Pepper Mannose-Binding Lectin Gene CaMBL1 Is Required to Regulate Cell Death and Defense Responses to Microbial Pathogens

Plant mannose-binding lectins (MBLs) are crucial for plant defense signaling during pathogen attack by recognizing specific carbohydrates on pathogen surfaces. In this study, we isolated and functionally characterized a novel pepper (Capsicum annuum) MBL gene, CaMBL1, from pepper leaves infected wit...

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Veröffentlicht in:Plant physiology (Bethesda) 2011-01, Vol.155 (1), p.447-463
Hauptverfasser: Hwang, In Sun, Hwang, Byung Kook
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description Plant mannose-binding lectins (MBLs) are crucial for plant defense signaling during pathogen attack by recognizing specific carbohydrates on pathogen surfaces. In this study, we isolated and functionally characterized a novel pepper (Capsicum annuum) MBL gene, CaMBL1, from pepper leaves infected with Xanthomonas campestris pv vesicatoria (Xcv). The CaMBL1 gene contains a predicted Galanthus nivalis agglutinin-related lectin domain responsible for the recognition of high-mannose N-glycans but lacks a middle S-locus glycoprotein domain and a carboxyl-terminal PAN-Apple domain. The CaMBL1 protein exhibits binding specificity for mannose and is mainly localized to the plasma membrane. Immunoblotting using a CaMBL1-specific antibody revealed that CaMBL1 is strongly expressed and accumulates in pepper leaves during avirulent Xcv infection. The transient expression of CaMBL1 induces the accumulation of salicylic acid (SA), the activation of defense-related genes, and the cell death phenotype in pepper. The G. nivalis agglutinin-related lectin domain of CaMBL1 is responsible for cell death induction. CaMBL1-silenced pepper plants are more susceptible to virulent or avirulent Xcv infection compared with unsilenced control plants, a phenotype that is accompanied by lowered reactive oxygen species accumulation, reduced expression of downstream SA target genes, and a concomitant decrease in SA accumulation. In contrast, CaMBL1 overexpression in Arabidopsis (Arabidopsis thaliana) confers enhanced resistance to Pseudomonas syringae pv tomato and Alternaria brassicicola infection. Together, these data suggest that CaMBL1 plays a key role in the regulation of plant cell death and defense responses through the induction of downstream defense-related genes and SA accumulation after the recognition of microbial pathogens.
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In this study, we isolated and functionally characterized a novel pepper (Capsicum annuum) MBL gene, CaMBL1, from pepper leaves infected with Xanthomonas campestris pv vesicatoria (Xcv). The CaMBL1 gene contains a predicted Galanthus nivalis agglutinin-related lectin domain responsible for the recognition of high-mannose N-glycans but lacks a middle S-locus glycoprotein domain and a carboxyl-terminal PAN-Apple domain. The CaMBL1 protein exhibits binding specificity for mannose and is mainly localized to the plasma membrane. Immunoblotting using a CaMBL1-specific antibody revealed that CaMBL1 is strongly expressed and accumulates in pepper leaves during avirulent Xcv infection. The transient expression of CaMBL1 induces the accumulation of salicylic acid (SA), the activation of defense-related genes, and the cell death phenotype in pepper. The G. nivalis agglutinin-related lectin domain of CaMBL1 is responsible for cell death induction. CaMBL1-silenced pepper plants are more susceptible to virulent or avirulent Xcv infection compared with unsilenced control plants, a phenotype that is accompanied by lowered reactive oxygen species accumulation, reduced expression of downstream SA target genes, and a concomitant decrease in SA accumulation. In contrast, CaMBL1 overexpression in Arabidopsis (Arabidopsis thaliana) confers enhanced resistance to Pseudomonas syringae pv tomato and Alternaria brassicicola infection. 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In this study, we isolated and functionally characterized a novel pepper (Capsicum annuum) MBL gene, CaMBL1, from pepper leaves infected with Xanthomonas campestris pv vesicatoria (Xcv). The CaMBL1 gene contains a predicted Galanthus nivalis agglutinin-related lectin domain responsible for the recognition of high-mannose N-glycans but lacks a middle S-locus glycoprotein domain and a carboxyl-terminal PAN-Apple domain. The CaMBL1 protein exhibits binding specificity for mannose and is mainly localized to the plasma membrane. Immunoblotting using a CaMBL1-specific antibody revealed that CaMBL1 is strongly expressed and accumulates in pepper leaves during avirulent Xcv infection. The transient expression of CaMBL1 induces the accumulation of salicylic acid (SA), the activation of defense-related genes, and the cell death phenotype in pepper. The G. nivalis agglutinin-related lectin domain of CaMBL1 is responsible for cell death induction. CaMBL1-silenced pepper plants are more susceptible to virulent or avirulent Xcv infection compared with unsilenced control plants, a phenotype that is accompanied by lowered reactive oxygen species accumulation, reduced expression of downstream SA target genes, and a concomitant decrease in SA accumulation. In contrast, CaMBL1 overexpression in Arabidopsis (Arabidopsis thaliana) confers enhanced resistance to Pseudomonas syringae pv tomato and Alternaria brassicicola infection. 