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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Autores principales: Georgina Fabro, Jens Steinbrenner, Mary Coates, Naveed Ishaque, Laura Baxter, David J Studholme, Evelyn Körner, Rebecca L Allen, Sophie J M Piquerez, Alejandra Rougon-Cardoso, David Greenshields, Rita Lei, Jorge L Badel, Marie-Cecile Caillaud, Kee-Hoon Sohn, Guido Van den Ackerveken, Jane E Parker, Jim Beynon, Jonathan D G Jones
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spelling oai:doaj.org-article:35933c994790406a8ab8418a112717332021-11-18T06:05:10ZMultiple candidate effectors from the oomycete pathogen Hyaloperonospora arabidopsidis suppress host plant immunity.1553-73661553-737410.1371/journal.ppat.1002348https://doaj.org/article/35933c994790406a8ab8418a112717332011-11-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/22072967/pdf/?tool=EBIhttps://doaj.org/toc/1553-7366https://doaj.org/toc/1553-7374Oomycete 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.Georgina FabroJens SteinbrennerMary CoatesNaveed IshaqueLaura BaxterDavid J StudholmeEvelyn KörnerRebecca L AllenSophie J M PiquerezAlejandra Rougon-CardosoDavid GreenshieldsRita LeiJorge L BadelMarie-Cecile CaillaudKee-Hoon SohnGuido Van den AckervekenJane E ParkerJim BeynonJonathan D G JonesPublic Library of Science (PLoS)articleImmunologic diseases. AllergyRC581-607Biology (General)QH301-705.5ENPLoS Pathogens, Vol 7, Iss 11, p e1002348 (2011)
institution DOAJ
collection DOAJ
language EN
topic Immunologic diseases. Allergy
RC581-607
Biology (General)
QH301-705.5
spellingShingle Immunologic diseases. Allergy
RC581-607
Biology (General)
QH301-705.5
Georgina Fabro
Jens Steinbrenner
Mary Coates
Naveed Ishaque
Laura Baxter
David J Studholme
Evelyn Körner
Rebecca L Allen
Sophie J M Piquerez
Alejandra Rougon-Cardoso
David Greenshields
Rita Lei
Jorge L Badel
Marie-Cecile Caillaud
Kee-Hoon Sohn
Guido Van den Ackerveken
Jane E Parker
Jim Beynon
Jonathan D G Jones
Multiple candidate effectors from the oomycete pathogen Hyaloperonospora arabidopsidis suppress host plant immunity.
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.
format article
author Georgina Fabro
Jens Steinbrenner
Mary Coates
Naveed Ishaque
Laura Baxter
David J Studholme
Evelyn Körner
Rebecca L Allen
Sophie J M Piquerez
Alejandra Rougon-Cardoso
David Greenshields
Rita Lei
Jorge L Badel
Marie-Cecile Caillaud
Kee-Hoon Sohn
Guido Van den Ackerveken
Jane E Parker
Jim Beynon
Jonathan D G Jones
author_facet Georgina Fabro
Jens Steinbrenner
Mary Coates
Naveed Ishaque
Laura Baxter
David J Studholme
Evelyn Körner
Rebecca L Allen
Sophie J M Piquerez
Alejandra Rougon-Cardoso
David Greenshields
Rita Lei
Jorge L Badel
Marie-Cecile Caillaud
Kee-Hoon Sohn
Guido Van den Ackerveken
Jane E Parker
Jim Beynon
Jonathan D G Jones
author_sort Georgina Fabro
title Multiple candidate effectors from the oomycete pathogen Hyaloperonospora arabidopsidis suppress host plant immunity.
title_short Multiple candidate effectors from the oomycete pathogen Hyaloperonospora arabidopsidis suppress host plant immunity.
title_full Multiple candidate effectors from the oomycete pathogen Hyaloperonospora arabidopsidis suppress host plant immunity.
title_fullStr Multiple candidate effectors from the oomycete pathogen Hyaloperonospora arabidopsidis suppress host plant immunity.
title_full_unstemmed Multiple candidate effectors from the oomycete pathogen Hyaloperonospora arabidopsidis suppress host plant immunity.
title_sort multiple candidate effectors from the oomycete pathogen hyaloperonospora arabidopsidis suppress host plant immunity.
publisher Public Library of Science (PLoS)
publishDate 2011
url https://doaj.org/article/35933c994790406a8ab8418a11271733
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