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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...

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Autores principales: 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
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2020
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.
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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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