Role of glutathione in methylglyoxal detoxification pathway during yellow mosaic virus (YMV) infection in black gram (Vigna mungo (L.) Hepper)

Horváth

et al. 2022

IJMS

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.

Section: Discussionsupporting

confidence: 93%

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

Horváth

et al. 2022

IJMS

“…Moreover, this statement is consistent with those of Vanacker et al [ 54 ] and Tolin et al [ 55 ], who indicated that in apoplast glutathione acts as a sensor signaling stress conditions, and if the apoplast content is more oxidized, glutathione can take part in adaptation to biotic stress. Our findings from two Potyvirus pathosystems are consistent with the reports of Singh et al [ 56 ], who postulated that the GSSG content was higher in resistant plants compared to susceptible ones. Moreover, Kunstler et al [ 57 ] and Kiraly et al [ 58 ] suggested that a high GSSG concentration can indicate the role of glutathione in the suppression of defense response in oxidative stress during resistance reaction to TMV.…”

Section: Discussionsupporting

confidence: 93%

“…Furthermore, Igbal et al [ 87 ] and Navrot et al [ 88 ] pointed out that AtGPXLs efficiently reduced lipid peroxides and plasma membrane-localized AtGPXLs play an important role in maintaining membrane integrity. Similar to our reports, Singh et al [ 56 ] stated that GPX activity was more dynamically induced in a susceptible cultivar during Yellow mosaic virus infection at 20 dpi. Additionally, in contrast to our findings, Kalapos et al [ 89 ] reported high induction of GST genes accompanied by markedly suppressed GPXL, based on the results of transcriptome profiling during ObPV– C. annuum HR.…”

Section: Discussionsupporting

confidence: 92%

Glutathione Contribution in Interactions between Turnip mosaic virus and Arabidopsis thaliana Mutants Lacking Respiratory Burst Oxidase Homologs D and F

Treder

et al. 2023

IJMS

Respiratory burst oxidase homologs (Rbohs) play crucial and diverse roles in plant tissue-mediated production of reactive oxygen species during the development, growth, and response of plants to abiotic and biotic stress. Many studies have demonstrated the contribution of RbohD and RbohF in stress signaling in pathogen response differentially modulating the immune response, but the potential role of the Rbohs-mediated response in plant–virus interactions remains unknown. The present study analyzed, for the first time, the metabolism of glutathione in rbohD-, rbohF-, and rbohD/F-transposon-knockout mutants in response to Turnip mosaic virus (TuMV) infection. rbohD–TuMV and Col-0–TuMV interactions were characterized by susceptible reaction to TuMV, associated with significant activity of GPXLs (glutathione peroxidase-like enzymes) and induction of lipid peroxidation in comparison to mock-inoculated plants, with reduced total cellular and apoplastic glutathione content observed at 7–14 dpi and dynamic induction of apoplast GSSG (oxidized glutathione) at 1–14 dpi. Systemic virus infection resulted in the induction of AtGSTU1 and AtGSTU24, which was highly correlated with significant downregulation of GSTs (glutathione transferases) and cellular and apoplastic GGT (γ-glutamyl transferase) with GR (glutathione reductase) activities. On the contrary, resistant rbohF–TuMV reactions, and especially enhanced rbohD/F–TuMV reactions, were characterized by a highly dynamic increase in total cellular and apoplastic glutathione content, with induction of relative expression of AtGGT1, AtGSTU13, and AtGSTU19 genes. Moreover, virus limitation was highly correlated with the upregulation of GSTs, as well as cellular and apoplastic GGT with GR activities. These findings clearly indicate that glutathione can act as a key signaling factor in not only susceptible rbohD reaction but also the resistance reaction presented by rbohF and rbohD/F mutants during TuMV interaction. Furthermore, by actively reducing the pool of glutathione in the apoplast, GGT and GR enzymes acted as a cell first line in the Arabidopsis–TuMV pathosystem response, protecting the cell from oxidative stress in resistant interactions. These dynamically changed signal transductions involved symplast and apoplast in mediated response to TuMV.

“…The GSSG concentration decreased in susceptible interactions, whereas a dynamic increase was observed in hypersensitive responses. This observation at 21 dpi was consistent with the data described by Singh et al [ 40 ], who showed that the oxidized glutathione content was the highest in resistant cultivars, in contrast to susceptible cultivars, where it was the lowest. On the other hand, the GSH/GSSG ratio in hypersensitive Neptun potato–PVY NTN interactions was quite different from TMV–tobacco Xanthi in the study by Fodor et al [ 23 ].…”

Section: Discussionsupporting

confidence: 93%

“…Furthermore, in the Irys potato, the glutathione content decreased after 7 days to the lower level compared to mock inoculated leaves. A similar trend was observed by Singh et al [ 40 ] in susceptible and resistance cultivars of Vigna mungo inoculated with Yellow mosaic virus (YMV) belonging to Begamovirus. The decrease in GSH content between 7 and 21 dpi in the susceptible Irys potato was accompanied by a dynamic increase in virus concentration, and reduced GSH content can be considered as responsible for the development of pathogen elicited symptoms in the susceptible plant, taking into account the conclusions presented by Hernandez et al [ 41 ].…”

Section: Discussionsupporting

confidence: 84%

Glutathione Modulation in PVYNTN Susceptible and Resistant Potato Plant Interactions

Przewodowski

et al. 2022

IJMS

Glutathione is a metabolite that plays an important role in plant response to biotic stress through its ability to remove reactive oxygen species, thereby limiting the degree of potential oxidative damage. It can couple changes in the intracellular redox state to the development, especially the defense responses, of plants. Several studies have focused on measuring glutathione levels in virus infected plants, but have not provided complete information. Therefore, we analyzed, for the first time, the content of glutathione as well as its ultrastructural distribution related to susceptible and hypersensitive potato–Potato virus Y NTN (PVYNTN) interaction, with an aim of providing new insight into interactive responses to PVYNTN stress. Our findings reported that the inoculation of PVYNTN caused a dynamic increase in the content of glutathione, not only in resistance but also in susceptible reaction, especially at the first steps of plant–virus interaction. Moreover, the increase in hypersensitive response was much more dynamic, and accompanied by a significant reduction in the content of PVYNTN. By contrast, in susceptible potato Irys, the content of glutathione decreased between 7 and 21 days after virus inoculation, which led to a significant increase in PVYNTN concentration. Additionally, our findings clearly indicated the steady induction of two selected potato glutathione S-transferase StGSTF1 and StGSTF2 genes after PVYNTN inoculation, regardless of the interaction type. However, the relative expression level of StGSTF1 did not significantly differ between resistant and susceptible plants, whereas the relative expression levels of StGSTF2 differed between susceptible and resistant reactions. Therefore, we proposed that StGSTF2 can act as a marker of the type of response to PVYNTN. Our observations indicated that glutathione is an important component of signaling as well as the regulatory network in the PVYNTN–potato pathosystem. In resistance responses to PVYNTN, this metabolite activates plant defenses by reducing potential damage to the host plant cell, causing a reduction in virus concentration, while it can also be involved in the development of PVYNTN elicited symptoms, as well as limiting oxidative stress, leading to systemic infection in susceptible potato plants.