Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes.
Identifieur interne : 000158 ( Main/Corpus ); précédent : 000157; suivant : 000159Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes.
Auteurs : Peter N. Dodds ; Gregory J. Lawrence ; Ann-Maree Catanzariti ; Trazel Teh ; Ching-I A. Wang ; Michael A. Ayliffe ; Bostjan Kobe ; Jeffrey G. EllisSource :
- Proceedings of the National Academy of Sciences of the United States of America [ 0027-8424 ] ; 2006.
English descriptors
- KwdEn :
- Amino Acid Sequence (MeSH), Amino Acids (genetics), Binding Sites (genetics), Evolution, Molecular (MeSH), Flax (genetics), Fungi (genetics), Fungi (pathogenicity), Genes, Plant (genetics), Molecular Sequence Data (MeSH), Mutation (genetics), Plant Diseases (genetics), Plant Diseases (microbiology), Plant Proteins (chemistry), Protein Binding (MeSH), Selection, Genetic (MeSH), Species Specificity (MeSH), Virulence (genetics).
- MESH :
- chemical , chemistry : Plant Proteins.
- chemical , genetics : Amino Acids.
- genetics : Binding Sites, Flax, Fungi, Genes, Plant, Mutation, Plant Diseases, Virulence.
- microbiology : Plant Diseases.
- pathogenicity : Fungi.
- Amino Acid Sequence, Evolution, Molecular, Molecular Sequence Data, Protein Binding, Selection, Genetic, Species Specificity.
Abstract
Plant resistance proteins (R proteins) recognize corresponding pathogen avirulence (Avr) proteins either indirectly through detection of changes in their host protein targets or through direct R-Avr protein interaction. Although indirect recognition imposes selection against Avr effector function, pathogen effector molecules recognized through direct interaction may overcome resistance through sequence diversification rather than loss of function. Here we show that the flax rust fungus AvrL567 genes, whose products are recognized by the L5, L6, and L7 R proteins of flax, are highly diverse, with 12 sequence variants identified from six rust strains. Seven AvrL567 variants derived from Avr alleles induce necrotic responses when expressed in flax plants containing corresponding resistance genes (R genes), whereas five variants from avr alleles do not. Differences in recognition specificity between AvrL567 variants and evidence for diversifying selection acting on these genes suggest they have been involved in a gene-specific arms race with the corresponding flax R genes. Yeast two-hybrid assays indicate that recognition is based on direct R-Avr protein interaction and recapitulate the interaction specificity observed in planta. Biochemical analysis of Escherichia coli-produced AvrL567 proteins shows that variants that escape recognition nevertheless maintain a conserved structure and stability, suggesting that the amino acid sequence differences directly affect the R-Avr protein interaction. We suggest that direct recognition associated with high genetic diversity at corresponding R and Avr gene loci represents an alternative outcome of plant-pathogen coevolution to indirect recognition associated with simple balanced polymorphisms for functional and nonfunctional R and Avr genes.
DOI: 10.1073/pnas.0602577103
PubMed: 16731621
PubMed Central: PMC1482673
Links to Exploration step
pubmed:16731621Le document en format XML
<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes.</title><author><name sortKey="Dodds, Peter N" sort="Dodds, Peter N" uniqKey="Dodds P" first="Peter N" last="Dodds">Peter N. Dodds</name><affiliation><nlm:affiliation>Commonwealth Scientific and Industrial Research Organization Plant Industry, GPO Box 1600, Canberra ACT 2601, Australia. peter.dodds@csiro.au</nlm:affiliation></affiliation></author><author><name sortKey="Lawrence, Gregory J" sort="Lawrence, Gregory J" uniqKey="Lawrence G" first="Gregory J" last="Lawrence">Gregory J. Lawrence</name></author><author><name sortKey="Catanzariti, Ann Maree" sort="Catanzariti, Ann Maree" uniqKey="Catanzariti A" first="Ann-Maree" last="Catanzariti">Ann-Maree Catanzariti</name></author><author><name sortKey="Teh, Trazel" sort="Teh, Trazel" uniqKey="Teh T" first="Trazel" last="Teh">Trazel Teh</name></author><author><name sortKey="Wang, Ching I A" sort="Wang, Ching I A" uniqKey="Wang C" first="Ching-I A" last="Wang">Ching-I A. Wang</name></author><author><name sortKey="Ayliffe, Michael A" sort="Ayliffe, Michael A" uniqKey="Ayliffe M" first="Michael A" last="Ayliffe">Michael A. Ayliffe</name></author><author><name sortKey="Kobe, Bostjan" sort="Kobe, Bostjan" uniqKey="Kobe B" first="Bostjan" last="Kobe">Bostjan Kobe</name></author><author><name sortKey="Ellis, Jeffrey G" sort="Ellis, Jeffrey G" uniqKey="Ellis J" first="Jeffrey G" last="Ellis">Jeffrey G. Ellis</name></author></titleStmt><publicationStmt><idno type="wicri:source">PubMed</idno><date when="2006">2006</date><idno type="RBID">pubmed:16731621</idno><idno type="pmid">16731621</idno><idno type="doi">10.1073/pnas.0602577103</idno><idno type="pmc">PMC1482673</idno><idno type="wicri:Area/Main/Corpus">000158</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Corpus" wicri:corpus="PubMed">000158</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en">Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes.