Genome-wide functional analyses of plant coiled-coil NLR-type pathogen receptors reveal essential roles of their N-terminal domain in oligomerization, networking, and immunity.

Maria José Truco,Dariusz Gozdowski,Andrei-Jose Petrescu,Keri Cavanaugh,Frank L.W Takken,Krzysztof Pawłowski,Laurentiu Spiridon,Huaqin Xu,Eliza Cristina Martin,Richard W Michelmore,Tadeusz Wróblewski

doi:10.1371/journal.pbio.2005821

Abstract

The ability to induce a defense response after pathogen attack is a critical feature of the immune system of any organism. Nucleotide-binding leucine-rich repeat receptors (NLRs) are key players in this process and perceive the occurrence of nonself-activities or foreign molecules. In plants, coevolution with a variety of pests and pathogens has resulted in repertoires of several hundred diverse NLRs in single individuals and many more in populations as a whole. However, the mechanism by which defense signaling is triggered by these NLRs in plants is poorly understood. Here, we show that upon pathogen perception, NLRs use their N-terminal domains to transactivate other receptors. Their N-terminal domains homo- and heterodimerize, suggesting that plant NLRs oligomerize upon activation, similar to the vertebrate NLRs; however, consistent with their large number in plants, the complexes are highly heterometric. Also, in contrast to metazoan NLRs, the N-terminus, rather than their centrally located nucleotide-binding (NB) domain, can mediate initial partner selection. The highly redundant network of NLR interactions in plants is proposed to provide resilience to perturbation by pathogens.

Highlights

Signal Transduction ATPases (STAND proteins) comprise an ancient group of modular proteins sharing a conserved nucleotide-binding (NB) domain [1]
The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript
Members of two major groups of STAND proteins, the nucleotide-binding oligomerization domain (NOD)-like receptors and the nucleotide-binding ARC [1] domain (NB–ARC or NB)-containing apoptotic proteins, include some of the key players involved in the induction of immune responses or programmed cell death, respectively [1,3]

Summary

Introduction

Signal Transduction ATPases (STAND proteins) comprise an ancient group of modular proteins sharing a conserved nucleotide-binding (NB) domain [1]. Members of two major groups of STAND proteins, the nucleotide-binding oligomerization domain (NOD)-like receptors ( referred to as NACHT [1] or animal nucleotide-binding leucine-rich repeat receptors [NLR]) and the nucleotide-binding ARC [1] domain (NB–ARC or NB)-containing apoptotic proteins, include some of the key players involved in the induction of immune responses or programmed cell death (pcd), respectively [1,3]. The bacterial transcription factor MalT, which is evolutionarily related to ancestral STAND proteins, oligomerizes to form a curved homopolymer upon its activation [12]. In all of these cases, oligomerization of the central NB or NOD domain serves to bring the N-terminal domains in close proximity, allowing their partners to interact and induce downstream signaling [13]. Formation of apoptosome-like complexes facilitating the induced proximity of N-terminal domains may represent a common feature of STAND proteins [13]

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Discussion

Conclusion