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ATM and ATR, two central players of the DNA damage response, are involved in the induction of systemic acquired resistance by extracellular DNA, but not the plant wound response

BACKGROUND: The plant immune response to DNA is highly self/nonself-specific. Self-DNA triggered stronger responses by early immune signals such as H(2)O(2) formation than nonself-DNA from closely related plant species. Plants lack known DNA receptors. Therefore, we aimed to investigate whether a di...

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Autores principales: Vega-Muñoz, Isaac, Herrera-Estrella, Alfredo, Martínez-de la Vega, Octavio, Heil, Martin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10225592/
https://www.ncbi.nlm.nih.gov/pubmed/37256140
http://dx.doi.org/10.3389/fimmu.2023.1175786
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author Vega-Muñoz, Isaac
Herrera-Estrella, Alfredo
Martínez-de la Vega, Octavio
Heil, Martin
author_facet Vega-Muñoz, Isaac
Herrera-Estrella, Alfredo
Martínez-de la Vega, Octavio
Heil, Martin
author_sort Vega-Muñoz, Isaac
collection PubMed
description BACKGROUND: The plant immune response to DNA is highly self/nonself-specific. Self-DNA triggered stronger responses by early immune signals such as H(2)O(2) formation than nonself-DNA from closely related plant species. Plants lack known DNA receptors. Therefore, we aimed to investigate whether a differential sensing of self-versus nonself DNA fragments as damage- versus pathogen-associated molecular patterns (DAMPs/PAMPs) or an activation of the DNA-damage response (DDR) represents the more promising framework to understand this phenomenon. RESULTS: We treated Arabidopsis thaliana Col-0 plants with sonicated self-DNA from other individuals of the same ecotype, nonself-DNA from another A. thaliana ecotype, or nonself-DNA from broccoli. We observed a highly self/nonself-DNA-specific induction of H(2)O(2) formation and of jasmonic acid (JA, the hormone controlling the wound response to chewing herbivores) and salicylic acid (SA, the hormone controlling systemic acquired resistance, SAR, to biotrophic pathogens). Mutant lines lacking Ataxia Telangiectasia Mutated (ATM) or ATM AND RAD3-RELATED (ATR) – the two DDR master kinases – retained the differential induction of JA in response to DNA treatments but completely failed to induce H(2)O(2) or SA. Moreover, we observed H(2)O(2) formation in response to in situ-damaged self-DNA from plants that had been treated with bleomycin or SA or infected with virulent bacteria Pseudomonas syringae pv. tomato DC3000 or pv. glycinea carrying effector avrRpt2, but not to DNA from H(2)O(2)-treated plants or challenged with non-virulent P. syringae pv. glycinea lacking avrRpt2. CONCLUSION: We conclude that both ATM and ATR are required for the complete activation of the plant immune response to extracellular DNA whereas an as-yet unknown mechanism allows for the self/nonself-differential activation of the JA-dependent wound response.
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spelling pubmed-102255922023-05-30 ATM and ATR, two central players of the DNA damage response, are involved in the induction of systemic acquired resistance by extracellular DNA, but not the plant wound response Vega-Muñoz, Isaac Herrera-Estrella, Alfredo Martínez-de la Vega, Octavio Heil, Martin Front Immunol Immunology BACKGROUND: The plant immune response to DNA is highly self/nonself-specific. Self-DNA triggered stronger responses by early immune signals such as H(2)O(2) formation than nonself-DNA from closely related plant species. Plants lack known DNA receptors. Therefore, we aimed to investigate whether a differential sensing of self-versus nonself DNA fragments as damage- versus pathogen-associated molecular patterns (DAMPs/PAMPs) or an activation of the DNA-damage response (DDR) represents the more promising framework to understand this phenomenon. RESULTS: We treated Arabidopsis thaliana Col-0 plants with sonicated self-DNA from other individuals of the same ecotype, nonself-DNA from another A. thaliana ecotype, or nonself-DNA from broccoli. We observed a highly self/nonself-DNA-specific induction of H(2)O(2) formation and of jasmonic acid (JA, the hormone controlling the wound response to chewing herbivores) and salicylic acid (SA, the hormone controlling systemic acquired resistance, SAR, to biotrophic pathogens). Mutant lines lacking Ataxia Telangiectasia Mutated (ATM) or ATM AND RAD3-RELATED (ATR) – the two DDR master kinases – retained the differential induction of JA in response to DNA treatments but completely failed to induce H(2)O(2) or SA. Moreover, we observed H(2)O(2) formation in response to in situ-damaged self-DNA from plants that had been treated with bleomycin or SA or infected with virulent bacteria Pseudomonas syringae pv. tomato DC3000 or pv. glycinea carrying effector avrRpt2, but not to DNA from H(2)O(2)-treated plants or challenged with non-virulent P. syringae pv. glycinea lacking avrRpt2. CONCLUSION: We conclude that both ATM and ATR are required for the complete activation of the plant immune response to extracellular DNA whereas an as-yet unknown mechanism allows for the self/nonself-differential activation of the JA-dependent wound response. Frontiers Media S.A. 2023-05-15 /pmc/articles/PMC10225592/ /pubmed/37256140 http://dx.doi.org/10.3389/fimmu.2023.1175786 Text en Copyright © 2023 Vega-Muñoz, Herrera-Estrella, Martínez-de la Vega and Heil 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 Immunology
Vega-Muñoz, Isaac
Herrera-Estrella, Alfredo
Martínez-de la Vega, Octavio
Heil, Martin
ATM and ATR, two central players of the DNA damage response, are involved in the induction of systemic acquired resistance by extracellular DNA, but not the plant wound response
title ATM and ATR, two central players of the DNA damage response, are involved in the induction of systemic acquired resistance by extracellular DNA, but not the plant wound response
title_full ATM and ATR, two central players of the DNA damage response, are involved in the induction of systemic acquired resistance by extracellular DNA, but not the plant wound response
title_fullStr ATM and ATR, two central players of the DNA damage response, are involved in the induction of systemic acquired resistance by extracellular DNA, but not the plant wound response
title_full_unstemmed ATM and ATR, two central players of the DNA damage response, are involved in the induction of systemic acquired resistance by extracellular DNA, but not the plant wound response
title_short ATM and ATR, two central players of the DNA damage response, are involved in the induction of systemic acquired resistance by extracellular DNA, but not the plant wound response
title_sort atm and atr, two central players of the dna damage response, are involved in the induction of systemic acquired resistance by extracellular dna, but not the plant wound response
topic Immunology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10225592/
https://www.ncbi.nlm.nih.gov/pubmed/37256140
http://dx.doi.org/10.3389/fimmu.2023.1175786
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