Divergent and convergent modes of interaction between wheat and Puccinia graminis f. sp. tritici isolates revealed by the comparative gene co-expression network and genome analyses.
Identifieur interne : 000063 ( Main/Curation ); précédent : 000062; suivant : 000064Divergent and convergent modes of interaction between wheat and Puccinia graminis f. sp. tritici isolates revealed by the comparative gene co-expression network and genome analyses.
Auteurs : William B. Rutter [États-Unis] ; Andres Salcedo [États-Unis] ; Alina Akhunova [États-Unis] ; Fei He [États-Unis] ; Shichen Wang [États-Unis] ; Hanquan Liang [États-Unis, République populaire de Chine] ; Robert L. Bowden [États-Unis] ; Eduard Akhunov [États-Unis]Source :
- BMC genomics [ 1471-2164 ] ; 2017.
Descripteurs français
- KwdFr :
- Analyse de profil d'expression de gènes (méthodes), Analyse de séquence d'ADN (méthodes), Analyse de séquence d'ARN (méthodes), Basidiomycota (classification), Basidiomycota (génétique), Basidiomycota (isolement et purification), Feuilles de plante (génétique), Feuilles de plante (microbiologie), Gènes fongiques (MeSH), Interactions hôte-pathogène (MeSH), Maladies des plantes (génétique), Maladies des plantes (microbiologie), Protéines végétales (génétique), Régulation de l'expression des gènes végétaux (MeSH), Réseaux de régulation génique (MeSH), Séquence conservée (MeSH), Séquence nucléotidique (MeSH), Tiges de plante (génétique), Tiges de plante (microbiologie), Triticum (génétique), Triticum (microbiologie), Évolution moléculaire (MeSH).
- MESH :
- génétique : Basidiomycota, Feuilles de plante, Maladies des plantes, Protéines végétales, Tiges de plante, Triticum.
- isolement et purification : Basidiomycota.
- microbiologie : Feuilles de plante, Maladies des plantes, Tiges de plante, Triticum.
- méthodes : Analyse de profil d'expression de gènes, Analyse de séquence d'ADN, Analyse de séquence d'ARN.
- Gènes fongiques, Interactions hôte-pathogène, Régulation de l'expression des gènes végétaux, Réseaux de régulation génique, Séquence conservée, Séquence nucléotidique, Évolution moléculaire.
English descriptors
- KwdEn :
- Base Sequence (MeSH), Basidiomycota (classification), Basidiomycota (genetics), Basidiomycota (isolation & purification), Conserved Sequence (MeSH), Evolution, Molecular (MeSH), Gene Expression Profiling (methods), Gene Expression Regulation, Plant (MeSH), Gene Regulatory Networks (MeSH), Genes, Fungal (MeSH), Host-Pathogen Interactions (MeSH), Plant Diseases (genetics), Plant Diseases (microbiology), Plant Leaves (genetics), Plant Leaves (microbiology), Plant Proteins (genetics), Plant Stems (genetics), Plant Stems (microbiology), Sequence Analysis, DNA (methods), Sequence Analysis, RNA (methods), Triticum (genetics), Triticum (microbiology).
- MESH :
- chemical , genetics : Plant Proteins.
- classification : Basidiomycota.
- genetics : Basidiomycota, Plant Diseases, Plant Leaves, Plant Stems, Triticum.
- isolation & purification : Basidiomycota.
- methods : Gene Expression Profiling, Sequence Analysis, DNA, Sequence Analysis, RNA.
- microbiology : Plant Diseases, Plant Leaves, Plant Stems, Triticum.
- Base Sequence, Conserved Sequence, Evolution, Molecular, Gene Expression Regulation, Plant, Gene Regulatory Networks, Genes, Fungal, Host-Pathogen Interactions.
Abstract
BACKGROUND
Two opposing evolutionary constraints exert pressure on plant pathogens: one to diversify virulence factors in order to evade plant defenses, and the other to retain virulence factors critical for maintaining a compatible interaction with the plant host. To better understand how the diversified arsenals of fungal genes promote interaction with the same compatible wheat line, we performed a comparative genomic analysis of two North American isolates of Puccinia graminis f. sp. tritici (Pgt).
