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

J.L. Lozano Torres, R.H.P. Wilbers, P. Gawronski, J.C. Boshoven, A.M. Finkers-Tomczak, J.H.G. Cordewener, A.H.P. America, 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 publicationImmunomodulation by plant-associated organisms, Fallen Leaf Lake, California, USA, 16-19 September 2012
Place of PublicationFallen Leaf Lake, California, USA
Pages68-68
Publication statusPublished - 2012
Event30th New Phytologist Symposium Immunomodulation by plant-associated organisms -
Duration: 16 Sep 201219 Sep 2012

Conference

Conference30th New Phytologist Symposium Immunomodulation by plant-associated organisms
Period16/09/1219/09/12

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disease resistance
virulence
Nematoda
tomatoes
Solanum pimpinellifolium
fungi
Globodera rostochiensis
proteins
red currants
Passalora fulva
receptors
papain
pathogens
nematode infections
cysteine proteinases
pathotypes
venoms
plant parasitic nematodes
allergens
active sites

Cite this

Lozano Torres, J. L., Wilbers, R. H. P., Gawronski, P., Boshoven, J. C., Finkers-Tomczak, A. M., Cordewener, J. H. G., ... Smant, G. (2012). Dual Cf-2-mediated disease resistance in tomato requires a common virulence target of a fungus and a nematode. In Immunomodulation by plant-associated organisms, Fallen Leaf Lake, California, USA, 16-19 September 2012 (pp. 68-68). Fallen Leaf Lake, California, USA.
Lozano Torres, J.L. ; 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 Cf-2-mediated disease resistance in tomato requires a common virulence target of a fungus and a nematode. Immunomodulation by plant-associated organisms, Fallen Leaf Lake, California, USA, 16-19 September 2012. Fallen Leaf Lake, California, USA, 2012. pp. 68-68
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title = "Dual Cf-2-mediated disease resistance in tomato requires a common virulence target of a fungus and a nematode",
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, Finkers-Tomczak, AM, Cordewener, JHG, America, AHP, 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, Dual Cf-2-mediated disease resistance in tomato requires a common virulence target of a fungus and a nematode. in Immunomodulation by plant-associated organisms, Fallen Leaf Lake, California, USA, 16-19 September 2012. Fallen Leaf Lake, California, USA, pp. 68-68, 30th New Phytologist Symposium Immunomodulation by plant-associated organisms, 16/09/12.

Dual Cf-2-mediated disease resistance in tomato requires a common virulence target of a fungus and a nematode. / Lozano Torres, J.L.; 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.

Immunomodulation by plant-associated organisms, Fallen Leaf Lake, California, USA, 16-19 September 2012. Fallen Leaf Lake, California, USA, 2012. p. 68-68.

Research output: Chapter in Book/Report/Conference proceedingAbstractAcademic

TY - CHAP

T1 - Dual Cf-2-mediated disease resistance in tomato requires a common virulence target of a fungus and a nematode

AU - Lozano Torres, J.L.

AU - Wilbers, R.H.P.

AU - Gawronski, P.

AU - Boshoven, J.C.

AU - Finkers-Tomczak, A.M.

AU - Cordewener, J.H.G.

AU - America, A.H.P.

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 - 68

EP - 68

BT - Immunomodulation by plant-associated organisms, Fallen Leaf Lake, California, USA, 16-19 September 2012

CY - Fallen Leaf Lake, California, USA

ER -

Lozano Torres JL, Wilbers RHP, Gawronski P, Boshoven JC, Finkers-Tomczak AM, Cordewener JHG et al. Dual Cf-2-mediated disease resistance in tomato requires a common virulence target of a fungus and a nematode. In Immunomodulation by plant-associated organisms, Fallen Leaf Lake, California, USA, 16-19 September 2012. Fallen Leaf Lake, California, USA. 2012. p. 68-68