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AtGSTU19 and AtGSTU24 as Moderators of the Response of Arabidopsis thaliana to Turnip mosaic virus

Plants produce glutathione as a response to the intercellular redox state. Glutathione actively participates in the reactive oxygen species (ROS)-dependent signaling pathway, especially under biotic stress conditions. Most of the glutathione S-transferases (GSTs) are induced in cells during the defe...

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Autores principales: Otulak-Kozieł, Katarzyna, Kozieł, Edmund, Horváth, Edit, Csiszár, Jolán
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9570173/
https://www.ncbi.nlm.nih.gov/pubmed/36232831
http://dx.doi.org/10.3390/ijms231911531
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author Otulak-Kozieł, Katarzyna
Kozieł, Edmund
Horváth, Edit
Csiszár, Jolán
author_facet Otulak-Kozieł, Katarzyna
Kozieł, Edmund
Horváth, Edit
Csiszár, Jolán
author_sort Otulak-Kozieł, Katarzyna
collection PubMed
description Plants produce glutathione as a response to the intercellular redox state. Glutathione actively participates in the reactive oxygen species (ROS)-dependent signaling pathway, especially under biotic stress conditions. Most of the glutathione S-transferases (GSTs) are induced in cells during the defense response of plants not only through highly specific glutathione-binding abilities but also by participating in the signaling function. The tau class of GSTs has been reported to be induced as a response under stress conditions. Although several studies have focused on the role of the tau class of GSTs in plant–pathogen interactions, knowledge about their contribution to the response to virus inoculation is still inadequate. Therefore, in this study, the response of Atgstu19 and Atgstu24 knockout mutants to mechanical inoculation of Turnip mosaic virus (TuMV) was examined. The systemic infection of TuMV was more dynamically promoted in Atgstu19 mutants than in wild-type (Col-0) plants, suggesting the role of GSTU19 in TuMV resistance. However, Atgstu24 mutants displayed virus limitation and downregulation of the relative expression of TuMV capsid protein, accompanied rarely by TuMV particles only in vacuoles, and ultrastructural analyses of inoculated leaves revealed the lack of virus cytoplasmic inclusions. These findings indicated that Atgstu24 mutants displayed a resistance-like reaction to TuMV, suggesting that GSTU24 may suppress the plant resistance. In addition, these findings confirmed that GSTU1 and GSTU24 are induced and contribute to the susceptible reaction to TuMV in the Atgstu19–TuMV interaction. However, the upregulation of GSTU19 and GSTU13 highly correlated with virus limitation in the resistance-like reaction in the Atgstu24–TuMV interaction. Furthermore, the highly dynamic upregulation of GST and glutathione reductase (GR) activities resulted in significant induction (between 1 and 14 days post inoculation [dpi]) of the total glutathione pool (GSH + GSSG) in response to TuMV, which was accompanied by the distribution of active glutathione in plant cells. On the contrary, in Atgstu19, which is susceptible to TuMV interaction, upregulation of GST and GR activity only up to 7 dpi symptom development was reported, which resulted in the induction of the total glutathione pool between 1 and 3 dpi. These observations indicated that GSTU19 and GSTU24 are important factors in modulating the response to TuMV in Arabidopsis thaliana. Moreover, it was clear that glutathione is an important component of the regulatory network in resistance and susceptible response of A. thaliana to TuMV. These results help achieve a better understanding of the mechanisms regulating the Arabidopsis–TuMV pathosystem.
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spelling pubmed-95701732022-10-17 AtGSTU19 and AtGSTU24 as Moderators of the Response of Arabidopsis thaliana to Turnip mosaic virus Otulak-Kozieł, Katarzyna Kozieł, Edmund Horváth, Edit Csiszár, Jolán Int J Mol Sci Article Plants produce glutathione as a response to the intercellular redox state. Glutathione actively participates in the reactive oxygen species (ROS)-dependent signaling pathway, especially under biotic stress conditions. Most of the glutathione S-transferases (GSTs) are induced in cells during the defense response of plants not only through highly specific glutathione-binding abilities but also by participating in the signaling function. The tau class of GSTs has been reported to be induced as a response under stress conditions. Although several studies have focused on the role of the tau class of GSTs in plant–pathogen interactions, knowledge about their contribution to the response to virus inoculation is still inadequate. Therefore, in this study, the response of Atgstu19 and Atgstu24 knockout mutants to mechanical inoculation of Turnip mosaic virus (TuMV) was examined. The systemic infection of TuMV was more dynamically promoted in Atgstu19 mutants than in wild-type (Col-0) plants, suggesting the role of GSTU19 in TuMV resistance. However, Atgstu24 mutants displayed virus limitation and downregulation of the relative expression of TuMV capsid protein, accompanied rarely by TuMV particles only in vacuoles, and ultrastructural analyses of inoculated leaves revealed the lack of virus cytoplasmic inclusions. These findings indicated that Atgstu24 mutants displayed a resistance-like reaction to TuMV, suggesting that GSTU24 may suppress the plant resistance. In addition, these findings confirmed that GSTU1 and GSTU24 are induced and contribute to the susceptible reaction to TuMV in the Atgstu19–TuMV interaction. However, the upregulation of GSTU19 and GSTU13 highly correlated with virus limitation in the resistance-like reaction in the Atgstu24–TuMV interaction. Furthermore, the highly dynamic upregulation of GST and glutathione reductase (GR) activities resulted in significant induction (between 1 and 14 days post inoculation [dpi]) of the total glutathione pool (GSH + GSSG) in response to TuMV, which was accompanied by the distribution of active glutathione in plant cells. On the contrary, in Atgstu19, which is susceptible to TuMV interaction, upregulation of GST and GR activity only up to 7 dpi symptom development was reported, which resulted in the induction of the total glutathione pool between 1 and 3 dpi. These observations indicated that GSTU19 and GSTU24 are important factors in modulating the response to TuMV in Arabidopsis thaliana. Moreover, it was clear that glutathione is an important component of the regulatory network in resistance and susceptible response of A. thaliana to TuMV. These results help achieve a better understanding of the mechanisms regulating the Arabidopsis–TuMV pathosystem. MDPI 2022-09-29 /pmc/articles/PMC9570173/ /pubmed/36232831 http://dx.doi.org/10.3390/ijms231911531 Text en © 2022 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Otulak-Kozieł, Katarzyna
Kozieł, Edmund
Horváth, Edit
Csiszár, Jolán
AtGSTU19 and AtGSTU24 as Moderators of the Response of Arabidopsis thaliana to Turnip mosaic virus
title AtGSTU19 and AtGSTU24 as Moderators of the Response of Arabidopsis thaliana to Turnip mosaic virus
title_full AtGSTU19 and AtGSTU24 as Moderators of the Response of Arabidopsis thaliana to Turnip mosaic virus
title_fullStr AtGSTU19 and AtGSTU24 as Moderators of the Response of Arabidopsis thaliana to Turnip mosaic virus
title_full_unstemmed AtGSTU19 and AtGSTU24 as Moderators of the Response of Arabidopsis thaliana to Turnip mosaic virus
title_short AtGSTU19 and AtGSTU24 as Moderators of the Response of Arabidopsis thaliana to Turnip mosaic virus
title_sort atgstu19 and atgstu24 as moderators of the response of arabidopsis thaliana to turnip mosaic virus
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9570173/
https://www.ncbi.nlm.nih.gov/pubmed/36232831
http://dx.doi.org/10.3390/ijms231911531
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