Characterization of the complex locus of bean encoding polygalacturonase-inhibiting proteins reveals subfunctionalization for defense against fungi and insects
Polygalacturonase-inhibiting proteins (PGIPs) are extracellular plant inhibitors of fungal endopolygalacturonases (PGs) that belong to the superfamily of Leu-rich repeat proteins. We have characterized the full complement of pgip genes in the bean (Phaseolus vulgaris) genotype BAT93. This comprises...
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| Veröffentlicht in: | Plant physiology (Bethesda) 2004-08, Vol.135 (4), p.2424-2435 |
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| creator | D'Ovidio, R Raiola, A Capodicasa, C Devoto, A Pontiggia, D Roberti, S Galletti, R Conti, E O'Sullivan, D De Lorenzo, G |
| description | Polygalacturonase-inhibiting proteins (PGIPs) are extracellular plant inhibitors of fungal endopolygalacturonases (PGs) that belong to the superfamily of Leu-rich repeat proteins. We have characterized the full complement of pgip genes in the bean (Phaseolus vulgaris) genotype BAT93. This comprises four clustered members that span a 50-kb region and, based on their similarity, form two pairs (Pvpgip1/Pvpgip2 and Pvpgip3/Pvpgip4). Characterization of the encoded products revealed both partial redundancy and subfunctionalization against fungal-derived PGs. Notably, the pair PvPGIP3/PvPGIP4 also inhibited PGs of two mirid bugs (Lygus rugulipennis and Adelphocoris lineolatus). Characterization of Pvpgip genes of Pinto bean showed variations limited to single synonymous substitutions or small deletions. A three-amino acid deletion encompassing a residue previously identified as crucial for recognition of PG of Fusarium moniliforme was responsible for the inability of BAT93 PvPGIP2 to inhibit this enzyme. Consistent with the large variations observed in the promoter sequences, reverse transcription-PCR expression analysis revealed that the different family members differentially respond to elicitors, wounding, and salicylic acid. We conclude that both biochemical and regulatory redundancy and subfunctionalization of pgip genes are important for the adaptation of plants to pathogenic fungi and phytophagous insects. |
| doi_str_mv | 10.1104/pp.104.044644 |
| format | Article |
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We have characterized the full complement of pgip genes in the bean (Phaseolus vulgaris) genotype BAT93. This comprises four clustered members that span a 50-kb region and, based on their similarity, form two pairs (Pvpgip1/Pvpgip2 and Pvpgip3/Pvpgip4). Characterization of the encoded products revealed both partial redundancy and subfunctionalization against fungal-derived PGs. Notably, the pair PvPGIP3/PvPGIP4 also inhibited PGs of two mirid bugs (Lygus rugulipennis and Adelphocoris lineolatus). Characterization of Pvpgip genes of Pinto bean showed variations limited to single synonymous substitutions or small deletions. A three-amino acid deletion encompassing a residue previously identified as crucial for recognition of PG of Fusarium moniliforme was responsible for the inability of BAT93 PvPGIP2 to inhibit this enzyme. Consistent with the large variations observed in the promoter sequences, reverse transcription-PCR expression analysis revealed that the different family members differentially respond to elicitors, wounding, and salicylic acid. We conclude that both biochemical and regulatory redundancy and subfunctionalization of pgip genes are important for the adaptation of plants to pathogenic fungi and phytophagous insects.