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

Abstract

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.

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

“…The changes in the expression of TuMV-CP during TuMV infection in rbohD , rbohF , and rbohD/F mutant plants confirmed the differences in the reaction of these plants to the presence of TuMV. Moreover, our previous works confirmed that RbohD [ 24 ] and glutathione [ 39 , 40 ] act as modulators of reaction to different Potyviruses. In normal physiological conditions, the levels of Rboh s and glutathione are precisely regulated in plants.…”

“…Moreover, the relative expression of AtGGT1 decreased systemically after 3 dpi by 4.45-fold in virus-inoculated Col-0 and by 21-fold in virus-inoculated rbohD plants. Our previous investigation showed that GSTs (glutathione S-transferases), especially class tau (GSTU), play an important role in the modulation of cell glutathione levels in TuMV infection [ 40 ]. Moreover, modification of the expression of different GST genes was found to be crucial for the precise modulation of the host’s response to this viral pathogen [ 40 ].…”

“…Our previous investigation showed that GSTs (glutathione S-transferases), especially class tau (GSTU), play an important role in the modulation of cell glutathione levels in TuMV infection [ 40 ]. Moreover, modification of the expression of different GST genes was found to be crucial for the precise modulation of the host’s response to this viral pathogen [ 40 ]. Therefore, in this study, we analyzed the relative expression of four GST genes— AtGSTU1 , AtGSTU13 , AtGSTU19 , and AtGSTU24 —which were previously identified to be involved in response to TuMV infection.…”

“…The glutathione induction was found to be much more dynamic in HR than in mock-inoculated plants and compared to susceptible potato response and was accompanied by statistically significant GSH induction and deposition in cell wall in HR reaction [ 39 ]. Moreover, the response of Atgstu19 - and Atgstu24 -knockout mutants to TuMV demonstrated that glutathione and glutathione metabolism enzymes play an important role and can be differentially modulated in the plant–virus pathosystem [ 40 ]. A quite similar tendency was reported by Hakmaoui et al [ 48 ], who observed that during Nicotiana benthamiana – Pepper mild mottle virus interactions the GSH content decreased and systemic infection was suppressed.…”

“…Our previous studies indicated that glutathione acts as a modulator in potato–PVY NTN pathosystem [ 39 ]. Moreover, our further studies examined the response of glutathione transferase class tau (GSTU)-knockout Arabidopsis mutants Atgstu19 and Atgstu24 to TuMV [ 40 ]. We assumed that AtGSTU19 and AtGSTU24 are important factors modulating the response of Arabidopsis plants to TuMV.…”