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.
Laboratory of Nematology, Wageningen University, 6708 PB, Wageningen, The Netherlands.
Jose L
JL
Lozano-Torres
Ruud H P
RH
Wilbers
Piotr
P
Gawronski
Jordi C
JC
Boshoven
Anna
A
Finkers-Tomczak
Jan H G
JH
Cordewener
Antoine H P
AH
America
Hein A
HA
Overmars
John W
JW
Van 't Klooster
Lukasz
L
Baranowski
Miroslaw
M
Sobczak
Muhammad
M
Ilyas
Renier A L
RA
van der Hoorn
Arjen
A
Schots
Pierre J G M
PJ
de Wit
Jaap
J
Bakker
Aska
A
Goverse
Geert
G
Smant
D000818:Animals; D002963:Cladosporium / Q000472:pathogenicity*; D018551:Solanum lycopersicum / Q000276:immunology*; D008969:Molecular Sequence Data; D009348:Nematoda / Q000472:pathogenicity*; D010935:Plant Diseases / Q000276:immunology*; D011971:Receptors, Immunologic / Q000502:physiology*; D014774:Virulence
D011971:Receptors, Immunologic