Convergent evolution of water conducting cells in Marchantia recruited the ZHOUPI gene promoting cell wall reinforcement and programmed cell death

A key adaptation of plants to life on land is the formation of water conducting cells (WCC) for efficient long-distance water transport. Based on morphological analyses it is thought that WCC have evolved independently on multiple occasions. For example, WCC have been lost in all but a few lineages of bryophytes but strikingly, within the liverworts a derived group, the complex thalloids, has evolved a novel externalised water conducting tissue composed of reinforced, hollow cells termed pegged rhizoids. Here we show that pegged rhizoid differentiation in Marchantia polymorpha is controlled by orthologues of the ZHOUPI and ICE bHLH transcription factors required for endosperm cell death in Arabidopsis seeds. By contrast, pegged rhizoid development was not affected by disruption of MpNAC5, the Marchantia orthologue of the VND genes that control WCC formation in flowering plants. We characterize the rapid, genetically controlled programmed cell death process that pegged rhizoids undergo to terminate cellular differentiation, and identify a corresponding upregulation of conserved putative plant cell death effector genes. Lastly, we show that ectopic expression of MpZOU1 increases production of pegged rhizoids and enhances drought tolerance. Our results support that pegged rhizoids having evolved independently of other WCC. We suggest that elements of the genetic control of developmental cell death are conserved throughout land plants and that the ZHOUPI/ICE regulatory module has been independently recruited to promote cell wall modification and programmed cell death in liverwort rhizoids and in the endosperm of flowering plant seed

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

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

The single Marchantia polymorpha FERONIA homolog reveals an ancestral role in regulating cellular expansion and integrity

Plant cells are surrounded by a cell wall, a rigid structure that is not only important for cell and organ shape, but is also crucial for intercellular communication and interactions with the environment. In the flowering plant Arabidopsis thaliana, the 17 members of the Catharanthus roseus RLK1-like (CrRLK1L) receptor kinase family are involved in a multitude of physiological and developmental processes, making it difficult to assess their primary or ancestral function. 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, and have reduced male fertility. In contrast, cell integrity and morphogenesis of the gametophyte are severely affected in Mpfer null mutants and MpFER overexpression lines. Thus, we conclude that 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 to fulfill a multitude of specialized physiological and developmental roles in the formation of both gametophytic and sporophytic structures essential to the life cycle of flowering plants