RESULTS
The patterns of inter-isolate divergence in the secreted candidate effector genes were compared with the levels of conservation and divergence of plant-pathogen gene co-expression networks (GCN) developed for each isolate. Comprative genomic analyses revealed substantial level of interisolate divergence in effector gene complement and sequence divergence. Gene Ontology (GO) analyses of the conserved and unique parts of the isolate-specific GCNs identified a number of conserved host pathways targeted by both isolates. Interestingly, the degree of inter-isolate sub-network conservation varied widely for the different host pathways and was positively associated with the proportion of conserved effector candidates associated with each sub-network. While different Pgt isolates tended to exploit similar wheat pathways for infection, the mode of plant-pathogen interaction varied for different pathways with some pathways being associated with the conserved set of effectors and others being linked with the diverged or isolate-specific effectors.
CONCLUSIONS
Our data suggest that at the intra-species level pathogen populations likely maintain divergent sets of effectors capable of targeting the same plant host pathways. This functional redundancy may play an important role in the dynamic of the "arms-race" between host and pathogen serving as the basis for diverse virulence strategies and creating conditions where mutations in certain effector groups will not have a major effect on the pathogen's ability to infect the host.
DOI: 10.1186/s12864-017-3678-6
PubMed: 28403814
PubMed Central: PMC5389088
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Rutter</name><affiliation wicri:level="1"><nlm:affiliation>Department of Plant Pathology, Kansas State University, Manhattan, KS, 66506, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Plant Pathology, Kansas State University, Manhattan, KS, 66506</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:affiliation>USDA-ARS, U.S. Vegetable Laboratory, 2700 Savannah Highway, Charleston, SC, 29414, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>USDA-ARS, U.S. Vegetable Laboratory, 2700 Savannah Highway, Charleston, SC, 29414</wicri:regionArea></affiliation></author><author><name sortKey="Salcedo, Andres" sort="Salcedo, Andres" uniqKey="Salcedo A" first="Andres" last="Salcedo">Andres Salcedo</name><affiliation wicri:level="1"><nlm:affiliation>Department of Plant Pathology, Kansas State University, Manhattan, KS, 66506, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Plant Pathology, Kansas State University, Manhattan, KS, 66506</wicri:regionArea></affiliation></author><author><name sortKey="Akhunova, Alina" sort="Akhunova, Alina" uniqKey="Akhunova A" first="Alina" last="Akhunova">Alina Akhunova</name><affiliation wicri:level="1"><nlm:affiliation>Integrated Genomics Facility, Kansas State University, Manhattan, KS, 66506, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Integrated Genomics Facility, Kansas State University, Manhattan, KS, 66506</wicri:regionArea></affiliation></author><author><name sortKey="He, Fei" sort="He, Fei" uniqKey="He F" first="Fei" last="He">Fei He</name><affiliation wicri:level="1"><nlm:affiliation>Department of Plant Pathology, Kansas State University, Manhattan, KS, 66506, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Plant Pathology, Kansas State University, Manhattan, KS, 66506</wicri:regionArea></affiliation></author><author><name sortKey="Wang, Shichen" sort="Wang, Shichen" uniqKey="Wang S" first="Shichen" last="Wang">Shichen Wang</name><affiliation wicri:level="1"><nlm:affiliation>Department of Plant Pathology, Kansas State University, Manhattan, KS, 66506, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Plant Pathology, Kansas State University, Manhattan, KS, 66506</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:affiliation>TEES-AgriLife Center for Bioinformatics and Genomic Systems Engineering, Texas A&M University, 101 Gateway, Suite A, College Station, TX, 77845, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>TEES-AgriLife Center for Bioinformatics and Genomic Systems Engineering, Texas A&M University, 101 Gateway, Suite A, College Station, TX, 77845</wicri:regionArea></affiliation></author><author><name sortKey="Liang, Hanquan" sort="Liang, Hanquan" uniqKey="Liang H" first="Hanquan" last="Liang">Hanquan Liang</name><affiliation wicri:level="1"><nlm:affiliation>Integrated Genomics Facility, Kansas State University, Manhattan, KS, 66506, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Integrated Genomics Facility, Kansas State University, Manhattan, KS, 66506</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:affiliation>School of Data and Computer Science, Sun Yat-sen University, Guangzhou, 510006, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>School of Data and Computer Science, Sun