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Eukaryotic-Acquired Gene by a Biotrophic Phytopathogen Allows Prolonged Survival on the Host by Counteracting the Shut-Down of Plant Photosynthesis
Xanthomonas citri pv. citri, the bacteria responsible for citrus canker posses a biological active plant natriuretic peptide (PNP)-like protein, not present in any other bacteria. PNPs are a class of extracellular, systemically mobile peptides that elicit a number of plant responses important in hom...
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Published in: | PloS one 2010-01, Vol.5 (1), p.e8950-e8950 |
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creator | Garavaglia, Betiana S Thomas, Ludivine Gottig, Natalia Dunger, Germán Garofalo, Cecilia G Daurelio, Lucas D Ndimba, Bongani Orellano, Elena G Gehring, Chris Ottado, Jorgelina |
description | Xanthomonas citri pv. citri, the bacteria responsible for citrus canker posses a biological active plant natriuretic peptide (PNP)-like protein, not present in any other bacteria. PNPs are a class of extracellular, systemically mobile peptides that elicit a number of plant responses important in homeostasis and growth. Previously, we showed that a Xanthomonas citri pv. citri mutant lacking the PNP-like protein XacPNP produced more necrotic lesions in citrus leaves than wild type infections and suggested a role for XacPNP in the regulation of host homeostasis. Here we have analyzed the proteome modifications observed in citrus leaves infected with the wild type and XacPNP deletion mutant bacteria. While both of them cause down-regulation of enzymes related to photosynthesis as well as chloroplastic ribosomal proteins, proteins related to defense responses are up-regulated. However, leaves infiltrated with the XacPNP deletion mutant show a more pronounced decrease in photosynthetic proteins while no reduction in defense related proteins as compared to the wild-type pathogen. This suggests that XacPNP serves the pathogen to maintain host photosynthetic efficiency during pathogenesis. The results from the proteomics analyses are consistent with our chlorophyll fluorescence data and transcript analyses of defense genes that show a more marked reduction in photosynthesis in the mutant but no difference in the induction of genes diagnostic for biotic-stress responses. We therefore conclude that XacPNP counteracts the shut-down of host photosynthesis during infection and in that way maintains the tissue in better conditions, suggesting that the pathogen has adapted a host gene to modify its natural host and render it a better reservoir for prolonged bacterial survival and thus for further colonization. |
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PNPs are a class of extracellular, systemically mobile peptides that elicit a number of plant responses important in homeostasis and growth. Previously, we showed that a Xanthomonas citri pv. citri mutant lacking the PNP-like protein XacPNP produced more necrotic lesions in citrus leaves than wild type infections and suggested a role for XacPNP in the regulation of host homeostasis. Here we have analyzed the proteome modifications observed in citrus leaves infected with the wild type and XacPNP deletion mutant bacteria. While both of them cause down-regulation of enzymes related to photosynthesis as well as chloroplastic ribosomal proteins, proteins related to defense responses are up-regulated. However, leaves infiltrated with the XacPNP deletion mutant show a more pronounced decrease in photosynthetic proteins while no reduction in defense related proteins as compared to the wild-type pathogen. This suggests that XacPNP serves the pathogen to maintain host photosynthetic efficiency during pathogenesis. The results from the proteomics analyses are consistent with our chlorophyll fluorescence data and transcript analyses of defense genes that show a more marked reduction in photosynthesis in the mutant but no difference in the induction of genes diagnostic for biotic-stress responses. We therefore conclude that XacPNP counteracts the shut-down of host photosynthesis during infection and in that way maintains the tissue in better conditions, suggesting that the pathogen has adapted a host gene to modify its natural host and render it a better reservoir for prolonged bacterial survival and thus for further colonization.