</description><identifier>ISSN: 0032-0889</identifier><identifier>EISSN: 1532-2548</identifier><identifier>DOI: 10.1104/pp.104.044644</identifier><identifier>PMID: 15299124</identifier><identifier>CODEN: PPHYA5</identifier><language>eng</language><publisher>Rockville, MD: American Society of Plant Biologists</publisher><subject>Adelphocoris lineolatus ; Agronomy. Soil science and plant productions ; Amino Acid Sequence ; amino acid sequences ; Amino acids ; Animals ; beans ; Biological and medical sciences ; DNA ; enzyme inhibition ; enzyme inhibitors ; Evolution ; Fundamental and applied biological sciences. Psychology ; Fungi ; Fusarium moniliforme ; gene expression regulation ; genetic variation ; Genetics and breeding of economic plants ; Genome, Plant ; Genotypes ; Gibberella fujikuroi ; Immunity, Innate ; Insecta ; Lygus rugulipennis ; mechanical damage ; Molecular Sequence Data ; mutation ; nucleotide sequences ; Open reading frames ; Pest resistance ; Phaseolus - genetics ; Phaseolus - metabolism ; Phaseolus vulgaris ; phytophagous insects ; plant damage ; Plant Diseases - microbiology ; Plant Diseases - parasitology ; plant pathogenic fungi ; Plant pathogens ; plant proteins ; Plant Proteins - chemistry ; Plant Proteins - genetics ; Plant Proteins - metabolism ; Plants ; Plants Interacting with Other Organisms ; polygalacturonase ; polygalacturonase-inhibiting protein ; Regional identity ; resistance mechanisms ; RNA ; Sequence Alignment ; Sequence Homology, Amino Acid ; Untranslated regions ; Varietal selection. Specialized plant breeding, plant breeding aims</subject><ispartof>Plant physiology (Bethesda), 2004-08, Vol.135 (4), p.2424-2435</ispartof><rights>Copyright 2004 American Society of Plant Biologists</rights><rights>2004 INIST-CNRS</rights><rights>Copyright © 2004, American Society of Plant Biologists 2004</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c525t-2327b148b886325e191b95e5537a0f20b2fb73488563cc3b54f2eae30cf908ab3</citedby><cites>FETCH-LOGICAL-c525t-2327b148b886325e191b95e5537a0f20b2fb73488563cc3b54f2eae30cf908ab3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/4356594$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/4356594$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,776,780,799,881,27901,27902,57992,58225</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=16040915$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/15299124$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>D'Ovidio, R</creatorcontrib><creatorcontrib>Raiola, A</creatorcontrib><creatorcontrib>Capodicasa, C</creatorcontrib><creatorcontrib>Devoto, A</creatorcontrib><creatorcontrib>Pontiggia, D</creatorcontrib><creatorcontrib>Roberti, S</creatorcontrib><creatorcontrib>Galletti, R</creatorcontrib><creatorcontrib>Conti, E</creatorcontrib><creatorcontrib>O'Sullivan, D</creatorcontrib><creatorcontrib>De Lorenzo, G</creatorcontrib><title>Characterization of the complex locus of bean encoding polygalacturonase-inhibiting proteins reveals subfunctionalization for defense against fungi and insects</title><title>Plant physiology (Bethesda)</title><addtitle>Plant Physiol</addtitle><description>Polygalacturonase-inhibiting proteins (PGIPs) are extracellular plant inhibitors of fungal endopolygalacturonases (PGs) that belong to the superfamily of Leu-rich repeat proteins. We have characterized the full complement of pgip genes in the bean (Phaseolus vulgaris) genotype BAT93. This comprises four clustered members that span a 50-kb region and, based on their similarity, form two pairs (Pvpgip1/Pvpgip2 and Pvpgip3/Pvpgip4). Characterization of the encoded products revealed both partial redundancy and subfunctionalization against fungal-derived PGs. Notably, the pair PvPGIP3/PvPGIP4 also inhibited PGs of two mirid bugs (Lygus rugulipennis and Adelphocoris lineolatus). Characterization of Pvpgip genes of Pinto bean showed variations limited to single