Whole Genome Re-sequencing Reveals Natural Variation and Adaptive Evolution of Phytophthora sojae.
Identifieur interne : 000346 ( Main/Exploration ); précédent : 000345; suivant : 000347Whole Genome Re-sequencing Reveals Natural Variation and Adaptive Evolution of Phytophthora sojae.
Auteurs : Xiong Zhang [République populaire de Chine] ; Bo Liu [République populaire de Chine] ; Fen Zou [République populaire de Chine] ; Danyu Shen [République populaire de Chine] ; Zhiyuan Yin [République populaire de Chine] ; Rongbo Wang [République populaire de Chine] ; Feng He [République populaire de Chine] ; Yuanchao Wang [République populaire de Chine] ; Brett M. Tyler [États-Unis] ; Wei Fan [République populaire de Chine] ; Wanqiang Qian [République populaire de Chine] ; Daolong Dou [République populaire de Chine]Source :
- Frontiers in microbiology [ 1664-302X ] ; 2019.
Abstract
Due to the monocultural basis of agricultural crops, mutated plant microbes with increased pathogenicity can easily spread in the field and lead to serious yield losses. As a major threat to a wide range of crop plants, oomycete pathogens continuously undergo adaptive evolution to overcome plant defense barriers. However, the genetic basis of their evolution at the molecular level remains largely unknown. Here, we investigated the nature variation and the population genomics of the soybean pathogen Phytophthora sojae by high-throughput genome re-sequencing. Genomic variation analysis revealed uneven "two-speed" evolutionary pattern with genes in gene-sparse regions (GSRs) showing higher rates of structural polymorphisms and positive selection. GSRs are enriched in effector genes and transposase-related genes. Our results also suggested that the NADH oxidase and MIP transporter gene families undergo rapid and diversifying selection. Furthermore, we demonstrated that P. sojae isolates possess varying numbers of RxLR effectors with diverse sequences, totaling 471 members. Among them, 42 core RxLR effectors are assumed to be important for infection. Finally, we observed that Avr genes exhibit abundant sequence variation in P. sojae isolates. Several novel variants lead to the evading of host resistance, including a complete deletion in Avr3c and amino acid mutations in Avr1a. Taken together, our results provide an adaptive landscape of P. sojae at single-nucleotide resolution, as well as resources for further resistance breeding and disease prevention against this important plant pathogen.
DOI: 10.3389/fmicb.2019.02792
PubMed: 31849921
PubMed Central: PMC6895562
Affiliations:
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wicri:level="1"><nlm:affiliation>Department of Plant Pathology, Nanjing Agricultural University, Nanjing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Plant Pathology, Nanjing Agricultural University, Nanjing</wicri:regionArea><wicri:noRegion>Nanjing</wicri:noRegion></affiliation></author><author><name sortKey="Shen, Danyu" sort="Shen, Danyu" uniqKey="Shen D" first="Danyu" last="Shen">Danyu Shen</name><affiliation wicri:level="1"><nlm:affiliation>Department of Plant Pathology, Nanjing Agricultural University, Nanjing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Plant Pathology, Nanjing Agricultural University, Nanjing</wicri:regionArea><wicri:noRegion>Nanjing</wicri:noRegion></affiliation></author><author><name sortKey="Yin, Zhiyuan" sort="Yin, Zhiyuan" uniqKey="Yin Z" first="Zhiyuan" last="Yin">Zhiyuan Yin</name><affiliation wicri:level="3"><nlm:affiliation>Department of Plant Pathology, China Agricultural University, Beijing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Plant Pathology, China Agricultural University, Beijing</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Wang, Rongbo" sort="Wang, Rongbo" uniqKey="Wang R" first="Rongbo" last="Wang">Rongbo Wang</name><affiliation wicri:level="1"><nlm:affiliation>Department of Plant Pathology, Nanjing Agricultural University, Nanjing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Plant Pathology, Nanjing Agricultural University, Nanjing</wicri:regionArea><wicri:noRegion>Nanjing</wicri:noRegion></affiliation></author><author><name sortKey="He, Feng" sort="He, Feng" uniqKey="He F" first="Feng" last="He">Feng He</name><affiliation wicri:level="1"><nlm:affiliation>Department of Plant Pathology, Nanjing Agricultural University, Nanjing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Plant Pathology, Nanjing Agricultural University, Nanjing</wicri:regionArea><wicri:noRegion>Nanjing</wicri:noRegion></affiliation></author><author><name sortKey="Wang, Yuanchao" sort="Wang, Yuanchao" uniqKey="Wang Y" first="Yuanchao" last="Wang">Yuanchao Wang</name><affiliation wicri:level="1"><nlm:affiliation>Department of Plant Pathology, Nanjing Agricultural University, Nanjing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Plant Pathology, Nanjing Agricultural University, Nanjing</wicri:regionArea><wicri:noRegion>Nanjing</wicri:noRegion></affiliation></author><author><name sortKey="Tyler, Brett M" sort="Tyler, Brett M" uniqKey="Tyler B" first="Brett M" last="Tyler">Brett M. Tyler</name><affiliation wicri:level="2"><nlm:affiliation>Center for Genome Research and Biocomputing, Oregon State University, Corvallis, OR, United States.