Revising the roles of phytochelatin synthases and their evolutionary history in different plant species

Abstract

The cytosolic enzyme phytochelatin synthase (PCS) is constitutively expressed and it has been studied for its role in metal(loid) detoxification in different organisms. It has been recognized that PCS enzymes detoxify Cd or other toxic heavy metals by catalysing the formation of thiol rich polymers, namely phytochelatins (PCs), from glutathione (GSH) and related thiols. PCs bind several metal(loid)s with high affinity and facilitate their sequestration into the vacuole mainly via ABC transporters. Other papers have reported another role played by the PCS enzyme, PCS is in fact also involved in the catabolism of glutathione-conjugates, catalysing the first reaction of degradation by the cleavage of glycine from the GS-conjugate, to generate a γ-EC-conjugate, without PC production. Furthermore, the transcript abundance of AtPCS1 (from the model plant Arabidopsis thaliana) increases under Fe deficiency and after treatment with a mimetic signal of a pathogen attack, a synthetic 22-amino acid peptide that corresponds to a highly conserved region of the eubacterial flagellin (Flg22). In this context, to revisit the role of PCSs and to elucidate their possible functions, we used Arabidopsis thaliana as an experimental model and an array of approaches including LC-ESI-MS-based metabolome analyses, gene expression studies, etc. We found a relationship between PCS and the secondary metabolism of A. thaliana, in detail with the glucosinolate and phenilpropanoid pathways. These studies were integrated by research aimed at elucidating the evolutionary roles of PCS, as well as the ability to synthesize PCs in chrophytes and basal land plants. We found the presence of constitutive and functional PCS enzymes in all the lineages of bryophytes, as well as in early tracheophytes. Indeed, the liverwort Lunularia cruciata showed to possess a PCS showing a (adaptive?) function aimed at regulating the Fe/Zn homeostasis, together with a role aimed at detoxifying Cd.