synonymous substitutions or small deletions. A three-amino acid deletion encompassing a residue previously identified as crucial for recognition of PG of Fusarium moniliforme was responsible for the inability of BAT93 PvPGIP2 to inhibit this enzyme. Consistent with the large variations observed in the promoter sequences, reverse transcription-PCR expression analysis revealed that the different family members differentially respond to elicitors, wounding, and salicylic acid. We conclude that both biochemical and regulatory redundancy and subfunctionalization of pgip genes are important for the adaptation of plants to pathogenic fungi and phytophagous insects.</description><subject>Adelphocoris lineolatus</subject><subject>Agronomy. Soil science and plant productions</subject><subject>Amino Acid Sequence</subject><subject>amino acid sequences</subject><subject>Amino acids</subject><subject>Animals</subject><subject>beans</subject><subject>Biological and medical sciences</subject><subject>DNA</subject><subject>enzyme inhibition</subject><subject>enzyme inhibitors</subject><subject>Evolution</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Fungi</subject><subject>Fusarium moniliforme</subject><subject>gene expression regulation</subject><subject>genetic variation</subject><subject>Genetics and breeding of economic plants</subject><subject>Genome, Plant</subject><subject>Genotypes</subject><subject>Gibberella fujikuroi</subject><subject>Immunity, Innate</subject><subject>Insecta</subject><subject>Lygus rugulipennis</subject><subject>mechanical damage</subject><subject>Molecular Sequence Data</subject><subject>mutation</subject><subject>nucleotide sequences</subject><subject>Open reading frames</subject><subject>Pest resistance</subject><subject>Phaseolus - genetics</subject><subject>Phaseolus - metabolism</subject><subject>Phaseolus vulgaris</subject><subject>phytophagous insects</subject><subject>plant damage</subject><subject>Plant Diseases - microbiology</subject><subject>Plant Diseases - parasitology</subject><subject>plant pathogenic fungi</subject><subject>Plant pathogens</subject><subject>plant proteins</subject><subject>Plant Proteins - chemistry</subject><subject>Plant Proteins - genetics</subject><subject>Plant Proteins - metabolism</subject><subject>Plants</subject><subject>Plants Interacting with Other Organisms</subject><subject>polygalacturonase</subject><subject>polygalacturonase-inhibiting protein</subject><subject>Regional identity</subject><subject>resistance mechanisms</subject><subject>RNA</subject><subject>Sequence Alignment</subject><subject>Sequence Homology, Amino Acid</subject><subject>Untranslated regions</subject><subject>Varietal selection. Specialized plant breeding, plant breeding aims</subject><issn>0032-0889</issn><issn>1532-2548</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2004</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkk1vEzEQhlcIREPgyA2BL3Db4M-N98ABReVDqsQBerZmnfHG1cZe7N2K8mf6V3FIaOHEaWy_z7wz9riqnjO6YozKt-O4KmFFpWykfFAtmBK85krqh9WC0rKmWrdn1ZOcryilTDD5uDpjirct43JR3W52kMBOmPxPmHwMJDoy7ZDYuB8H_EGGaOd8OOwQAsFg49aHnoxxuOlhKJlzigEy1j7sfOen32KKE_qQScJrhCGTPHduDvbgD8OfQi4mskWHISOBHgo_kUL1nkDYkrJFO-Wn1SNXHPDZKS6ryw_n3zaf6osvHz9v3l_UVnE11Vzwdcek7rRuBFfIWta1CpUSa6CO0467bi2k1qoR1opOSccRUFDrWqqhE8vq3dF3nLs9bi2GKcFgxuT3kG5MBG_-VYLfmT5eG8Wppm3Jf3PKT_H7jHkye58tDgMEjHM2TaPL25fq_wM5ZZSztS5gfQRtijkndHfNMGoOozfjaA7hOPrCv_z7Bvf0adYFeH0CIFsYXIJgfb7nGippW77Psnpx5K7yFNOdLoVqVHuweXWUHUQDfSoWl19L14LSVpanUOIXVITO0A</recordid><startdate>20040801</startdate><enddate>20040801</enddate><creator>D'Ovidio, R</creator><creator>Raiola, A</creator><creator>Capodicasa, C</creator><creator>Devoto, A</creator><creator>Pontiggia, D</creator><creator>Roberti, S</creator><creator>Galletti, R</creator><creator>Conti, E</creator><creator>O'Sullivan, D</creator><creator>De