Identification of tomato phosphatidylinositol-specific phospholipase-C (PI-PLC) family members and the role of PLC4 and PLC6 in HR and disease resistance

Autores
Vossen, Jack H.; Abd El Haliem, Ahmed; Fradin, Emilie F.; Berg, Grardy C. M. van den; Ekengren, Sophia K.; Meijer, Harold J. G.; Seifi, Alireza; Bai, Yuling; Ten Have, Arjen; Munnik, Teun; Thomma, Bart P. H. J.; Joosten, Matthieu H. A. J.
Año de publicación
2010
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
The perception of pathogen-derived elicitors by plants has been suggested to involve phosphatidylinositol-specific phospholipase-C (PI-PLC) signalling. Here we show that PLC isoforms are required for the hypersensitive response (HR) and disease resistance. We characterised the tomato [Solanum lycopersicum (Sl)] PLC gene family. Six Sl PLC-encoding cDNAs were isolated and their expression in response to infection with the pathogenic fungus Cladosporium fulvum was studied. We found significant regulation at the transcriptional level of the various SlPLCs, and SlPLC4 and SlPLC6 showed distinct expression patterns in C. fulvum-resistant Cf-4 tomato. We produced the encoded proteins in Escherichia coli and found that both genes encode catalytically active PI-PLCs. To test the requirement of these Sl PLCs for full Cf-4-mediated recognition of the effector Avr4, we knocked down the expression of the encoding genes by virus-induced gene silencing. Silencing of SlPLC4 impaired the Avr4/Cf-4-induced HR and resulted in increased colonisation of Cf-4 plants by C. fulvum expressing Avr4. Furthermore, expression of the gene in Nicotiana benthamiana enhanced the Avr4/Cf-4-induced HR. Silencing of SlPLC6 did not affect HR, whereas it caused increased colonisation of Cf-4 plants by the fungus. Interestingly, Sl PLC6, but not Sl PLC4, was also required for resistance to Verticillium dahliae, mediated by the transmembrane Ve1 resistance protein, and to Pseudomonas syringae, mediated by the intracellular Pto/Prf resistance protein couple. We conclude that there is a differential requirement of PLC isoforms for the plant immune response and that Sl PLC4 is specifically required for Cf-4 function, while Sl PLC6 may be a more general component of resistance protein signalling.
Fil: Vossen, Jack H.. Wageningen University; Países Bajos
Fil: Abd El Haliem, Ahmed. Wageningen University; Países Bajos
Fil: Fradin, Emilie F.. Wageningen University; Países Bajos
Fil: Berg, Grardy C. M. van den . Wageningen University; Países Bajos
Fil: Ekengren, Sophia K.. Boyce Thompson Institute for Plant Research; Estados Unidos
Fil: Meijer, Harold J. G.. Wageningen University; Países Bajos
Fil: Seifi, Alireza. Wageningen University; Países Bajos
Fil: Bai, Yuling. Wageningen University; Países Bajos
Fil: Ten Have, Arjen. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Mar del Plata. Instituto de Investigaciones Biológicas; Argentina. Universidad Nacional de Mar del Plata. Facultad de Ciencias Exactas y Naturales. Instituto de Investigaciones Biológicas; Argentina
Fil: Munnik, Teun. University Of Amsterdam; Países Bajos
Fil: Thomma, Bart P. H. J.. Wageningen University; Países Bajos
Fil: Joosten, Matthieu H. A. J.. Wageningen University; Países Bajos
Materia
Disease Resistance
Nucleotide-Binding Leucine-Rich Repeat
Phospholipid Signalling
Receptor-Like Protein
Virus-Induced Gene Silencing
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/13371

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oai_identifier_str oai:ri.conicet.gov.ar:11336/13371
