asexual), which strongly impacts control measures and breeding programs aimed at controlling this disease.
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spelling Population genomics provide insights into the global genetic structure of Colletotrichum graminicola, the causal agent of maize anthracnose.MilhoAntracnoseColletotrichum GraminicolaVariação GenéticaFungal diseases of plantsAnthracnoseCornPopulation geneticsPhylogeographyGenetic recombinationGenomicsAbstract: Understanding the genetic diversity and mechanisms underlying genetic variation in pathogen populations is crucial to the development of effective control strategies. We investigated the genetic diversity and reproductive biology of Colletotrichum graminicola isolates which infect maize by sequencing the genomes of 108 isolates collected from 14 countries using restriction site-associated DNA sequencing (RAD-seq) and whole-genome sequencing (WGS). Clustering analyses based on single-nucleotide polymorphisms revealed three genetic groups delimited by continental origin, compatible with short-dispersal of the pathogen and geographic subdivision. Intra- and intercontinental migration was observed between Europe and South America, likely associated with the movement of contaminated germplasm. Low clonality, evidence of genetic recombination, and high phenotypic diversity were detected. We show evidence that, although it is rare (possibly due to losses of sexual reproduction- and meiosis-associated genes) C. graminicola can undergo sexual recombination. Our results support the hypotheses that intra- and intercontinental pathogen migration and genetic recombination have great impacts on the C. graminicola population structure. Importance: Plant pathogens cause significant reductions in yield and crop quality and cause enormous economic losses worldwide. Reducing these losses provides an obvious strategy to increase food production without further degrading natural ecosystems; however, this requires knowledge of the biology and evolution of the pathogens in agroecosystems. We employed a population genomics approach to investigate the genetic diversity and reproductive biology of the maize anthracnose pathogen (Colletotrichum graminicola) in 14 countries. We found that the populations are correlated with their geographical origin and that migration between countries is ongoing, possibly caused by the movement of infected plant material. This result has direct implications for disease management because migration can cause the movement of more virulent and/or fungicide-resistant genotypes. We conclude that genetic recombination is frequent (in contrast to the traditional view of C. graminicola being mainly asexual), which strongly impacts control measures and breeding programs aimed at controlling this disease.FLÁVIA ROGÉRIO, UNIVERSIDAD DE SALAMANCA; RICCARDO BARONCELLI, UNIVERSITÀ DI BOLOGNA; FRANCISCO BORJA CUEVAS-FERNÁNDEZ, UNIVERSIDAD DE SALAMANCA; SIOLY BECERRA, UNIVERSIDAD DE SALAMANCA; JOANNE CROUCH, UNITED STATES DEPARTMENT OF AGRICULTURE; WAGNER BETTIOL, CNPMA; MARIA ANDREA AZCÁRATE-PERIL, UNIVERSITY OF NORTH CAROLINE; MARTHA MALAPI-WIGHT, UNITED STATES DEPARTMENT OF AGRICULTURE; VERONIQUE ORTEGA, SYNGENTA SEEDS; JAVIER BETRAN, BAYER CROP SCIENCE; ALBERT TENUTA, UNIVERSITY OF GUELPH-RIDGETOWN; JOSÉ S DAMBOLENA, UNIVERSIDAD NACIONAL DE CÓRDOBA; PAUL D ESKER, THE PENNSYLVANIA STATE UNIVERSITY; PEDRO REVILLA, CONSEJO SUPERIOR DE INVESTIGACIONES CIENTÍFICAS; TAMRA A JACKSON-ZIEMS, UNIVERSITY OF NEBRASKA-LINCOLN; JÜRG HILTBRUNNER, DÉPARTEMENT FÉDÉRAL DE L'ÉCONOMIE, DE LA FORMATION ET DE LA RECHERCHE; GARY MUNKVOLD, IOWA STATE UNIVERSITY; IVICA BUHINICEK, BC INSTITUTE FOR BREEDING AND PRODUCTION OF FIELD CROPS; JOSÉ LUIS VICENTE-VILLARDÓN, UNIVERSIDAD DE SALAMANCA; SERENELLA A SUKNO, UNIVERSIDAD DE SALAMANCA; MICHAEL R THON, UNIVERSIDAD DE SALAMANCA.ROGÉRIO, F.BARONCELLI, R.CUEVAS-FERNÁNDEZ, F. B.BECERRA, S.CROUCH, J.BETTIOL, W.AZCÁRATE-PERIL, M. A.MALAPI-WIGHT, M.ORTEGA, V.BETRAN, J.TENUTA, A.DAMBOLENA, J. S.ESKER, P. D.REVILLA, P.JACKSON-ZIEMSHILTBRUNNER, J.MUNKVOLD, G.BUHINICEK, I.VICENTE-VILLARDÓN, J. L.''''SUKNO, S. A.THON, M. R.2023-04-27T10:52:28Z2023-04-27T10:52:28Z2023-02-142022info:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articleMBio, v. 14, n. 1, e0287822, 2022.2150-7511http://www.alice.cnptia.embrapa.br/alice/handle/doc/1151733https://doi.org/10.1128/mbio.02878-22enginfo:eu-repo/semantics/openAccessreponame:Repositório Institucional da EMBRAPA (Repository Open Access to Scientific Information from EMBRAPA - Alice)instname:Empresa Brasileira de Pesquisa Agropecuária (Embrapa)instacron:EMBRAPA2023-04-27T10:52:28Zoai:www.alice.cnptia.embrapa.br:doc/1151733Repositório InstitucionalPUBhttps://www.alice.cnptia.embrapa.br/oai/requestopendoar:21542023-04-27T10:52:28falseRepositório InstitucionalPUBhttps://www.alice.cnptia.embrapa.br/oai/requestcg-riaa@embrapa.bropendoar:21542023-04-27T10:52:28Repositório Institucional da EMBRAPA (Repository Open Access to Scientific Information from EMBRAPA - Alice) - Empresa Brasileira de Pesquisa Agropecuária (Embrapa)false
dc.title.none.fl_str_mv Population genomics provide insights into the global genetic structure of Colletotrichum graminicola, the causal agent of maize anthracnose.