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Center for Genome Research and Biocomputing, Oregon State University, Corvallis, OR</wicri:regionArea><placeName><region type="state">Oregon</region></placeName></affiliation></author><author><name sortKey="Fan, Wei" sort="Fan, Wei" uniqKey="Fan W" first="Wei" last="Fan">Wei Fan</name><affiliation wicri:level="3"><nlm:affiliation>Agricultural Genomic Institute, Chinese Academy of Agricultural Sciences, Shenzhen, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Agricultural Genomic Institute, Chinese Academy of Agricultural Sciences, Shenzhen</wicri:regionArea><placeName><settlement type="city">Shenzhen</settlement><region type="province">Guangdong</region></placeName></affiliation></author><author><name sortKey="Qian, Wanqiang" sort="Qian, Wanqiang" uniqKey="Qian W" first="Wanqiang" last="Qian">Wanqiang Qian</name><affiliation wicri:level="3"><nlm:affiliation>Agricultural Genomic Institute, Chinese Academy of Agricultural Sciences, Shenzhen, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Agricultural Genomic Institute, Chinese Academy of Agricultural Sciences, Shenzhen</wicri:regionArea><placeName><settlement type="city">Shenzhen</settlement><region type="province">Guangdong</region></placeName></affiliation></author><author><name sortKey="Dou, Daolong" sort="Dou, Daolong" uniqKey="Dou D" first="Daolong" last="Dou">Daolong Dou</name><affiliation wicri:level="1"><nlm:affiliation>Department of Plant Pathology, Nanjing Agricultural University, Nanjing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Plant Pathology, Nanjing Agricultural University, Nanjing</wicri:regionArea><wicri:noRegion>Nanjing</wicri:noRegion></affiliation><affiliation wicri:level="3"><nlm:affiliation>Department of Plant Pathology, China Agricultural University, Beijing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Plant Pathology, China Agricultural University, Beijing</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author></analytic><series><title level="j">Frontiers in microbiology</title><idno type="ISSN">1664-302X</idno><imprint><date when="2019" type="published">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Due to the monocultural basis of agricultural crops, mutated plant microbes with increased pathogenicity can easily spread in the field and lead to serious yield losses. As a major threat to a wide range of crop plants, oomycete pathogens continuously undergo adaptive evolution to overcome plant defense barriers. However, the genetic basis of their evolution at the molecular level remains largely unknown. Here, we investigated the nature variation and the population genomics of the soybean pathogen <i>Phytophthora sojae</i> by high-throughput genome re-sequencing. Genomic variation analysis revealed uneven "two-speed" evolutionary pattern with genes in gene-sparse regions (GSRs) showing higher rates of structural polymorphisms and positive selection. GSRs are enriched in effector genes and transposase-related genes. Our results also suggested that the NADH oxidase and MIP transporter gene families undergo rapid and diversifying selection. Furthermore, we demonstrated that <i>P. sojae</i> isolates possess varying numbers of RxLR effectors with diverse sequences, totaling 471 members. Among them, 42 core RxLR effectors are assumed to be important for infection. Finally, we observed that <i>Avr</i> genes exhibit abundant sequence variation in <i>P. sojae</i> isolates. Several novel variants lead to the evading of host resistance, including a complete deletion in <i>Avr3c</i> and amino acid mutations in <i>Avr1a</i>. Taken together, our results provide an adaptive landscape of <i>P. sojae</i> at single-nucleotide resolution, as well as resources for further resistance breeding and disease prevention against this important plant pathogen.</div></front></TEI><pubmed><MedlineCitation Status="PubMed-not-MEDLINE" Owner="NLM"><PMID Version="1">31849921</PMID><DateRevised><Year>2020</Year><Month>10</Month><Day>01</Day></DateRevised><Article PubModel="Electronic-eCollection"><Journal><ISSN IssnType="Print">1664-302X</ISSN><JournalIssue CitedMedium="Print"><Volume>10</Volume><PubDate><Year>2019</Year></PubDate></JournalIssue><Title>Frontiers in microbiology</Title><ISOAbbreviation>Front Microbiol</ISOAbbreviation></Journal><ArticleTitle>Whole Genome Re-sequencing Reveals Natural Variation and Adaptive Evolution of <i>Phytophthora sojae</i>.