Evolution and regulation of a large effector family of Pyricularia oryzae.
Identifieur interne : 000174 ( Main/Exploration ); précédent : 000173; suivant : 000175Evolution and regulation of a large effector family of Pyricularia oryzae.
Auteurs : Daniel J. Ebbole [États-Unis] ; Meilian Chen [États-Unis, Oman] ; Zhenhui Zhong [République populaire de Chine, Oman] ; Nicholas Farmer [États-Unis] ; Wenhui Zheng [Oman] ; Yijuan Han [Oman] ; Guodong Lu [Oman] ; Zonghua Wang [République populaire de Chine, Oman]Source :
- Molecular plant-microbe interactions : MPMI [ 0894-0282 ] ; 2020.
Abstract
Plant pathogen effectors play important roles in parasitism, including countering plant immunity. However, investigations of the emergence and diversification of fungal effectors across host-adapted populations has been limited. We previously identified a gene encoding a suppressor of plant cell death in Pyricularia oryzae (Syn. Magnaporthe oryzae). Here we report the gene is one of a 21-member gene family and we characterize sequence diversity in different populations. Within the rice pathogen population, nucleotide diversity is low, however, the majority of gene family members display presence-absence polymorphism or other null alleles. Gene family allelic diversity is greater between host-adapted populations and we thus named them host adapted genes (HAGs). Multiple copies of HAGs were found in some genome assemblies and sequence divergence between the alleles in two cases suggested they were the result of repeat-induced point mutagenesis. Transfer of family members between populations and novel HAG haplotypes resulting from apparent recombination were observed. HAG family transcripts were induced in planta and a subset of HAGs are dependent on a key regulator of pathogenesis, PMK1. We also found differential intron splicing for some HAGs that would prevent ex planta protein expression. For some genes, spliced transcript was expressed in anti-phase with an overlapping antisense transcript. Characterization of HAG expression patterns and allelic diversity reveal novel mechanisms for HAG regulation and mechanisms generating sequence diversity and novel allele combinations. This evidence of strong in planta-specific expression and selection operating on the HAG family is suggestive of a role in parasitism.
DOI: 10.1094/MPMI-07-20-0210-R
PubMed: 33211639
Affiliations:
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Ebbole</name><affiliation wicri:level="2"><nlm:affiliation>Texas A&M University College Station, 14736, Plant Pathology and Microbiology, College Station, Texas, United States; d-ebbole@tamu.edu.</nlm:affiliation><country wicri:rule="url">États-Unis</country><wicri:regionArea>Texas A&M University College Station, 14736, Plant Pathology and Microbiology, College Station, Texas</wicri:regionArea><placeName><region type="state">Texas</region></placeName></affiliation></author><author><name sortKey="Chen, Meilian" sort="Chen, Meilian" uniqKey="Chen M" first="Meilian" last="Chen">Meilian Chen</name><affiliation wicri:level="2"><nlm:affiliation>Texas A&M University College Station, 14736, Department of Plant Pathology & Microbiology, College Station, Texas, United States.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Texas A&M University College Station, 14736, Department of Plant Pathology & Microbiology, College Station, Texas</wicri:regionArea><placeName><region type="state">Texas</region></placeName></affiliation><affiliation wicri:level="1"><nlm:affiliation>Minjiang University, 26465, Institute of Oceanography, Fuzhou, Fujian, China; stellalian6@163.com.</nlm:affiliation><country wicri:rule="url">Oman</country><wicri:regionArea>Minjiang University, 26465, Institute of Oceanography, Fuzhou, Fujian</wicri:regionArea><wicri:noRegion>Fujian</wicri:noRegion></affiliation></author><author><name sortKey="Zhong, Zhenhui" sort="Zhong, Zhenhui" uniqKey="Zhong Z" first="Zhenhui" last="Zhong">Zhenhui Zhong</name><affiliation wicri:level="1"><nlm:affiliation>Fujian Agriculture and Forestry University, 12449, State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, College of Plant Protection, Fuzhou, Fujian, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Fujian Agriculture and Forestry University, 12449, State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, College of Plant Protection, Fuzhou, Fujian</wicri:regionArea><wicri:noRegion>Fujian</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>University of California Los Angeles, 8783, Department of Molecular, Cell and Developmental Biology, Los Angeles, California, United States; zhenhuizhong@gmail.com.