Multiple candidate effectors from the oomycete pathogen Hyaloperonospora arabidopsidis suppress host plant immunity
Oomycete pathogens cause diverse plant diseases. To successfully colonize their hosts, they deliver a suite of effector proteins that can attenuate plant defenses. In the oomycete downy mildews, effectors carry a signal peptide and an RxLR motif. Hyaloperonospora arabidopsidis (Hpa) causes downy mil...
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| Veröffentlicht in: | PLoS pathogens 2011-11, Vol.7 (11), p.e1002348-e1002348 |
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| creator | Fabro, Georgina Steinbrenner, Jens Coates, Mary Ishaque, Naveed Baxter, Laura Studholme, David J Körner, Evelyn Allen, Rebecca L Piquerez, Sophie J M Rougon-Cardoso, Alejandra Greenshields, David Lei, Rita Badel, Jorge L Caillaud, Marie-Cecile Sohn, Kee-Hoon Van den Ackerveken, Guido Parker, Jane E Beynon, Jim Jones, Jonathan D G |
| description | Oomycete pathogens cause diverse plant diseases. To successfully colonize their hosts, they deliver a suite of effector proteins that can attenuate plant defenses. In the oomycete downy mildews, effectors carry a signal peptide and an RxLR motif. Hyaloperonospora arabidopsidis (Hpa) causes downy mildew on the model plant Arabidopsis thaliana (Arabidopsis). We investigated if candidate effectors predicted in the genome sequence of Hpa isolate Emoy2 (HaRxLs) were able to manipulate host defenses in different Arabidopsis accessions. We developed a rapid and sensitive screening method to test HaRxLs by delivering them via the bacterial type-three secretion system (TTSS) of Pseudomonas syringae pv tomato DC3000-LUX (Pst-LUX) and assessing changes in Pst-LUX growth in planta on 12 Arabidopsis accessions. The majority (~70%) of the 64 candidates tested positively contributed to Pst-LUX growth on more than one accession indicating that Hpa virulence likely involves multiple effectors with weak accession-specific effects. Further screening with a Pst mutant (ΔCEL) showed that HaRxLs that allow enhanced Pst-LUX growth usually suppress callose deposition, a hallmark of pathogen-associated molecular pattern (PAMP)-triggered immunity (PTI). We found that HaRxLs are rarely strong avirulence determinants. Although some decreased Pst-LUX growth in particular accessions, none activated macroscopic cell death. Fewer HaRxLs conferred enhanced Pst growth on turnip, a non-host for Hpa, while several reduced it, consistent with the idea that turnip's non-host resistance against Hpa could involve a combination of recognized HaRxLs and ineffective HaRxLs. We verified our results by constitutively expressing in Arabidopsis a sub-set of HaRxLs. Several transgenic lines showed increased susceptibility to Hpa and attenuation of Arabidopsis PTI responses, confirming the HaRxLs' role in Hpa virulence. This study shows TTSS screening system provides a useful tool to test whether candidate effectors from eukaryotic pathogens can suppress/trigger plant defense mechanisms and to rank their effectiveness prior to subsequent mechanistic investigation. |
| doi_str_mv | 10.1371/journal.ppat.1002348 |
| format | Article |
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To successfully colonize their hosts, they deliver a suite of effector proteins that can attenuate plant defenses. In the oomycete downy mildews, effectors carry a signal peptide and an RxLR motif. Hyaloperonospora arabidopsidis (Hpa) causes downy mildew on the model plant Arabidopsis thaliana (Arabidopsis). We investigated if candidate effectors predicted in the genome sequence of Hpa isolate Emoy2 (HaRxLs) were able to manipulate host defenses in different Arabidopsis accessions. We developed a rapid and sensitive screening method to test HaRxLs by delivering them via the bacterial type-three secretion system (TTSS) of Pseudomonas syringae pv tomato DC3000-LUX (Pst-LUX) and assessing changes in Pst-LUX growth in planta on 12 Arabidopsis