A Pectate Lyase-Coding Gene Abundantly Expressed during Early Stages of Infection Is Required for Full Virulence in Alternaria brassicicola
Alternaria brassicicola causes black spot disease of Brassica species. The functional importance of pectin digestion enzymes and unidentified phytotoxins in fungal pathogenesis has been suspected but not verified in A. brassicicola. The fungal transcription factor AbPf2 is essential for pathogenicit...
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| description | Alternaria brassicicola causes black spot disease of Brassica species. The functional importance of pectin digestion enzymes and unidentified phytotoxins in fungal pathogenesis has been suspected but not verified in A. brassicicola. The fungal transcription factor AbPf2 is essential for pathogenicity and induces 106 genes during early pathogenesis, including the pectate lyase-coding gene, PL1332. The aim of this study was to test the importance and roles of PL1332 in pathogenesis. We generated deletion strains of the PL1332 gene, produced heterologous PL1332 proteins, and evaluated their association with virulence. Deletion strains of the PL1332 gene were approximately 30% less virulent than wild-type A. brassicicola, without showing differences in colony expansion on solid media and mycelial growth in nutrient-rich liquid media or minimal media with pectins as a major carbon source. Heterologous PL1332 expressed as fusion proteins digested polygalacturons in vitro. When the fusion proteins were injected into the apoplast between leaf veins of host plants the tissues turned dark brown and soft, resembling necrotic leaf tissue. The PL1332 gene was the first example identified as a general toxin-coding gene and virulence factor among the 106 genes regulated by the transcription factor, AbPf2. It was also the first gene to have its functions investigated among the 19 pectate lyase genes and several hundred putative cell-wall degrading enzymes in A. brassicicola. These results further support the importance of the AbPf2 gene as a key pathogenesis regulator and possible target for agrochemical development. |
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The functional importance of pectin digestion enzymes and unidentified phytotoxins in fungal pathogenesis has been suspected but not verified in A. brassicicola. The fungal transcription factor AbPf2 is essential for pathogenicity and induces 106 genes during early pathogenesis, including the pectate lyase-coding gene, PL1332. The aim of this study was to test the importance and roles of PL1332 in pathogenesis. We generated deletion strains of the PL1332 gene, produced heterologous PL1332 proteins, and evaluated their association with virulence. Deletion strains of the PL1332 gene were approximately 30% less virulent than wild-type A. brassicicola, without showing differences in colony expansion on solid media and mycelial growth in nutrient-rich liquid media or minimal media with pectins as a major carbon source. Heterologous PL1332 expressed as fusion proteins digested polygalacturons in vitro. When the fusion proteins were injected into the apoplast between leaf veins of host plants the tissues turned dark brown and soft, resembling necrotic leaf tissue. The PL1332 gene was the first example identified as a general toxin-coding gene and virulence factor among the 106 genes regulated by the transcription factor, AbPf2. It was also the first gene to have its functions investigated among the 19 pectate lyase genes and several hundred putative cell-wall degrading enzymes in A. brassicicola. These results further support the importance of the AbPf2 gene as a key pathogenesis regulator and possible target for agrochemical development.