Yat-sen University, Guangzhou, 510006</wicri:regionArea></affiliation></author><author><name sortKey="Bowden, Robert L" sort="Bowden, Robert L" uniqKey="Bowden R" first="Robert L" last="Bowden">Robert L. Bowden</name><affiliation wicri:level="1"><nlm:affiliation>USDA ARS, Hard Winter Wheat Genetics Research Unit, Throckmorton Plant Sciences Center, Manhattan, KS, 66506, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>USDA ARS, Hard Winter Wheat Genetics Research Unit, Throckmorton Plant Sciences Center, Manhattan, KS, 66506</wicri:regionArea></affiliation></author><author><name sortKey="Akhunov, Eduard" sort="Akhunov, Eduard" uniqKey="Akhunov E" first="Eduard" last="Akhunov">Eduard Akhunov</name><affiliation wicri:level="1"><nlm:affiliation>Department of Plant Pathology, Kansas State University, Manhattan, KS, 66506, USA. eakhunov@ksu.edu.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Plant Pathology, Kansas State University, Manhattan, KS, 66506</wicri:regionArea></affiliation></author></analytic><series><title level="j">BMC genomics</title><idno type="eISSN">1471-2164</idno><imprint><date when="2017" type="published">2017</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Base Sequence (MeSH)</term><term>Basidiomycota (classification)</term><term>Basidiomycota (genetics)</term><term>Basidiomycota (isolation & purification)</term><term>Conserved Sequence (MeSH)</term><term>Evolution, Molecular (MeSH)</term><term>Gene Expression Profiling (methods)</term><term>Gene Expression Regulation, Plant (MeSH)</term><term>Gene Regulatory Networks (MeSH)</term><term>Genes, Fungal (MeSH)</term><term>Host-Pathogen Interactions (MeSH)</term><term>Plant Diseases (genetics)</term><term>Plant Diseases (microbiology)</term><term>Plant Leaves (genetics)</term><term>Plant Leaves (microbiology)</term><term>Plant Proteins (genetics)</term><term>Plant Stems (genetics)</term><term>Plant Stems (microbiology)</term><term>Sequence Analysis, DNA (methods)</term><term>Sequence Analysis, RNA (methods)</term><term>Triticum (genetics)</term><term>Triticum (microbiology)</term></keywords><keywords scheme="KwdFr" xml:lang="fr"><term>Analyse de profil d'expression de gènes (méthodes)</term><term>Analyse de séquence d'ADN (méthodes)</term><term>Analyse de séquence d'ARN (méthodes)</term><term>Basidiomycota (classification)</term><term>Basidiomycota (génétique)</term><term>Basidiomycota (isolement et purification)</term><term>Feuilles de plante (génétique)</term><term>Feuilles de plante (microbiologie)</term><term>Gènes fongiques (MeSH)</term><term>Interactions hôte-pathogène (MeSH)</term><term>Maladies des plantes (génétique)</term><term>Maladies des plantes (microbiologie)</term><term>Protéines végétales (génétique)</term><term>Régulation de l'expression des gènes végétaux (MeSH)</term><term>Réseaux de régulation génique (MeSH)</term><term>Séquence conservée (MeSH)</term><term>Séquence nucléotidique (MeSH)</term><term>Tiges de plante (génétique)</term><term>Tiges de plante (microbiologie)</term><term>Triticum (génétique)</term><term>Triticum (microbiologie)</term><term>Évolution moléculaire (MeSH)</term></keywords><keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en"><term>Plant Proteins</term></keywords><keywords scheme="MESH" qualifier="classification" xml:lang="en"><term>Basidiomycota</term></keywords><keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Basidiomycota</term><term>Plant Diseases</term><term>Plant Leaves</term><term>Plant Stems</term><term>Triticum</term></keywords><keywords scheme="MESH" qualifier="génétique" xml:lang="fr"><term>Basidiomycota</term><term>Feuilles de plante</term><term>Maladies des plantes</term><term>Protéines végétales</term><term>Tiges de plante</term><term>Triticum</term></keywords><keywords scheme="MESH" qualifier="isolation & purification" xml:lang="en"><term>Basidiomycota</term></keywords><keywords scheme="MESH" qualifier="isolement et purification" xml:lang="fr"><term>Basidiomycota</term></keywords><keywords scheme="MESH" qualifier="methods" xml:lang="en"><term>Gene Expression Profiling</term><term>Sequence Analysis, DNA</term><term>Sequence Analysis, RNA</term></keywords><keywords scheme="MESH" qualifier="microbiologie" xml:lang="fr"><term>Feuilles de plante</term><term>Maladies des plantes</term><term>Tiges de plante</term><term>Triticum</term></keywords><keywords scheme="MESH" qualifier="microbiology" xml:lang="en"><term>Plant Diseases</term><term>Plant Leaves</term><term>Plant Stems</term><term>Triticum</term></keywords><keywords scheme="MESH" qualifier="méthodes" xml:lang="fr"><term>Analyse de profil d'expression de gènes</term><term>Analyse de séquence d'ADN</term><term>Analyse de séquence d'ARN</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Base Sequence</term><term>Conserved Sequence</term><term>Evolution, Molecular</term><term>Gene Expression