Evolutionary gain and loss of a plant pattern-recognition receptor for HAMP recognition
As a first step in innate immunity, pattern recognition receptors (PRRs) recognize distinct pathogen and herbivore-associated molecular patterns and mediate activation of immune responses, but specific steps in the evolution of new PRR sensing functions are not well understood. We employed comparative genomic and functional analyses to define evolutionary events leading to the sensing of the herbivore-associated peptide inceptin (In11) by the PRR Inceptin Receptor (INR) in legume plant species. Existing and de novo genome assemblies revealed that the presence of a functional INR gene corresponded with ability to respond to In11 across ~53 million years (my) of evolution. In11 recognition is unique to the clade of Phaseoloid legumes, and only a single clade of INR homologues from Phaseoloids was functional in a heterologous model. The syntenic loci of several non-Phaseoloid outgroup species nonetheless contain non-functional INR-like homologues, suggesting that an ancestral gene insertion event and diversification preceded the evolution of a specific INR receptor function ~28 mya. Chimeric and ancestrally reconstructed receptors indicated that 16 amino acid differences in the C1 leucine-rich repeat domain and C2 intervening motif mediate gain of In11 recognition. Thus, high PRR diversity was likely followed by a small number of mutations to expand innate immune recognition to a novel peptide elicitor. Analysis of INR evolution provides a model for functional diversification of other germline-encoded PRRs.
Sequencing data and genome assemblies have been deposited on NCBI under the following bioprojects: PRJNA817236, PRJNA817235, PRJNA817241, PRJNA817237 and PRJNA817234.Figure 1 - Suppl. data 2 contains the numerical data used to generate this figure.
Hylodesmum podocarpum, de novogenome assemblyNCBI BioProject, PRJNA817236.
Canavalia ensiformis, genome assemblyNCBI BioProject, PRJNA817235.
Macroptilium lathyroides Raw sequence readsNCBI BioProject, PRJNA817241.
Cyamopsis tetragonoloba, de novo genome assemblyNCBI BioProject, PRJNA817237.
Pachyrhizus erosus, de novo genome assemblyNCBI BioProject, PRJNA817234.
Article and author information
Belgian American Educational Foundation (/)
- Simon Snoeck
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
- Rebecca Bart, The Donald Danforth Plant Science Center, United States
- Preprint posted: April 1, 2022 (view preprint)
- Received: June 14, 2022
- Accepted: October 28, 2022
- Accepted Manuscript published: November 15, 2022 (version 1)
- Version of Record published: December 2, 2022 (version 2)
© 2022, Snoeck et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Funding: RD is supported by the National Institute of General Medical Sciences of the National Institutes of Health (NIH) (R35-GM124836) and the National Heart, Lung, and Blood Institute of the NIH (R01-HL139865 and R01-HL155915).