</nlm:affiliation><country wicri:rule="url">Oman</country><wicri:regionArea>University of California Los Angeles, 8783, Department of Molecular, Cell and Developmental Biology, Los Angeles, California</wicri:regionArea><wicri:noRegion>California</wicri:noRegion></affiliation></author><author><name sortKey="Farmer, Nicholas" sort="Farmer, Nicholas" uniqKey="Farmer N" first="Nicholas" last="Farmer">Nicholas Farmer</name><affiliation wicri:level="2"><nlm:affiliation>Texas A&M University College Station, 14736, Plant Pathology and Microbiology, College Station, Texas, United States; nfarmer@tamu.edu.</nlm:affiliation><country wicri:rule="url">États-Unis</country><wicri:regionArea>Texas A&M University College Station, 14736, Plant Pathology and Microbiology, College Station, Texas</wicri:regionArea><placeName><region type="state">Texas</region></placeName></affiliation></author><author><name sortKey="Zheng, Wenhui" sort="Zheng, Wenhui" uniqKey="Zheng W" first="Wenhui" last="Zheng">Wenhui Zheng</name><affiliation wicri:level="1"><nlm:affiliation>Fujian Agriculture and Forestry University, 12449, State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, College of Plant Protection, Fuzhou, Fujian, China; wenhuiz@126.com.</nlm:affiliation><country wicri:rule="url">Oman</country><wicri:regionArea>Fujian Agriculture and Forestry University, 12449, State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, College of Plant Protection, Fuzhou, Fujian</wicri:regionArea><wicri:noRegion>Fujian</wicri:noRegion></affiliation></author><author><name sortKey="Han, Yijuan" sort="Han, Yijuan" uniqKey="Han Y" first="Yijuan" last="Han">Yijuan Han</name><affiliation wicri:level="1"><nlm:affiliation>Minjiang University, 26465, Institute of Oceanography, Fuzhou, Fujian, China; hanyijuan@126.com.</nlm:affiliation><country wicri:rule="url">Oman</country><wicri:regionArea>Minjiang University, 26465, Institute of Oceanography, Fuzhou, Fujian</wicri:regionArea><wicri:noRegion>Fujian</wicri:noRegion></affiliation></author><author><name sortKey="Lu, Guodong" sort="Lu, Guodong" uniqKey="Lu G" first="Guodong" last="Lu">Guodong Lu</name><affiliation wicri:level="1"><nlm:affiliation>Fujian Agriculture and Forestry University, 12449, State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, College of Plant Protection, Fuzhou, Fujian, China; gdlufafu@163.com.</nlm:affiliation><country wicri:rule="url">Oman</country><wicri:regionArea>Fujian Agriculture and Forestry University, 12449, State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, College of Plant Protection, Fuzhou, Fujian</wicri:regionArea><wicri:noRegion>Fujian</wicri:noRegion></affiliation></author><author><name sortKey="Wang, Zonghua" sort="Wang, Zonghua" uniqKey="Wang Z" first="Zonghua" last="Wang">Zonghua Wang</name><affiliation wicri:level="1"><nlm:affiliation>Fujian Agriculture and Forestry University, 12449, State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, College of Plant Protection, Fuzhou, Fujian, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Fujian Agriculture and Forestry University, 12449, State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, College of Plant Protection, Fuzhou, Fujian</wicri:regionArea><wicri:noRegion>Fujian</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Minjiang University, 26465, Institute of Oceanography, Fuzhou, Fujian, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Minjiang University, 26465, Institute of Oceanography, Fuzhou, Fujian</wicri:regionArea><wicri:noRegion>Fujian</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Fujian Agriculture and Forestry University, 12449, Fujian Universities Key Laboratory of Plant-Microbe Interactions, College of Life Science, Fuzhou, Fujian, China; zonghuaw@163.com.</nlm:affiliation><country wicri:rule="url">Oman</country><wicri:regionArea>Fujian Agriculture and Forestry University, 12449, Fujian Universities Key Laboratory of Plant-Microbe Interactions, College of Life Science, Fuzhou, Fujian</wicri:regionArea><wicri:noRegion>Fujian</wicri:noRegion></affiliation></author></analytic><series><title level="j">Molecular plant-microbe interactions : MPMI</title><idno type="ISSN">0894-0282</idno><imprint><date when="2020" type="published">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Plant pathogen effectors play important roles in parasitism, including countering plant immunity. However, investigations of the emergence and diversification of fungal effectors across host-adapted populations has been limited. We previously identified a gene encoding a suppressor of plant cell death in <i>Pyricularia oryzae</i> (Syn. <i>Magnaporthe oryzae</i>). Here we report the gene is one of a 21-member gene family and we characterize sequence diversity in different populations. Within the rice pathogen population, nucleotide diversity is low, however, the majority of gene family members display presence-absence polymorphism or