Comparative analysis of plant immune receptor architectures uncovers host proteins likely targeted by pathogens.

Panagiotis F Sarris,Jonathan D G Jones,Ksenia V Krasileva,Gulay Dagdas,Volkan Cevik

doi:10.1186/s12915-016-0228-7

Panagiotis F Sarris, Jonathan D G Jones + Show 3 more

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https://doi.org/10.1186/s12915-016-0228-7

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Abstract

BackgroundPlants deploy immune receptors to detect pathogen-derived molecules and initiate defense responses. Intracellular plant immune receptors called nucleotide-binding leucine-rich repeat (NLR) proteins contain a central nucleotide-binding (NB) domain followed by a series of leucine-rich repeats (LRRs), and are key initiators of plant defense responses. However, recent studies demonstrated that NLRs with non-canonical domain architectures play an important role in plant immunity. These composite immune receptors are thought to arise from fusions between NLRs and additional domains that serve as “baits” for the pathogen-derived effector proteins, thus enabling pathogen recognition. Several names have been proposed to describe these proteins, including “integrated decoys” and “integrated sensors”. We adopt and argue for “integrated domains” or NLR-IDs, which describes the product of the fusion without assigning a universal mode of action.ResultsWe have scanned available plant genome sequences for the full spectrum of NLR-IDs to evaluate the diversity of integrations of potential sensor/decoy domains across flowering plants, including 19 crop species. We manually curated wheat and brassicas and experimentally validated a subset of NLR-IDs in wild and cultivated wheat varieties. We have examined NLR fusions that occur in multiple plant families and identified that some domains show re-occurring integration across lineages. Domains fused to NLRs overlap with previously identified pathogen targets confirming that they act as baits for the pathogen. While some of the integrated domains have been previously implicated in disease resistance, others provide new targets for engineering durable resistance to plant pathogens.ConclusionsWe have built a robust reproducible pipeline for detecting variable domain architectures in plant immune receptors across species. We hypothesize that NLR-IDs that we revealed provide clues to the host proteins targeted by pathogens, and that this information can be deployed to discover new sources of disease resistance.Electronic supplementary materialThe online version of this article (doi:10.1186/s12915-016-0228-7) contains supplementary material, which is available to authorized users.

Highlights

Plants deploy immune receptors to detect pathogen-derived molecules and initiate defense responses
Benchmarking on Arabidopsis showed that the NB-ARC domain is specific to nucleotide-binding leucine-rich repeat (NLR) proteins with 169 proteins detected (215 splice variants), including 149 previously published NLR sequences [13] and 20 NB-ARCcontaining proteins with no leucine-rich repeats (LRR), and no false positive other ATPases detected
We have found the WRKY domain to be present in 35 NLR-integrated domain (ID) genes from 13 plant species, in monocots and dicots, including previously reported A. thaliana, A. lyrata, Fragaria vesca, Capsella rubella, Glycine max, Theobroma cacao, Sorghum bicolor, Setaria italica, O. sativa [62] as well as in M. domestica, Conradina grandiflora, B. distachyon, Hordeum vulgare, T. aestivum and T. urartu (Table 1, Additional file 15)

Summary

Introduction

Plants deploy immune receptors to detect pathogen-derived molecules and initiate defense responses. Recent studies demonstrated that NLRs with non-canonical domain architectures play an important role in plant immunity These composite immune receptors are thought to arise from fusions between NLRs and additional domains that serve as “baits” for the pathogen-derived effector proteins, enabling pathogen recognition. ETI is initiated by plant receptors called nucleotide-binding leucine-rich repeat (NLR) proteins, which detect the presence of pathogen-derived effectors within plant cells and activate defense via as yet poorly understood mechanisms [2, 4]. Since one of the functions of the effectors inside plant cells is to disarm plant defense responses, there is a constant evolutionary arms race between pathogen effectors and components of plant immunity This puts immense selection on pathogen effector genes [7,8,9] and on the effector targets and immune receptors in the plant [10,11,12]. Plant receptors evolve rapidly via various mechanisms, including point mutations, gene duplications and gene rearrangements [13, 14]

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