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A molecular mechanosensor for real-time visualization of appressorium membrane tension in Magnaporthe oryzae

The rice blast fungus Magnaporthe oryzae uses a pressurized infection cell called an appressorium to drive a rigid penetration peg through the leaf cuticle. The vast internal pressure of an appressorium is very challenging to investigate, leaving our understanding of the cellular mechanics of plant...

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Autores principales: Ryder, Lauren S., Lopez, Sergio G., Michels, Lucile, Eseola, Alice B., Sprakel, Joris, Ma, Weibin, Talbot, Nicholas J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10390335/
https://www.ncbi.nlm.nih.gov/pubmed/37474734
http://dx.doi.org/10.1038/s41564-023-01430-x
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author Ryder, Lauren S.
Lopez, Sergio G.
Michels, Lucile
Eseola, Alice B.
Sprakel, Joris
Ma, Weibin
Talbot, Nicholas J.
author_facet Ryder, Lauren S.
Lopez, Sergio G.
Michels, Lucile
Eseola, Alice B.
Sprakel, Joris
Ma, Weibin
Talbot, Nicholas J.
author_sort Ryder, Lauren S.
collection PubMed
description The rice blast fungus Magnaporthe oryzae uses a pressurized infection cell called an appressorium to drive a rigid penetration peg through the leaf cuticle. The vast internal pressure of an appressorium is very challenging to investigate, leaving our understanding of the cellular mechanics of plant infection incomplete. Here, using fluorescence lifetime imaging of a membrane-targeting molecular mechanoprobe, we quantify changes in membrane tension in M. oryzae. We show that extreme pressure in the appressorium leads to large-scale spatial heterogeneities in membrane mechanics, much greater than those observed in any cell type previously. By contrast, non-pathogenic melanin-deficient mutants, exhibit low spatially homogeneous membrane tension. The sensor kinase ∆sln1 mutant displays significantly higher membrane tension during inflation of the appressorium, providing evidence that Sln1 controls turgor throughout plant infection. This non-invasive, live cell imaging technique therefore provides new insight into the enormous invasive forces deployed by pathogenic fungi to invade their hosts, offering the potential for new disease intervention strategies.
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spelling pubmed-103903352023-08-02 A molecular mechanosensor for real-time visualization of appressorium membrane tension in Magnaporthe oryzae Ryder, Lauren S. Lopez, Sergio G. Michels, Lucile Eseola, Alice B. Sprakel, Joris Ma, Weibin Talbot, Nicholas J. Nat Microbiol Article The rice blast fungus Magnaporthe oryzae uses a pressurized infection cell called an appressorium to drive a rigid penetration peg through the leaf cuticle. The vast internal pressure of an appressorium is very challenging to investigate, leaving our understanding of the cellular mechanics of plant infection incomplete. Here, using fluorescence lifetime imaging of a membrane-targeting molecular mechanoprobe, we quantify changes in membrane tension in M. oryzae. We show that extreme pressure in the appressorium leads to large-scale spatial heterogeneities in membrane mechanics, much greater than those observed in any cell type previously. By contrast, non-pathogenic melanin-deficient mutants, exhibit low spatially homogeneous membrane tension. The sensor kinase ∆sln1 mutant displays significantly higher membrane tension during inflation of the appressorium, providing evidence that Sln1 controls turgor throughout plant infection. This non-invasive, live cell imaging technique therefore provides new insight into the enormous invasive forces deployed by pathogenic fungi to invade their hosts, offering the potential for new disease intervention strategies. Nature Publishing Group UK 2023-07-20 2023 /pmc/articles/PMC10390335/ /pubmed/37474734 http://dx.doi.org/10.1038/s41564-023-01430-x Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This 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 license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license 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 license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Ryder, Lauren S.
Lopez, Sergio G.
Michels, Lucile
Eseola, Alice B.
Sprakel, Joris
Ma, Weibin
Talbot, Nicholas J.
A molecular mechanosensor for real-time visualization of appressorium membrane tension in Magnaporthe oryzae
title A molecular mechanosensor for real-time visualization of appressorium membrane tension in Magnaporthe oryzae
title_full A molecular mechanosensor for real-time visualization of appressorium membrane tension in Magnaporthe oryzae
title_fullStr A molecular mechanosensor for real-time visualization of appressorium membrane tension in Magnaporthe oryzae
title_full_unstemmed A molecular mechanosensor for real-time visualization of appressorium membrane tension in Magnaporthe oryzae
title_short A molecular mechanosensor for real-time visualization of appressorium membrane tension in Magnaporthe oryzae
title_sort molecular mechanosensor for real-time visualization of appressorium membrane tension in magnaporthe oryzae
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10390335/
https://www.ncbi.nlm.nih.gov/pubmed/37474734
http://dx.doi.org/10.1038/s41564-023-01430-x
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