Regulation of cell wall-bound invertase in pepper leaves by Xanthomonas campestris pv. vesicatoria type three effectors
Xanthomonas campestris pv. vesicatoria (Xcv) possess a type 3 secretion system (T3SS) to deliver effector proteins into its Solanaceous host plants. These proteins are involved in suppression of plant defense and in reprogramming of plant metabolism to favour bacterial propagation. There is increasi...
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| Veröffentlicht in: | PloS one 2012-12, Vol.7 (12), p.e51763 |
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| description | Xanthomonas campestris pv. vesicatoria (Xcv) possess a type 3 secretion system (T3SS) to deliver effector proteins into its Solanaceous host plants. These proteins are involved in suppression of plant defense and in reprogramming of plant metabolism to favour bacterial propagation. There is increasing evidence that hexoses contribute to defense responses. They act as substrates for metabolic processes and as metabolic semaphores to regulate gene expression. Especially an increase in the apoplastic hexose-to-sucrose ratio has been suggested to strengthen plant defense. This shift is brought about by the activity of cell wall-bound invertase (cw-Inv). We examined the possibility that Xcv may employ type 3 effector (T3E) proteins to suppress cw-Inv activity during infection. Indeed, pepper leaves infected with a T3SS-deficient Xcv strain showed a higher level of cw-Inv mRNA and enzyme activity relative to Xcv wild type infected leaves. Higher cw-Inv activity was paralleled by an increase in hexoses and mRNA abundance for the pathogenesis-related gene PRQ. These results suggest that Xcv suppresses cw-Inv activity in a T3SS-dependent manner, most likely to prevent sugar-mediated defense signals. To identify Xcv T3Es that regulate cw-Inv activity, a screen was performed with eighteen Xcv strains, each deficient in an individual T3E. Seven Xcv T3E deletion strains caused a significant change in cw-Inv activity compared to Xcv wild type. Among them, Xcv lacking the xopB gene (Xcv ΔxopB) caused the most prominent increase in cw-Inv activity. Deletion of xopB increased the mRNA abundance of PRQ in Xcv ΔxopB-infected pepper leaves, but not of Pti5 and Acre31, two PAMP-triggered immunity markers. Inducible expression of XopB in transgenic tobacco inhibited Xcv-mediated induction of cw-Inv activity observed in wild type plants and resulted in severe developmental phenotypes. Together, these data suggest that XopB interferes with cw-Inv activity in planta to suppress sugar-enhanced defense responses during Xcv infection. |
| doi_str_mv | 10.1371/journal.pone.0051763 |
| format | Article |
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These proteins are involved in suppression of plant defense and in reprogramming of plant metabolism to favour bacterial propagation. There is increasing evidence that hexoses contribute to defense responses. They act as substrates for metabolic processes and as metabolic semaphores to regulate gene expression. Especially an increase in the apoplastic hexose-to-sucrose ratio has been suggested to strengthen plant defense. This shift is brought about by the activity of cell wall-bound invertase (cw-Inv). We examined the possibility that Xcv may employ type 3 effector (T3E) proteins to suppress cw-Inv activity during infection. Indeed, pepper leaves infected with a T3SS-deficient Xcv strain showed a higher level of cw-Inv mRNA and enzyme activity relative to Xcv wild type infected leaves. Higher cw-Inv activity was paralleled by an increase in hexoses and mRNA abundance for the pathogenesis-related gene PRQ. These results suggest that Xcv suppresses cw-Inv activity in a T3SS-dependent manner, most likely to prevent sugar-mediated defense signals. To identify Xcv T3Es that regulate cw-Inv activity, a screen was performed with eighteen Xcv strains, each deficient in an individual T3E. Seven Xcv T3E deletion strains caused a significant change in cw-Inv activity compared to Xcv wild type. Among them, Xcv lacking the xopB gene (Xcv ΔxopB) caused the most prominent increase in cw-Inv activity. Deletion of xopB increased the mRNA abundance of PRQ in Xcv ΔxopB-infected pepper leaves, but not of Pti5 and Acre31, two PAMP-triggered immunity markers. Inducible expression of XopB in transgenic tobacco inhibited Xcv-mediated induction of cw-Inv activity observed in wild type plants and resulted in severe developmental phenotypes. Together, these data suggest that XopB interferes with cw-Inv activity in planta to suppress sugar-enhanced defense responses during Xcv infection.