</ArticleTitle><Pagination><MedlinePgn>2792</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.3389/fmicb.2019.02792</ELocationID><Abstract><AbstractText>Due to the monocultural basis of agricultural crops, mutated plant microbes with increased pathogenicity can easily spread in the field and lead to serious yield losses. As a major threat to a wide range of crop plants, oomycete pathogens continuously undergo adaptive evolution to overcome plant defense barriers. However, the genetic basis of their evolution at the molecular level remains largely unknown. Here, we investigated the nature variation and the population genomics of the soybean pathogen <i>Phytophthora sojae</i> by high-throughput genome re-sequencing. Genomic variation analysis revealed uneven "two-speed" evolutionary pattern with genes in gene-sparse regions (GSRs) showing higher rates of structural polymorphisms and positive selection. GSRs are enriched in effector genes and transposase-related genes. Our results also suggested that the NADH oxidase and MIP transporter gene families undergo rapid and diversifying selection. Furthermore, we demonstrated that <i>P. sojae</i> isolates possess varying numbers of RxLR effectors with diverse sequences, totaling 471 members. Among them, 42 core RxLR effectors are assumed to be important for infection. Finally, we observed that <i>Avr</i> genes exhibit abundant sequence variation in <i>P. sojae</i> isolates. Several novel variants lead to the evading of host resistance, including a complete deletion in <i>Avr3c</i> and amino acid mutations in <i>Avr1a</i>. Taken together, our results provide an adaptive landscape of <i>P. sojae</i> at single-nucleotide resolution, as well as resources for further resistance breeding and disease prevention against this important plant pathogen.</AbstractText><CopyrightInformation>Copyright © 2019 Zhang, Liu, Zou, Shen, Yin, Wang, He, Wang, Tyler, Fan, Qian and Dou.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Zhang</LastName><ForeName>Xiong</ForeName><Initials>X</Initials><AffiliationInfo><Affiliation>Department of Plant Pathology, Nanjing Agricultural University, Nanjing, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Plant Pathology, China Agricultural University, Beijing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Liu</LastName><ForeName>Bo</ForeName><Initials>B</Initials><AffiliationInfo><Affiliation>Agricultural Genomic Institute, Chinese Academy of Agricultural Sciences, Shenzhen, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zou</LastName><ForeName>Fen</ForeName><Initials>F</Initials><AffiliationInfo><Affiliation>Department of Plant Pathology, Nanjing Agricultural University, Nanjing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Shen</LastName><ForeName>Danyu</ForeName><Initials>D</Initials><AffiliationInfo><Affiliation>Department of Plant Pathology, Nanjing Agricultural University, Nanjing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Yin</LastName><ForeName>Zhiyuan</ForeName><Initials>Z</Initials><AffiliationInfo><Affiliation>Department of Plant Pathology, China Agricultural University, Beijing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wang</LastName><ForeName>Rongbo</ForeName><Initials>R</Initials><AffiliationInfo><Affiliation>Department of Plant Pathology, Nanjing Agricultural University, Nanjing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>He</LastName><ForeName>Feng</ForeName><Initials>F</Initials><AffiliationInfo><Affiliation>Department of Plant Pathology, Nanjing Agricultural University, Nanjing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wang</LastName><ForeName>Yuanchao</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>Department of Plant Pathology, Nanjing Agricultural University, Nanjing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Tyler</LastName><ForeName>Brett M</ForeName><Initials>BM</Initials><AffiliationInfo><Affiliation>Center for Genome Research and Biocomputing, Oregon State University, Corvallis, OR, United States.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Fan</LastName><ForeName>Wei</ForeName><Initials>W</Initials><AffiliationInfo><Affiliation>Agricultural Genomic Institute, Chinese Academy of Agricultural Sciences, Shenzhen, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Qian</LastName><ForeName>Wanqiang</ForeName><Initials>W</Initials><AffiliationInfo><Affiliation>Agricultural Genomic Institute, Chinese Academy of Agricultural Sciences, Shenzhen, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Dou</LastName><ForeName>Daolong</ForeName><Initials>D</Initials><AffiliationInfo><Affiliation>Department of Plant Pathology, Nanjing Agricultural University, Nanjing, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Plant Pathology, China Agricultural University, Beijing, China.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2019</Year><Month>11</Month><Day>29</Day></ArticleDate></Article><MedlineJournalInfo><Country>Switzerland</Country><MedlineTA>Front Microbiol</MedlineTA><NlmUniqueID>101548977</NlmUniqueID><ISSNLinking>1664-302X</ISSNLinking></MedlineJournalInfo><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">Phytophthora sojae</Keyword><Keyword MajorTopicYN="N">RxLR effectors</Keyword><Keyword MajorTopicYN="N">adaptive evolution</Keyword><Keyword MajorTopicYN="N">avirulent genes</Keyword><Keyword MajorTopicYN="N">genome re-sequencing</Keyword><Keyword MajorTopicYN="N">natural variation</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2019</Year><Month>09</Month><Day>05</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2019</Year><Month>11</Month><Day>18</Day></PubMedPubDate><PubMedPubDate 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