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0127140</identifier><identifier>PMID: 25996954</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Alternaria - genetics ; Alternaria - pathogenicity ; Analysis ; Apoplast ; Biology ; Biosynthesis ; Biotechnology ; Black spot ; Brassica ; Brassica - microbiology ; Brassicaceae ; Carbon sources ; Cell walls ; Clonal deletion ; Disease ; Enzyme Activation ; Enzymes ; Escherichia coli - genetics ; Escherichia coli - metabolism ; Fungal Proteins - genetics ; Fungi ; Gene Deletion ; Gene expression ; Gene Expression Regulation, Fungal ; Genes ; Host plants ; Infections ; Influence ; Leaves ; Mutation ; Mycelia ; Necrosis - genetics ; Pathogenesis ; Pathogenicity ; Pathogens ; Pectate lyase ; Pectin ; Phenotype ; Physiological aspects ; Phytotoxins ; Plant Diseases - microbiology ; Plant tissues ; Polysaccharide-Lyases - genetics ; Proteins ; Toxins ; Transcription factors ; Virulence ; Virulence (Microbiology) ; Virulence - genetics ; Virulence factors</subject><ispartof>PloS one, 2015-05, Vol.10 (5), p.e0127140-e0127140</ispartof><rights>COPYRIGHT 2015 Public Library of Science</rights><rights>2015 Cho et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://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>2015 Cho et al 2015 Cho et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c692t-95dff3998c7dd58a4e7097f467ca6b773a062d6fe2b5abadb75d5590584597893</citedby><cites>FETCH-LOGICAL-c692t-95dff3998c7dd58a4e7097f467ca6b773a062d6fe2b5abadb75d5590584597893</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/PMC4440746/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4440746/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79342,79343</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25996954$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Cho, Yangrae</creatorcontrib><creatorcontrib>Jang, Mina</creatorcontrib><creatorcontrib>Srivastava, Akhil</creatorcontrib><creatorcontrib>Jang, Jae-Hyuk</creatorcontrib><creatorcontrib>Soung, Nak-Kyun</creatorcontrib><creatorcontrib>Ko, Sung-Kyun</creatorcontrib><creatorcontrib>Kang, Dae-Ook</creatorcontrib><creatorcontrib>Ahn, Jong Seog</creatorcontrib><creatorcontrib>Kim, Bo Yeon</creatorcontrib><title>A Pectate Lyase-Coding Gene Abundantly Expressed during Early Stages of Infection Is Required for Full Virulence in Alternaria brassicicola</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Alternaria brassicicola causes black spot disease of Brassica species. The functional importance of pectin digestion enzymes and unidentified phytotoxins in fungal pathogenesis has been suspected but not verified in A. brassicicola. The fungal transcription factor AbPf2 is essential for pathogenicity and induces 106 genes during early pathogenesis, including the pectate lyase-coding gene, PL1332. The aim of this study was to test the importance and roles of PL1332 in pathogenesis. We generated deletion strains of the PL1332 gene, produced heterologous PL1332 proteins, and evaluated their association with virulence. Deletion strains of the PL1332 gene were approximately 30% less virulent than wild-type A. brassicicola, without showing differences in colony expansion on solid media and mycelial growth in nutrient-rich liquid media or minimal media with pectins as a major carbon source. Heterologous PL1332 expressed as fusion proteins digested polygalacturons in vitro. When the fusion proteins were injected into the apoplast between leaf veins of host plants the tissues turned dark brown and soft, resembling necrotic leaf tissue. The PL1332 gene was the first example identified as a general toxin-coding gene and virulence factor among the 106 genes regulated by the transcription factor, AbPf2. It was also the first gene to have its functions investigated among the 19 pectate lyase genes and several hundred putative cell-wall degrading enzymes in A. brassicicola. These results further support the importance of the AbPf2 gene as a key pathogenesis regulator and possible target for agrochemical development.</description><subject>Alternaria - genetics</subject><subject>Alternaria - pathogenicity</subject><subject>Analysis</subject><subject>Apoplast</subject><subject>Biology</subject><subject>Biosynthesis</subject><subject>Biotechnology</subject><subject>Black spot</subject><subject>Brassica</subject><subject>Brassica - microbiology</subject><subject>Brassicaceae</subject><subject>Carbon sources</subject><subject>Cell walls</subject><subject>Clonal deletion</subject><subject>Disease</subject><subject>Enzyme Activation</subject><subject>Enzymes</subject><subject>Escherichia coli - genetics</subject><subject>Escherichia coli - metabolism</subject><subject>Fungal Proteins - genetics</subject><subject>Fungi</subject><subject>Gene Deletion</subject><subject>Gene expression</subject><subject>Gene Expression Regulation, Fungal</subject><subject>Genes</subject><subject>Host plants</subject><subject>Infections</subject><subject>Influence</subject><subject>Leaves</subject><subject>Mutation</subject><subject>Mycelia</subject><subject>Necrosis - genetics</subject><subject>Pathogenesis</subject><subject>Pathogenicity</subject><subject>Pathogens</subject><subject>Pectate lyase</subject><subject>Pectin</subject><subject>Phenotype</subject><subject>Physiological aspects</subject><subject>Phytotoxins</subject><subject>Plant Diseases - microbiology</subject><subject>Plant tissues</subject><subject>Polysaccharide-Lyases - genetics</subject><subject>Proteins</subject><subject>Toxins</subject><subject>Transcription factors</subject><subject>Virulence</subject><subject>Virulence (Microbiology)</subject><subject>Virulence - genetics</subject><subject>Virulence factors</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><sourceid>DOA</sourceid><recordid>eNqNk91qFDEUxwdRbK2-gWhAEL3YNTP5mMlNYVnaurBQabW3IZOc2aZkk20yI-0z-NJm2m3pSi8kFwknv_M_H8kpivclnpakLr9dhSF65aab4GGKy6ouKX5R7JeCVBNeYfLyyXmveJPSFcaMNJy_LvYqJgQXjO4Xf2boB-he9YCWtyrBZB6M9St0Ah7QrB28Ub53t-joZhMhJTDIDHEEjlTM5vNerSCh0KGF77KODR4tEjqD68HGDHchouPBOXRh4-DAa0DWo5nrIecerUJtVClZbXVw6m3xqlMuwbvtflD8Oj76Of8-WZ6eLOaz5URzUfUTwUzXESEaXRvDGkWhxqLuKK-14m1dE4V5ZXgHVctUq0xbM8OYwKyhTNSNIAfFx3vdjQtJbvuYZMmbilZE4CYTi3vCBHUlN9GuVbyVQVl5ZwhxJVXsrXYggfGal6UhmBqqK5yjKdN0vCU8p8W6rHW4jTa0azAafB-V2xHdvfH2Uq7Cb0kpxTXlWeDLViCG6wFSL9c2aXBOeQjDXd6E1RSTsbJP_6DPV7elVioXYH0Xclw9isoZJRXBApcjNX2GysvAOj-Xh85m-47D1x2HzPRw06_UkJJcnJ_9P3t6sct-fsJegnL9ZQpuGD9b2gXpPahjSClC99jkEstxZh66IceZkduZyW4fnj7Qo9PDkJC_BGERew</recordid><startdate>20150521</startdate><enddate>20150521</enddate><creator>Cho, Yangrae</creator><creator>Jang, Mina</creator><creator>Srivastava, Akhil</creator><creator>Jang, Jae-Hyuk</creator><creator>Soung, Nak-Kyun</creator><creator>Ko, Sung-Kyun</creator><creator>Kang, Dae-Ook</creator><creator>Ahn, Jong Seog</creator><creator>Kim, Bo Yeon</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><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>AEUYN</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>20150521</creationdate><title>A Pectate Lyase-Coding Gene Abundantly Expressed during Early Stages of Infection Is Required for Full Virulence in Alternaria brassicicola</title><author>Cho, Yangrae ; Jang, Mina ; Srivastava, Akhil ; Jang, Jae-Hyuk ; Soung, Nak-Kyun ; Ko, Sung-Kyun ; Kang, Dae-Ook ; Ahn, Jong Seog ; Kim, Bo Yeon</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c692t-95dff3998c7dd58a4e7097f467ca6b773a062d6fe2b5abadb75d5590584597893</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Alternaria - genetics</topic><topic>Alternaria - pathogenicity</topic><topic>Analysis</topic><topic>Apoplast</topic><topic>Biology</topic><topic>Biosynthesis</topic><topic>Biotechnology</topic><topic>Black spot</topic><topic>Brassica</topic><topic>Brassica - microbiology</topic><topic>Brassicaceae</topic><topic>Carbon sources</topic><topic>Cell walls</topic><topic>Clonal deletion</topic><topic>Disease</topic><topic>Enzyme Activation</topic><topic>Enzymes</topic><topic>Escherichia coli - genetics</topic><topic>Escherichia coli - metabolism</topic><topic>Fungal Proteins - genetics</topic><topic>Fungi</topic><topic>Gene Deletion</topic><topic>Gene expression</topic><topic>Gene Expression Regulation, Fungal</topic><topic>Genes</topic><topic>Host plants</topic><topic>Infections</topic><topic>Influence</topic><topic>Leaves</topic><topic>Mutation</topic><topic>Mycelia</topic><topic>Necrosis - genetics</topic><topic>Pathogenesis</topic><topic>Pathogenicity</topic><topic>Pathogens</topic><topic>Pectate lyase</topic><topic>Pectin</topic><topic>Phenotype</topic><topic>Physiological aspects</topic><topic>Phytotoxins</topic><topic>Plant Diseases - microbiology</topic><topic>Plant tissues</topic><topic>Polysaccharide-Lyases - genetics</topic><topic>Proteins</topic><topic>Toxins</topic><topic>Transcription factors</topic><topic>Virulence</topic><topic>Virulence (Microbiology)</topic><topic>Virulence - genetics</topic><topic>Virulence