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0051763</identifier><identifier>PMID: 23272161</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Abundance ; Bacteria ; Bacterial Proteins - genetics ; Bacterial Proteins - metabolism ; Bacterial Secretion Systems ; beta-Fructofuranosidase - genetics ; beta-Fructofuranosidase - metabolism ; Biology ; Capsicum - genetics ; Capsicum - immunology ; Capsicum - metabolism ; Capsicum - microbiology ; Carbohydrate Metabolism ; Carbohydrates ; Cell Wall - metabolism ; Cell walls ; Clonal deletion ; Defense industry ; Enzymatic activity ; Enzyme activity ; Enzymes ; Gene Deletion ; Gene expression ; Gene Expression Regulation, Plant ; Genes ; Genetic engineering ; Glucose ; Health aspects ; Hexose ; Hexoses ; Host plants ; Immunity ; Infections ; International economic relations ; Invertase ; Kinases ; Leaves ; Monosaccharides ; Pathogenesis ; Pathogens ; Photosynthesis ; Physiological aspects ; Plant diseases ; Plant Diseases - genetics ; Plant Diseases - immunology ; Plant Diseases - microbiology ; Plant Leaves - genetics ; Plant Leaves - immunology ; Plant Leaves - metabolism ; Plant Leaves - microbiology ; Plant metabolism ; Plant Proteins - genetics ; Plant Proteins - immunology ; Plant resistance ; Plants, Genetically Modified ; Plasmids ; Potatoes ; Propagation ; Proteins ; RNA ; Signal transduction ; Strains (organisms) ; Substrates ; Sucrose ; Sugar ; Tobacco ; Transgenic plants ; Xanthomonas campestris ; Xanthomonas campestris - genetics ; Xanthomonas campestris - immunology ; Xanthomonas campestris - metabolism ; Xanthomonas vesicatoria - genetics ; Xanthomonas vesicatoria - immunology ; Xanthomonas vesicatoria - metabolism</subject><ispartof>PloS one, 2012-12, Vol.7 (12), p.e51763</ispartof><rights>COPYRIGHT 2012 Public Library of Science</rights><rights>2012 Sonnewald 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>2012 Sonnewald et al 2012 Sonnewald et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c758t-4526a82919b4f40eff395246dc7d7f6eb63ce056da8faea5fc8f7506c5cb5c8c3</citedby><cites>FETCH-LOGICAL-c758t-4526a82919b4f40eff395246dc7d7f6eb63ce056da8faea5fc8f7506c5cb5c8c3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3522709/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3522709/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2102,2928,23866,27924,27925,53791,53793,79600,79601</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23272161$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Grebe, Markus</contributor><creatorcontrib>Sonnewald, Sophia</creatorcontrib><creatorcontrib>Priller, Johannes P R</creatorcontrib><creatorcontrib>Schuster, Julia</creatorcontrib><creatorcontrib>Glickmann, Eric</creatorcontrib><creatorcontrib>Hajirezaei, Mohammed-Reza</creatorcontrib><creatorcontrib>Siebig, Stefan</creatorcontrib><creatorcontrib>Mudgett, Mary Beth</creatorcontrib><creatorcontrib>Sonnewald, Uwe</creatorcontrib><title>Regulation of cell wall-bound invertase in pepper leaves by Xanthomonas campestris pv. vesicatoria type three effectors</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Xanthomonas campestris pv. vesicatoria (Xcv) possess a type 3 secretion system (T3SS) to deliver effector proteins into its Solanaceous host plants. These proteins are involved in suppression of plant defense and in reprogramming of plant metabolism to favour bacterial propagation. There is increasing evidence that hexoses contribute to defense responses. They act as substrates for metabolic processes and as metabolic semaphores to regulate gene expression. Especially