Lorenzo, G</creator><general>American Society of Plant Biologists</general><general>American Society of Plant Physiologists</general><scope>FBQ</scope><scope>IQODW</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7SS</scope><scope>7T7</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20040801</creationdate><title>Characterization of the complex locus of bean encoding polygalacturonase-inhibiting proteins reveals subfunctionalization for defense against fungi and insects</title><author>D'Ovidio, R ; Raiola, A ; Capodicasa, C ; Devoto, A ; Pontiggia, D ; Roberti, S ; Galletti, R ; Conti, E ; O'Sullivan, D ; De Lorenzo, G</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c525t-2327b148b886325e191b95e5537a0f20b2fb73488563cc3b54f2eae30cf908ab3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2004</creationdate><topic>Adelphocoris lineolatus</topic><topic>Agronomy. Soil science and plant productions</topic><topic>Amino Acid Sequence</topic><topic>amino acid sequences</topic><topic>Amino acids</topic><topic>Animals</topic><topic>beans</topic><topic>Biological and medical sciences</topic><topic>DNA</topic><topic>enzyme inhibition</topic><topic>enzyme inhibitors</topic><topic>Evolution</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Fungi</topic><topic>Fusarium moniliforme</topic><topic>gene expression regulation</topic><topic>genetic variation</topic><topic>Genetics and breeding of economic plants</topic><topic>Genome, Plant</topic><topic>Genotypes</topic><topic>Gibberella fujikuroi</topic><topic>Immunity, Innate</topic><topic>Insecta</topic><topic>Lygus rugulipennis</topic><topic>mechanical damage</topic><topic>Molecular Sequence Data</topic><topic>mutation</topic><topic>nucleotide sequences</topic><topic>Open reading frames</topic><topic>Pest resistance</topic><topic>Phaseolus - genetics</topic><topic>Phaseolus - metabolism</topic><topic>Phaseolus vulgaris</topic><topic>phytophagous insects</topic><topic>plant damage</topic><topic>Plant Diseases - microbiology</topic><topic>Plant Diseases - parasitology</topic><topic>plant pathogenic fungi</topic><topic>Plant pathogens</topic><topic>plant proteins</topic><topic>Plant Proteins - chemistry</topic><topic>Plant Proteins - genetics</topic><topic>Plant Proteins - metabolism</topic><topic>Plants</topic><topic>Plants Interacting with Other Organisms</topic><topic>polygalacturonase</topic><topic>polygalacturonase-inhibiting protein</topic><topic>Regional identity</topic><topic>resistance mechanisms</topic><topic>RNA</topic><topic>Sequence Alignment</topic><topic>Sequence Homology, Amino Acid</topic><topic>Untranslated regions</topic><topic>Varietal selection. Specialized plant breeding, plant breeding aims</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>D'Ovidio, R</creatorcontrib><creatorcontrib>Raiola, A</creatorcontrib><creatorcontrib>Capodicasa, C</creatorcontrib><creatorcontrib>Devoto, A</creatorcontrib><creatorcontrib>Pontiggia, D</creatorcontrib><creatorcontrib>Roberti, S</creatorcontrib><creatorcontrib>Galletti, R</creatorcontrib><creatorcontrib>Conti, E</creatorcontrib><creatorcontrib>O'Sullivan, D</creatorcontrib><creatorcontrib>De Lorenzo, G</creatorcontrib><collection>AGRIS</collection><collection>Pascal-Francis</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Plant physiology (Bethesda)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>D'Ovidio, R</au><au>Raiola, A</au><au>Capodicasa, C</au><au>Devoto, A</au><au>Pontiggia, D</au><au>Roberti, S</au><au>Galletti, R</au><au>Conti, E</au><au>O'Sullivan, D</au><au>De Lorenzo, G</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Characterization of the complex locus of bean encoding