</title><author><name sortKey="Dodds, Peter N" sort="Dodds, Peter N" uniqKey="Dodds P" first="Peter N" last="Dodds">Peter N. Dodds</name><affiliation><nlm:affiliation>Commonwealth Scientific and Industrial Research Organization Plant Industry, GPO Box 1600, Canberra ACT 2601, Australia. peter.dodds@csiro.au</nlm:affiliation></affiliation></author><author><name sortKey="Lawrence, Gregory J" sort="Lawrence, Gregory J" uniqKey="Lawrence G" first="Gregory J" last="Lawrence">Gregory J. Lawrence</name></author><author><name sortKey="Catanzariti, Ann Maree" sort="Catanzariti, Ann Maree" uniqKey="Catanzariti A" first="Ann-Maree" last="Catanzariti">Ann-Maree Catanzariti</name></author><author><name sortKey="Teh, Trazel" sort="Teh, Trazel" uniqKey="Teh T" first="Trazel" last="Teh">Trazel Teh</name></author><author><name sortKey="Wang, Ching I A" sort="Wang, Ching I A" uniqKey="Wang C" first="Ching-I A" last="Wang">Ching-I A. Wang</name></author><author><name sortKey="Ayliffe, Michael A" sort="Ayliffe, Michael A" uniqKey="Ayliffe M" first="Michael A" last="Ayliffe">Michael A. Ayliffe</name></author><author><name sortKey="Kobe, Bostjan" sort="Kobe, Bostjan" uniqKey="Kobe B" first="Bostjan" last="Kobe">Bostjan Kobe</name></author><author><name sortKey="Ellis, Jeffrey G" sort="Ellis, Jeffrey G" uniqKey="Ellis J" first="Jeffrey G" last="Ellis">Jeffrey G. Ellis</name></author></analytic><series><title level="j">Proceedings of the National Academy of Sciences of the United States of America</title><idno type="ISSN">0027-8424</idno><imprint><date when="2006" type="published">2006</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Amino Acid Sequence (MeSH)</term><term>Amino Acids (genetics)</term><term>Binding Sites (genetics)</term><term>Evolution, Molecular (MeSH)</term><term>Flax (genetics)</term><term>Fungi (genetics)</term><term>Fungi (pathogenicity)</term><term>Genes, Plant (genetics)</term><term>Molecular Sequence Data (MeSH)</term><term>Mutation (genetics)</term><term>Plant Diseases (genetics)</term><term>Plant Diseases (microbiology)</term><term>Plant Proteins (chemistry)</term><term>Protein Binding (MeSH)</term><term>Selection, Genetic (MeSH)</term><term>Species Specificity (MeSH)</term><term>Virulence (genetics)</term></keywords><keywords scheme="MESH" type="chemical" qualifier="chemistry" xml:lang="en"><term>Plant Proteins</term></keywords><keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en"><term>Amino Acids</term></keywords><keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Binding Sites</term><term>Flax</term><term>Fungi</term><term>Genes, Plant</term><term>Mutation</term><term>Plant Diseases</term><term>Virulence</term></keywords><keywords scheme="MESH" qualifier="microbiology" xml:lang="en"><term>Plant Diseases</term></keywords><keywords scheme="MESH" qualifier="pathogenicity" xml:lang="en"><term>Fungi</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Amino Acid Sequence</term><term>Evolution, Molecular</term><term>Molecular Sequence Data</term><term>Protein Binding</term><term>Selection, Genetic</term><term>Species Specificity</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Plant resistance proteins (R proteins) recognize corresponding pathogen avirulence (Avr) proteins either indirectly through detection of changes in their host protein targets or through direct R-Avr protein interaction. Although indirect recognition imposes selection against Avr effector function, pathogen effector molecules recognized through direct interaction may overcome resistance through sequence diversification rather than loss of function. Here we show that the flax rust fungus AvrL567 genes, whose products are recognized by the L5, L6, and L7 R proteins of flax, are highly diverse, with 12 sequence variants identified from six rust strains. Seven AvrL567 variants derived from Avr alleles induce necrotic responses when expressed in flax plants containing corresponding resistance genes (R genes), whereas five variants from avr alleles do not. Differences in recognition specificity between AvrL567 variants