accessions. The majority (~70%) of the 64 candidates tested positively contributed to Pst-LUX growth on more than one accession indicating that Hpa virulence likely involves multiple effectors with weak accession-specific effects. Further screening with a Pst mutant (ΔCEL) showed that HaRxLs that allow enhanced Pst-LUX growth usually suppress callose deposition, a hallmark of pathogen-associated molecular pattern (PAMP)-triggered immunity (PTI). We found that HaRxLs are rarely strong avirulence determinants. Although some decreased Pst-LUX growth in particular accessions, none activated macroscopic cell death. Fewer HaRxLs conferred enhanced Pst growth on turnip, a non-host for Hpa, while several reduced it, consistent with the idea that turnip's non-host resistance against Hpa could involve a combination of recognized HaRxLs and ineffective HaRxLs. We verified our results by constitutively expressing in Arabidopsis a sub-set of HaRxLs. Several transgenic lines showed increased susceptibility to Hpa and attenuation of Arabidopsis PTI responses, confirming the HaRxLs' role in Hpa virulence. This study shows TTSS screening system provides a useful tool to test whether candidate effectors from eukaryotic pathogens can suppress/trigger plant defense mechanisms and to rank their effectiveness prior to subsequent mechanistic investigation.</description><identifier>ISSN: 1553-7374</identifier><identifier>ISSN: 1553-7366</identifier><identifier>EISSN: 1553-7374</identifier><identifier>DOI: 10.1371/journal.ppat.1002348</identifier><identifier>PMID: 22072967</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Airborne microorganisms ; Apoptosis ; Arabidopsis - genetics ; Arabidopsis - immunology ; Arabidopsis - microbiology ; Arabidopsis thaliana ; Bacteria ; Bacterial Secretion Systems ; Biology ; Brassica napus - immunology ; Brassica napus - microbiology ; Candidates ; Cell death ; Cells, Cultured ; Cloning ; Experiments ; Flowers & plants ; Gene Expression Regulation, Plant ; Genomes ; Glucans - biosynthesis ; Glucans - metabolism ; Health aspects ; Host-Pathogen Interactions ; Oomycetes - genetics ; Oomycetes - growth & development ; Oomycetes - metabolism ; Pathogens ; Physiological aspects ; Plant diseases ; Plant Diseases - genetics ; Plant Diseases - immunology ; Plant Diseases - microbiology ; Plants, Genetically Modified ; Proteins ; Proteins - metabolism ; Pseudomonas syringae - enzymology ; Pseudomonas syringae - growth & development ; Pseudomonas syringae - immunology ; Recombinant Fusion Proteins - metabolism ; Risk factors ; Tomatoes ; Water molds</subject><ispartof>PLoS pathogens, 2011-11, Vol.7 (11), p.e1002348-e1002348</ispartof><rights>COPYRIGHT 2011 Public Library of Science</rights><rights>2011 Fabro et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Fabro G, Steinbrenner J, Coates M, Ishaque N, Baxter L, et al. (2011) Multiple Candidate Effectors from the Oomycete Pathogen Hyaloperonospora arabidopsidis Suppress Host Plant Immunity. PLoS Pathog 7(11): e1002348. doi:10.1371/journal.ppat.1002348</rights><rights>Fabro et al. 2011</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c726t-c52bee4582ae089af92f44deb223573ca66e8509eb0993045d7615c9f872cc7b3</citedby><cites>FETCH-LOGICAL-c726t-c52bee4582ae089af92f44deb223573ca66e8509eb0993045d7615c9f872cc7b3</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/PMC3207932/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3207932/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,724,777,781,861,882,2096,2915,23847,27905,27906,53772,53774,79349,79350</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/22072967$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Ausubel, Frederick M.