Diversification of MSL proteins in extant land plants with intrinsically disordered regions depict their functional enhancement in stress response

Abstract

Mechanosensitive (MS) ion channels are transmembrane protein channels that regulate intracellular ion fluxes across the membrane in response to mechanical/oxidative stresses such as osmotic, cell injury, sound, touch, gravity, and germination. The mechanosensitive ion channels of small conductance (MscS) and their homologs MscS-like (MSL) are well studied in bacteria and flowering plants but not in algae and early land plants, particularly in terms of their physico-physiological properties and environmentally sensitive intrinsically disordered regions in relation to their functions. In this study, 51 algal and 57 bryophyte MSL proteins were characterized and compared with 66 MSL proteins in angiosperms. We noticed that the MSL proteins evolved independently in algae and expanded in early land plants from liverworts to mosses, involving both tandem and segmental gene duplication events. Nine different topological variants were observed with 1 to 9 transmembrane helices, depicting the increase in TMH number along the evolution from algae to monocots. Further, these proteins exhibit evolutionarily related intrinsically disordered regions (IDR), possessing putative binding sites for ligands and protein-protein interactions, indicating their conserved role in perception and transduction of environmental stresses. Enrichment of the stress-responsive cis-regulatory elements over the MSL promoters are quite evident in early land plants. Moreover, the functional and physico-physiological characteristics of MSL proteins are conserved across all groups despite their evolutionary divergence. Additionally, the transcript levels of 16 MSL genes identified in Physcomitrium patens varied under mechanical (gravity) stress, indicating their role in stress response. Our investigation provides in-depth evolutionary insights related to the function of MSL proteins in stress response.