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0008950</identifier><identifier>PMID: 20126632</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Arabidopsis ; Bacteria ; bacterial diseases of plants ; bacterial proteins ; Biotechnology ; Canker ; cankers (plants) ; Carotenoids ; Chlorophyll ; Chloroplasts ; Citrus - microbiology ; Citrus sinensis ; Colonization ; Corn ; Data processing ; Deletion mutant ; Diagnostic systems ; Disease ; Electrophoresis, Gel, Two-Dimensional ; Fluorescence ; Gene expression ; Genes ; Genes, Plant ; Genetic engineering ; Glycine max ; Health aspects ; Homeostasis ; Host plants ; host-pathogen relationships ; Infections ; Leaves ; Lesions ; lesions (plant) ; Metabolism ; Microbiology/Plant-Biotic Interactions ; Molecular biology ; oranges ; Pathogenesis ; Pathogens ; Peptides ; Photosynthesis ; Physiology ; Plant biochemistry ; Plant Biology/Plant Biochemistry and Physiology ; Plant Biology/Plant-Biotic Interactions ; Plant Leaves - metabolism ; plant natriuretic peptide ; Plant photosynthesis ; Plant Proteins - metabolism ; Proteins ; Proteome ; Proteomics ; Pseudomonas syringae ; Reduction ; Ribosomal proteins ; signs and symptoms (plants) ; Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization ; Survival ; Transcription ; Ustilago maydis ; Xanthomonas - physiology ; Xanthomonas citri ; Xanthomonas citri pv. citri</subject><ispartof>PloS one, 2010-01, Vol.5 (1), p.e8950-e8950</ispartof><rights>COPYRIGHT 2010 Public Library of Science</rights><rights>2010 Garavaglia et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>Garavaglia et al. 2010</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c715t-32edd2ed2ca7d6c1fa772ff053519890f6af46190adadb6b20e69e136624900b3</citedby></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/1289252045/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/1289252045?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,25753,27924,27925,37012,37013,44590,53791,53793,75126</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/20126632$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Ausubel, Frederick M.</contributor><creatorcontrib>Garavaglia, Betiana S</creatorcontrib><creatorcontrib>Thomas, Ludivine</creatorcontrib><creatorcontrib>Gottig, Natalia</creatorcontrib><creatorcontrib>Dunger, Germán</creatorcontrib><creatorcontrib>Garofalo, Cecilia G</creatorcontrib><creatorcontrib>Daurelio, Lucas D</creatorcontrib><creatorcontrib>Ndimba, Bongani</creatorcontrib><creatorcontrib>Orellano, Elena G</creatorcontrib><creatorcontrib>Gehring, Chris</creatorcontrib><creatorcontrib>Ottado, Jorgelina</creatorcontrib><title>Eukaryotic-Acquired Gene by a Biotrophic Phytopathogen Allows Prolonged Survival on the Host by Counteracting the Shut-Down of Plant Photosynthesis</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Xanthomonas citri pv. citri, the bacteria responsible for citrus canker posses a biological active plant natriuretic peptide (PNP)-like protein, not present in any other bacteria. PNPs are a class of extracellular, systemically mobile peptides that elicit a number of plant responses important in homeostasis and growth. Previously, we showed that a Xanthomonas citri pv. citri mutant lacking the PNP-like protein XacPNP produced more necrotic lesions in citrus leaves than wild type infections and suggested a role for XacPNP in the regulation of host homeostasis. Here we have analyzed the proteome modifications observed in citrus leaves infected with the wild type and XacPNP deletion mutant bacteria. While both of them cause down-regulation of enzymes related to photosynthesis as well as chloroplastic ribosomal proteins, proteins related to defense responses are up-regulated. However, leaves infiltrated with the XacPNP deletion mutant show a more pronounced decrease in photosynthetic proteins while no reduction in defense related proteins as compared to the wild-type pathogen. This suggests that XacPNP serves the pathogen to maintain host photosynthetic efficiency during pathogenesis. The results from the proteomics analyses are consistent with our chlorophyll fluorescence data and transcript analyses of defense genes that show a more marked reduction in photosynthesis in the mutant but no difference in the induction of genes diagnostic for biotic-stress responses. We therefore conclude that XacPNP counteracts the shut-down of host photosynthesis during infection and in that way maintains the tissue in better conditions, suggesting that the pathogen has adapted a host gene to modify its natural host and render it a better reservoir for prolonged bacterial survival and thus for further colonization.