other null alleles. Gene family allelic diversity is greater between host-adapted populations and we thus named them <i>h</i>ost <i>a</i>dapted <i>g</i>enes (<i>HAGs</i>). Multiple copies of <i>HAGs</i> were found in some genome assemblies and sequence divergence between the alleles in two cases suggested they were the result of repeat-induced point mutagenesis. Transfer of family members between populations and novel <i>HAG</i> haplotypes resulting from apparent recombination were observed. <i>HAG</i> family transcripts were induced <i>in planta</i> and a subset of <i>HAGs</i> are dependent on a key regulator of pathogenesis, <i>PMK1</i>. We also found differential intron splicing for some <i>HAGs</i> that would prevent <i>ex planta</i> protein expression. For some genes, spliced transcript was expressed in anti-phase with an overlapping antisense transcript. Characterization of <i>HAG</i> expression patterns and allelic diversity reveal novel mechanisms for <i>HAG</i> regulation and mechanisms generating sequence diversity and novel allele combinations. This evidence of strong <i>in planta</i>-specific expression and selection operating on the <i>HAG</i> family is suggestive of a role in parasitism.</div></front></TEI><pubmed><MedlineCitation Status="Publisher" Owner="NLM"><PMID Version="1">33211639</PMID><DateRevised><Year>2020</Year><Month>11</Month><Day>19</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Print">0894-0282</ISSN><JournalIssue CitedMedium="Print"><PubDate><Year>2020</Year><Month>Nov</Month><Day>19</Day></PubDate></JournalIssue><Title>Molecular plant-microbe interactions : MPMI</Title><ISOAbbreviation>Mol Plant Microbe Interact</ISOAbbreviation></Journal><ArticleTitle>Evolution and regulation of a large effector family of <i>Pyricularia oryzae</i>.</ArticleTitle><ELocationID EIdType="doi" ValidYN="Y">10.1094/MPMI-07-20-0210-R</ELocationID><Abstract><AbstractText>Plant pathogen effectors play important roles in parasitism, including countering plant immunity. However, investigations of the emergence and diversification of fungal effectors across host-adapted populations has been limited. We previously identified a gene encoding a suppressor of plant cell death in <i>Pyricularia oryzae</i> (Syn. <i>Magnaporthe oryzae</i>). Here we report the gene is one of a 21-member gene family and we characterize sequence diversity in different populations. Within the rice pathogen population, nucleotide diversity is low, however, the majority of gene family members display presence-absence polymorphism or other null alleles. Gene family allelic diversity is greater between host-adapted populations and we thus named them <i>h</i>ost <i>a</i>dapted <i>g</i>enes (<i>HAGs</i>). Multiple copies of <i>HAGs</i> were found in some genome assemblies and sequence divergence between the alleles in two cases suggested they were the result of repeat-induced point mutagenesis. Transfer of family members between populations and novel <i>HAG</i> haplotypes resulting from apparent recombination were observed. <i>HAG</i> family transcripts were induced <i>in planta</i> and a subset of <i>HAGs</i> are dependent on a key regulator of pathogenesis, <i>PMK1</i>. We also found differential intron splicing for some <i>HAGs</i> that would prevent <i>ex planta</i> protein expression. For some genes, spliced transcript was expressed in anti-phase with an overlapping antisense transcript. Characterization of <i>HAG</i> expression patterns and allelic diversity reveal novel mechanisms for <i>HAG</i> regulation and mechanisms generating sequence diversity and novel allele combinations. This evidence of strong <i>in planta</i>-specific expression and selection operating on the <i>HAG</i> family is suggestive of a role in parasitism.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Ebbole</LastName><ForeName>Daniel J</ForeName><Initials>DJ</Initials><AffiliationInfo><Affiliation>Texas A&M University College Station, 14736, Plant Pathology and Microbiology, College Station, Texas, United States; d-ebbole@tamu.edu.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Chen</LastName><ForeName>Meilian</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>Texas A&M University College Station, 14736, Department of Plant Pathology & Microbiology, College Station, Texas, United States.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Minjiang University, 26465, Institute of Oceanography, Fuzhou, Fujian, China; stellalian6@163.com.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zhong</LastName><ForeName>Zhenhui</ForeName><Initials>Z</Initials><AffiliationInfo><Affiliation>Fujian Agriculture and Forestry University, 12449, State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, College of Plant Protection, Fuzhou, Fujian, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>University of California Los Angeles, 8783, Department of Molecular, Cell and Developmental Biology, Los Angeles, California, United States; zhenhuizhong@gmail.com.