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Population genomic footprints of host adaptation, introgression and recombination in coffee leaf rust

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Resumo:Coffee leaf rust, caused by Hemileia vastatrix (Hv), represents the biggest threat to coffee production worldwide and ranks amongst the most serious fungal diseases in history. Despite a recent series of outbreaks and emergence of hypervirulent strains, the population evolutionary history and potential of this pathogen remain poorly understood. To address this issue, we used restriction site-associated DNA sequencing (RADseq) to generate ∼19 000 single nucleotide polymorphisms (SNPs) across a worldwide collection of 37 Hv samples. Contrary to the long-standing idea that Hv represents a genetically unstructured and cosmopolitan species, our results reveal the existence of a cryptic species complex with marked host tropism. Using phylogenetic and pathological data, we show that one of these lineages (C3) infects almost exclusively the most economically valuable coffee species (tetraploids that include Coffea arabica and interspecific hybrids), whereas the other lineages (C1 and C2) are severely maladapted to these hosts, but successfully infect diploid coffee species. Population dynamic analyses suggest that the C3 group may be a recent ‘domesticated’ lineage that emerged via host shift from diploid coffee hosts. We also found evidence of recombination occurring within this group, which could explain the high pace of pathotype emergence despite the low genetic variation. Moreover, genomic footprints of introgression between the C3 and C2 groups were discovered and raise the possibility that virulence factors may be quickly exchanged between groups with different pathogenic abilities. This work advances our understanding of the evolutionary strategies used by plant pathogens in agro-ecosystems with direct and far-reaching implications for disease control.
Autores principais:Silva, Diogo Nuno
Outros Autores:Várzea, Vítor; Paulo, Octávio S.; Batista, Dora
Ano:2018
País:Portugal
Tipo de documento:artigo
Tipo de acesso:acesso aberto
Instituição associada:Universidade de Lisboa
Idioma:inglês
Origem:Repositório da Universidade de Lisboa
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author Silva, Diogo Nuno
author2 Várzea, Vítor
Paulo, Octávio S.
Batista, Dora
author2_role author
author
author
author_facet Silva, Diogo Nuno
Várzea, Vítor
Paulo, Octávio S.
Batista, Dora
author_role author
contributor_name_str_mv Repositório Científico de Acesso Aberto da ULisboa
country_str PT
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datacite.contributors.contributor.contributorName.fl_str_mv Repositório Científico de Acesso Aberto da ULisboa
datacite.creators.creator.creatorName.fl_str_mv Silva, Diogo Nuno
Várzea, Vítor
Paulo, Octávio S.
Batista, Dora
datacite.date.Accepted.fl_str_mv 2018-07-01T00:00:00Z
datacite.date.available.fl_str_mv 2024-01-31T17:59:28Z
datacite.date.embargoed.fl_str_mv 2024-01-31T17:59:28Z
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datacite.titles.title.fl_str_mv Population genomic footprints of host adaptation, introgression and recombination in coffee leaf rust
dc.contributor.none.fl_str_mv Repositório Científico de Acesso Aberto da ULisboa
dc.creator.none.fl_str_mv Silva, Diogo Nuno
Várzea, Vítor
Paulo, Octávio S.
Batista, Dora
dc.date.Accepted.fl_str_mv 2018-07-01T00:00:00Z
dc.date.available.fl_str_mv 2024-01-31T17:59:28Z
dc.date.embargoed.fl_str_mv 2024-01-31T17:59:28Z
dc.format.none.fl_str_mv application/pdf
dc.identifier.none.fl_str_mv http://hdl.handle.net/10451/62349
dc.language.none.fl_str_mv eng
dc.publisher.none.fl_str_mv Wiley
dc.rights.cclincense.fl_str_mv http://creativecommons.org/licenses/by/4.0/
dc.rights.none.fl_str_mv http://purl.org/coar/access_right/c_abf2
dc.title.fl_str_mv Population genomic footprints of host adaptation, introgression and recombination in coffee leaf rust
dc.type.none.fl_str_mv http://purl.org/coar/resource_type/c_6501
description Coffee leaf rust, caused by Hemileia vastatrix (Hv), represents the biggest threat to coffee production worldwide and ranks amongst the most serious fungal diseases in history. Despite a recent series of outbreaks and emergence of hypervirulent strains, the population evolutionary history and potential of this pathogen remain poorly understood. To address this issue, we used restriction site-associated DNA sequencing (RADseq) to generate ∼19 000 single nucleotide polymorphisms (SNPs) across a worldwide collection of 37 Hv samples. Contrary to the long-standing idea that Hv represents a genetically unstructured and cosmopolitan species, our results reveal the existence of a cryptic species complex with marked host tropism. Using phylogenetic and pathological data, we show that one of these lineages (C3) infects almost exclusively the most economically valuable coffee species (tetraploids that include Coffea arabica and interspecific hybrids), whereas the other lineages (C1 and C2) are severely maladapted to these hosts, but successfully infect diploid coffee species. Population dynamic analyses suggest that the C3 group may be a recent ‘domesticated’ lineage that emerged via host shift from diploid coffee hosts. We also found evidence of recombination occurring within this group, which could explain the high pace of pathotype emergence despite the low genetic variation. Moreover, genomic footprints of introgression between the C3 and C2 groups were discovered and raise the possibility that virulence factors may be quickly exchanged between groups with different pathogenic abilities. This work advances our understanding of the evolutionary strategies used by plant pathogens in agro-ecosystems with direct and far-reaching implications for disease control.