Regulation, Plant</term><term>Gene Regulatory Networks</term><term>Genes, Fungal</term><term>Host-Pathogen Interactions</term></keywords><keywords scheme="MESH" xml:lang="fr"><term>Gènes fongiques</term><term>Interactions hôte-pathogène</term><term>Régulation de l'expression des gènes végétaux</term><term>Réseaux de régulation génique</term><term>Séquence conservée</term><term>Séquence nucléotidique</term><term>Évolution moléculaire</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p><b>BACKGROUND</b></p><p>Two opposing evolutionary constraints exert pressure on plant pathogens: one to diversify virulence factors in order to evade plant defenses, and the other to retain virulence factors critical for maintaining a compatible interaction with the plant host. To better understand how the diversified arsenals of fungal genes promote interaction with the same compatible wheat line, we performed a comparative genomic analysis of two North American isolates of Puccinia graminis f. sp. tritici (Pgt).</p></div><div type="abstract" xml:lang="en"><p><b>RESULTS</b></p><p>The patterns of inter-isolate divergence in the secreted candidate effector genes were compared with the levels of conservation and divergence of plant-pathogen gene co-expression networks (GCN) developed for each isolate. Comprative genomic analyses revealed substantial level of interisolate divergence in effector gene complement and sequence divergence. Gene Ontology (GO) analyses of the conserved and unique parts of the isolate-specific GCNs identified a number of conserved host pathways targeted by both isolates. Interestingly, the degree of inter-isolate sub-network conservation varied widely for the different host pathways and was positively associated with the proportion of conserved effector candidates associated with each sub-network. While different Pgt isolates tended to exploit similar wheat pathways for infection, the mode of plant-pathogen interaction varied for different pathways with some pathways being associated with the conserved set of effectors and others being linked with the diverged or isolate-specific effectors.</p></div><div type="abstract" xml:lang="en"><p><b>CONCLUSIONS</b></p><p>Our data suggest that at the intra-species level pathogen populations likely maintain divergent sets of effectors capable of targeting the same plant host pathways. This functional redundancy may play an important role in the dynamic of the "arms-race" between host and pathogen serving as the basis for diverse virulence strategies and creating conditions where mutations in certain effector groups will not have a major effect on the pathogen's ability to infect the host.</p></div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">28403814</PMID><DateCompleted><Year>2017</Year><Month>04</Month><Day>21</Day></DateCompleted><DateRevised><Year>2018</Year><Month>11</Month><Day>13</Day></DateRevised><Article PubModel="Electronic"><Journal><ISSN IssnType="Electronic">1471-2164</ISSN><JournalIssue CitedMedium="Internet"><Volume>18</Volume><Issue>1</Issue><PubDate><Year>2017</Year><Month>Apr</Month><Day>12</Day></PubDate></JournalIssue><Title>BMC genomics</Title><ISOAbbreviation>BMC Genomics</ISOAbbreviation></Journal><ArticleTitle>Divergent and convergent modes of interaction between wheat and Puccinia graminis f. sp. tritici isolates revealed by the comparative gene co-expression network and genome analyses.</ArticleTitle><Pagination><MedlinePgn>291</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1186/s12864-017-3678-6</ELocationID><Abstract><AbstractText Label="BACKGROUND" NlmCategory="BACKGROUND">Two opposing evolutionary constraints exert pressure on plant pathogens: one to diversify virulence factors in order to evade plant defenses, and the other to retain virulence factors critical for maintaining a compatible interaction with the plant host. To better understand how the diversified arsenals of fungal genes promote interaction with the same compatible wheat line, we performed a comparative genomic analysis of two North American isolates of Puccinia graminis f. sp. tritici (Pgt).</AbstractText><AbstractText Label="RESULTS" NlmCategory="RESULTS">The patterns of inter-isolate divergence in the secreted candidate effector genes were compared with the levels of conservation and divergence of plant-pathogen gene co-expression networks (GCN) developed for each isolate. Comprative genomic analyses revealed substantial level of interisolate divergence in effector gene complement and sequence divergence. Gene Ontology (GO) analyses of the conserved and unique parts of the isolate-specific GCNs identified a number of conserved host pathways targeted by both isolates. Interestingly, the degree of inter-isolate sub-network conservation varied widely for the different host pathways and was positively associated with the proportion of conserved effector candidates associated with each sub-network. While different Pgt isolates tended to exploit similar wheat pathways for infection, the mode of plant-pathogen interaction varied for different pathways with some pathways being associated with the conserved set of effectors and others being linked with the diverged or isolate-specific effectors.