Glutathione and phytochelatins jointly allow intracellular and extracellular detoxification of cadmium in the liverwort Marchantia polymorpha

Abstract

Plants have evolved a set of mechanisms that control and respond to the uptake and accumulation of both essential and non-essential metals, including chelation and sequestration of these elements by thiol ligands, such as glutathione and phytochelatins. Indeed, such thiol peptides can chelate some metals, quickly form thiol-metal complexes, and segregate them in the vacuolar compartment. Reasonably, conceptually similar mechanisms can be assumed to be responsible for the transport of metal complexes ̶ in particular thiol-cadmium complexes ̶ across the plasma membrane, with the consequent release of this toxic metal in the extracellular environment. Such hypothesis, focusing on prevention and detoxification mechanisms, was here verified in axenically-grown gametophytes of the model liverwort Marchantia polymorpha, exposed to three different cadmium concentrations over five exposure times. From the data obtained, it can be deduced that the cell wall of M. polymorpha moderately reduced the influx of cadmium into the cells, since it was rapidly saturated by this metal. At an intracellular level, cadmium induced the activity, but not the gene expression, of the phytochelatin synthase enzyme, leading to synthesis of phytochelatins. Moreover, both glutathione and phytochelatins chelated cadmium at the cytosolic level and allowed its detoxification, possibly involving tonoplast transporters belonging to type-C ABC subfamily (Mp7g13860 and Mp4g11930). Likewise, cadmium, glutathione and phytochelatins were released extracellularly, thus highlighting a possible novel role in cadmium detoxification, in a pH-dependent manner. The overall results suggest that, in M. polymorpha, glutathione and phytochelatins can accomplish intracellular and extracellular detoxification of cadmium.