Functional evidence for the partial conservation of arsenic tolerance mechanisms in Marchantia polymorpha and Arabidopsis thaliana

Arsenic is a widespread metalloid that even at low concentrations is highly toxic to most plant species. While the transcriptional responses associated to arsenic tolerance have been widely investigated in vascular plants, comparatively little is known in their sister lineage, the bryophytes. Most importantly, functional evidence of whether the same genes play major roles in arsenic tolerance responses in these two anciently diverged land plant lineages is currently largely missing. In this study, we identified by RNA-Seq a highly reliable set of differentially expressed genes (DEGs) responding to arsenite toxicity in the model bryophyte Marchantia polymorpha. We then explored the evolutionary level of functional conservation of seven upregulated DEGs by Agrobacterium-mediated transformation in the highly arsenic-sensitive cad1–3 mutant of Arabidopsis thaliana as a representative of tracheophytes, and characterized fresh weight, malondialdehyde production and total arsenic content in dry biomass of transgenic lines. While two of the tested M. polymorpha DEGs did not significantly enhance arsenic tolerance, the remaining five DEGs, when overexpressed in cad1–3, conferred maximal levels of tolerance, measured as biomass accumulation, between 56 % and 100 % of WT Col-0 plants. Among them, a putative 1-cys peroxiredoxin restored growth, protection from lipid peroxidation and capacity to accumulate arsenic to levels indistinguishable from those of WT. These results provide functional evidence for the considerable conservation of arsenic tolerance responses between M. polymorpha and A. thaliana, suggesting that M. polymorpha can be a valid model for the identification of evolutionarily deeply conserved genes for the genetic improvement of crops for arsenic tolerance.