Dual disease resistance mediated by the immune receptor Cf-2 in tomato requires a common virulence target of a fungus and a nematode

Plants lack the seemingly unlimited receptor diversity of a somatic adaptive immune system as found in vertebrates and rely on only a relatively small set of innate immune receptors to resist a myriad of pathogens. Here, we show that disease-resistant tomato plants use an efficient mechanism to leverage the limited nonself recognition capacity of their innate immune system. We found that the extracellular plant immune receptor protein Cf-2 of the red currant tomato (Solanum pimpinellifolium) has acquired dual resistance specificity by sensing perturbations in a common virulence target of two independently evolved effectors of a fungus and a nematode. The Cf-2 protein, originally identified as a monospecific immune receptor for the leaf mold fungus Cladosporium fulvum, also mediates disease resistance to the root parasitic nematode Globodera rostochiensis pathotype Ro1-Mierenbos. The Cf-2-mediated dual resistance is triggered by effector-induced perturbations of the apoplastic Rcr3(pim) protein of S. pimpinellifolium. Binding of the venom allergen-like effector protein Gr-VAP1 of G. rostochiensis to Rcr3(pim) perturbs the active site of this papain-like cysteine protease. In the absence of the Cf-2 receptor, Rcr3(pim) increases the susceptibility of tomato plants to G. rostochiensis, thus showing its role as a virulence target of these nematodes. Furthermore, both nematode infection and transient expression of Gr-VAP1 in tomato plants harboring Cf-2 and Rcr3(pim) trigger a defense-related programmed cell death in plant cells. Our data demonstrate that monitoring host proteins targeted by multiple pathogens broadens the spectrum of disease resistances mediated by single plant immune receptors.

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Main Authors: Lozano, J., Wilbers, R.H.P., Gawronski, P., Boshoven, J.C., Finkers-Tomczak, A.M., Cordewener, J.H.G., America, A.H.P., Overmars, H.A., van t Klooster, J.W., Baranowski, L., Sobczak, M., Ilyas, M., van der Hoorn, R.A.L., Schots, A., de Wit, P.J.G.M., Bakker, J., Goverse, A., Smant, G.
Format: Article/Letter to editor biblioteca
Language:English
Subjects:confers resistance, defense, effector, for-gene specificity, globodera-rostochiensis, physical interaction, phytophthora-infestans, plant-pathogens, potato cyst-nematodes, protein,
Online Access:https://research.wur.nl/en/publications/dual-disease-resistance-mediated-by-the-immune-receptor-cf-2-in-t
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spelling dig-wur-nl-wurpubs-4247452024-09-23 Lozano, J. Wilbers, R.H.P. Gawronski, P. Boshoven, J.C. Finkers-Tomczak, A.M. Cordewener, J.H.G. America, A.H.P. Overmars, H.A. van t Klooster, J.W. Baranowski, L. Sobczak, M. Ilyas, M. van der Hoorn, R.A.L. Schots, A. de Wit, P.J.G.M. Bakker, J. Goverse, A. Smant, G. Article/Letter to editor Proceedings of the National Academy of Sciences of the United States of America 109 (2012) 25 ISSN: 0027-8424 Dual disease resistance mediated by the immune receptor Cf-2 in tomato requires a common virulence target of a fungus and a nematode 2012 Plants lack the seemingly unlimited receptor diversity of a somatic adaptive immune system as found in vertebrates and rely on only a relatively small set of innate immune receptors to resist a myriad of pathogens. Here, we show that disease-resistant tomato plants use an efficient mechanism to leverage the limited nonself recognition capacity of their innate immune system. We found that the extracellular plant immune receptor protein Cf-2 of the red currant tomato (Solanum pimpinellifolium) has acquired dual resistance specificity by sensing perturbations in a common virulence target of two independently evolved effectors of a fungus and a nematode. The Cf-2 protein, originally identified as a monospecific immune receptor for the leaf mold fungus Cladosporium fulvum, also mediates disease resistance to the root parasitic nematode Globodera rostochiensis pathotype Ro1-Mierenbos. The Cf-2-mediated dual resistance is triggered by effector-induced perturbations of the apoplastic Rcr3(pim) protein of S. pimpinellifolium. Binding of the venom allergen-like effector protein Gr-VAP1 of G. rostochiensis to Rcr3(pim) perturbs the active site of this papain-like cysteine protease. In the absence of the Cf-2 receptor, Rcr3(pim) increases the susceptibility of tomato plants to G. rostochiensis, thus showing its role as a virulence target of these nematodes. Furthermore, both nematode infection and transient expression of Gr-VAP1 in tomato plants harboring Cf-2 and Rcr3(pim) trigger a defense-related programmed cell death in plant cells. Our data demonstrate that monitoring host proteins targeted by multiple pathogens broadens the spectrum of disease resistances mediated by single plant immune receptors. en application/pdf https://research.wur.nl/en/publications/dual-disease-resistance-mediated-by-the-immune-receptor-cf-2-in-t 10.1073/pnas.1202867109 https://edepot.wur.nl/212481 confers resistance defense effector for-gene specificity globodera-rostochiensis physical interaction phytophthora-infestans plant-pathogens potato cyst-nematodes protein (c) publisher Wageningen University & Research
institution WUR NL
collection DSpace
country Países bajos
countrycode NL
component Bibliográfico
access En linea
databasecode dig-wur-nl
tag biblioteca
region Europa del Oeste
libraryname WUR Library Netherlands
language English
topic confers resistance
defense
effector
for-gene specificity
globodera-rostochiensis
physical interaction
phytophthora-infestans
plant-pathogens
potato cyst-nematodes
protein
confers resistance
defense
effector
for-gene specificity
globodera-rostochiensis
physical interaction
phytophthora-infestans
plant-pathogens
potato cyst-nematodes
protein
spellingShingle confers resistance
defense
effector
for-gene specificity
globodera-rostochiensis
physical interaction
phytophthora-infestans
plant-pathogens
potato cyst-nematodes
protein
confers resistance
defense
effector
for-gene specificity
globodera-rostochiensis
physical interaction
phytophthora-infestans
plant-pathogens
potato cyst-nematodes
protein
Lozano, J.