</contributor><creatorcontrib>Fabro, Georgina</creatorcontrib><creatorcontrib>Steinbrenner, Jens</creatorcontrib><creatorcontrib>Coates, Mary</creatorcontrib><creatorcontrib>Ishaque, Naveed</creatorcontrib><creatorcontrib>Baxter, Laura</creatorcontrib><creatorcontrib>Studholme, David J</creatorcontrib><creatorcontrib>Körner, Evelyn</creatorcontrib><creatorcontrib>Allen, Rebecca L</creatorcontrib><creatorcontrib>Piquerez, Sophie J M</creatorcontrib><creatorcontrib>Rougon-Cardoso, Alejandra</creatorcontrib><creatorcontrib>Greenshields, David</creatorcontrib><creatorcontrib>Lei, Rita</creatorcontrib><creatorcontrib>Badel, Jorge L</creatorcontrib><creatorcontrib>Caillaud, Marie-Cecile</creatorcontrib><creatorcontrib>Sohn, Kee-Hoon</creatorcontrib><creatorcontrib>Van den Ackerveken, Guido</creatorcontrib><creatorcontrib>Parker, Jane E</creatorcontrib><creatorcontrib>Beynon, Jim</creatorcontrib><creatorcontrib>Jones, Jonathan D G</creatorcontrib><title>Multiple candidate effectors from the oomycete pathogen Hyaloperonospora arabidopsidis suppress host plant immunity</title><title>PLoS pathogens</title><addtitle>PLoS Pathog</addtitle><description>Oomycete pathogens cause diverse plant diseases. To successfully colonize their hosts, they deliver a suite of effector proteins that can attenuate plant defenses. In the oomycete downy mildews, effectors carry a signal peptide and an RxLR motif. Hyaloperonospora arabidopsidis (Hpa) causes downy mildew on the model plant Arabidopsis thaliana (Arabidopsis). We investigated if candidate effectors predicted in the genome sequence of Hpa isolate Emoy2 (HaRxLs) were able to manipulate host defenses in different Arabidopsis accessions. We developed a rapid and sensitive screening method to test HaRxLs by delivering them via the bacterial type-three secretion system (TTSS) of Pseudomonas syringae pv tomato DC3000-LUX (Pst-LUX) and assessing changes in Pst-LUX growth in planta on 12 Arabidopsis accessions. The majority (~70%) of the 64 candidates tested positively contributed to Pst-LUX growth on more than one accession indicating that Hpa virulence likely involves multiple effectors with weak accession-specific effects. Further screening with a Pst mutant (ΔCEL) showed that HaRxLs that allow enhanced Pst-LUX growth usually suppress callose deposition, a hallmark of pathogen-associated molecular pattern (PAMP)-triggered immunity (PTI). We found that HaRxLs are rarely strong avirulence determinants. Although some decreased Pst-LUX growth in particular accessions, none activated macroscopic cell death. Fewer HaRxLs conferred enhanced Pst growth on turnip, a non-host for Hpa, while several reduced it, consistent with the idea that turnip's non-host resistance against Hpa could involve a combination of recognized HaRxLs and ineffective HaRxLs. We verified our results by constitutively expressing in Arabidopsis a sub-set of HaRxLs. Several transgenic lines showed increased susceptibility to Hpa and attenuation of Arabidopsis PTI responses, confirming the HaRxLs' role in Hpa virulence. This study shows TTSS screening system provides a useful tool to test whether candidate effectors from eukaryotic pathogens can suppress/trigger plant defense mechanisms and to rank their effectiveness prior to subsequent mechanistic investigation.</description><subject>Airborne microorganisms</subject><subject>Apoptosis</subject><subject>Arabidopsis - genetics</subject><subject>Arabidopsis - immunology</subject><subject>Arabidopsis - microbiology</subject><subject>Arabidopsis thaliana</subject><subject>Bacteria</subject><subject>Bacterial Secretion Systems</subject><subject>Biology</subject><subject>Brassica napus - immunology</subject><subject>Brassica napus - microbiology</subject><subject>Candidates</subject><subject>Cell death</subject><subject>Cells, Cultured</subject><subject>Cloning</subject><subject>Experiments</subject><subject>Flowers & plants</subject><subject>Gene Expression Regulation, Plant</subject><subject>Genomes</subject><subject>Glucans - biosynthesis</subject><subject>Glucans - metabolism</subject><subject>Health aspects</subject><subject>Host-Pathogen Interactions</subject><subject>Oomycetes - genetics</subject><subject>Oomycetes - growth & development</subject><subject>Oomycetes - metabolism</subject><subject>Pathogens</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>Plants, Genetically Modified</subject><subject>Proteins</subject><subject>Proteins - metabolism</subject><subject>Pseudomonas syringae - enzymology</subject><subject>Pseudomonas syringae - growth & development</subject><subject>Pseudomonas syringae - immunology</subject><subject>Recombinant Fusion Proteins - metabolism</subject><subject>Risk factors</subject><subject>Tomatoes</subject><subject>Water molds</subject><issn>1553-7374</issn><issn>1553-7366</issn><issn>1553-7374</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2011</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNqVkk1v1DAQhiMEoh_wDxBE4lBx2MVfieMLUlUBXamAxMfZmjiTXa-SONgOYv89XjatuqgX5IOtmWfe1x5Plr2gZEm5pG-3bvIDdMtxhLikhDAuqkfZKS0KvpBcisf3zifZWQhbQgTltHyanTBGJFOlPM3Cp6mLduwwNzA0toGIObYtmuh8yFvv-jxuMHeu3xlMuWS2cWsc8usddG5E7wYXRuchBw-1bdwYbGNDHqZx9BhCvnEh5mMHQ8xt30-Djbtn2ZMWuoDP5_08-_Hh_fer68XNl4-rq8ubhZGsjAtTsBpRFBUDJJWCVrFWiAZrxnghuYGyxKogCmuiFCeiaGRJC6PaSjJjZM3Ps1cH3bFzQc_9CpqySpGKEEkSsToQjYOtHr3twe-0A6v_Bpxfa_DRmg41LxTnRikhFRGkhArqStAKKGWSSs6T1rvZbap7bAwO0UN3JHqcGexGr90vzdNnKM6SwMUs4N3PCUPUvQ0Gu9Q7dFPQivCykFLsrV7_Qz78uJlaQ7q_HVqXbM1eU18yyUtaFpQmavkAlVaDvTVuwNam-FHBm6OCxET8HdcwhaBX377-B_v5mBUH1ngXgsf2rnWU6P3E3z5S7ydezxOfyl7eb_td0e2I8z-NWP1C</recordid><startdate>20111101</startdate><enddate>20111101</enddate><creator>Fabro, Georgina</creator><creator>Steinbrenner, Jens</creator><creator>Coates, Mary</creator><creator>Ishaque, Naveed</creator><creator>Baxter, Laura</creator><creator>Studholme, David J</creator><creator>Körner, Evelyn</creator><creator>Allen, Rebecca L</creator><creator>Piquerez, Sophie J M</creator><creator>Rougon-Cardoso, Alejandra</creator><creator>Greenshields, David</creator><creator>Lei, Rita</creator><creator>Badel, Jorge L</creator><creator>Caillaud, Marie-Cecile</creator><creator>Sohn, Kee-Hoon</creator><creator>Van den Ackerveken, Guido</creator><creator>Parker, Jane E</creator><creator>Beynon, Jim</creator><creator>Jones, Jonathan D G</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>ISN</scope><scope>ISR</scope><scope>3V.</scope><scope>7QL</scope><scope>7U9</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7P</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20111101</creationdate><title>Multiple candidate effectors from the oomycete pathogen Hyaloperonospora arabidopsidis suppress host plant immunity</title><author>Fabro, Georgina ; Steinbrenner, Jens ; Coates, Mary ; Ishaque, Naveed ; Baxter, Laura ; Studholme, David J ; Körner, Evelyn ; Allen, Rebecca L ; Piquerez, Sophie J M ; Rougon-Cardoso, Alejandra ; Greenshields, David ; Lei, Rita ; Badel, Jorge L ; Caillaud, Marie-Cecile ; Sohn, Kee-Hoon ; Van den Ackerveken, Guido ; Parker, Jane E ; Beynon, Jim ; Jones, Jonathan D G</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c726t-c52bee4582ae089af92f44deb223573ca66e8509eb0993045d7615c9f872cc7b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2011</creationdate><topic>Airborne microorganisms</topic><topic>Apoptosis</topic><topic>Arabidopsis - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PLoS pathogens</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Fabro, Georgina</au><au>Steinbrenner, Jens</au><au>Coates, Mary</au><au>Ishaque, Naveed</au><au>Baxter, Laura</au><au>Studholme, David J</au><au>Körner, Evelyn</au><au>Allen, Rebecca L</au><au>Piquerez, Sophie J M</au><au>Rougon-Cardoso, Alejandra</au><au>Greenshields, David</au><au>Lei, Rita</au><au>Badel, Jorge L</au><au>Caillaud, Marie-Cecile</au><au>Sohn, Kee-Hoon</au><au>Van den Ackerveken, Guido</au><au>Parker, Jane E</au><au>Beynon, Jim</au><au>Jones, Jonathan D G</au><au>Ausubel, Frederick M.