Genome analysis of poplar LRR-RLP gene clusters reveals RISP, a defense-related gene coding a candidate endogenous peptide elicitor.

Benjamin Petre,StÃ©phane Hacquard,SÃ©bastien Duplessis,Nicolas Rouhier

doi:10.3389/fpls.2014.00111

Abstract

In plants, cell-surface receptors control immunity and development through the recognition of extracellular ligands. Leucine-rich repeat receptor-like proteins (LRR-RLPs) constitute a large multigene family of cell-surface receptors. Although this family has been intensively studied, a limited number of ligands has been identified so far, mostly because methods used for their identification and characterization are complex and fastidious. In this study, we combined genome and transcriptome analyses to describe the LRR-RLP gene family in the model tree poplar (Populus trichocarpa). In total, 82 LRR-RLP genes have been identified in P. trichocarpa genome, among which 66 are organized in clusters of up to seven members. In these clusters, LRR-RLP genes are interspersed by orphan, poplar-specific genes encoding small proteins of unknown function (SPUFs). In particular, the nine largest clusters of LRR-RLP genes (47 LRR-RLPs) include 71 SPUF genes that account for 59% of the non-LRR-RLP gene content within these clusters. Forty-four LRR-RLP and 55 SPUF genes are expressed in poplar leaves, mostly at low levels, except for members of some clusters that show higher and sometimes coordinated expression levels. Notably, wounding of poplar leaves strongly induced the expression of a defense SPUF gene named Rust-Induced Secreted protein (RISP) that has been previously reported as a marker of poplar defense responses. Interestingly, we show that the RISP-associated LRR-RLP gene is highly expressed in poplar leaves and slightly induced by wounding. Both gene promoters share a highly conserved region of ~300 nucleotides. This led us to hypothesize that the corresponding pair of proteins could be involved in poplar immunity, possibly as a ligand/receptor couple. In conclusion, we speculate that some poplar SPUFs, such as RISP, represent candidate endogenous peptide ligands of the associated LRR-RLPs and we discuss how to investigate further this hypothesis.

Highlights

Plants possess cell-surface receptors able to recognize extracellular molecules for subsequent intracellular signaling (Monaghan and Zipfel, 2012)
In this study, by analysing the leucine-rich repeats (LRRs)-RLP gene family in poplar, we observed that LRR-RLP genes are arranged into large clusters which are interspaced by genes coding SPUFs
Based on the observed co-regulation upon wounding of Rust-Induced Secreted protein (RISP) and its physically associated LRR-RLP and on the presence of similar regulatory elements in their promoter regions, we hypothesize that both gene products may be functionally linked and by extension we suggest that some SPUFs could represent candidate endogenous ligands of their genome associated LRR-RLPs

Summary

Introduction

Plants possess cell-surface receptors able to recognize extracellular molecules for subsequent intracellular signaling (Monaghan and Zipfel, 2012). Cell-surface receptors are organized into distinct families, which present a common architecture with a cytoplasmic part, a transmembrane domain and an extracellular part. In order to trigger signaling, RLKs use their own kinase domain, whereas RLPs likely require association with RLKs at the plasma membrane (Liebrand et al, 2013). A variety of extracellular domains, which directly interact with apoplastic ligands, have been described; the most common being composed of leucine-rich repeats (LRRs) (Monaghan and Zipfel, 2012; Sun et al, 2013). RLKs and RLPs with extracellular LRRs are abbreviated LRR-RLKs and LRR-RLPs, respectively

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