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Identification of tomato phosphatidylinositol-specific phospholipase-C (PI-PLC) family members and the role of PLC4 and PLC6 in HR and disease resistanceVossen, Jack H.Abd El Haliem, AhmedFradin, Emilie F.Berg, Grardy C. M. van den Ekengren, Sophia K.Meijer, Harold J. G.Seifi, AlirezaBai, YulingTen Have, ArjenMunnik, TeunThomma, Bart P. H. J.Joosten, Matthieu H. A. J.Disease ResistanceNucleotide-Binding Leucine-Rich RepeatPhospholipid SignallingReceptor-Like ProteinVirus-Induced Gene Silencinghttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1The perception of pathogen-derived elicitors by plants has been suggested to involve phosphatidylinositol-specific phospholipase-C (PI-PLC) signalling. Here we show that PLC isoforms are required for the hypersensitive response (HR) and disease resistance. We characterised the tomato [Solanum lycopersicum (Sl)] PLC gene family. Six Sl PLC-encoding cDNAs were isolated and their expression in response to infection with the pathogenic fungus Cladosporium fulvum was studied. We found significant regulation at the transcriptional level of the various SlPLCs, and SlPLC4 and SlPLC6 showed distinct expression patterns in C. fulvum-resistant Cf-4 tomato. We produced the encoded proteins in Escherichia coli and found that both genes encode catalytically active PI-PLCs. To test the requirement of these Sl PLCs for full Cf-4-mediated recognition of the effector Avr4, we knocked down the expression of the encoding genes by virus-induced gene silencing. Silencing of SlPLC4 impaired the Avr4/Cf-4-induced HR and resulted in increased colonisation of Cf-4 plants by C. fulvum expressing Avr4. Furthermore, expression of the gene in Nicotiana benthamiana enhanced the Avr4/Cf-4-induced HR. Silencing of SlPLC6 did not affect HR, whereas it caused increased colonisation of Cf-4 plants by the fungus. Interestingly, Sl PLC6, but not Sl PLC4, was also required for resistance to Verticillium dahliae, mediated by the transmembrane Ve1 resistance protein, and to Pseudomonas syringae, mediated by the intracellular Pto/Prf resistance protein couple. We conclude that there is a differential requirement of PLC isoforms for the plant immune response and that Sl PLC4 is specifically required for Cf-4 function, while Sl PLC6 may be a more general component of resistance protein signalling.Fil: Vossen, Jack H.. Wageningen University; Países BajosFil: Abd El Haliem, Ahmed. Wageningen University; Países BajosFil: Fradin, Emilie F.. Wageningen University; Países BajosFil: Berg, Grardy C. M. van den . Wageningen University; Países BajosFil: Ekengren, Sophia K.. Boyce Thompson Institute for Plant Research; Estados UnidosFil: Meijer, Harold J. G.. Wageningen University; Países BajosFil: Seifi, Alireza. Wageningen University; Países BajosFil: Bai, Yuling. Wageningen University; Países BajosFil: Ten Have, Arjen. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Mar del Plata. Instituto de Investigaciones Biológicas; Argentina. Universidad Nacional de Mar del Plata. Facultad de Ciencias Exactas y Naturales. Instituto de Investigaciones Biológicas; ArgentinaFil: Munnik, Teun. University Of Amsterdam; Países BajosFil: Thomma, Bart P. H. J.. Wageningen University; Países BajosFil: Joosten, Matthieu H. A. J.. Wageningen University; Países BajosWiley2010-05info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/13371Vossen, Jack H.; Abd El Haliem, Ahmed; Fradin, Emilie F.; Berg, Grardy C. M. van den ; Ekengren, Sophia K.; et al.; Identification of tomato phosphatidylinositol-specific phospholipase-C (PI-PLC) family members and the role of PLC4 and PLC6 in HR and disease resistance; Wiley; Plant Journal; 62; 2; 5-2010; 224-2390960-74121365-313Xenginfo:eu-repo/semantics/altIdentifier/url/http://onlinelibrary.wiley.com/doi/10.1111/j.1365-313X.2010.04136.x/abstractinfo:eu-repo/semantics/altIdentifier/doi/10.1111/j.1365-313X.2010.04136.xinfo:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-11-12T09:40:20Zoai:ri.conicet.gov.ar:11336/13371instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-11-12 09:40:20.887CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Identification of tomato phosphatidylinositol-specific phospholipase-C (PI-PLC) family members and the role of PLC4 and PLC6 in HR and disease resistance
title Identification of tomato phosphatidylinositol-specific phospholipase-C (PI-PLC) family members and the role of PLC4 and PLC6 in HR and disease resistance
spellingShingle Identification of tomato phosphatidylinositol-specific phospholipase-C (PI-PLC) family members and the role of PLC4 and PLC6 in HR and disease resistance
Vossen, Jack H.
