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Extracellular ATP targets Arabidopsis RIBONUCLEASE 1 to suppress mycotoxin stress‐induced cell death

Extracellular ATP is a purinergic signal with important functions in regulating plant growth and stress‐adaptive responses, including programmed cell death. While signalling events proximate to receptor activation at the plasma membrane have been characterised, downstream protein targets and the mec...

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Autores principales: Goodman, Heather L., Kroon, Johan T. M., Tomé, Daniel F. A., Hamilton, John M. U., Alqarni, Ali O., Chivasa, Stephen
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9545236/
https://www.ncbi.nlm.nih.gov/pubmed/35524456
http://dx.doi.org/10.1111/nph.18211
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author Goodman, Heather L.
Kroon, Johan T. M.
Tomé, Daniel F. A.
Hamilton, John M. U.
Alqarni, Ali O.
Chivasa, Stephen
author_facet Goodman, Heather L.
Kroon, Johan T. M.
Tomé, Daniel F. A.
Hamilton, John M. U.
Alqarni, Ali O.
Chivasa, Stephen
author_sort Goodman, Heather L.
collection PubMed
description Extracellular ATP is a purinergic signal with important functions in regulating plant growth and stress‐adaptive responses, including programmed cell death. While signalling events proximate to receptor activation at the plasma membrane have been characterised, downstream protein targets and the mechanism of cell death activation/regulation are unknown. We designed a proteomic screen to identify ATP‐responsive proteins in Arabidopsis cell cultures exposed to mycotoxin stress via fumonisin B1 (FB1) application. Arabidopsis RIBONUCLEASE 1 (RNS1) was identified by the screen, and transgenic plants overexpressing native RNS1 showed greater susceptibility to FB1, while a gene knockout rns1 mutant and antisense RNS1 transgenic plants were resistant to FB1‐induced cell death. Native RNS1 complemented rns1 mutants and restored the cell death response to FB1, while a catalytically inactive version of the ribonuclease could not. The FB1 resistance of salicylic acid (SA)‐depleted nahG‐expressing plants was abolished by transformation with native RNS1, but not the catalytically dead version. The mechanism of FB1‐induced cell death is activation of RNS1‐dependent RNA cleavage, which is blocked by ATP via RNS1 suppression, or enhanced by SA through induction of RNS1 expression. Our study reveals RNS1 as a previously unknown convergence point of ATP and SA signalling in the regulation of stress‐induced cell death.
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spelling pubmed-95452362022-10-14 Extracellular ATP targets Arabidopsis RIBONUCLEASE 1 to suppress mycotoxin stress‐induced cell death Goodman, Heather L. Kroon, Johan T. M. Tomé, Daniel F. A. Hamilton, John M. U. Alqarni, Ali O. Chivasa, Stephen New Phytol Research Extracellular ATP is a purinergic signal with important functions in regulating plant growth and stress‐adaptive responses, including programmed cell death. While signalling events proximate to receptor activation at the plasma membrane have been characterised, downstream protein targets and the mechanism of cell death activation/regulation are unknown. We designed a proteomic screen to identify ATP‐responsive proteins in Arabidopsis cell cultures exposed to mycotoxin stress via fumonisin B1 (FB1) application. Arabidopsis RIBONUCLEASE 1 (RNS1) was identified by the screen, and transgenic plants overexpressing native RNS1 showed greater susceptibility to FB1, while a gene knockout rns1 mutant and antisense RNS1 transgenic plants were resistant to FB1‐induced cell death. Native RNS1 complemented rns1 mutants and restored the cell death response to FB1, while a catalytically inactive version of the ribonuclease could not. The FB1 resistance of salicylic acid (SA)‐depleted nahG‐expressing plants was abolished by transformation with native RNS1, but not the catalytically dead version. The mechanism of FB1‐induced cell death is activation of RNS1‐dependent RNA cleavage, which is blocked by ATP via RNS1 suppression, or enhanced by SA through induction of RNS1 expression. Our study reveals RNS1 as a previously unknown convergence point of ATP and SA signalling in the regulation of stress‐induced cell death. John Wiley and Sons Inc. 2022-05-31 2022-08 /pmc/articles/PMC9545236/ /pubmed/35524456 http://dx.doi.org/10.1111/nph.18211 Text en © 2022 The Authors. New Phytologist © 2022 New Phytologist Foundation https://creativecommons.org/licenses/by/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research
Goodman, Heather L.
Kroon, Johan T. M.
Tomé, Daniel F. A.
Hamilton, John M. U.
Alqarni, Ali O.
Chivasa, Stephen
Extracellular ATP targets Arabidopsis RIBONUCLEASE 1 to suppress mycotoxin stress‐induced cell death
title Extracellular ATP targets Arabidopsis RIBONUCLEASE 1 to suppress mycotoxin stress‐induced cell death
title_full Extracellular ATP targets Arabidopsis RIBONUCLEASE 1 to suppress mycotoxin stress‐induced cell death
title_fullStr Extracellular ATP targets Arabidopsis RIBONUCLEASE 1 to suppress mycotoxin stress‐induced cell death
title_full_unstemmed Extracellular ATP targets Arabidopsis RIBONUCLEASE 1 to suppress mycotoxin stress‐induced cell death
title_short Extracellular ATP targets Arabidopsis RIBONUCLEASE 1 to suppress mycotoxin stress‐induced cell death
title_sort extracellular atp targets arabidopsis ribonuclease 1 to suppress mycotoxin stress‐induced cell death
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9545236/
https://www.ncbi.nlm.nih.gov/pubmed/35524456
http://dx.doi.org/10.1111/nph.18211
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