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PreprintCited by 119Plant-Microbe Interactions and ImmunityPlant Molecular Biology ResearchImmune Response and Inflammation

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Evolutionary Trajectory of Pattern Recognition Receptors in Plants

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Ngou, Bruno Pok Man, Wyler, Michele, Schmid, Marc W, Kadota, Yasuhiro, Shirasu, Ken·2023·Nature Communications
DOI 10.1101/2023.07.04.547604PMC PMC10834447

Preprint — published as 10.1038/s41467-023-44408-3

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Abstract

Plants perceive pathogen-associated molecular patterns (PAMPs) via pattern recognition receptors (PRRs) to activate PRR-triggered immunity (PTI). Despite extensive research on PTI in model plant species, the evolutionary trajectory and emergence of PRRs remain elusive. Here we conducted a comparative genomic analysis of cell-surface receptors and downstream signalling components among 350 plant species. Our findings reveal that cell-surface receptors comprise two major classes, receptor-like proteins (RLPs) and receptor-like kinases (RLKs), with RLP being more ancient whereas RLK families have undergone significant expansion. We also demonstrate that multiple downstream signalling components have an ancient origin within the plant lineage. To shed light on the immune-specificity of PRRs, we traced the evolutionary origin of immune-specific leucine-rich repeat-RLPs (LRR-RLPs) in plants. Surprisingly, we discovered that the last four LRR motifs crucial for co-receptor interaction in LRR-RLPs are closely related to those of the LRR-RLK subgroup Xb, which primarily governs growth and development. Functional characterisation further reveals that LRR-RLPs initiate immune responses through their juxtamembrane and transmembrane regions, while LRR-RLK-Xb members regulate development through their cytosolic kinase domains. Our data suggest modular evolution of cell-surface receptors in which immunity- and development-specific cell-surface receptors share a common origin. After diversification, their ectodomains, juxtamembrane, transmembrane, and cytosolic regions have either diversified or stabilised to recognize ligands that activate different downstream responses. We propose that cell-surface receptors and downstream signalling components are ancient, and likely predate the emergence of land plants, subsequently evolving to exhibit greater complexity and specificity within the land plant lineage.

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Metadata

Authors
Ngou, B. P. M., Wyler, M., Schmid, M. W., Kadota, Y., & Shirasu, K.
Affiliations
RIKEN Center for Sustainable Resource Science (JP)
Corresponding author
  • Kadota, Yasuhiro
  • Shirasu, Ken
ORCID
Venue
Nature Communications
Publisher
openRxiv
Published
2023-07-05
Volume
15
Issue
1
Pages
308-308
ISSN
2041-1723 (ISSN-L)
DOI
10.1101/2023.07.04.547604
PMC
PMC10834447
OpenAlex
W4391448474
Cited by
119
References
1
Citations by year
2026: 41 · 2025: 45 · 2024: 30 · 2023: 3
FWCI
28.31
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • Nature Communications (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • RePEc: Research Papers in Economics (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Funders
  • Japan Society for the Promotion of Science London (21F21793)
  • Ministry of Education, Culture, Sports, Science and Technology (20H05909, JPJSBP1-20193222, 21K19128, 22H00364, 20H02994)
  • Japan Society for the Promotion of Science (20H05909, 21K19128, 22KF0398, JPJSBP1-20193222, 22H00364, JPJSBP1, 20H02994, 21F21793)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant-Microbe Interactions and Immunity
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Molecular Biology Research
  • Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
Keywords
pattern recognition receptors, plant immunity, receptor evolution, juxtamembrane domain, transmembrane domain, plant development, signal perception, plant genome
MeSH terms
Biological Evolution, Phylogeny, Plants, Receptors, Immunologic, Receptors, Pattern Recognition

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