Evolutionary gain and loss of a plant pattern-recognition receptor for HAMP recognition

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Abstract

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.

Data availability

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.

The following data sets were generated

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NCBI BioProject, PRJNA817236.

https://www.ncbi.nlm.nih.gov/bioproject/?term=PRJNA817236
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(2022) Canavalia ensiformis, genome assembly
NCBI BioProject, PRJNA817235.

https://www.ncbi.nlm.nih.gov/bioproject/?term=PRJNA817235
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(2022) Macroptilium lathyroides Raw sequence reads
NCBI BioProject, PRJNA817241.

https://www.ncbi.nlm.nih.gov/bioproject/?term=PRJNA817241
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2. et al
(2022) Cyamopsis tetragonoloba, de novo genome assembly
NCBI BioProject, PRJNA817237.

https://www.ncbi.nlm.nih.gov/bioproject/?term=PRJNA817237
1. Snoeck S
2. et al
(2022) Pachyrhizus erosus, de novo genome assembly
NCBI BioProject, PRJNA817234.

https://www.ncbi.nlm.nih.gov/bioproject/?term=PRJNA817234

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PRJNA175619.

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PRJNA414658.

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PRJNA72815.

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PRJNA19861.

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PRJNA381312.

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PRJNA474418.

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PRJNA596114.

https://www.ncbi.nlm.nih.gov/bioproject/?term=PRJNA596114
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Article and author information

Author details

Simon Snoeck

Department of Biology, University of Washington, Seattle, United States

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-5288-0308
Bradley W Abramson

The Plant Molecular and Cellular Biology Laboratory, Salk Institute for Biological Studies, La Jolla, United States

Competing interests
The authors declare that no competing interests exist.
Anthony G K Garcia

Department of Biology, University of Washington, Seattle, United States

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0003-4650-1348
Ashley N Egan

Department of Biology, Utah Valley University, Orem, United States

Competing interests
The authors declare that no competing interests exist.
Todd P Michael

The Plant Molecular and Cellular Biology Laboratory, Salk Institute for Biological Studies, La Jolla, United States

Competing interests
The authors declare that no competing interests exist.
Adam Steinbrenner

Department of Biology, University of Washington, Seattle, United States

For correspondence
astein10@uw.edu

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-7493-678X

Funding

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.

Copyright

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.