</AbstractText><AbstractText Label="CONCLUSIONS" NlmCategory="CONCLUSIONS">Our data suggest that at the intra-species level pathogen populations likely maintain divergent sets of effectors capable of targeting the same plant host pathways. This functional redundancy may play an important role in the dynamic of the "arms-race" between host and pathogen serving as the basis for diverse virulence strategies and creating conditions where mutations in certain effector groups will not have a major effect on the pathogen's ability to infect the host.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Rutter</LastName><ForeName>William B</ForeName><Initials>WB</Initials><AffiliationInfo><Affiliation>Department of Plant Pathology, Kansas State University, Manhattan, KS, 66506, USA.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>USDA-ARS, U.S. Vegetable Laboratory, 2700 Savannah Highway, Charleston, SC, 29414, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Salcedo</LastName><ForeName>Andres</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Department of Plant Pathology, Kansas State University, Manhattan, KS, 66506, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Akhunova</LastName><ForeName>Alina</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Integrated Genomics Facility, Kansas State University, Manhattan, KS, 66506, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>He</LastName><ForeName>Fei</ForeName><Initials>F</Initials><AffiliationInfo><Affiliation>Department of Plant Pathology, Kansas State University, Manhattan, KS, 66506, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wang</LastName><ForeName>Shichen</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>Department of Plant Pathology, Kansas State University, Manhattan, KS, 66506, USA.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>TEES-AgriLife Center for Bioinformatics and Genomic Systems Engineering, Texas A&M University, 101 Gateway, Suite A, College Station, TX, 77845, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Liang</LastName><ForeName>Hanquan</ForeName><Initials>H</Initials><AffiliationInfo><Affiliation>Integrated Genomics Facility, Kansas State University, Manhattan, KS, 66506, USA.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>School of Data and Computer Science, Sun Yat-sen University, Guangzhou, 510006, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Bowden</LastName><ForeName>Robert L</ForeName><Initials>RL</Initials><AffiliationInfo><Affiliation>USDA ARS, Hard Winter Wheat Genetics Research Unit, Throckmorton Plant Sciences Center, Manhattan, KS, 66506, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Akhunov</LastName><ForeName>Eduard</ForeName><Initials>E</Initials><Identifier Source="ORCID">http://orcid.org/0000-0002-0416-5211</Identifier><AffiliationInfo><Affiliation>Department of Plant Pathology, Kansas State University, Manhattan, KS, 66506, USA. eakhunov@ksu.edu.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D003160">Comparative Study</PublicationType><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2017</Year><Month>04</Month><Day>12</Day></ArticleDate></Article><MedlineJournalInfo><Country>England</Country><MedlineTA>BMC Genomics</MedlineTA><NlmUniqueID>100965258</NlmUniqueID><ISSNLinking>1471-2164</ISSNLinking></MedlineJournalInfo><ChemicalList><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D010940">Plant Proteins</NameOfSubstance></Chemical></ChemicalList><CitationSubset>IM</CitationSubset><MeshHeadingList><MeshHeading><DescriptorName UI="D001483" MajorTopicYN="N">Base Sequence</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D001487" MajorTopicYN="N">Basidiomycota</DescriptorName><QualifierName UI="Q000145" 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MajorTopicYN="N">Host-Pathogen Interactions</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D010935" MajorTopicYN="N">Plant Diseases</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName><QualifierName UI="Q000382" MajorTopicYN="N">microbiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D018515" MajorTopicYN="N">Plant Leaves</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName><QualifierName UI="Q000382" MajorTopicYN="N">microbiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D010940" MajorTopicYN="N">Plant Proteins</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D018547" MajorTopicYN="N">Plant Stems</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName><QualifierName UI="Q000382" 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