an increase in the apoplastic hexose-to-sucrose ratio has been suggested to strengthen plant defense. This shift is brought about by the activity of cell wall-bound invertase (cw-Inv). We examined the possibility that Xcv may employ type 3 effector (T3E) proteins to suppress cw-Inv activity during infection. Indeed, pepper leaves infected with a T3SS-deficient Xcv strain showed a higher level of cw-Inv mRNA and enzyme activity relative to Xcv wild type infected leaves. Higher cw-Inv activity was paralleled by an increase in hexoses and mRNA abundance for the pathogenesis-related gene PRQ. These results suggest that Xcv suppresses cw-Inv activity in a T3SS-dependent manner, most likely to prevent sugar-mediated defense signals. To identify Xcv T3Es that regulate cw-Inv activity, a screen was performed with eighteen Xcv strains, each deficient in an individual T3E. Seven Xcv T3E deletion strains caused a significant change in cw-Inv activity compared to Xcv wild type. Among them, Xcv lacking the xopB gene (Xcv ΔxopB) caused the most prominent increase in cw-Inv activity. Deletion of xopB increased the mRNA abundance of PRQ in Xcv ΔxopB-infected pepper leaves, but not of Pti5 and Acre31, two PAMP-triggered immunity markers. Inducible expression of XopB in transgenic tobacco inhibited Xcv-mediated induction of cw-Inv activity observed in wild type plants and resulted in severe developmental phenotypes. Together, these data suggest that XopB interferes with cw-Inv activity in planta to suppress sugar-enhanced defense responses during Xcv infection.</description><subject>Abundance</subject><subject>Bacteria</subject><subject>Bacterial Proteins - genetics</subject><subject>Bacterial Proteins - metabolism</subject><subject>Bacterial Secretion Systems</subject><subject>beta-Fructofuranosidase - genetics</subject><subject>beta-Fructofuranosidase - metabolism</subject><subject>Biology</subject><subject>Capsicum - genetics</subject><subject>Capsicum - immunology</subject><subject>Capsicum - metabolism</subject><subject>Capsicum - microbiology</subject><subject>Carbohydrate Metabolism</subject><subject>Carbohydrates</subject><subject>Cell Wall - metabolism</subject><subject>Cell walls</subject><subject>Clonal deletion</subject><subject>Defense industry</subject><subject>Enzymatic activity</subject><subject>Enzyme activity</subject><subject>Enzymes</subject><subject>Gene Deletion</subject><subject>Gene expression</subject><subject>Gene Expression Regulation, Plant</subject><subject>Genes</subject><subject>Genetic engineering</subject><subject>Glucose</subject><subject>Health aspects</subject><subject>Hexose</subject><subject>Hexoses</subject><subject>Host plants</subject><subject>Immunity</subject><subject>Infections</subject><subject>International economic relations</subject><subject>Invertase</subject><subject>Kinases</subject><subject>Leaves</subject><subject>Monosaccharides</subject><subject>Pathogenesis</subject><subject>Pathogens</subject><subject>Photosynthesis</subject><subject>Physiological aspects</subject><subject>Plant diseases</subject><subject>Plant Diseases - genetics</subject><subject>Plant Diseases - immunology</subject><subject>Plant Diseases - microbiology</subject><subject>Plant Leaves - genetics</subject><subject>Plant Leaves - immunology</subject><subject>Plant Leaves - metabolism</subject><subject>Plant Leaves - microbiology</subject><subject>Plant metabolism</subject><subject>Plant Proteins - genetics</subject><subject>Plant Proteins - immunology</subject><subject>Plant resistance</subject><subject>Plants, Genetically Modified</subject><subject>Plasmids</subject><subject>Potatoes</subject><subject>Propagation</subject><subject>Proteins</subject><subject>RNA</subject><subject>Signal transduction</subject><subject>Strains (organisms)</subject><subject>Substrates</subject><subject>Sucrose</subject><subject>Sugar</subject><subject>Tobacco</subject><subject>Transgenic plants</subject><subject>Xanthomonas campestris</subject><subject>Xanthomonas campestris - genetics</subject><subject>Xanthomonas campestris - immunology</subject><subject>Xanthomonas