and evidence for diversifying selection acting on these genes suggest they have been involved in a gene-specific arms race with the corresponding flax R genes. Yeast two-hybrid assays indicate that recognition is based on direct R-Avr protein interaction and recapitulate the interaction specificity observed in planta. Biochemical analysis of Escherichia coli-produced AvrL567 proteins shows that variants that escape recognition nevertheless maintain a conserved structure and stability, suggesting that the amino acid sequence differences directly affect the R-Avr protein interaction. We suggest that direct recognition associated with high genetic diversity at corresponding R and Avr gene loci represents an alternative outcome of plant-pathogen coevolution to indirect recognition associated with simple balanced polymorphisms for functional and nonfunctional R and Avr genes.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">16731621</PMID><DateCompleted><Year>2006</Year><Month>07</Month><Day>19</Day></DateCompleted><DateRevised><Year>2018</Year><Month>11</Month><Day>13</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Print">0027-8424</ISSN><JournalIssue CitedMedium="Print"><Volume>103</Volume><Issue>23</Issue><PubDate><Year>2006</Year><Month>Jun</Month><Day>06</Day></PubDate></JournalIssue><Title>Proceedings of the National Academy of Sciences of the United States of America</Title><ISOAbbreviation>Proc Natl Acad Sci U S A</ISOAbbreviation></Journal><ArticleTitle>Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes.</ArticleTitle><Pagination><MedlinePgn>8888-93</MedlinePgn></Pagination><Abstract><AbstractText>Plant resistance proteins (R proteins) recognize corresponding pathogen avirulence (Avr) proteins either indirectly through detection of changes in their host protein targets or through direct R-Avr protein interaction. Although indirect recognition imposes selection against Avr effector function, pathogen effector molecules recognized through direct interaction may overcome resistance through sequence diversification rather than loss of function. Here we show that the flax rust fungus AvrL567 genes, whose products are recognized by the L5, L6, and L7 R proteins of flax, are highly diverse, with 12 sequence variants identified from six rust strains. Seven AvrL567 variants derived from Avr alleles induce necrotic responses when expressed in flax plants containing corresponding resistance genes (R genes), whereas five variants from avr alleles do not. Differences in recognition specificity between AvrL567 variants and evidence for diversifying selection acting on these genes suggest they have been involved in a gene-specific arms race with the corresponding flax R genes. Yeast two-hybrid assays indicate that recognition is based on direct R-Avr protein interaction and recapitulate the interaction specificity observed in planta. Biochemical analysis of Escherichia coli-produced AvrL567 proteins shows that variants that escape recognition nevertheless maintain a conserved structure and stability, suggesting that the amino acid sequence differences directly affect the R-Avr protein interaction. We suggest that direct recognition associated with high genetic diversity at corresponding R and Avr gene loci represents an alternative outcome of plant-pathogen coevolution to indirect recognition associated with simple balanced polymorphisms for functional and nonfunctional R and Avr genes.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Dodds</LastName><ForeName>Peter N</ForeName><Initials>PN</Initials><AffiliationInfo><Affiliation>Commonwealth Scientific and Industrial Research Organization Plant Industry, GPO Box 1600, Canberra ACT 2601, Australia. peter.dodds@csiro.au</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Lawrence</LastName><ForeName>Gregory J</ForeName><Initials>GJ</Initials></Author><Author ValidYN="Y"><LastName>Catanzariti</LastName><ForeName>Ann-Maree</ForeName><Initials>AM</Initials></Author><Author ValidYN="Y"><LastName>Teh</LastName><ForeName>Trazel</ForeName><Initials>T</Initials></Author><Author ValidYN="Y"><LastName>Wang</LastName><ForeName>Ching-I A</ForeName><Initials>CI</Initials></Author><Author ValidYN="Y"><LastName>Ayliffe</LastName><ForeName>Michael A</ForeName><Initials>MA</Initials></Author><Author ValidYN="Y"><LastName>Kobe</LastName><ForeName>Bostjan</ForeName><Initials>B</Initials></Author><Author ValidYN="Y"><LastName>Ellis</LastName><ForeName>Jeffrey G</ForeName><Initials>JG</Initials></Author></AuthorList><Language>eng</Language><DataBankList 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