A nematode venom allergen/ASP-like protein is required for plant-parasitism and induces a hypersensitive response through an extracellular leucine-rich repeat receptor

J.L. Lozano Torres, R.H.P. Wilbers, P. Gawronski, J.C. Boshoven, H.A. Overmars, J.W. van t Klooster, L. Baranowski, M. Sobczak, M. Ilyas, R.A.L. van der Hoorn, A. Schots, P.J.G.M. de Wit, J. Bakker, A. Goverse, G. Smant

Research output: Chapter in Book/Report/Conference proceedingAbstractAcademic

Abstract

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 Rcr3pim protein of S. pimpinellifolium. Binding of the venom allergen-like effector protein Gr-VAP1 of G.rostochiensis to Rcr3pim perturbs the active site of this papain-like cysteine protease. In the absence of the Cf-2 receptor, Rcr3pim 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 Rcr3pim 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.
Original languageEnglish
Title of host publicationProceedings of the Molecular and cellular biology of helminth parasites VII, 02- 09 September 2012, Hydra, Greece
Pages31-31
Publication statusPublished - 2012
EventThe 2012 HYDRA Conference on Molecular and cellular biology of helminth parasites VII, Hydra, Greece -
Duration: 2 Sep 20129 Sep 2012

Conference

ConferenceThe 2012 HYDRA Conference on Molecular and cellular biology of helminth parasites VII, Hydra, Greece
Period2/09/129/09/12

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venoms
hypersensitive response
allergens
leucine
parasitism
Nematoda
receptors
Solanum pimpinellifolium
proteins
Globodera rostochiensis
tomatoes
disease resistance
virulence
red currants
Passalora fulva
fungi
papain
pathogens
nematode infections
cysteine proteinases

Cite this

Lozano Torres, J.L. ; Wilbers, R.H.P. ; Gawronski, P. ; Boshoven, J.C. ; 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. / A nematode venom allergen/ASP-like protein is required for plant-parasitism and induces a hypersensitive response through an extracellular leucine-rich repeat receptor. Proceedings of the Molecular and cellular biology of helminth parasites VII, 02- 09 September 2012, Hydra, Greece. 2012. pp. 31-31
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abstract = "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 Rcr3pim protein of S. pimpinellifolium. Binding of the venom allergen-like effector protein Gr-VAP1 of G.rostochiensis to Rcr3pim perturbs the active site of this papain-like cysteine protease. In the absence of the Cf-2 receptor, Rcr3pim 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 Rcr3pim 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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Lozano Torres, JL, Wilbers, RHP, Gawronski, P, Boshoven, JC, Overmars, HA, van t Klooster, JW, Baranowski, L, Sobczak, M, Ilyas, M, van der Hoorn, RAL, Schots, A, de Wit, PJGM, Bakker, J, Goverse, A & Smant, G 2012, A nematode venom allergen/ASP-like protein is required for plant-parasitism and induces a hypersensitive response through an extracellular leucine-rich repeat receptor. in Proceedings of the Molecular and cellular biology of helminth parasites VII, 02- 09 September 2012, Hydra, Greece. pp. 31-31, The 2012 HYDRA Conference on Molecular and cellular biology of helminth parasites VII, Hydra, Greece, 2/09/12.

A nematode venom allergen/ASP-like protein is required for plant-parasitism and induces a hypersensitive response through an extracellular leucine-rich repeat receptor. / Lozano Torres, J.L.; Wilbers, R.H.P.; Gawronski, P.; Boshoven, J.C.; 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.

Proceedings of the Molecular and cellular biology of helminth parasites VII, 02- 09 September 2012, Hydra, Greece. 2012. p. 31-31.

Research output: Chapter in Book/Report/Conference proceedingAbstractAcademic

TY - CHAP

T1 - A nematode venom allergen/ASP-like protein is required for plant-parasitism and induces a hypersensitive response through an extracellular leucine-rich repeat receptor

AU - Lozano Torres, J.L.

AU - Wilbers, R.H.P.

AU - Gawronski, P.

AU - Boshoven, J.C.

AU - Overmars, H.A.

AU - van t Klooster, J.W.

AU - Baranowski, L.

AU - Sobczak, M.

AU - Ilyas, M.

AU - van der Hoorn, R.A.L.

AU - Schots, A.

AU - de Wit, P.J.G.M.

AU - Bakker, J.

AU - Goverse, A.

AU - Smant, G.

PY - 2012

Y1 - 2012

N2 - 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 Rcr3pim protein of S. pimpinellifolium. Binding of the venom allergen-like effector protein Gr-VAP1 of G.rostochiensis to Rcr3pim perturbs the active site of this papain-like cysteine protease. In the absence of the Cf-2 receptor, Rcr3pim 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 Rcr3pim 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.

AB - 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 Rcr3pim protein of S. pimpinellifolium. Binding of the venom allergen-like effector protein Gr-VAP1 of G.rostochiensis to Rcr3pim perturbs the active site of this papain-like cysteine protease. In the absence of the Cf-2 receptor, Rcr3pim 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 Rcr3pim 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.

M3 - Abstract

SP - 31

EP - 31

BT - Proceedings of the Molecular and cellular biology of helminth parasites VII, 02- 09 September 2012, Hydra, Greece

ER -

Lozano Torres JL, Wilbers RHP, Gawronski P, Boshoven JC, Overmars HA, van t Klooster JW et al. A nematode venom allergen/ASP-like protein is required for plant-parasitism and induces a hypersensitive response through an extracellular leucine-rich repeat receptor. In Proceedings of the Molecular and cellular biology of helminth parasites VII, 02- 09 September 2012, Hydra, Greece. 2012. p. 31-31