Receptor-like kinase SOBIR1/EVR interacts with receptor-like proteins in plant immunity against fungal infection

Thomas W. H. Liebrand; Grardy C. M. van den Berg; Zhao Zhang; Patrick Smit; Jan H. G. Cordewener; Antione H. P. America; Jan Sklenar; Alexandra M. E. Jones; Wladimir I. L. Tameling; Silke Robatzek; Bart P. H. J. Thomma; Matthieu H. A. J. Joosten

doi:10.1073/pnas.1220015110

Edited by Paul Schulze-Lefert, Max Planck Institute for Plant Breeding Research, Cologne, Germany, and approved April 30, 2013 (received for review November 16, 2012)

Abstract

The plant immune system is activated by microbial patterns that are detected as nonself molecules. Such patterns are recognized by immune receptors that are cytoplasmic or localized at the plasma membrane. Cell surface receptors are represented by receptor-like kinases (RLKs) that frequently contain extracellular leucine-rich repeats and an intracellular kinase domain for activation of downstream signaling, as well as receptor-like proteins (RLPs) that lack this signaling domain. It is therefore hypothesized that RLKs are required for RLPs to activate downstream signaling. The RLPs Cf-4 and Ve1 of tomato (Solanum lycopersicum) mediate resistance to the fungal pathogens Cladosporium fulvum and Verticillium dahliae, respectively. Despite their importance, the mechanism by which these immune receptors mediate downstream signaling upon recognition of their matching ligand, Avr4 and Ave1, remained enigmatic. Here we show that the tomato ortholog of the Arabidopsis thaliana RLK Suppressor Of BIR1-1/Evershed (SOBIR1/EVR) and its close homolog S. lycopersicum (Sl)SOBIR1-like interact in planta with both Cf-4 and Ve1 and are required for the Cf-4– and Ve1-mediated hypersensitive response and immunity. Tomato SOBIR1/EVR interacts with most of the tested RLPs, but not with the RLKs FLS2, SERK1, SERK3a, BAK1, and CLV1. SOBIR1/EVR is required for stability of the Cf-4 and Ve1 receptors, supporting our observation that these RLPs are present in a complex with SOBIR1/EVR in planta. We show that SOBIR1/EVR is essential for RLP-mediated immunity and propose that the protein functions as a regulatory RLK of this type of cell-surface receptors.

Footnotes

↵¹To whom correspondence should be addressed. E-mail: matthieu.joosten{at}wur.nl.

Author contributions: T.W.H.L., P.S., W.I.L.T., S.R., B.P.H.J.T., and M.H.A.J.J. designed research; T.W.H.L., G.C.M.v.d.B., Z.Z., P.S., J.H.G.C., A.H.P.A., J.S., and A.M.E.J. performed research; T.W.H.L., A.H.P.A., A.M.E.J., W.I.L.T., S.R., B.P.H.J.T., and M.H.A.J.J. analyzed data; and T.W.H.L., W.I.L.T., S.R., B.P.H.J.T., and M.H.A.J.J. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
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