A genetically linked pair of NLR immune receptors shows contrasting patterns of evolution

Motoki Shimizu, Akiko Hirabuchi, Yu Sugihara, Akira Abe, Takumi Takeda, Michie Kobayashi, Yukie Hiraka, Eiko Kanzaki, Kaori Oikawa, Hiromasa Saitoh, Thorsten Langner, Mark J. Banfield, Sophien Kamoun, Ryohei Terauchi

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27 Citations (Scopus)
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Abstract

Throughout their evolution, plant nucleotide-binding leucine-rich-repeat receptors (NLRs) have acquired widely divergent unconventional integrated domains that enhance their ability to detect pathogen effectors. However, the functional dynamics that drive the evolution of NLRs with integrated domains (NLR-IDs) remain poorly understood. Here, we reconstructed the evolutionary history of an NLR locus prone to unconventional domain integration and experimentally tested hypotheses about the evolution of NLR-IDs. We show that the rice (Oryza sativa) NLR Pias recognizes the effector AVR-Pias of the blast fungal pathogen Magnaporthe oryzae. Pias consists of a functionally specialized NLR pair, the helper Pias-1 and the sensor Pias-2, that is allelic to the previously characterized Pia pair of NLRs: the helper RGA4 and the sensor RGA5. Remarkably, Pias-2 carries a C-terminal DUF761 domain at a similar position to the heavy metal–associated (HMA) domain of RGA5. Phylogenomic analysis showed that Pias-2/RGA5 sensor NLRs have undergone recurrent genomic recombination within the genus Oryza, resulting in up to six sequence-divergent domain integrations. Allelic NLRs with divergent functions have been maintained transspecies in different Oryza lineages to detect sequence-divergent pathogen effectors. By contrast, Pias-1 has retained its NLR helper activity throughout evolution and is capable of functioning together with the divergent sensor-NLR RGA5 to respond to AVR-Pia. These results suggest that opposite selective forces have driven the evolution of paired NLRs: highly dynamic domain integration events maintained by balancing selection for sensor NLRs, in sharp contrast to purifying selection and functional conservation of immune signaling for helper NLRs.

Original languageEnglish
Article numbere2116896119
JournalProceedings of the National Academy of Sciences of the United States of America
Volume119
Issue number27
Early online date30 Jun 2022
DOIs
Publication statusPublished - 5 Jul 2022

Keywords

  • evolution
  • integrated domains
  • nucleotide-binding leucine-rich-repeat receptors (NLRs)
  • paired NLR
  • rice

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