campestris - 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genetics</topic><topic>Plant Diseases - immunology</topic><topic>Plant Diseases - microbiology</topic><topic>Plant Leaves - genetics</topic><topic>Plant Leaves - immunology</topic><topic>Plant Leaves - metabolism</topic><topic>Plant Leaves - microbiology</topic><topic>Plant metabolism</topic><topic>Plant Proteins - genetics</topic><topic>Plant Proteins - immunology</topic><topic>Plant resistance</topic><topic>Plants, Genetically Modified</topic><topic>Plasmids</topic><topic>Potatoes</topic><topic>Propagation</topic><topic>Proteins</topic><topic>RNA</topic><topic>Signal transduction</topic><topic>Strains (organisms)</topic><topic>Substrates</topic><topic>Sucrose</topic><topic>Sugar</topic><topic>Tobacco</topic><topic>Transgenic plants</topic><topic>Xanthomonas campestris</topic><topic>Xanthomonas campestris - genetics</topic><topic>Xanthomonas campestris - immunology</topic><topic>Xanthomonas campestris - metabolism</topic><topic>Xanthomonas vesicatoria - genetics</topic><topic>Xanthomonas vesicatoria - immunology</topic><topic>Xanthomonas vesicatoria - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Sonnewald, Sophia</creatorcontrib><creatorcontrib>Priller, Johannes P R</creatorcontrib><creatorcontrib>Schuster, Julia</creatorcontrib><creatorcontrib>Glickmann, Eric</creatorcontrib><creatorcontrib>Hajirezaei, Mohammed-Reza</creatorcontrib><creatorcontrib>Siebig, Stefan</creatorcontrib><creatorcontrib>Mudgett, Mary Beth</creatorcontrib><creatorcontrib>Sonnewald, Uwe</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Opposing Viewpoints</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Biotechnology Research Abstracts</collection><collection>Nursing & Allied Health Database</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Meteorological & Geoastrophysical Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Agricultural Science Collection</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Public Health Database</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Technology Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>Materials Science & Engineering Collection</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>Advanced Technologies & Aerospace Collection</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Technology Collection</collection><collection>Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Materials Science Collection</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Materials Science Database</collection><collection>Nursing & Allied Health Database (Alumni Edition)</collection><collection>Meteorological & Geoastrophysical Abstracts - Academic</collection><collection>ProQuest Engineering Collection</collection><collection>ProQuest Biological Science Collection</collection><collection>Agricultural Science Database</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biological Science Database</collection><collection>Engineering Database</collection><collection>Nursing & Allied Health Premium</collection><collection>Advanced Technologies & Aerospace Database</collection><collection>ProQuest Advanced Technologies & Aerospace Collection</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environmental Science Database</collection><collection>Materials Science Collection</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>Engineering Collection</collection><collection>Environmental Science Collection</collection><collection>Genetics Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Sonnewald, Sophia</au><au>Priller, Johannes P R</au><au>Schuster, Julia</au><au>Glickmann, Eric</au><au>Hajirezaei, Mohammed-Reza</au><au>Siebig, Stefan</au><au>Mudgett, Mary Beth</au><au>Sonnewald, Uwe</au><au>Grebe, Markus</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Regulation of cell wall-bound invertase in pepper leaves by Xanthomonas campestris pv. vesicatoria type three effectors</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2012-12-14</date><risdate>2012</risdate><volume>7</volume><issue>12</issue><spage>e51763</spage><pages>e51763-</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Xanthomonas