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Farmer</LastName><ForeName>Nicholas</ForeName><Initials>N</Initials><AffiliationInfo><Affiliation>Texas A&M University College Station, 14736, Plant Pathology and Microbiology, College Station, Texas, United States; nfarmer@tamu.edu.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zheng</LastName><ForeName>Wenhui</ForeName><Initials>W</Initials><AffiliationInfo><Affiliation>Fujian Agriculture and Forestry University, 12449, State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, College of Plant Protection, Fuzhou, Fujian, China; wenhuiz@126.com.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Han</LastName><ForeName>Yijuan</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>Minjiang University, 26465, Institute of Oceanography, Fuzhou, Fujian, China; hanyijuan@126.com.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Lu</LastName><ForeName>Guodong</ForeName><Initials>G</Initials><AffiliationInfo><Affiliation>Fujian Agriculture and Forestry University, 12449, State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, College of Plant Protection, Fuzhou, Fujian, China; gdlufafu@163.com.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wang</LastName><ForeName>Zonghua</ForeName><Initials>Z</Initials><AffiliationInfo><Affiliation>Fujian Agriculture and Forestry University, 12449, State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, College of Plant Protection, Fuzhou, Fujian, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Minjiang University, 26465, Institute of Oceanography, Fuzhou, Fujian, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Fujian Agriculture and Forestry University, 12449, Fujian Universities Key Laboratory of Plant-Microbe Interactions, College of Life Science, Fuzhou, Fujian, China; zonghuaw@163.com.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>11</Month><Day>19</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>Mol Plant Microbe Interact</MedlineTA><NlmUniqueID>9107902</NlmUniqueID><ISSNLinking>0894-0282</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="entrez"><Year>2020</Year><Month>11</Month><Day>19</Day><Hour>17</Hour><Minute>10</Minute></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2020</Year><Month>11</Month><Day>20</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>11</Month><Day>20</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>aheadofprint</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">33211639</ArticleId><ArticleId IdType="doi">10.1094/MPMI-07-20-0210-R</ArticleId></ArticleIdList></PubmedData></pubmed><affiliations><list><country><li>Oman</li><li>République populaire de Chine</li><li>États-Unis</li></country><region><li>Texas</li></region></list><tree><country name="États-Unis"><region name="Texas"><name sortKey="Ebbole, Daniel J" sort="Ebbole, Daniel J" uniqKey="Ebbole D" first="Daniel J" last="Ebbole">Daniel J. Ebbole</name></region><name sortKey="Chen, Meilian" sort="Chen, Meilian" uniqKey="Chen M" first="Meilian" last="Chen">Meilian Chen</name><name sortKey="Farmer, Nicholas" sort="Farmer, Nicholas" uniqKey="Farmer N" first="Nicholas" last="Farmer">Nicholas Farmer</name></country><country name="Oman"><noRegion><name sortKey="Chen, Meilian" sort="Chen, Meilian" uniqKey="Chen M" first="Meilian" last="Chen">Meilian Chen</name></noRegion><name sortKey="Han, Yijuan" sort="Han, Yijuan" uniqKey="Han Y" first="Yijuan" last="Han">Yijuan Han</name><name sortKey="Lu, Guodong" sort="Lu, Guodong" uniqKey="Lu G" first="Guodong" last="Lu">Guodong Lu</name><name sortKey="Wang, Zonghua" sort="Wang, Zonghua" uniqKey="Wang Z" first="Zonghua" last="Wang">Zonghua Wang</name><name sortKey="Zheng, Wenhui" sort="Zheng, Wenhui" uniqKey="Zheng W" first="Wenhui" last="Zheng">Wenhui Zheng</name><name sortKey="Zhong, Zhenhui" sort="Zhong, Zhenhui" uniqKey="Zhong Z" first="Zhenhui" last="Zhong">Zhenhui Zhong</name></country><country name="République populaire de Chine"><noRegion><name sortKey="Zhong, Zhenhui" sort="Zhong, Zhenhui" uniqKey="Zhong Z" first="Zhenhui" last="Zhong">Zhenhui Zhong</name></noRegion><name sortKey="Wang, Zonghua" sort="Wang, Zonghua" uniqKey="Wang Z" first="Zonghua" last="Wang">Zonghua Wang</name><name sortKey="Wang, Zonghua" sort="Wang, Zonghua" uniqKey="Wang Z" first="Zonghua" last="Wang">Zonghua Wang</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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|texte= Evolution and regulation of a large effector family of Pyricularia oryzae.
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