Plant pathogens convergently evolved to counteract redundant nodes of an NLR immune receptor network.

Lida Derevnina,Sophien Kamoun,Jessica Upson,Mauricio P Contreras,Aska Goverse,Jan Skłenar,Dan Maclean,Rongrong Xie,Sam T Mugford,Angel Vergara Cruces,Abbas Maqbool,Frank L H Menke,Saskia A Hogenhout,Wenbo Ma,Chih-Hang Wu,Hiroaki Adachi,Xinnian Dong

doi:10.1371/journal.pbio.3001136

Abstract

In plants, nucleotide-binding domain and leucine-rich repeat (NLR)-containing proteins can form receptor networks to confer hypersensitive cell death and innate immunity. One class of NLRs, known as NLR required for cell death (NRCs), are central nodes in a complex network that protects against multiple pathogens and comprises up to half of the NLRome of solanaceous plants. Given the prevalence of this NLR network, we hypothesised that pathogens convergently evolved to secrete effectors that target NRC activities. To test this, we screened a library of 165 bacterial, oomycete, nematode, and aphid effectors for their capacity to suppress the cell death response triggered by the NRC-dependent disease resistance proteins Prf and Rpi-blb2. Among 5 of the identified suppressors, 1 cyst nematode protein and 1 oomycete protein suppress the activity of autoimmune mutants of NRC2 and NRC3, but not NRC4, indicating that they specifically counteract a subset of NRC proteins independently of their sensor NLR partners. Whereas the cyst nematode effector SPRYSEC15 binds the nucleotide-binding domain of NRC2 and NRC3, the oomycete effector AVRcap1b suppresses the response of these NRCs via the membrane trafficking-associated protein NbTOL9a (Target of Myb 1-like protein 9a). We conclude that plant pathogens have evolved to counteract central nodes of the NRC immune receptor network through different mechanisms. Coevolution with pathogen effectors may have driven NRC diversification into functionally redundant nodes in a massively expanded NLR network.

Highlights

Our view of the pathogenicity mechanisms of plant pathogens and pests has significantly broadened over the years
We confirmed this hypothesis by carrying out an effectoromics screen, which yielded 5 effectors that can compromise the NLR required for cell death (NRC) network: SS10, SS15, and SS34 from the cyst nematode G. rostochiensis and AVRcap1b and PITG-15278 from the potato late blight pathogen P. infestans
These 5 effectors can suppress the hypersensitive cell death induced in N. benthamiana by either Prf or Rpiblb2, 2 NRC-dependent sensor NLRs that function as bona fide disease resistance proteins

Summary

Introduction

Our view of the pathogenicity mechanisms of plant pathogens and pests has significantly broadened over the years. As a consequence, deciphering the biochemical activities of effectors to understand how parasites successfully colonise and reproduce has become a major conceptual paradigm in the field of molecular plant pathology [1,2]. Most effectors studied to date suppress immune pathways induced by pathogen-associated molecular patterns (PAMPs). This so-called PAMP or pattern recognition receptor (PRR)triggered immunity (PTI) response is mediated by cell surface PRRs [3,4] (S1A Fig). Understanding how effectors suppress NLR functions should provide important insights into the black box of how these immune receptors activate cell death and innate immunity, one of the major unsolved questions in the field of plant pathology [15]

Objectives

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Results

Conclusion