campestris pv. vesicatoria (Xcv) possess a type 3 secretion system (T3SS) to deliver effector proteins into its Solanaceous host plants. These proteins are involved in suppression of plant defense and in reprogramming of plant metabolism to favour bacterial propagation. There is increasing evidence that hexoses contribute to defense responses. They act as substrates for metabolic processes and as metabolic semaphores to regulate gene expression. Especially an increase in the apoplastic hexose-to-sucrose ratio has been suggested to strengthen plant defense. This shift is brought about by the activity of cell wall-bound invertase (cw-Inv). We examined the possibility that Xcv may employ type 3 effector (T3E) proteins to suppress cw-Inv activity during infection. Indeed, pepper leaves infected with a T3SS-deficient Xcv strain showed a higher level of cw-Inv mRNA and enzyme activity relative to Xcv wild type infected leaves. Higher cw-Inv activity was paralleled by an increase in hexoses and mRNA abundance for the pathogenesis-related gene PRQ. These results suggest that Xcv suppresses cw-Inv activity in a T3SS-dependent manner, most likely to prevent sugar-mediated defense signals. To identify Xcv T3Es that regulate cw-Inv activity, a screen was performed with eighteen Xcv strains, each deficient in an individual T3E. Seven Xcv T3E deletion strains caused a significant change in cw-Inv activity compared to Xcv wild type. Among them, Xcv lacking the xopB gene (Xcv ΔxopB) caused the most prominent increase in cw-Inv activity. Deletion of xopB increased the mRNA abundance of PRQ in Xcv ΔxopB-infected pepper leaves, but not of Pti5 and Acre31, two PAMP-triggered immunity markers. Inducible expression of XopB in transgenic tobacco inhibited Xcv-mediated induction of cw-Inv activity observed in wild type plants and resulted in severe developmental phenotypes. Together, these data suggest that XopB interferes with cw-Inv activity in planta to suppress sugar-enhanced defense responses during Xcv infection.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>23272161</pmid><doi>10.1371/journal.pone.0051763</doi><tpages>e51763</tpages><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1932-6203 |
| ispartof | PloS one, 2012-12, Vol.7 (12), p.e51763 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_1327136192 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Public Library of Science (PLoS); PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | Abundance Bacteria Bacterial Proteins - genetics Bacterial Proteins - metabolism Bacterial Secretion Systems beta-Fructofuranosidase - genetics beta-Fructofuranosidase - metabolism Biology Capsicum - genetics Capsicum - immunology Capsicum - metabolism Capsicum - microbiology Carbohydrate Metabolism Carbohydrates Cell Wall - metabolism Cell walls Clonal deletion Defense industry Enzymatic activity Enzyme activity Enzymes Gene Deletion Gene expression Gene Expression Regulation, Plant Genes Genetic engineering Glucose Health aspects Hexose Hexoses Host plants Immunity Infections International economic relations Invertase Kinases Leaves Monosaccharides Pathogenesis Pathogens Photosynthesis Physiological aspects Plant diseases Plant Diseases - genetics Plant Diseases - immunology Plant Diseases - microbiology Plant Leaves - genetics Plant Leaves - immunology Plant Leaves - metabolism Plant Leaves - microbiology Plant metabolism Plant Proteins - genetics Plant Proteins - immunology Plant resistance Plants, Genetically Modified Plasmids Potatoes Propagation Proteins RNA Signal transduction Strains (organisms) Substrates Sucrose Sugar Tobacco Transgenic plants Xanthomonas campestris Xanthomonas campestris - genetics Xanthomonas campestris - immunology Xanthomonas campestris - metabolism Xanthomonas vesicatoria - genetics Xanthomonas vesicatoria - immunology Xanthomonas vesicatoria - metabolism |
| title | Regulation of cell wall-bound invertase in pepper leaves by Xanthomonas campestris pv. vesicatoria type three effectors |
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