</description><subject>Arabidopsis</subject><subject>Bacteria</subject><subject>bacterial diseases of plants</subject><subject>bacterial proteins</subject><subject>Biotechnology</subject><subject>Canker</subject><subject>cankers (plants)</subject><subject>Carotenoids</subject><subject>Chlorophyll</subject><subject>Chloroplasts</subject><subject>Citrus - microbiology</subject><subject>Citrus sinensis</subject><subject>Colonization</subject><subject>Corn</subject><subject>Data processing</subject><subject>Deletion mutant</subject><subject>Diagnostic systems</subject><subject>Disease</subject><subject>Electrophoresis, Gel, Two-Dimensional</subject><subject>Fluorescence</subject><subject>Gene expression</subject><subject>Genes</subject><subject>Genes, Plant</subject><subject>Genetic engineering</subject><subject>Glycine max</subject><subject>Health aspects</subject><subject>Homeostasis</subject><subject>Host plants</subject><subject>host-pathogen relationships</subject><subject>Infections</subject><subject>Leaves</subject><subject>Lesions</subject><subject>lesions (plant)</subject><subject>Metabolism</subject><subject>Microbiology/Plant-Biotic Interactions</subject><subject>Molecular biology</subject><subject>oranges</subject><subject>Pathogenesis</subject><subject>Pathogens</subject><subject>Peptides</subject><subject>Photosynthesis</subject><subject>Physiology</subject><subject>Plant biochemistry</subject><subject>Plant Biology/Plant Biochemistry and Physiology</subject><subject>Plant Biology/Plant-Biotic Interactions</subject><subject>Plant Leaves - metabolism</subject><subject>plant natriuretic peptide</subject><subject>Plant photosynthesis</subject><subject>Plant Proteins - metabolism</subject><subject>Proteins</subject><subject>Proteome</subject><subject>Proteomics</subject><subject>Pseudomonas syringae</subject><subject>Reduction</subject><subject>Ribosomal proteins</subject><subject>signs and symptoms (plants)</subject><subject>Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization</subject><subject>Survival</subject><subject>Transcription</subject><subject>Ustilago maydis</subject><subject>Xanthomonas - physiology</subject><subject>Xanthomonas citri</subject><subject>Xanthomonas citri pv. citri</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2010</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><sourceid>DOA</sourceid><recordid>eNqNk99u0zAUxiMEYmPwBggiIYG4aPGfxIlvJpUxtkmTNlHGreU6TuLh-nS2s9Hn4IVx126saBcoimL5_L4v9mefLHuN0RjTCn-6hME7accLcHqMEKp5iZ5ku5hTMmIE0acPxjvZixAuESppzdjzbIcgTBijZDf7fTj8lH4J0ajRRF0NxusmP9JO57NlLvPPBqKHRW9Uft4vIyxk7KHTLp9YCzchP_dgwXVJMx38tbmWNgeXx17nxxDiyuMABhe1lyoa191Wpv0QR1_gxuXQ5udWupi8IUJYulQOJrzMnrXSBv1q893LLr4efj84Hp2eHZ0cTE5HqsJlHFGimya9RMmqYQq3sqpI26ZNlpjXHLVMtgXDHMlGNjM2I0gzrjFljBQcoRndy96ufRcWgtjkGQQmNSclQUWZiJM10YC8FAtv5ikrAdKI2wnwnZA-RWe1qBs24xVSSU0KTbTkjSS05YorXaMSJa_9zd-G2Vw3Srvopd0y3a4404sOrgWpMSnxajEfNgYergYdopiboLRNCWoYgqgoLQvMK5bId_-Qj29uQ3Uyrd-4Nh21VCtPMSkqyjFbL3v8CJWeRs-NSnevNWl-S_BxS5CYqH_FTg4hiJPpt_9nz35ss-8fsL2WNvYB7BANuLANFmtQeQjB6_Y-Y4zEqnXu0hCr1hGb1kmyNw_P51501yt_r0srQcjOmyAupqlKEa4JxpzTP6O8HtA</recordid><startdate>20100128</startdate><enddate>20100128</enddate><creator>Garavaglia, Betiana S</creator><creator>Thomas, Ludivine</creator><creator>Gottig, Natalia</creator><creator>Dunger, Germán</creator><creator>Garofalo, Cecilia G</creator><creator>Daurelio, Lucas D</creator><creator>Ndimba, Bongani</creator><creator>Orellano, Elena G</creator><creator>Gehring, Chris</creator><creator>Ottado, Jorgelina</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>FBQ</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>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20100128</creationdate><title>Eukaryotic-Acquired Gene by a Biotrophic Phytopathogen Allows Prolonged Survival on the Host by Counteracting the Shut-Down of Plant Photosynthesis</title><author>Garavaglia, Betiana S ; Thomas, Ludivine ; Gottig, Natalia ; Dunger, Germán ; Garofalo, Cecilia G ; Daurelio, Lucas D ; Ndimba, Bongani ; Orellano, Elena G ; Gehring, Chris ; Ottado, Jorgelina</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c715t-32edd2ed2ca7d6c1fa772ff053519890f6af46190adadb6b20e69e136624900b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2010</creationdate><topic>Arabidopsis</topic><topic>Bacteria</topic><topic>bacterial diseases of plants</topic><topic>bacterial proteins</topic><topic>Biotechnology</topic><topic>Canker</topic><topic>cankers (plants)</topic><topic>Carotenoids</topic><topic>Chlorophyll</topic><topic>Chloroplasts</topic><topic>Citrus - microbiology</topic><topic>Citrus sinensis</topic><topic>Colonization</topic><topic>Corn</topic><topic>Data processing</topic><topic>Deletion mutant</topic><topic>Diagnostic systems</topic><topic>Disease</topic><topic>Electrophoresis, Gel, Two-Dimensional</topic><topic>Fluorescence</topic><topic>Gene expression</topic><topic>Genes</topic><topic>Genes, Plant</topic><topic>Genetic engineering</topic><topic>Glycine max</topic><topic>Health aspects</topic><topic>Homeostasis</topic><topic>Host plants</topic><topic>host-pathogen relationships</topic><topic>Infections</topic><topic>Leaves</topic><topic>Lesions</topic><topic>lesions (plant)</topic><topic>Metabolism</topic><topic>Microbiology/Plant-Biotic Interactions</topic><topic>Molecular biology</topic><topic>oranges</topic><topic>Pathogenesis</topic><topic>Pathogens</topic><topic>Peptides</topic><topic>Photosynthesis</topic><topic>Physiology</topic><topic>Plant biochemistry</topic><topic>Plant Biology/Plant Biochemistry and Physiology</topic><topic>Plant Biology/Plant-Biotic Interactions</topic><topic>Plant Leaves - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Garavaglia, Betiana S</au><au>Thomas, Ludivine</au><au>Gottig, Natalia</au><au>Dunger, Germán</au><au>Garofalo, Cecilia G</au><au>Daurelio, Lucas D</au><au>Ndimba, Bongani</au><au>Orellano, Elena G</au><au>Gehring, Chris</au><au>Ottado, Jorgelina</au><au>Ausubel, Frederick M.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Eukaryotic-Acquired Gene by a Biotrophic Phytopathogen Allows Prolonged Survival on the Host by Counteracting the Shut-Down of Plant Photosynthesis</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2010-01-28</date><risdate>2010</risdate><volume>5</volume><issue>1</issue><spage>e8950</spage><epage>e8950</epage><pages>e8950-e8950</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Xanthomonas citri pv. citri, the bacteria responsible for citrus canker posses a biological active plant natriuretic peptide (PNP)-like protein, not present in any other bacteria. PNPs are a class of extracellular, systemically mobile peptides that elicit a number of plant responses important in homeostasis and growth. Previously, we showed that a Xanthomonas citri pv. citri mutant lacking the PNP-like protein XacPNP produced more necrotic lesions in citrus leaves than wild type infections and suggested a role for XacPNP in the regulation of host homeostasis. Here we have analyzed the proteome modifications observed in citrus leaves infected with the wild type and XacPNP deletion mutant bacteria. While both of them cause down-regulation of enzymes related to photosynthesis as well as chloroplastic ribosomal proteins, proteins related to defense responses are up-regulated. However, leaves infiltrated with the XacPNP deletion mutant show a more pronounced decrease in photosynthetic proteins while no reduction in defense related proteins as compared to the wild-type pathogen. This suggests that XacPNP serves the pathogen to maintain host photosynthetic efficiency during pathogenesis. The results from the proteomics analyses are consistent with our chlorophyll fluorescence data and transcript analyses of defense genes that show a more marked reduction in photosynthesis in the mutant but no difference in the induction of genes diagnostic for biotic-stress responses. We therefore conclude that XacPNP counteracts the shut-down of host photosynthesis during infection and in that way maintains the tissue in better conditions, suggesting that the pathogen has adapted a host gene to modify its natural host and render it a better reservoir for prolonged bacterial survival and thus for further colonization.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>20126632</pmid><doi>10.1371/journal.pone.0008950</doi><tpages>e8950</tpages><oa>free_for_read</oa></addata></record> |
fulltext | fulltext |
identifier | ISSN: 1932-6203 |
ispartof | PloS one, 2010-01, Vol.5 (1), p.e8950-e8950 |
issn | 1932-6203 1932-6203 |
language | eng |
recordid | cdi_plos_journals_1289252045 |
source | Publicly Available Content Database; PubMed Central |
subjects | Arabidopsis Bacteria bacterial diseases of plants bacterial proteins Biotechnology Canker cankers (plants) Carotenoids Chlorophyll Chloroplasts Citrus - microbiology Citrus sinensis Colonization Corn Data processing Deletion mutant Diagnostic systems Disease Electrophoresis, Gel, Two-Dimensional Fluorescence Gene expression Genes Genes, Plant Genetic engineering Glycine max Health aspects Homeostasis Host plants host-pathogen relationships Infections Leaves Lesions lesions (plant) Metabolism Microbiology/Plant-Biotic Interactions Molecular biology oranges Pathogenesis Pathogens Peptides Photosynthesis Physiology Plant biochemistry Plant Biology/Plant Biochemistry and Physiology Plant Biology/Plant-Biotic Interactions Plant Leaves - metabolism plant natriuretic peptide Plant photosynthesis Plant Proteins - metabolism Proteins Proteome Proteomics Pseudomonas syringae Reduction Ribosomal proteins signs and symptoms (plants) Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization Survival Transcription Ustilago maydis Xanthomonas - physiology Xanthomonas citri Xanthomonas citri pv. citri |
title | Eukaryotic-Acquired Gene by a Biotrophic Phytopathogen Allows Prolonged Survival on the Host by Counteracting the Shut-Down of Plant Photosynthesis |
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