Back to Search Start Over

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

Authors :
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
Source :
Proceedings of the National Academy of Sciences. 119
Publication Year :
2022
Publisher :
Proceedings of the National Academy of Sciences, 2022.

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.

Details

ISSN :
10916490 and 00278424
Volume :
119
Database :
OpenAIRE
Journal :
Proceedings of the National Academy of Sciences
Accession number :
edsair.doi.dedup.....6411eed3746bb9b452f0ee89d886d6b9