Glutathione regulates ACC synthase transcription via WRKY33 and ACC oxidase by modulating mRNA stability to induce ethylene synthesis during stress

Abstract

Glutathione (GSH) plays a fundamental role in plant defense-signaling network. Recently, we have established the involvement of GSH with ethylene (ET) to combat environmental stress. However, the mechanism of GSH-ET interplay still remains unexplored. Here, we demonstrate that GSH induces ET biosynthesis by modulating the transcriptional and posttranscriptional regulations of its key enzymes, 1-aminocyclopropane-1-carboxylate synthase (ACS) and 1-aminocyclopropane-1-carboxylate oxidase (ACO). Transgenic Arabidopsis (Arabidopsis thaliana) plants with enhanced GSH content (AtECS) exhibited remarkable up-regulation of ACS2, ACS6, and ACO1 at transcript as well as protein levels, while they were down-regulated in the GSH-depleted phytoalexin deficient2-1 (pad2-1) mutant. We further observed that GSH induced ACS2 and ACS6 transcription in a WRKY33-dependent manner, while ACO1 transcription remained unaffected. On the other hand, the messenger RNA stability for ACO1 was found to be increased by GSH, which explains our above observations. In addition, we also identified the ACO1 protein to be a subject for S-glutathionylation, which is consistent with our in silico data. However, S-glutathionylation of ACS2 and ACS6 proteins was not detected. Further, the AtECS plants exhibited resistance to necrotrophic infection and salt stress, while the pad2-1 mutant was sensitive. Exogenously applied GSH could improve stress tolerance in wild-type plants but not in the ET-signaling mutant ethylene insensitive2-1, indicating that GSH-mediated resistance to these stresses occurs via an ET-mediated pathway. Together, our investigation reveals a dual-level regulation of ET biosynthesis by GSH during stress.

Transcriptome analysis of Arabidopsis mutants suggests a crosstalk between ABA, ethylene and GSH against combined cold and osmotic stress

“…The role of glutathione in regulating ACC synthase to induce ethylene in stress condition has already been established in our lab14. Ethylene and salicylic acid regulated the glutathione biosynthesis in ozone-exposed A. thaliana 15.…”

Ethylene Potentiates Sulfur-Mediated Reversal of Cadmium Inhibited Photosynthetic Responses in Mustard

“…Fu et al (2014) studied the regulatory interaction between S-assimilation and ethylene for tolerance to arsenic in Arabidopsis Col-0. Exogenously applied GSH positively modulates ethylene biosynthetic pathways enzyme and improves stress tolerance in Arabidopsis Col-0 showing that GSH mediated resistance to stresses occurs via an ethylene signaling pathway (Datta et al, 2015). Recent studies showed that ethylene signaling pathways might be involved in the accumulation of GSH under Cd stress (Guan et al, 2015).…”

The ethylene response factor VaERF092 from Amur grape regulates the transcription factor VaWRKY33, improving cold tolerance

“…AtWRKY33 is the homolog of VaWRKY33 , and is positive regulator of pathogen‐induced autophagy, which plays a critical role in plant resistance to necrotrophic fungal pathogens (Zheng et al ., ; Lai et al ., ), as well as being critical for abiotic stress tolerance (Jiang and Deyholos, ; Li et al ., ). Furthermore, AtWRKY33 plays an essential role in glutathione‐mediated transcriptional regulation of the key components of the ethylene signal pathway, ACS2 and ACS6, by binding to their promoters and promoting ethylene synthesis (Datta et al ., ). We infer from these observations that VaWRKY33 may also participate in the production of ethylene, resulting in enhanced cold tolerance.…”