polygalacturonase-inhibiting proteins reveals subfunctionalization for defense against fungi and insects</atitle><jtitle>Plant physiology (Bethesda)</jtitle><addtitle>Plant Physiol</addtitle><date>2004-08-01</date><risdate>2004</risdate><volume>135</volume><issue>4</issue><spage>2424</spage><epage>2435</epage><pages>2424-2435</pages><issn>0032-0889</issn><eissn>1532-2548</eissn><coden>PPHYA5</coden><abstract>Polygalacturonase-inhibiting proteins (PGIPs) are extracellular plant inhibitors of fungal endopolygalacturonases (PGs) that belong to the superfamily of Leu-rich repeat proteins. We have characterized the full complement of pgip genes in the bean (Phaseolus vulgaris) genotype BAT93. This comprises four clustered members that span a 50-kb region and, based on their similarity, form two pairs (Pvpgip1/Pvpgip2 and Pvpgip3/Pvpgip4). Characterization of the encoded products revealed both partial redundancy and subfunctionalization against fungal-derived PGs. Notably, the pair PvPGIP3/PvPGIP4 also inhibited PGs of two mirid bugs (Lygus rugulipennis and Adelphocoris lineolatus). Characterization of Pvpgip genes of Pinto bean showed variations limited to single synonymous substitutions or small deletions. A three-amino acid deletion encompassing a residue previously identified as crucial for recognition of PG of Fusarium moniliforme was responsible for the inability of BAT93 PvPGIP2 to inhibit this enzyme. Consistent with the large variations observed in the promoter sequences, reverse transcription-PCR expression analysis revealed that the different family members differentially respond to elicitors, wounding, and salicylic acid. We conclude that both biochemical and regulatory redundancy and subfunctionalization of pgip genes are important for the adaptation of plants to pathogenic fungi and phytophagous insects.</abstract><cop>Rockville, MD</cop><pub>American Society of Plant Biologists</pub><pmid>15299124</pmid><doi>10.1104/pp.104.044644</doi><tpages>12</tpages><oa>free_for_read</oa></addata></record> |
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| ispartof | Plant physiology (Bethesda), 2004-08, Vol.135 (4), p.2424-2435 |
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| source | Jstor Complete Legacy; Oxford University Press Journals All Titles (1996-Current); MEDLINE; EZB-FREE-00999 freely available EZB journals |
| subjects | Adelphocoris lineolatus Agronomy. Soil science and plant productions Amino Acid Sequence amino acid sequences Amino acids Animals beans Biological and medical sciences DNA enzyme inhibition enzyme inhibitors Evolution Fundamental and applied biological sciences. Psychology Fungi Fusarium moniliforme gene expression regulation genetic variation Genetics and breeding of economic plants Genome, Plant Genotypes Gibberella fujikuroi Immunity, Innate Insecta Lygus rugulipennis mechanical damage Molecular Sequence Data mutation nucleotide sequences Open reading frames Pest resistance Phaseolus - genetics Phaseolus - metabolism Phaseolus vulgaris phytophagous insects plant damage Plant Diseases - microbiology Plant Diseases - parasitology plant pathogenic fungi Plant pathogens plant proteins Plant Proteins - chemistry Plant Proteins - genetics Plant Proteins - metabolism Plants Plants Interacting with Other Organisms polygalacturonase polygalacturonase-inhibiting protein Regional identity resistance mechanisms RNA Sequence Alignment Sequence Homology, Amino Acid Untranslated regions Varietal selection. Specialized plant breeding, plant breeding aims |
| title | Characterization of the complex locus of bean encoding polygalacturonase-inhibiting proteins reveals subfunctionalization for defense against fungi and insects |
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