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A genetically linked pair of NLR immune receptors shows contrasting patterns of evolution
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 domain...
Autores principales: | , , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
National Academy of Sciences
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9271155/ https://www.ncbi.nlm.nih.gov/pubmed/35771942 http://dx.doi.org/10.1073/pnas.2116896119 |
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author | 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 Terauchi, Ryohei |
author_facet | 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 Terauchi, Ryohei |
author_sort | Shimizu, Motoki |
collection | PubMed |
description | 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. |
format | Online Article Text |
id | pubmed-9271155 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | National Academy of Sciences |
record_format | MEDLINE/PubMed |
spelling | pubmed-92711552022-07-11 A genetically linked pair of NLR immune receptors shows contrasting patterns of evolution 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 Terauchi, Ryohei Proc Natl Acad Sci U S A Biological Sciences 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. National Academy of Sciences 2022-06-30 2022-07-05 /pmc/articles/PMC9271155/ /pubmed/35771942 http://dx.doi.org/10.1073/pnas.2116896119 Text en Copyright © 2022 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) . |
spellingShingle | Biological Sciences 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 Terauchi, Ryohei A genetically linked pair of NLR immune receptors shows contrasting patterns of evolution |
title | A genetically linked pair of NLR immune receptors shows contrasting patterns of evolution |
title_full | A genetically linked pair of NLR immune receptors shows contrasting patterns of evolution |
title_fullStr | A genetically linked pair of NLR immune receptors shows contrasting patterns of evolution |
title_full_unstemmed | A genetically linked pair of NLR immune receptors shows contrasting patterns of evolution |
title_short | A genetically linked pair of NLR immune receptors shows contrasting patterns of evolution |
title_sort | genetically linked pair of nlr immune receptors shows contrasting patterns of evolution |
topic | Biological Sciences |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9271155/ https://www.ncbi.nlm.nih.gov/pubmed/35771942 http://dx.doi.org/10.1073/pnas.2116896119 |
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