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Pathogen manipulation of chloroplast function triggers a light-dependent immune recognition
In plants and animals, nucleotide-binding leucine-rich repeat (NLR) proteins are intracellular immune sensors that recognize and eliminate a wide range of invading pathogens. NLR-mediated immunity is known to be modulated by environmental factors. However, how pathogen recognition by NLRs is influen...
Autores principales: | , , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
National Academy of Sciences
2020
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7196767/ https://www.ncbi.nlm.nih.gov/pubmed/32284406 http://dx.doi.org/10.1073/pnas.2002759117 |
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author | Gao, Chuyun Xu, Huawei Huang, Jie Sun, Biying Zhang, Fan Savage, Zachary Duggan, Cian Yan, Tingxiu Wu, Chih-hang Wang, Yuanchao Vleeshouwers, Vivianne G. A. A. Kamoun, Sophien Bozkurt, Tolga O. Dong, Suomeng |
author_facet | Gao, Chuyun Xu, Huawei Huang, Jie Sun, Biying Zhang, Fan Savage, Zachary Duggan, Cian Yan, Tingxiu Wu, Chih-hang Wang, Yuanchao Vleeshouwers, Vivianne G. A. A. Kamoun, Sophien Bozkurt, Tolga O. Dong, Suomeng |
author_sort | Gao, Chuyun |
collection | PubMed |
description | In plants and animals, nucleotide-binding leucine-rich repeat (NLR) proteins are intracellular immune sensors that recognize and eliminate a wide range of invading pathogens. NLR-mediated immunity is known to be modulated by environmental factors. However, how pathogen recognition by NLRs is influenced by environmental factors such as light remains unclear. Here, we show that the agronomically important NLR Rpi-vnt1.1 requires light to confer disease resistance against races of the Irish potato famine pathogen Phytophthora infestans that secrete the effector protein AVRvnt1. The activation of Rpi-vnt1.1 requires a nuclear-encoded chloroplast protein, glycerate 3-kinase (GLYK), implicated in energy production. The pathogen effector AVRvnt1 binds the full-length chloroplast-targeted GLYK isoform leading to activation of Rpi-vnt1.1. In the dark, Rpi-vnt1.1–mediated resistance is compromised because plants produce a shorter GLYK—lacking the intact chloroplast transit peptide—that is not bound by AVRvnt1. The transition between full-length and shorter plant GLYK transcripts is controlled by a light-dependent alternative promoter selection mechanism. In plants that lack Rpi-vnt1.1, the presence of AVRvnt1 reduces GLYK accumulation in chloroplasts counteracting GLYK contribution to basal immunity. Our findings revealed that pathogen manipulation of chloroplast functions has resulted in a light-dependent immune response. |
format | Online Article Text |
id | pubmed-7196767 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2020 |
publisher | National Academy of Sciences |
record_format | MEDLINE/PubMed |
spelling | pubmed-71967672020-05-06 Pathogen manipulation of chloroplast function triggers a light-dependent immune recognition Gao, Chuyun Xu, Huawei Huang, Jie Sun, Biying Zhang, Fan Savage, Zachary Duggan, Cian Yan, Tingxiu Wu, Chih-hang Wang, Yuanchao Vleeshouwers, Vivianne G. A. A. Kamoun, Sophien Bozkurt, Tolga O. Dong, Suomeng Proc Natl Acad Sci U S A Biological Sciences In plants and animals, nucleotide-binding leucine-rich repeat (NLR) proteins are intracellular immune sensors that recognize and eliminate a wide range of invading pathogens. NLR-mediated immunity is known to be modulated by environmental factors. However, how pathogen recognition by NLRs is influenced by environmental factors such as light remains unclear. Here, we show that the agronomically important NLR Rpi-vnt1.1 requires light to confer disease resistance against races of the Irish potato famine pathogen Phytophthora infestans that secrete the effector protein AVRvnt1. The activation of Rpi-vnt1.1 requires a nuclear-encoded chloroplast protein, glycerate 3-kinase (GLYK), implicated in energy production. The pathogen effector AVRvnt1 binds the full-length chloroplast-targeted GLYK isoform leading to activation of Rpi-vnt1.1. In the dark, Rpi-vnt1.1–mediated resistance is compromised because plants produce a shorter GLYK—lacking the intact chloroplast transit peptide—that is not bound by AVRvnt1. The transition between full-length and shorter plant GLYK transcripts is controlled by a light-dependent alternative promoter selection mechanism. In plants that lack Rpi-vnt1.1, the presence of AVRvnt1 reduces GLYK accumulation in chloroplasts counteracting GLYK contribution to basal immunity. Our findings revealed that pathogen manipulation of chloroplast functions has resulted in a light-dependent immune response. National Academy of Sciences 2020-04-28 2020-04-13 /pmc/articles/PMC7196767/ /pubmed/32284406 http://dx.doi.org/10.1073/pnas.2002759117 Text en Copyright © 2020 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/ 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 Gao, Chuyun Xu, Huawei Huang, Jie Sun, Biying Zhang, Fan Savage, Zachary Duggan, Cian Yan, Tingxiu Wu, Chih-hang Wang, Yuanchao Vleeshouwers, Vivianne G. A. A. Kamoun, Sophien Bozkurt, Tolga O. Dong, Suomeng Pathogen manipulation of chloroplast function triggers a light-dependent immune recognition |
title | Pathogen manipulation of chloroplast function triggers a light-dependent immune recognition |
title_full | Pathogen manipulation of chloroplast function triggers a light-dependent immune recognition |
title_fullStr | Pathogen manipulation of chloroplast function triggers a light-dependent immune recognition |
title_full_unstemmed | Pathogen manipulation of chloroplast function triggers a light-dependent immune recognition |
title_short | Pathogen manipulation of chloroplast function triggers a light-dependent immune recognition |
title_sort | pathogen manipulation of chloroplast function triggers a light-dependent immune recognition |
topic | Biological Sciences |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7196767/ https://www.ncbi.nlm.nih.gov/pubmed/32284406 http://dx.doi.org/10.1073/pnas.2002759117 |
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