Cargando…

Plasma membrane aquaporins of the PIP1 and PIP2 subfamilies facilitate hydrogen peroxide diffusion into plant roots

BACKGROUND: The permeability of plasma membrane aquaporins (PIPs) to small solutes other than water greatly diversifies their potential functions in plant development and metabolic processes. One such process is stress signalling in which hydrogen peroxide (H(2)O(2)) plays a major role. Based on tra...

Descripción completa

Detalles Bibliográficos
Autores principales: Israel, David, Lee, Seong Hee, Robson, Thomas Matthew, Zwiazek, Janusz Jerzy
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9721007/
https://www.ncbi.nlm.nih.gov/pubmed/36471241
http://dx.doi.org/10.1186/s12870-022-03962-6
_version_ 1784843673251348480
author Israel, David
Lee, Seong Hee
Robson, Thomas Matthew
Zwiazek, Janusz Jerzy
author_facet Israel, David
Lee, Seong Hee
Robson, Thomas Matthew
Zwiazek, Janusz Jerzy
author_sort Israel, David
collection PubMed
description BACKGROUND: The permeability of plasma membrane aquaporins (PIPs) to small solutes other than water greatly diversifies their potential functions in plant development and metabolic processes. One such process is stress signalling in which hydrogen peroxide (H(2)O(2)) plays a major role. Based on transport assays carried out in yeast, there are differences in the degree to which PIPs of Arabidopsis thaliana, are permeable to H(2)O(2) and thus they may differentially facilitate transmembrane diffusion. Here, we test whether specific PIPs aid in the transmembrane diffusion of H(2)O(2) to such an extent that knocking-out PIPs affects plant phenotype. We examined changes in growth and morphology, including biomass accumulation, root system architecture and relative water content, as well as gas exchange, across two H(2)O(2) treatments in knockout mutants of A. thaliana. RESULTS: We could infer that PIP-type aquaporins are permeable to H(2)O(2) in planta and that this permeability is physiologically relevant in a plant’s response to oxidative stress. In particular, the lack of functional PIP2;3 confers resistance to exogenously applied H(2)O(2) indicating that it facilitates H(2)O(2) entry into root cells. Additionally, PIP1;1 and PIP2;6 were found to facilitate H(2)O(2) diffusion, while PIP2;2 is required for proper root growth under controlled conditions. MAIN FINDINGS: We conclude that PIPs are physiologically relevant conduits for H(2)O(2) diffusion in the A. thaliana roots and participate in the regulation of stress responses. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-022-03962-6.
format Online
Article
Text
id pubmed-9721007
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-97210072022-12-06 Plasma membrane aquaporins of the PIP1 and PIP2 subfamilies facilitate hydrogen peroxide diffusion into plant roots Israel, David Lee, Seong Hee Robson, Thomas Matthew Zwiazek, Janusz Jerzy BMC Plant Biol Research Article BACKGROUND: The permeability of plasma membrane aquaporins (PIPs) to small solutes other than water greatly diversifies their potential functions in plant development and metabolic processes. One such process is stress signalling in which hydrogen peroxide (H(2)O(2)) plays a major role. Based on transport assays carried out in yeast, there are differences in the degree to which PIPs of Arabidopsis thaliana, are permeable to H(2)O(2) and thus they may differentially facilitate transmembrane diffusion. Here, we test whether specific PIPs aid in the transmembrane diffusion of H(2)O(2) to such an extent that knocking-out PIPs affects plant phenotype. We examined changes in growth and morphology, including biomass accumulation, root system architecture and relative water content, as well as gas exchange, across two H(2)O(2) treatments in knockout mutants of A. thaliana. RESULTS: We could infer that PIP-type aquaporins are permeable to H(2)O(2) in planta and that this permeability is physiologically relevant in a plant’s response to oxidative stress. In particular, the lack of functional PIP2;3 confers resistance to exogenously applied H(2)O(2) indicating that it facilitates H(2)O(2) entry into root cells. Additionally, PIP1;1 and PIP2;6 were found to facilitate H(2)O(2) diffusion, while PIP2;2 is required for proper root growth under controlled conditions. MAIN FINDINGS: We conclude that PIPs are physiologically relevant conduits for H(2)O(2) diffusion in the A. thaliana roots and participate in the regulation of stress responses. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-022-03962-6. BioMed Central 2022-12-05 /pmc/articles/PMC9721007/ /pubmed/36471241 http://dx.doi.org/10.1186/s12870-022-03962-6 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Israel, David
Lee, Seong Hee
Robson, Thomas Matthew
Zwiazek, Janusz Jerzy
Plasma membrane aquaporins of the PIP1 and PIP2 subfamilies facilitate hydrogen peroxide diffusion into plant roots
title Plasma membrane aquaporins of the PIP1 and PIP2 subfamilies facilitate hydrogen peroxide diffusion into plant roots
title_full Plasma membrane aquaporins of the PIP1 and PIP2 subfamilies facilitate hydrogen peroxide diffusion into plant roots
title_fullStr Plasma membrane aquaporins of the PIP1 and PIP2 subfamilies facilitate hydrogen peroxide diffusion into plant roots
title_full_unstemmed Plasma membrane aquaporins of the PIP1 and PIP2 subfamilies facilitate hydrogen peroxide diffusion into plant roots
title_short Plasma membrane aquaporins of the PIP1 and PIP2 subfamilies facilitate hydrogen peroxide diffusion into plant roots
title_sort plasma membrane aquaporins of the pip1 and pip2 subfamilies facilitate hydrogen peroxide diffusion into plant roots
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9721007/
https://www.ncbi.nlm.nih.gov/pubmed/36471241
http://dx.doi.org/10.1186/s12870-022-03962-6
work_keys_str_mv AT israeldavid plasmamembraneaquaporinsofthepip1andpip2subfamiliesfacilitatehydrogenperoxidediffusionintoplantroots
AT leeseonghee plasmamembraneaquaporinsofthepip1andpip2subfamiliesfacilitatehydrogenperoxidediffusionintoplantroots
AT robsonthomasmatthew plasmamembraneaquaporinsofthepip1andpip2subfamiliesfacilitatehydrogenperoxidediffusionintoplantroots
AT zwiazekjanuszjerzy plasmamembraneaquaporinsofthepip1andpip2subfamiliesfacilitatehydrogenperoxidediffusionintoplantroots