factors</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Cho, Yangrae</creatorcontrib><creatorcontrib>Jang, Mina</creatorcontrib><creatorcontrib>Srivastava, Akhil</creatorcontrib><creatorcontrib>Jang, Jae-Hyuk</creatorcontrib><creatorcontrib>Soung, Nak-Kyun</creatorcontrib><creatorcontrib>Ko, Sung-Kyun</creatorcontrib><creatorcontrib>Kang, Dae-Ook</creatorcontrib><creatorcontrib>Ahn, Jong Seog</creatorcontrib><creatorcontrib>Kim, Bo Yeon</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 One Sustainability</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 - 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The functional importance of pectin digestion enzymes and unidentified phytotoxins in fungal pathogenesis has been suspected but not verified in A. brassicicola. The fungal transcription factor AbPf2 is essential for pathogenicity and induces 106 genes during early pathogenesis, including the pectate lyase-coding gene, PL1332. The aim of this study was to test the importance and roles of PL1332 in pathogenesis. We generated deletion strains of the PL1332 gene, produced heterologous PL1332 proteins, and evaluated their association with virulence. Deletion strains of the PL1332 gene were approximately 30% less virulent than wild-type A. brassicicola, without showing differences in colony expansion on solid media and mycelial growth in nutrient-rich liquid media or minimal media with pectins as a major carbon source. Heterologous PL1332 expressed as fusion proteins digested polygalacturons in vitro. When the fusion proteins were injected into the apoplast between leaf veins of host plants the tissues turned dark brown and soft, resembling necrotic leaf tissue. The PL1332 gene was the first example identified as a general toxin-coding gene and virulence factor among the 106 genes regulated by the transcription factor, AbPf2. It was also the first gene to have its functions investigated among the 19 pectate lyase genes and several hundred putative cell-wall degrading enzymes in A. brassicicola. These results further support the importance of the AbPf2 gene as a key pathogenesis regulator and possible target for agrochemical development.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>25996954</pmid><doi>10.1371/journal.pone.0127140</doi><oa>free_for_read</oa></addata></record> |
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| identifier | ISSN: 1932-6203 |
| ispartof | PloS one, 2015-05, Vol.10 (5), p.e0127140-e0127140 |
| issn | 1932-6203 1932-6203 |
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| subjects | Alternaria - genetics Alternaria - pathogenicity Analysis Apoplast Biology Biosynthesis Biotechnology Black spot Brassica Brassica - microbiology Brassicaceae Carbon sources Cell walls Clonal deletion Disease Enzyme Activation Enzymes Escherichia coli - genetics Escherichia coli - metabolism Fungal Proteins - genetics Fungi Gene Deletion Gene expression Gene Expression Regulation, Fungal Genes Host plants Infections Influence Leaves Mutation Mycelia Necrosis - genetics Pathogenesis Pathogenicity Pathogens Pectate lyase Pectin Phenotype Physiological aspects Phytotoxins Plant Diseases - microbiology Plant tissues Polysaccharide-Lyases - genetics Proteins Toxins Transcription factors Virulence Virulence (Microbiology) Virulence - genetics Virulence factors |
| title | A Pectate Lyase-Coding Gene Abundantly Expressed during Early Stages of Infection Is Required for Full Virulence in Alternaria brassicicola |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-09T17%3A27%3A51IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=A%20Pectate%20Lyase-Coding%20Gene%20Abundantly%20Expressed%20during%20Early%20Stages%20of%20Infection%20Is%20Required%20for%20Full%20Virulence%20in%20Alternaria%20brassicicola&rft.jtitle=PloS%20one&rft.au=Cho,%20Yangrae&rft.date=2015-05-21&rft.volume=10&rft.issue=5&rft.spage=e0127140&rft.epage=e0127140&rft.pages=e0127140-e0127140&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0127140&rft_dat=%3Cgale_plos_%3EA432309018%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1682423908&rft_id=info:pmid/25996954&rft_galeid=A432309018&rft_doaj_id=oai_doaj_org_article_e567611d304d4c20b75ad8f6b367095f&rfr_iscdi=true |