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Shimizu, Motoki, Hirabuchi, Akiko, Sugihara, Yu, Abe, Akira, Takeda, Takumi, Kobayashi, Michie, Hiraka, Yukie, Kanzaki, Eiko, Oikawa, Kaori, Saitoh, Hiromasa, Langner, Thorsten, Banfield, Mark J., Kamoun, Sophien 
ORCID: https://orcid.org/0000-0002-0290-0315 and Terauchi, Ryohei
(2022)
A genetically linked pair of NLR immune receptors shows contrasting patterns of evolution.
Proceedings of the National Academy of Sciences of the United States of America, 119 (27).
ISSN 0027-8424
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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.
| Item Type: | Article |
|---|---|
| Additional Information: | Data Availability Statement: The DNA-seq and RNA-seq data from this study are listed in Dataset S6 and have been deposited in the DNA Databank of Japan (BioProject accession nos. PRJDB9440, PRJDB12353, PRJDB12884, PRJDB12891, and PRJDB12902). The nucleotide sequences of Pias-1, Pias-2, and AVR-Pias have been deposited in the DNA Databank of Japan (Pias-1: LC672059; Pias-2: LC672060; and AVR-Pias: LC672061). All study data are included in the article and/or supporting information. Funding Information: This study was supported by Japan Society for the Promotion of Science KAKENHI 15H05779, 20H05681, and 16H06279 (PAGS) (to R.T.) and 21K14834 (to M.S.), Royal Society UK\u2013Japan International Exchange Grants JPJSBP120215702 and IEC\\R3\\203081 (to R.T., S.K., and M.J.B.), the Biotechnology and Biological Sciences Research Council (UKRI-BBSRC, UK Grant BB/P012574), European Research Council (ERC BLASTOFF Project 743165), John Innes Foundation, and Gatsby Charitable Foundation. Computations were partially performed on the supercomputer at the Research Organization of Information and Systems, National Institute of Genetics. We also thank the National Institute of Genetics (National BioResource Project), Japan, and the Genebank at the National Agriculture and Food Research Organization, Japan, for providing the seeds of wild rice and WRC17, respectively. Publisher Copyright: Copyright © 2022 the Author(s). |
| Uncontrolled Keywords: | evolution,integrated domains,nucleotide-binding leucine-rich-repeat receptors (nlrs),paired nlr,rice |
| Faculty \ School: | Faculty of Science > School of Biological Sciences |
| UEA Research Groups: | Faculty of Science > Research Groups > Plant Sciences |
| Related URLs: | |
| Depositing User: | LivePure Connector |
| Date Deposited: | 31 Oct 2024 16:30 |
| Last Modified: | 01 Nov 2024 11:30 |
| URI: | https://ueaeprints.uea.ac.uk/id/eprint/97392 |
| DOI: | 10.1073/pnas.2116896119 |
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