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Psychology</subject><subject>Galanthus nivalis</subject><subject>Gene Expression Regulation, Plant</subject><subject>Gene Silencing</subject><subject>Genes, Plant - genetics</subject><subject>Infections</subject><subject>Inoculation</subject><subject>Leaves</subject><subject>Lectins</subject><subject>Lycopersicon esculentum</subject><subject>Mannose - metabolism</subject><subject>Mannose-Binding Lectin - chemistry</subject><subject>Mannose-Binding Lectin - genetics</subject><subject>Mannose-Binding Lectin - metabolism</subject><subject>Models, Biological</subject><subject>Molecular Sequence Data</subject><subject>Pathogens</subject><subject>Peppers</subject><subject>Plant Diseases - microbiology</subject><subject>Plant Leaves - cytology</subject><subject>Plant Leaves - microbiology</subject><subject>Plant physiology and development</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>Protein Binding</subject><subject>Protein Structure, Tertiary</subject><subject>Protein Transport</subject><subject>Proteins</subject><subject>Pseudomonas syringae</subject><subject>Pseudomonas syringae - physiology</subject><subject>Subcellular Fractions - metabolism</subject><subject>Xanthomonas campestris</subject><subject>Xanthomonas campestris - physiology</subject><issn>0032-0889</issn><issn>1532-2548</issn><issn>1532-2548</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2011</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkktv1DAUhS0EosPAkiXgDWKVcv1I7Gwq0SmUSjOigrK2PI4zdZWxUztB6r-vowwDrFjdI51Px_dhhF4TOCUE-Me-n-opqbjk8glakJLRgpZcPkULgKxByvoEvUjpDgAII_w5OqGEQlkxukAP17bvbcQb7X1Itjh3vnF-h9fWDM7jS-stXunN-Zrgq4S_2_vRRdvgIWS9Gzs9ZNt2Hb6werjF2jdZtdYnm_3UhyzSBG-ciWHrdIevMxd2mXiJnrW6S_bVoS7RzZfPN6uvxfrb5dXq07owZQVDIZmVJPdatUCZqTkxtKGyYZSWojZCNhWtRAlEVryU3FYcGNOtAQktiC1hS3Q2x_bjdm8bY_0Qdaf66PY6PqignfrX8e5W7cIvxUCUQvAc8OEQEMP9aNOg9i6ZPLP2NoxJSZG3WWf0_ySlAmrOpqaKmcxbSSna9tgPATWdVfX9VNV81sy__XuII_37jhl4fwB0Mrpro_bGpT8cExwknx5-M3N3aQjx6HPCGYf8dZbo3ey3Oii9iznj5w-avw2QmvGK1uwRTka7wA</recordid><startdate>20110101</startdate><enddate>20110101</enddate><creator>Hwang, In Sun</creator><creator>Hwang, Byung Kook</creator><general>American Society of Plant Biologists</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>7X8</scope><scope>7T7</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>P64</scope><scope>RC3</scope><scope>5PM</scope></search><sort><creationdate>20110101</creationdate><title>Pepper Mannose-Binding Lectin Gene CaMBL1 Is Required to Regulate Cell Death and Defense Responses to Microbial Pathogens</title><author>Hwang, In Sun ; Hwang, Byung Kook</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c560t-83e815636f023c941c2d28d322579c78d6267501864584e64033afc080f07b13</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2011</creationdate><topic>Alternaria brassicicola</topic><topic>Arabidopsis - microbiology</topic><topic>Arabidopsis thaliana</topic><topic>Biological and medical sciences</topic><topic>Capsicum - cytology</topic><topic>Capsicum - genetics</topic><topic>Capsicum - immunology</topic><topic>Capsicum - microbiology</topic><topic>Capsicum annuum</topic><topic>Cell death</topic><topic>Cell Death - genetics</topic><topic>Directional control</topic><topic>DNA, Complementary - genetics</topic><topic>DNA, Complementary - isolation &amp; purification</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Galanthus nivalis</topic><topic>Gene Expression Regulation, Plant</topic><topic>Gene Silencing</topic><topic>Genes, Plant - genetics</topic><topic>Infections</topic><topic>Inoculation</topic><topic>Leaves</topic><topic>Lectins</topic><topic>Lycopersicon esculentum</topic><topic>Mannose - metabolism</topic><topic>Mannose-Binding Lectin - chemistry</topic><topic>Mannose-Binding Lectin - genetics</topic><topic>Mannose-Binding Lectin - metabolism</topic><topic>Models, Biological</topic><topic>Molecular Sequence Data</topic><topic>Pathogens</topic><topic>Peppers</topic><topic>Plant Diseases - microbiology</topic><topic>Plant Leaves - cytology</topic><topic>Plant Leaves - microbiology</topic><topic>Plant physiology and development</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>Protein