Analysis of intraspecies diversity reveals a subset of highly variable plant immune receptors and predicts their binding sites.

Daniil M Prigozhin,Ksenia V Krasileva

doi:10.1093/plcell/koab013

Abstract

The evolution of recognition specificities by the immune system depends on the generation of receptor diversity and on connecting the binding of new antigens with the initiation of downstream signaling. In plant immunity, the innate Nucleotide-Binding Leucine-Rich Repeat (NLR) receptor family enables antigen binding and immune signaling. In this study, we surveyed the NLR complements of 62 ecotypes of Arabidopsis thaliana and 54 lines of Brachypodium distachyon and identified a limited number of NLR subfamilies that show high allelic diversity. We show that the predicted specificity-determining residues cluster on the surfaces of Leucine-Rich Repeat domains, but the locations of the clusters vary among NLR subfamilies. By comparing NLR phylogeny, allelic diversity, and known functions of the Arabidopsis NLRs, we formulate a hypothesis for the emergence of direct and indirect pathogen-sensing receptors and of the autoimmune NLRs. These findings reveal the recurring patterns of evolution of innate immunity and can inform NLR engineering efforts.

Highlights

Plants lack the adaptive immunity of vertebrates
Two types of plant immune receptors form the basis of pathogen recognition: extracellular receptors, including receptor-like kinases (RLK) and receptor-like proteins (RLP); and intracellular Nucleotide-binding Leucine Rich Repeat (NLR) proteins (Dangl et al, 2013)
Even before the first NLR structure or the extensive sequence datasets were available, Michelmore and Meyers predicted that hypervariable amino acid positions in the NLRs would map to the concave surface of the LRR domain based on the signatures of positive selection in a number of selected examples (Michelmore and Meyers, 1998)

Summary

Introduction

Plants lack the adaptive immunity of vertebrates. With their immune receptor specificities encoded in the germline, plants can achieve remarkable receptor diversity at the population level (Bakker et al, 2006). The mechanisms that generate this diversity and select for useful (and against deleterious) receptor variants are of great importance to both basic science and crop improvement (Dangl et al, 2013). Ongoing efforts at pan-genome sequencing of both model and crop species reveal the intraspecies diversity of plant immune receptors, their natural history, mechanisms of action, and the evolutionary forces that shape plant immunity (Van de Weyer et al, 2019; Stam et al, 2019a, 2019b; Seong et al, 2020; Gordon et al, 2017).

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