title Population genomics provide insights into the global genetic structure of Colletotrichum graminicola, the causal agent of maize anthracnose.
spellingShingle Population genomics provide insights into the global genetic structure of Colletotrichum graminicola, the causal agent of maize anthracnose.
ROGÉRIO, F.
Milho
Antracnose
Colletotrichum Graminicola
Variação Genética
Fungal diseases of plants
Anthracnose
Corn
Population genetics
Phylogeography
Genetic recombination
Genomics
title_short Population genomics provide insights into the global genetic structure of Colletotrichum graminicola, the causal agent of maize anthracnose.
title_full Population genomics provide insights into the global genetic structure of Colletotrichum graminicola, the causal agent of maize anthracnose.
title_fullStr Population genomics provide insights into the global genetic structure of Colletotrichum graminicola, the causal agent of maize anthracnose.
title_full_unstemmed Population genomics provide insights into the global genetic structure of Colletotrichum graminicola, the causal agent of maize anthracnose.
title_sort Population genomics provide insights into the global genetic structure of Colletotrichum graminicola, the causal agent of maize anthracnose.
author ROGÉRIO, F.
author_facet ROGÉRIO, F.
BARONCELLI, R.
CUEVAS-FERNÁNDEZ, F. B.
BECERRA, S.
CROUCH, J.
BETTIOL, W.
AZCÁRATE-PERIL, M. A.
MALAPI-WIGHT, M.
ORTEGA, V.
BETRAN, J.
TENUTA, A.
DAMBOLENA, J. S.
ESKER, P. D.
REVILLA, P.
JACKSON-ZIEMS
HILTBRUNNER, J.
MUNKVOLD, G.
BUHINICEK, I.
VICENTE-VILLARDÓN, J. L.''''
SUKNO, S. A.
THON, M. R.
author_role author
author2 BARONCELLI, R.
CUEVAS-FERNÁNDEZ, F. B.
BECERRA, S.
CROUCH, J.
BETTIOL, W.
AZCÁRATE-PERIL, M. A.
MALAPI-WIGHT, M.
ORTEGA, V.
BETRAN, J.
TENUTA, A.
DAMBOLENA, J. S.
ESKER, P. D.
REVILLA, P.
JACKSON-ZIEMS
HILTBRUNNER, J.
MUNKVOLD, G.
BUHINICEK, I.
VICENTE-VILLARDÓN, J. L.''''
SUKNO, S. A.
THON, M. R.
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv FLÁVIA ROGÉRIO, UNIVERSIDAD DE SALAMANCA; RICCARDO BARONCELLI, UNIVERSITÀ DI BOLOGNA; FRANCISCO BORJA CUEVAS-FERNÁNDEZ, UNIVERSIDAD DE SALAMANCA; SIOLY BECERRA, UNIVERSIDAD DE SALAMANCA; JOANNE CROUCH, UNITED STATES DEPARTMENT OF AGRICULTURE; WAGNER BETTIOL, CNPMA; MARIA ANDREA AZCÁRATE-PERIL, UNIVERSITY OF NORTH CAROLINE; MARTHA MALAPI-WIGHT, UNITED STATES DEPARTMENT OF AGRICULTURE; VERONIQUE ORTEGA, SYNGENTA SEEDS; JAVIER BETRAN, BAYER CROP SCIENCE; ALBERT TENUTA, UNIVERSITY OF GUELPH-RIDGETOWN; JOSÉ S DAMBOLENA, UNIVERSIDAD NACIONAL DE CÓRDOBA; PAUL D ESKER, THE PENNSYLVANIA STATE UNIVERSITY; PEDRO REVILLA, CONSEJO SUPERIOR DE INVESTIGACIONES CIENTÍFICAS; TAMRA A JACKSON-ZIEMS, UNIVERSITY OF NEBRASKA-LINCOLN; JÜRG HILTBRUNNER, DÉPARTEMENT FÉDÉRAL DE L'ÉCONOMIE, DE LA FORMATION ET DE LA RECHERCHE; GARY MUNKVOLD, IOWA STATE UNIVERSITY; IVICA BUHINICEK, BC INSTITUTE FOR BREEDING AND PRODUCTION OF FIELD CROPS; JOSÉ LUIS VICENTE-VILLARDÓN, UNIVERSIDAD DE SALAMANCA; SERENELLA A SUKNO, UNIVERSIDAD DE SALAMANCA; MICHAEL R THON, UNIVERSIDAD DE SALAMANCA.
dc.contributor.author.fl_str_mv ROGÉRIO, F.