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person_str_mv Silva, Diogo Nuno
Várzea, Vítor
Paulo, Octávio S.
Paulo, Octávio S.
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spelling engWileypt_PTCoffee leaf rust, caused by Hemileia vastatrix (Hv), represents the biggest threat to coffee production worldwide and ranks amongst the most serious fungal diseases in history. Despite a recent series of outbreaks and emergence of hypervirulent strains, the population evolutionary history and potential of this pathogen remain poorly understood. To address this issue, we used restriction site-associated DNA sequencing (RADseq) to generate ∼19 000 single nucleotide polymorphisms (SNPs) across a worldwide collection of 37 Hv samples. Contrary to the long-standing idea that Hv represents a genetically unstructured and cosmopolitan species, our results reveal the existence of a cryptic species complex with marked host tropism. Using phylogenetic and pathological data, we show that one of these lineages (C3) infects almost exclusively the most economically valuable coffee species (tetraploids that include Coffea arabica and interspecific hybrids), whereas the other lineages (C1 and C2) are severely maladapted to these hosts, but successfully infect diploid coffee species. Population dynamic analyses suggest that the C3 group may be a recent ‘domesticated’ lineage that emerged via host shift from diploid coffee hosts. We also found evidence of recombination occurring within this group, which could explain the high pace of pathotype emergence despite the low genetic variation. Moreover, genomic footprints of introgression between the C3 and C2 groups were discovered and raise the possibility that virulence factors may be quickly exchanged between groups with different pathogenic abilities. This work advances our understanding of the evolutionary strategies used by plant pathogens in agro-ecosystems with direct and far-reaching implications for disease control.application/pdfpt_PTPopulation genomic footprints of host adaptation, introgression and recombination in coffee leaf rustSilva, Diogo NunoVárzea, VítorPersonalPaulo, Octávio S.DSpacehttp://dspace.org/items/2be59178-7c2d-4df6-9d6f-3aaef29c0a53DSpacehttp://dspace.org/items/2be59178-7c2d-4df6-9d6f-3aaef29c0a53PauloOctávioCiência IDhttps://www.ciencia-id.pt471A-1219-9C5FORCIDhttp://orcid.org0000-0001-5408-5212Researcher IDhttps://www.researcherid.comD-9921-2011Scopus Author IDhttps://www.scopus.com6602677193Batista, DoraHostingInstitutionOrganizationalRepositório Científico de Acesso Aberto da ULisboae-mailmailto:repositorio@reitoria.ulisboa.ptrepositorio@reitoria.ulisboa.ptDOIIsPartOf10.1111/mpp.126572024-01-31T17:59:28Z2018-072018-07-01T00:00:00ZHandlehttp://hdl.handle.net/10451/62349http://purl.org/coar/access_right/c_abf2open access598874 bytesliteraturehttp://purl.org/coar/resource_type/c_6501journal article2018-07http://creativecommons.org/licenses/by/4.0/http://purl.org/coar/access_right/c_abf2application/pdffulltexthttps://repositorio.ulisboa.pt/bitstreams/7adabb67-9090-4ef6-86e9-ea4bee05091d/downloadMolecular Plant Pathology19717421753
spellingShingle Population genomic footprints of host adaptation, introgression and recombination in coffee leaf rust
Silva, Diogo Nuno
status SINGLETON
title Population genomic footprints of host adaptation, introgression and recombination in coffee leaf rust
title_full Population genomic footprints of host adaptation, introgression and recombination in coffee leaf rust
title_fullStr Population genomic footprints of host adaptation, introgression and recombination in coffee leaf rust
title_full_unstemmed Population genomic footprints of host adaptation, introgression and recombination in coffee leaf rust
title_short Population genomic footprints of host adaptation, introgression and recombination in coffee leaf rust
title_sort Population genomic footprints of host adaptation, introgression and recombination in coffee leaf rust
url http://hdl.handle.net/10451/62349
visible 1