Multiomics analyses of mutants for Marchantia polymorpha FERONIA and MARIS reveal a link between cell wall integrity and abscisic acid responses

At the core of cell wall integrity mechanisms that enable plant cells to coordinate their growth with their cell wall status lies the transmembrane malectin-like receptor kinase FERONIA (FER) and its family members. FER itself controls a myriad of plant developmental processes, including sexual reproduction, cell growth, and morphogenesis, often intersecting with phytohormone-dependent pathways such as abscisic acid (ABA) signaling or plant immunity. Interestingly, FER, together with its downstream receptor-like cytoplasmic kinase MARIS (MRI), has been shown to similarly control root hair and rhizoid integrity in the vascular angiosperm Arabidopsis thaliana and the early diverging bryophyte Marchantia polymorpha, respectively. It remains uncertain however whether FER and MRI cooperate beyond tip growth in Marchantia, and which of their functions in Arabidopsis originate from mechanisms established early in land plant evolution. Here, we conducted comparative transcriptomic and proteomic analyses on the M. polymorpha mutant plants, Mpfer-1 and Mpmri-1, alongside their corresponding wild-type accessions. We observed large and significant overlaps between differentially expressed genes and abundant proteins between both mutants. Our multiomics approach revealed that MpFER and MpMRI largely cooperate to repress transcriptional networks, particularly those associated with plant defense and ABA responses. Nonetheless, our phenotypic analyses showed that MpFER and MpMRI exert distinct functions in response to abiotic stresses such as ABA and salt treatment. Specifically, Mpfer-1, but not Mpmri-1, plants exhibited hypersensitivity to ABA-dependent growth inhibition, indicating that FER's role in negatively regulating ABA-mediated growth responses is conserved between bryophytes and vascular plants.