BARONCELLI, R.
CUEVAS-FERNÁNDEZ, F. B.
BECERRA, S.
CROUCH, J.
BETTIOL, W.
AZCÁRATE-PERIL, M. A.
MALAPI-WIGHT, M.
ORTEGA, V.
BETRAN, J.
TENUTA, A.
DAMBOLENA, J. S.
ESKER, P. D.
REVILLA, P.
JACKSON-ZIEMS
HILTBRUNNER, J.
MUNKVOLD, G.
BUHINICEK, I.
VICENTE-VILLARDÓN, J. L.''''
SUKNO, S. A.
THON, M. R.
dc.subject.por.fl_str_mv Milho
Antracnose
Colletotrichum Graminicola
Variação Genética
Fungal diseases of plants
Anthracnose
Corn
Population genetics
Phylogeography
Genetic recombination
Genomics
topic Milho
Antracnose
Colletotrichum Graminicola
Variação Genética
Fungal diseases of plants
Anthracnose
Corn
Population genetics
Phylogeography
Genetic recombination
Genomics
description Abstract: Understanding the genetic diversity and mechanisms underlying genetic variation in pathogen populations is crucial to the development of effective control strategies. We investigated the genetic diversity and reproductive biology of Colletotrichum graminicola isolates which infect maize by sequencing the genomes of 108 isolates collected from 14 countries using restriction site-associated DNA sequencing (RAD-seq) and whole-genome sequencing (WGS). Clustering analyses based on single-nucleotide polymorphisms revealed three genetic groups delimited by continental origin, compatible with short-dispersal of the pathogen and geographic subdivision. Intra- and intercontinental migration was observed between Europe and South America, likely associated with the movement of contaminated germplasm. Low clonality, evidence of genetic recombination, and high phenotypic diversity were detected. We show evidence that, although it is rare (possibly due to losses of sexual reproduction- and meiosis-associated genes) C. graminicola can undergo sexual recombination. Our results support the hypotheses that intra- and intercontinental pathogen migration and genetic recombination have great impacts on the C. graminicola population structure. Importance: Plant pathogens cause significant reductions in yield and crop quality and cause enormous economic losses worldwide. Reducing these losses provides an obvious strategy to increase food production without further degrading natural ecosystems; however, this requires knowledge of the biology and evolution of the pathogens in agroecosystems. We employed a population genomics approach to investigate the genetic diversity and reproductive biology of the maize anthracnose pathogen (Colletotrichum graminicola) in 14 countries. We found that the populations are correlated with their geographical origin and that migration between countries is ongoing, possibly caused by the movement of infected plant material. This result has direct implications for disease management because migration can cause the movement of more virulent and/or fungicide-resistant genotypes. We conclude that genetic recombination is frequent (in contrast to the traditional view of C. graminicola being mainly asexual), which strongly impacts control measures and breeding programs aimed at controlling this disease.
publishDate 2022
dc.date.none.fl_str_mv 2022
2023-04-27T10:52:28Z
2023-04-27T10:52:28Z
2023-02-14
dc.type.driver.fl_str_mv info:eu-repo/semantics/publishedVersion
info:eu-repo/semantics/article
format article
status_str publishedVersion
dc.identifier.uri.fl_str_mv MBio, v. 14, n. 1, e0287822, 2022.
2150-7511
http://www.alice.cnptia.embrapa.br/alice/handle/doc/1151733
https://doi.org/10.1128/mbio.02878-22
identifier_str_mv MBio, v. 14, n. 1, e0287822, 2022.
2150-7511
url http://www.alice.cnptia.embrapa.br/alice/handle/doc/1151733
https://doi.org/10.1128/mbio.02878-22
dc.language.iso.fl_str_mv eng
language eng
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instname:Empresa Brasileira de Pesquisa Agropecuária (Embrapa)
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instname_str Empresa Brasileira de Pesquisa Agropecuária (Embrapa)
instacron_str EMBRAPA
institution EMBRAPA
reponame_str Repositório Institucional da EMBRAPA (Repository Open Access to Scientific Information from EMBRAPA - Alice)
collection Repositório Institucional da EMBRAPA (Repository Open Access to Scientific Information from EMBRAPA - Alice)
repository.name.fl_str_mv Repositório Institucional da EMBRAPA (Repository Open Access to Scientific Information from EMBRAPA - Alice) - Empresa Brasileira de Pesquisa Agropecuária (Embrapa)
repository.mail.fl_str_mv cg-riaa@embrapa.br
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