Dominant integration locus drives continuous diversification of plant immune receptors with exogenous domain fusions

Abstract

BackgroundThe plant immune system is innate and encoded in the germline. Using it efficiently, plants are capable of recognizing a diverse range of rapidly evolving pathogens. A recently described phenomenon shows that plant immune receptors are able to recognize pathogen effectors through the acquisition of exogenous protein domains from other plant genes.ResultsWe show that plant immune receptors with integrated domains are distributed unevenly across their phylogeny in grasses. Using phylogenetic analysis, we uncover a major integration clade, whose members underwent repeated independent integration events producing diverse fusions. This clade is ancestral in grasses with members often found on syntenic chromosomes. Analyses of these fusion events reveals that homologous receptors can be fused to diverse domains. Furthermore, we discover a 43 amino acid long motif associated with this dominant integration clade which is located immediately upstream of the fusion site. Sequence analysis reveals that DNA transposition and/or ectopic recombination are the most likely mechanisms of formation for nucleotide binding leucine rich repeat proteins with integrated domains.ConclusionsThe identification of this subclass of plant immune receptors that is naturally adapted to new domain integration will inform biotechnological approaches for generating synthetic receptors with novel pathogen “baits.”Electronic supplementary materialThe online version of this article (10.1186/s13059-018-1392-6) contains supplementary material, which is available to authorized users.

Multiple strategies for pathogen perception by plant immune receptors

“…It is then crucial to determine which NLRs are best to engineer and whether exogenous domain integration has occurred randomly in the broad NLR family through evolution or more frequently in some NLR clades than others. Genomewide investigation of NLR evolution in monocot species revealed that integration and diversification of IDs has occurred in three main clades (Bailey et al, 2017), suggesting that not all NLRs are prone to integrate potential decoys and that some provide better platforms than others.…”

“…New Phytologist or more frequently in some NLR clades than others. Genomewide investigation of NLR evolution in monocot species revealed that integration and diversification of IDs has occurred in three main clades (Bailey et al, 2017), suggesting that not all NLRs are prone to integrate potential decoys and that some provide better platforms than others. Although modulation of NLRs seems promising for the design of new specificities, it will not necessarily lead to extended durability.…”

The coming of age of EvoMPMI: evolutionary molecular plant-microbe interactions across multiple timescales

“…The mechanisms underpinning the emergence of NLR-ID fusions are poorly understood. Bailey et al recently proposed that ectopic recombination is a major driver of domain integration in Poaceae (Bailey et al 2017). A "major integration clade", which includes RGA5, Pi-ta and Rpg5, underwent repeated independent integration events (Bailey et al 2017).…”

Convergent loss of an EDS1/PAD4 signalling pathway in several plant lineages predicts new components of plant immunity and drought response

“…Furthermore, insects commonly act as vectors for plant infection (65)(66)(67). There was no significant association between differential gene expression and rice ASTRAL genes upon X. oryzae infection with only 5 of the Drought and immunity pathway reduction in aquatic environments 22 34 ASTRAL genes differentially expressed upon infection when comparing all isolates of X. oryzae to control treatments (One sided fisher-exact test, p-value = 0.3054) ( Fig. 7B).…”

“…A subset of NLRs have undergone functional specialisation to serve downstream of other NLRs in the signalling cascade (18)(19)(20)(21). This mechanism is referred to as an NLR sensor-helper pair, where genomically the two NLR genes are often adjacent in a head to head orientation with a shared promoter (22,23) . The sensor NLR is required to recognise changes upon infection, whilst the helper NLR is activated upon a change in its paired NLR rather than via pathogen induced change (18).…”