AtGSTU19 and AtGSTU24 as Moderators of the Response of <i>Arabidopsis thaliana</i> to <i>Turnip mosaic virus</i>

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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Main Authors: Katarzyna Otulak-Kozieł, Edmund Kozieł, Edit Horváth, Jolán Csiszár
Format: Article
Language:English
Published: MDPI AG 2022-09-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:https://www.mdpi.com/1422-0067/23/19/11531
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author Katarzyna Otulak-Kozieł
Edmund Kozieł
Edit Horváth
Jolán Csiszár
author_facet Katarzyna Otulak-Kozieł
Edmund Kozieł
Edit Horváth
Jolán Csiszár
author_sort Katarzyna Otulak-Kozieł
collection DOAJ
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 <i>Atgstu19</i> and <i>Atgstu24</i> knockout mutants to mechanical inoculation of <i>Turnip mosaic virus</i> (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, <i>Atgstu24</i> 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 <i>Atgstu19</i>–TuMV interaction. However, the upregulation of GSTU19 and GSTU13 highly correlated with virus limitation in the resistance-like reaction in the <i>Atgstu24</i>–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 <i>Atgstu19</i>, 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 <i>Arabidopsis thaliana</i>. Moreover, it was clear that glutathione is an important component of the regulatory network in resistance and susceptible response of <i>A. thaliana</i> to TuMV. These results help achieve a better understanding of the mechanisms regulating the Arabidopsis–TuMV pathosystem.
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spelling doaj.art-60ca02fe132247ab8ad9bef0deb886562023-11-23T20:34:50ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672022-09-0123191153110.3390/ijms231911531AtGSTU19 and AtGSTU24 as Moderators of the Response of <i>Arabidopsis thaliana</i> to <i>Turnip mosaic virus</i>Katarzyna Otulak-Kozieł0Edmund Kozieł1Edit Horváth2Jolán Csiszár3Institute of Biology, Department of Botany, Warsaw University of Life Sciences, Nowoursynowska 159, 02-776 Warsaw, PolandInstitute of Biology, Department of Botany, Warsaw University of Life Sciences, Nowoursynowska 159, 02-776 Warsaw, PolandDepartment of Plant Biology, Faculty of Science and Informatics, University of Szeged, Közěp fasor 52, H-6726 Szeged, HungaryDepartment of Plant Biology, Faculty of Science and Informatics, University of Szeged, Közěp fasor 52, H-6726 Szeged, HungaryPlants 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 <i>Atgstu19</i> and <i>Atgstu24</i> knockout mutants to mechanical inoculation of <i>Turnip mosaic virus</i> (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, <i>Atgstu24</i> 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 <i>Atgstu19</i>–TuMV interaction. However, the upregulation of GSTU19 and GSTU13 highly correlated with virus limitation in the resistance-like reaction in the <i>Atgstu24</i>–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 <i>Atgstu19</i>, 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 <i>Arabidopsis thaliana</i>. Moreover, it was clear that glutathione is an important component of the regulatory network in resistance and susceptible response of <i>A. thaliana</i> to TuMV. These results help achieve a better understanding of the mechanisms regulating the Arabidopsis–TuMV pathosystem.https://www.mdpi.com/1422-0067/23/19/11531glutathioneglutathione S-transferase <i>tau</i> classplant–virus interactionplant cell ultrastructure
spellingShingle Katarzyna Otulak-Kozieł
Edmund Kozieł
Edit Horváth
Jolán Csiszár
AtGSTU19 and AtGSTU24 as Moderators of the Response of <i>Arabidopsis thaliana</i> to <i>Turnip mosaic virus</i>
International Journal of Molecular Sciences
glutathione
glutathione S-transferase <i>tau</i> class
plant–virus interaction
plant cell ultrastructure
title AtGSTU19 and AtGSTU24 as Moderators of the Response of <i>Arabidopsis thaliana</i> to <i>Turnip mosaic virus</i>
title_full AtGSTU19 and AtGSTU24 as Moderators of the Response of <i>Arabidopsis thaliana</i> to <i>Turnip mosaic virus</i>
title_fullStr AtGSTU19 and AtGSTU24 as Moderators of the Response of <i>Arabidopsis thaliana</i> to <i>Turnip mosaic virus</i>
title_full_unstemmed AtGSTU19 and AtGSTU24 as Moderators of the Response of <i>Arabidopsis thaliana</i> to <i>Turnip mosaic virus</i>
title_short AtGSTU19 and AtGSTU24 as Moderators of the Response of <i>Arabidopsis thaliana</i> to <i>Turnip mosaic virus</i>
title_sort atgstu19 and atgstu24 as moderators of the response of i arabidopsis thaliana i to i turnip mosaic virus i
topic glutathione
glutathione S-transferase <i>tau</i> class
plant–virus interaction
plant cell ultrastructure
url https://www.mdpi.com/1422-0067/23/19/11531
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