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Multiple candidate effectors from the oomycete pathogen Hyaloperonospora arabidopsidis suppress host plant immunity</atitle><jtitle>PLoS pathogens</jtitle><addtitle>PLoS Pathog</addtitle><date>2011-11-01</date><risdate>2011</risdate><volume>7</volume><issue>11</issue><spage>e1002348</spage><epage>e1002348</epage><pages>e1002348-e1002348</pages><issn>1553-7374</issn><issn>1553-7366</issn><eissn>1553-7374</eissn><abstract>Oomycete pathogens cause diverse plant diseases. To successfully colonize their hosts, they deliver a suite of effector proteins that can attenuate plant defenses. In the oomycete downy mildews, effectors carry a signal peptide and an RxLR motif. Hyaloperonospora arabidopsidis (Hpa) causes downy mildew on the model plant Arabidopsis thaliana (Arabidopsis). We investigated if candidate effectors predicted in the genome sequence of Hpa isolate Emoy2 (HaRxLs) were able to manipulate host defenses in different Arabidopsis accessions. We developed a rapid and sensitive screening method to test HaRxLs by delivering them via the bacterial type-three secretion system (TTSS) of Pseudomonas syringae pv tomato DC3000-LUX (Pst-LUX) and assessing changes in Pst-LUX growth in planta on 12 Arabidopsis accessions. The majority (~70%) of the 64 candidates tested positively contributed to Pst-LUX growth on more than one accession indicating that Hpa virulence likely involves multiple effectors with weak accession-specific effects. Further screening with a Pst mutant (ΔCEL) showed that HaRxLs that allow enhanced Pst-LUX growth usually suppress callose deposition, a hallmark of pathogen-associated molecular pattern (PAMP)-triggered immunity (PTI). We found that HaRxLs are rarely strong avirulence determinants. Although some decreased Pst-LUX growth in particular accessions, none activated macroscopic cell death. Fewer HaRxLs conferred enhanced Pst growth on turnip, a non-host for Hpa, while several reduced it, consistent with the idea that turnip's non-host resistance against Hpa could involve a combination of recognized HaRxLs and ineffective HaRxLs. We verified our results by constitutively expressing in Arabidopsis a sub-set of HaRxLs. Several transgenic lines showed increased susceptibility to Hpa and attenuation of Arabidopsis PTI responses, confirming the HaRxLs' role in Hpa virulence. This study shows TTSS screening system provides a useful tool to test whether candidate effectors from eukaryotic pathogens can suppress/trigger plant defense mechanisms and to rank their effectiveness prior to subsequent mechanistic investigation.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>22072967</pmid><doi>10.1371/journal.ppat.1002348</doi><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1553-7374 |
| ispartof | PLoS pathogens, 2011-11, Vol.7 (11), p.e1002348-e1002348 |
| issn | 1553-7374 1553-7366 1553-7374 |
| language | eng |
| recordid | cdi_plos_journals_1289080070 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; PubMed Central Open Access; Public Library of Science (PLoS); EZB-FREE-00999 freely available EZB journals; PubMed Central |
| subjects | Airborne microorganisms Apoptosis Arabidopsis - genetics Arabidopsis - immunology Arabidopsis - microbiology Arabidopsis thaliana Bacteria Bacterial Secretion Systems Biology Brassica napus - immunology Brassica napus - microbiology Candidates Cell death Cells, Cultured Cloning Experiments Flowers & plants Gene Expression Regulation, Plant Genomes Glucans - biosynthesis Glucans - metabolism Health aspects Host-Pathogen Interactions Oomycetes - genetics Oomycetes - growth & development Oomycetes - metabolism Pathogens Physiological aspects Plant diseases Plant Diseases - genetics Plant Diseases - immunology Plant Diseases - microbiology Plants, Genetically Modified Proteins Proteins - metabolism Pseudomonas syringae - enzymology Pseudomonas syringae - growth & development Pseudomonas syringae - immunology Recombinant Fusion Proteins - metabolism Risk factors Tomatoes Water molds |
| title | Multiple candidate effectors from the oomycete pathogen Hyaloperonospora arabidopsidis suppress host plant immunity |
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