Receptor-like cytoplasmic kinase MARIS functions downstream of Cr RLK1L-dependent signaling during tip growth

Plant cells constantly survey their environment to fine-tune their internal processes. Plant receptor-like kinases (RLKs) of the Catharanthus roseus RLK1-like ( Cr RLK1L) subfamily have been implicated in many signaling processes, including the coordination of the intracellular growth machinery with the performance of the extracellular matrix, i.e. the cell wall (CW). To avoid loss of integrity and growth and to adapt their CWs to developmental and environmental perturbations, growing plant cells have developed complex sensing mechanisms. The Cr RLK1Ls ANXUR1 and ANXUR2 and their closest homolog FERONIA control CW integrity in the tip-growing pollen tubes and root hairs, respectively. Here, we identify and characterize the receptor-like cytoplasmic kinase MARIS as a novel downstream component of the Cr RLK1L-dependent signaling cascade that controls CW integrity in tip-growing cells. Growing plant cells need to rigorously coordinate external signals with internal processes. For instance, the maintenance of cell wall (CW) integrity requires the coordination of CW sensing with CW remodeling and biosynthesis to avoid growth arrest or integrity loss. Despite the involvement of receptor-like kinases (RLKs) of the Catharanthus roseus RLK1-like ( Cr RLK1L) subfamily and the reactive oxygen species-producing NADPH oxidases, it remains largely unknown how this coordination is achieved. ANXUR1 (ANX1) and ANX2, two redundant members of the Cr RLK1L subfamily, are required for tip growth of the pollen tube (PT), and their closest homolog, FERONIA, controls root-hair tip growth. Previously, we showed that ANX1 overexpression mildly inhibits PT growth by oversecretion of CW material, whereas pollen tubes of anx1 anx2 double mutants burst spontaneously after germination. Here, we report the identification of suppressor mutants with improved fertility caused by the rescue of anx1 anx2 pollen tube bursting. Mapping of one these mutants revealed an R240C nonsynonymous substitution in the activation loop of a receptor-like cytoplasmic kinase (RLCK), which we named MARIS (MRI). We show that MRI is a plasma membrane-localized member of the RLCK-VIII subfamily and is preferentially expressed in both PTs and root hairs. Interestingly, mri -knockout mutants display spontaneous PT and root-hair bursting. Moreover, expression of the MRI R240C mutant, but not its wild-type form, partially rescues the bursting phenotypes of anx1 anx2 PTs and fer root hairs but strongly inhibits wild-