Binding</topic><topic>Protein Structure, Tertiary</topic><topic>Protein Transport</topic><topic>Proteins</topic><topic>Pseudomonas syringae</topic><topic>Pseudomonas syringae - physiology</topic><topic>Subcellular Fractions - metabolism</topic><topic>Xanthomonas campestris</topic><topic>Xanthomonas campestris - physiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Hwang, In Sun</creatorcontrib><creatorcontrib>Hwang, Byung Kook</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>MEDLINE - Academic</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>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</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>Hwang, In Sun</au><au>Hwang, Byung Kook</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Pepper Mannose-Binding Lectin Gene CaMBL1 Is Required to Regulate Cell Death and Defense Responses to Microbial Pathogens</atitle><jtitle>Plant physiology (Bethesda)</jtitle><addtitle>Plant Physiol</addtitle><date>2011-01-01</date><risdate>2011</risdate><volume>155</volume><issue>1</issue><spage>447</spage><epage>463</epage><pages>447-463</pages><issn>0032-0889</issn><issn>1532-2548</issn><eissn>1532-2548</eissn><coden>PPHYA5</coden><abstract>Plant mannose-binding lectins (MBLs) are crucial for plant defense signaling during pathogen attack by recognizing specific carbohydrates on pathogen surfaces. In this study, we isolated and functionally characterized a novel pepper (Capsicum annuum) MBL gene, CaMBL1, from pepper leaves infected with Xanthomonas campestris pv vesicatoria (Xcv). The CaMBL1 gene contains a predicted Galanthus nivalis agglutinin-related lectin domain responsible for the recognition of high-mannose N-glycans but lacks a middle S-locus glycoprotein domain and a carboxyl-terminal PAN-Apple domain. The CaMBL1 protein exhibits binding specificity for mannose and is mainly localized to the plasma membrane. Immunoblotting using a CaMBL1-specific antibody revealed that CaMBL1 is strongly expressed and accumulates in pepper leaves during avirulent Xcv infection. The transient expression of CaMBL1 induces the accumulation of salicylic acid (SA), the activation of defense-related genes, and the cell death phenotype in pepper. The G. nivalis agglutinin-related lectin domain of CaMBL1 is responsible for cell death induction. CaMBL1-silenced pepper plants are more susceptible to virulent or avirulent Xcv infection compared with unsilenced control plants, a phenotype that is accompanied by lowered reactive oxygen species accumulation, reduced expression of downstream SA target genes, and a concomitant decrease in SA accumulation. In contrast, CaMBL1 overexpression in Arabidopsis (Arabidopsis thaliana) confers enhanced resistance to Pseudomonas syringae pv tomato and Alternaria brassicicola infection. Together, these data suggest that CaMBL1 plays a key role in the regulation of plant cell death and defense responses through the induction of downstream defense-related genes and SA accumulation after the recognition of microbial pathogens.</abstract><cop>Rockville, MD</cop><pub>American Society of Plant Biologists</pub><pmid>21205632</pmid><doi>10.1104/pp.110.164848</doi><tpages>17</tpages><oa>free_for_read</oa></addata></record>
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source Jstor Complete Legacy; Oxford University Press Journals All Titles (1996-Current); MEDLINE; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals
subjects Alternaria brassicicola
Arabidopsis - microbiology
Arabidopsis thaliana
Biological and medical sciences
Capsicum - cytology
Capsicum - genetics
Capsicum - immunology
Capsicum - microbiology
Capsicum annuum
Cell death
Cell Death - genetics
Directional control
DNA, Complementary - genetics
DNA, Complementary - isolation & purification
Fundamental and applied biological sciences. Psychology
Galanthus nivalis
Gene Expression Regulation, Plant
Gene Silencing
Genes, Plant - genetics
Infections
Inoculation
Leaves
Lectins
Lycopersicon esculentum
Mannose - metabolism
Mannose-Binding Lectin - chemistry
Mannose-Binding Lectin - genetics
Mannose-Binding Lectin - metabolism
Models, Biological
Molecular Sequence Data
Pathogens
Peppers
Plant Diseases - microbiology
Plant Leaves - cytology
Plant Leaves - microbiology
Plant physiology and development
Plant Proteins - chemistry
Plant Proteins - genetics
Plant Proteins - metabolism
Plants
PLANTS INTERACTING WITH OTHER ORGANISMS
Protein Binding
Protein Structure, Tertiary
Protein Transport
Proteins
Pseudomonas syringae
Pseudomonas syringae - physiology
Subcellular Fractions - metabolism
Xanthomonas campestris
Xanthomonas campestris - physiology
title Pepper Mannose-Binding Lectin Gene CaMBL1 Is Required to Regulate Cell Death and Defense Responses to Microbial Pathogens
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