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Serendipita indica E5′NT modulates extracellular nucleotide levels in the plant apoplast and affects fungal colonization

Extracellular adenosine 5′‐triphosphate (eATP) is an essential signaling molecule that mediates different cellular processes through its interaction with membrane‐associated receptor proteins in animals and plants. eATP regulates plant growth, development, and responses to biotic and abiotic stresse...

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Autores principales: Nizam, Shadab, Qiang, Xiaoyu, Wawra, Stephan, Nostadt, Robin, Getzke, Felix, Schwanke, Florian, Dreyer, Ingo, Langen, Gregor, Zuccaro, Alga
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6362346/
https://www.ncbi.nlm.nih.gov/pubmed/30642845
http://dx.doi.org/10.15252/embr.201847430
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author Nizam, Shadab
Qiang, Xiaoyu
Wawra, Stephan
Nostadt, Robin
Getzke, Felix
Schwanke, Florian
Dreyer, Ingo
Langen, Gregor
Zuccaro, Alga
author_facet Nizam, Shadab
Qiang, Xiaoyu
Wawra, Stephan
Nostadt, Robin
Getzke, Felix
Schwanke, Florian
Dreyer, Ingo
Langen, Gregor
Zuccaro, Alga
author_sort Nizam, Shadab
collection PubMed
description Extracellular adenosine 5′‐triphosphate (eATP) is an essential signaling molecule that mediates different cellular processes through its interaction with membrane‐associated receptor proteins in animals and plants. eATP regulates plant growth, development, and responses to biotic and abiotic stresses. Its accumulation in the apoplast induces ROS production and cytoplasmic calcium increase mediating a defense response to invading microbes. We show here that perception of extracellular nucleotides, such as eATP, is important in plant–fungus interactions and that during colonization by the beneficial root endophyte Serendipita indica eATP accumulates in the apoplast at early symbiotic stages. Using liquid chromatography–tandem mass spectrometry, and cytological and functional analysis, we show that S. indica secrets SiE5′NT, an enzymatically active ecto‐5′‐nucleotidase capable of hydrolyzing nucleotides in the apoplast. Arabidopsis thaliana lines producing extracellular SiE5′NT are significantly better colonized, have reduced eATP levels, and altered responses to biotic stresses, indicating that SiE5′NT functions as a compatibility factor. Our data suggest that extracellular bioactive nucleotides and their perception play an important role in fungus–root interactions and that fungal‐derived enzymes can modify apoplastic metabolites to promote fungal accommodation.
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spelling pubmed-63623462019-02-14 Serendipita indica E5′NT modulates extracellular nucleotide levels in the plant apoplast and affects fungal colonization Nizam, Shadab Qiang, Xiaoyu Wawra, Stephan Nostadt, Robin Getzke, Felix Schwanke, Florian Dreyer, Ingo Langen, Gregor Zuccaro, Alga EMBO Rep Articles Extracellular adenosine 5′‐triphosphate (eATP) is an essential signaling molecule that mediates different cellular processes through its interaction with membrane‐associated receptor proteins in animals and plants. eATP regulates plant growth, development, and responses to biotic and abiotic stresses. Its accumulation in the apoplast induces ROS production and cytoplasmic calcium increase mediating a defense response to invading microbes. We show here that perception of extracellular nucleotides, such as eATP, is important in plant–fungus interactions and that during colonization by the beneficial root endophyte Serendipita indica eATP accumulates in the apoplast at early symbiotic stages. Using liquid chromatography–tandem mass spectrometry, and cytological and functional analysis, we show that S. indica secrets SiE5′NT, an enzymatically active ecto‐5′‐nucleotidase capable of hydrolyzing nucleotides in the apoplast. Arabidopsis thaliana lines producing extracellular SiE5′NT are significantly better colonized, have reduced eATP levels, and altered responses to biotic stresses, indicating that SiE5′NT functions as a compatibility factor. Our data suggest that extracellular bioactive nucleotides and their perception play an important role in fungus–root interactions and that fungal‐derived enzymes can modify apoplastic metabolites to promote fungal accommodation. John Wiley and Sons Inc. 2019-02-05 2019-02 /pmc/articles/PMC6362346/ /pubmed/30642845 http://dx.doi.org/10.15252/embr.201847430 Text en © 2019 The Authors. Published under the terms of the CC BY 4.0 license. This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Articles
Nizam, Shadab
Qiang, Xiaoyu
Wawra, Stephan
Nostadt, Robin
Getzke, Felix
Schwanke, Florian
Dreyer, Ingo
Langen, Gregor
Zuccaro, Alga
Serendipita indica E5′NT modulates extracellular nucleotide levels in the plant apoplast and affects fungal colonization
title Serendipita indica E5′NT modulates extracellular nucleotide levels in the plant apoplast and affects fungal colonization
title_full Serendipita indica E5′NT modulates extracellular nucleotide levels in the plant apoplast and affects fungal colonization
title_fullStr Serendipita indica E5′NT modulates extracellular nucleotide levels in the plant apoplast and affects fungal colonization
title_full_unstemmed Serendipita indica E5′NT modulates extracellular nucleotide levels in the plant apoplast and affects fungal colonization
title_short Serendipita indica E5′NT modulates extracellular nucleotide levels in the plant apoplast and affects fungal colonization
title_sort serendipita indica e5′nt modulates extracellular nucleotide levels in the plant apoplast and affects fungal colonization
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6362346/
https://www.ncbi.nlm.nih.gov/pubmed/30642845
http://dx.doi.org/10.15252/embr.201847430
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