Disease Resistance
Nucleotide-Binding Leucine-Rich Repeat
Phospholipid Signalling
Receptor-Like Protein
Virus-Induced Gene Silencing
title_short Identification of tomato phosphatidylinositol-specific phospholipase-C (PI-PLC) family members and the role of PLC4 and PLC6 in HR and disease resistance
title_full Identification of tomato phosphatidylinositol-specific phospholipase-C (PI-PLC) family members and the role of PLC4 and PLC6 in HR and disease resistance
title_fullStr Identification of tomato phosphatidylinositol-specific phospholipase-C (PI-PLC) family members and the role of PLC4 and PLC6 in HR and disease resistance
title_full_unstemmed Identification of tomato phosphatidylinositol-specific phospholipase-C (PI-PLC) family members and the role of PLC4 and PLC6 in HR and disease resistance
title_sort Identification of tomato phosphatidylinositol-specific phospholipase-C (PI-PLC) family members and the role of PLC4 and PLC6 in HR and disease resistance
dc.creator.none.fl_str_mv Vossen, Jack H.
Abd El Haliem, Ahmed
Fradin, Emilie F.
Berg, Grardy C. M. van den
Ekengren, Sophia K.
Meijer, Harold J. G.
Seifi, Alireza
Bai, Yuling
Ten Have, Arjen
Munnik, Teun
Thomma, Bart P. H. J.
Joosten, Matthieu H. A. J.
author Vossen, Jack H.
author_facet Vossen, Jack H.
Abd El Haliem, Ahmed
Fradin, Emilie F.
Berg, Grardy C. M. van den
Ekengren, Sophia K.
Meijer, Harold J. G.
Seifi, Alireza
Bai, Yuling
Ten Have, Arjen
Munnik, Teun
Thomma, Bart P. H. J.
Joosten, Matthieu H. A. J.
author_role author
author2 Abd El Haliem, Ahmed
Fradin, Emilie F.
Berg, Grardy C. M. van den
Ekengren, Sophia K.
Meijer, Harold J. G.
Seifi, Alireza
Bai, Yuling
Ten Have, Arjen
Munnik, Teun
Thomma, Bart P. H. J.
Joosten, Matthieu H. A. J.
author2_role author
author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Disease Resistance
Nucleotide-Binding Leucine-Rich Repeat
Phospholipid Signalling
Receptor-Like Protein
Virus-Induced Gene Silencing
topic Disease Resistance
Nucleotide-Binding Leucine-Rich Repeat
Phospholipid Signalling
Receptor-Like Protein
Virus-Induced Gene Silencing
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv The perception of pathogen-derived elicitors by plants has been suggested to involve phosphatidylinositol-specific phospholipase-C (PI-PLC) signalling. Here we show that PLC isoforms are required for the hypersensitive response (HR) and disease resistance. We characterised the tomato [Solanum lycopersicum (Sl)] PLC gene family. Six Sl PLC-encoding cDNAs were isolated and their expression in response to infection with the pathogenic fungus Cladosporium fulvum was studied. We found significant regulation at the transcriptional level of the various SlPLCs, and SlPLC4 and SlPLC6 showed distinct expression patterns in C. fulvum-resistant Cf-4 tomato. We produced the encoded proteins in Escherichia coli and found that both genes encode catalytically active PI-PLCs. To test the requirement of these Sl PLCs for full Cf-4-mediated recognition of the effector Avr4, we knocked down the expression of the encoding genes by virus-induced gene silencing. Silencing of SlPLC4 impaired the Avr4/Cf-4-induced HR and resulted in increased colonisation of Cf-4 plants by C. fulvum expressing Avr4. Furthermore, expression of the gene in Nicotiana benthamiana enhanced the Avr4/Cf-4-induced HR. Silencing of SlPLC6 did not affect HR, whereas it caused increased colonisation of Cf-4 plants by the fungus. Interestingly, Sl PLC6, but not Sl PLC4, was also required for resistance to Verticillium dahliae, mediated by the transmembrane Ve1 resistance protein, and to Pseudomonas syringae, mediated by the intracellular Pto/Prf resistance protein couple. We conclude that there is a differential requirement of PLC isoforms for the plant immune response and that Sl PLC4 is specifically required for Cf-4 function, while Sl PLC6 may be a more general component of resistance protein signalling.
