Characterization of the single FERONIA homolog in Marchantia polymorpha reveals an ancestral role of CrRLK1L receptor kinases in regulating cell expansion and morphological integrity

Abstract

Plant cells are surrounded by a cell wall, a rigid structure rich in polysaccharides and glycoproteins. The cell wall is not only important for cell and organ shape, but crucial for intercellular communication, plant-microbe interactions, and as a barrier to the environment. In the flowering plant Arabidopsis thaliana, the 17 members of the Catharanthus roseus RLK1-like (CrRLK1L) receptor kinase subfamily are involved in a multitude of physiological and developmental processes involving the cell wall, including reproduction, hormone signaling, cell expansion, innate immunity, and various stress responses. Due to genetic redundancy and the fact that individual CrRLK1Ls can have distinct and sometimes opposing functions, it is difficult to assess the primary or ancestral function of CrRLK1Ls. To reduce genetic complexity, we characterized the single CrRLK1L gene of Marchantia polymorpha, MpFERONIA (MpFER). Plants with reduced MpFER levels show defects in vegetative development, i.e., rhizoid formation and cell expansion, but also affect male fertility. In contrast, Mpfer null mutants and overexpression lines severely affect cell integrity and morphogenesis of the gametophyte. Thus, the CrRLK1L gene family originated from a single gene with an ancestral function in cell expansion and the maintenance of cellular integrity. During land plant evolution, this ancestral gene diversified and was recruited to fulfil a multitude of specialized physiological and developmental and roles in the formation of both gametophytic and sporophytic structures essential to the life cycle of flowering plants.