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Pathogen-Mediated Stomatal Opening: A Previously Overlooked Pathogenicity Strategy in the Oomycete Pathogen Phytophthora infestans

Phytophthora infestans, the most damaging oomycete pathogen of potato, is specialized to grow sporangiophore through opened stomata for secondary inoculum production. However, it is still unclear which metabolic pathways in potato are manipulated by P. infestans in the guard cell–pathogen interactio...

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Autores principales: Yang, Li-Na, Liu, Hao, Wang, Yan-Ping, Seematti, Jenifer, Grenville-Briggs, Laura J., Wang, Zonghua, Zhan, Jiasui
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8311186/
https://www.ncbi.nlm.nih.gov/pubmed/34322141
http://dx.doi.org/10.3389/fpls.2021.668797
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author Yang, Li-Na
Liu, Hao
Wang, Yan-Ping
Seematti, Jenifer
Grenville-Briggs, Laura J.
Wang, Zonghua
Zhan, Jiasui
author_facet Yang, Li-Na
Liu, Hao
Wang, Yan-Ping
Seematti, Jenifer
Grenville-Briggs, Laura J.
Wang, Zonghua
Zhan, Jiasui
author_sort Yang, Li-Na
collection PubMed
description Phytophthora infestans, the most damaging oomycete pathogen of potato, is specialized to grow sporangiophore through opened stomata for secondary inoculum production. However, it is still unclear which metabolic pathways in potato are manipulated by P. infestans in the guard cell–pathogen interactions to open the stomata. Here microscopic observations and cell biology were used to investigate antagonistic interactions between guard cells and the oomycete pathogen. We observed that the antagonistic interactions started at the very beginning of infection. Stomatal movement is an important part of the immune response of potato to P. infestans infection and this occurs through guard cell death and stomatal closure. We observed that P. infestans appeared to manipulate metabolic processes in guard cells, such as triacylglycerol (TAG) breakdown, starch degradation, H(2)O(2) scavenging, and NO catabolism, which are involved in stomatal movement, to evade these stomatal defense responses. The signal transduction pathway of P. infestans-induced stomatal opening likely starts from H(2)O(2) and NO scavenging, along with TAG breakdown while the subsequent starch degradation reinforces the opening process by strengthening guard cell turgor and opening the stomata to their maximum aperture. These results suggest that stomata are a barrier stopping P. infestans from completing its life cycle, but this host defense system can be bypassed through the manipulation of diverse metabolic pathways that may be induced by P. infestans effector proteins.
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spelling pubmed-83111862021-07-27 Pathogen-Mediated Stomatal Opening: A Previously Overlooked Pathogenicity Strategy in the Oomycete Pathogen Phytophthora infestans Yang, Li-Na Liu, Hao Wang, Yan-Ping Seematti, Jenifer Grenville-Briggs, Laura J. Wang, Zonghua Zhan, Jiasui Front Plant Sci Plant Science Phytophthora infestans, the most damaging oomycete pathogen of potato, is specialized to grow sporangiophore through opened stomata for secondary inoculum production. However, it is still unclear which metabolic pathways in potato are manipulated by P. infestans in the guard cell–pathogen interactions to open the stomata. Here microscopic observations and cell biology were used to investigate antagonistic interactions between guard cells and the oomycete pathogen. We observed that the antagonistic interactions started at the very beginning of infection. Stomatal movement is an important part of the immune response of potato to P. infestans infection and this occurs through guard cell death and stomatal closure. We observed that P. infestans appeared to manipulate metabolic processes in guard cells, such as triacylglycerol (TAG) breakdown, starch degradation, H(2)O(2) scavenging, and NO catabolism, which are involved in stomatal movement, to evade these stomatal defense responses. The signal transduction pathway of P. infestans-induced stomatal opening likely starts from H(2)O(2) and NO scavenging, along with TAG breakdown while the subsequent starch degradation reinforces the opening process by strengthening guard cell turgor and opening the stomata to their maximum aperture. These results suggest that stomata are a barrier stopping P. infestans from completing its life cycle, but this host defense system can be bypassed through the manipulation of diverse metabolic pathways that may be induced by P. infestans effector proteins. Frontiers Media S.A. 2021-07-12 /pmc/articles/PMC8311186/ /pubmed/34322141 http://dx.doi.org/10.3389/fpls.2021.668797 Text en Copyright © 2021 Yang, Liu, Wang, Seematti, Grenville-Briggs, Wang and Zhan. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Plant Science
Yang, Li-Na
Liu, Hao
Wang, Yan-Ping
Seematti, Jenifer
Grenville-Briggs, Laura J.
Wang, Zonghua
Zhan, Jiasui
Pathogen-Mediated Stomatal Opening: A Previously Overlooked Pathogenicity Strategy in the Oomycete Pathogen Phytophthora infestans
title Pathogen-Mediated Stomatal Opening: A Previously Overlooked Pathogenicity Strategy in the Oomycete Pathogen Phytophthora infestans
title_full Pathogen-Mediated Stomatal Opening: A Previously Overlooked Pathogenicity Strategy in the Oomycete Pathogen Phytophthora infestans
title_fullStr Pathogen-Mediated Stomatal Opening: A Previously Overlooked Pathogenicity Strategy in the Oomycete Pathogen Phytophthora infestans
title_full_unstemmed Pathogen-Mediated Stomatal Opening: A Previously Overlooked Pathogenicity Strategy in the Oomycete Pathogen Phytophthora infestans
title_short Pathogen-Mediated Stomatal Opening: A Previously Overlooked Pathogenicity Strategy in the Oomycete Pathogen Phytophthora infestans
title_sort pathogen-mediated stomatal opening: a previously overlooked pathogenicity strategy in the oomycete pathogen phytophthora infestans
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8311186/
https://www.ncbi.nlm.nih.gov/pubmed/34322141
http://dx.doi.org/10.3389/fpls.2021.668797
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