Fil: Vossen, Jack H.. Wageningen University; Países Bajos
Fil: Abd El Haliem, Ahmed. Wageningen University; Países Bajos
Fil: Fradin, Emilie F.. Wageningen University; Países Bajos
Fil: Berg, Grardy C. M. van den . Wageningen University; Países Bajos
Fil: Ekengren, Sophia K.. Boyce Thompson Institute for Plant Research; Estados Unidos
Fil: Meijer, Harold J. G.. Wageningen University; Países Bajos
Fil: Seifi, Alireza. Wageningen University; Países Bajos
Fil: Bai, Yuling. Wageningen University; Países Bajos
Fil: Ten Have, Arjen. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Mar del Plata. Instituto de Investigaciones Biológicas; Argentina. Universidad Nacional de Mar del Plata. Facultad de Ciencias Exactas y Naturales. Instituto de Investigaciones Biológicas; Argentina
Fil: Munnik, Teun. University Of Amsterdam; Países Bajos
Fil: Thomma, Bart P. H. J.. Wageningen University; Países Bajos
Fil: Joosten, Matthieu H. A. J.. Wageningen University; Países Bajos
description The perception of pathogen-derived elicitors by plants has been suggested to involve phosphatidylinositol-specific phospholipase-C (PI-PLC) signalling. Here we show that PLC isoforms are required for the hypersensitive response (HR) and disease resistance. We characterised the tomato [Solanum lycopersicum (Sl)] PLC gene family. Six Sl PLC-encoding cDNAs were isolated and their expression in response to infection with the pathogenic fungus Cladosporium fulvum was studied. We found significant regulation at the transcriptional level of the various SlPLCs, and SlPLC4 and SlPLC6 showed distinct expression patterns in C. fulvum-resistant Cf-4 tomato. We produced the encoded proteins in Escherichia coli and found that both genes encode catalytically active PI-PLCs. To test the requirement of these Sl PLCs for full Cf-4-mediated recognition of the effector Avr4, we knocked down the expression of the encoding genes by virus-induced gene silencing. Silencing of SlPLC4 impaired the Avr4/Cf-4-induced HR and resulted in increased colonisation of Cf-4 plants by C. fulvum expressing Avr4. Furthermore, expression of the gene in Nicotiana benthamiana enhanced the Avr4/Cf-4-induced HR. Silencing of SlPLC6 did not affect HR, whereas it caused increased colonisation of Cf-4 plants by the fungus. Interestingly, Sl PLC6, but not Sl PLC4, was also required for resistance to Verticillium dahliae, mediated by the transmembrane Ve1 resistance protein, and to Pseudomonas syringae, mediated by the intracellular Pto/Prf resistance protein couple. We conclude that there is a differential requirement of PLC isoforms for the plant immune response and that Sl PLC4 is specifically required for Cf-4 function, while Sl PLC6 may be a more general component of resistance protein signalling.
publishDate 2010
dc.date.none.fl_str_mv 2010-05
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/13371
Vossen, Jack H.; Abd El Haliem, Ahmed; Fradin, Emilie F.; Berg, Grardy C. M. van den ; Ekengren, Sophia K.; et al.; Identification of tomato phosphatidylinositol-specific phospholipase-C (PI-PLC) family members and the role of PLC4 and PLC6 in HR and disease resistance; Wiley; Plant Journal; 62; 2; 5-2010; 224-239
0960-7412
1365-313X
url http://hdl.handle.net/11336/13371
identifier_str_mv Vossen, Jack H.; Abd El Haliem, Ahmed; Fradin, Emilie F.; Berg, Grardy C. M. van den ; Ekengren, Sophia K.; et al.; Identification of tomato phosphatidylinositol-specific phospholipase-C (PI-PLC) family members and the role of PLC4 and PLC6 in HR and disease resistance; Wiley; Plant Journal; 62; 2; 5-2010; 224-239
0960-7412
1365-313X
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/url/http://onlinelibrary.wiley.com/doi/10.1111/j.1365-313X.2010.04136.x/abstract
info:eu-repo/semantics/altIdentifier/doi/10.1111/j.1365-313X.2010.04136.x
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Wiley
publisher.none.fl_str_mv Wiley
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
collection CONICET Digital (CONICET)
instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
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