Wilbers, R.H.P.
Gawronski, P.
Boshoven, J.C.
Finkers-Tomczak, A.M.
Cordewener, J.H.G.
America, A.H.P.
Overmars, H.A.
van t Klooster, J.W.
Baranowski, L.
Sobczak, M.
Ilyas, M.
van der Hoorn, R.A.L.
Schots, A.
de Wit, P.J.G.M.
Bakker, J.
Goverse, A.
Smant, G.
Dual disease resistance mediated by the immune receptor Cf-2 in tomato requires a common virulence target of a fungus and a nematode
description Plants lack the seemingly unlimited receptor diversity of a somatic adaptive immune system as found in vertebrates and rely on only a relatively small set of innate immune receptors to resist a myriad of pathogens. Here, we show that disease-resistant tomato plants use an efficient mechanism to leverage the limited nonself recognition capacity of their innate immune system. We found that the extracellular plant immune receptor protein Cf-2 of the red currant tomato (Solanum pimpinellifolium) has acquired dual resistance specificity by sensing perturbations in a common virulence target of two independently evolved effectors of a fungus and a nematode. The Cf-2 protein, originally identified as a monospecific immune receptor for the leaf mold fungus Cladosporium fulvum, also mediates disease resistance to the root parasitic nematode Globodera rostochiensis pathotype Ro1-Mierenbos. The Cf-2-mediated dual resistance is triggered by effector-induced perturbations of the apoplastic Rcr3(pim) protein of S. pimpinellifolium. Binding of the venom allergen-like effector protein Gr-VAP1 of G. rostochiensis to Rcr3(pim) perturbs the active site of this papain-like cysteine protease. In the absence of the Cf-2 receptor, Rcr3(pim) increases the susceptibility of tomato plants to G. rostochiensis, thus showing its role as a virulence target of these nematodes. Furthermore, both nematode infection and transient expression of Gr-VAP1 in tomato plants harboring Cf-2 and Rcr3(pim) trigger a defense-related programmed cell death in plant cells. Our data demonstrate that monitoring host proteins targeted by multiple pathogens broadens the spectrum of disease resistances mediated by single plant immune receptors.
format Article/Letter to editor
topic_facet confers resistance
defense
effector
for-gene specificity
globodera-rostochiensis
physical interaction
phytophthora-infestans
plant-pathogens
potato cyst-nematodes
protein
author Lozano, J.
Wilbers, R.H.P.
Gawronski, P.
Boshoven, J.C.
Finkers-Tomczak, A.M.
Cordewener, J.H.G.
America, A.H.P.
Overmars, H.A.
van t Klooster, J.W.
Baranowski, L.
Sobczak, M.
Ilyas, M.
van der Hoorn, R.A.L.
Schots, A.
de Wit, P.J.G.M.
Bakker, J.
Goverse, A.
Smant, G.
author_facet Lozano, J.
Wilbers, R.H.P.
Gawronski, P.
Boshoven, J.C.
Finkers-Tomczak, A.M.
Cordewener, J.H.G.
America, A.H.P.
Overmars, H.A.
van t Klooster, J.W.
Baranowski, L.
Sobczak, M.
Ilyas, M.
van der Hoorn, R.A.L.
Schots, A.
de Wit, P.J.G.M.
Bakker, J.
Goverse, A.
Smant, G.
author_sort Lozano, J.
title Dual disease resistance mediated by the immune receptor Cf-2 in tomato requires a common virulence target of a fungus and a nematode
title_short Dual disease resistance mediated by the immune receptor Cf-2 in tomato requires a common virulence target of a fungus and a nematode
title_full Dual disease resistance mediated by the immune receptor Cf-2 in tomato requires a common virulence target of a fungus and a nematode
title_fullStr Dual disease resistance mediated by the immune receptor Cf-2 in tomato requires a common virulence target of a fungus and a nematode
title_full_unstemmed Dual disease resistance mediated by the immune receptor Cf-2 in tomato requires a common virulence target of a fungus and a nematode
title_sort dual disease resistance mediated by the immune receptor cf-2 in tomato requires a common virulence target of a fungus and a nematode
url https://research.wur.nl/en/publications/dual-disease-resistance-mediated-by-the-immune-receptor-cf-2-in-t
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