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

Abstract

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 (CrRLK1L) 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 CrRLK1L 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 membranelocalized 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-type tip growth. Thus, our findings identify a novel positive component of the CrRLK1L-dependent signaling cascade that coordinates CW integrity and tip growth.receptor-like kinase signaling | cell wall integrity | pollen tube | root hair | Arabidopsis

Receptor kinase complex transmits RALF peptide signal to inhibit root growth in Arabidopsis

“…Likewise, each RLCK may partner with more than one RLK to regulate distinct responses. In support of this notion, a RLCK-VIII subfamily member, MARIS, was recently reported to participate in the ANX1 pathway in PT growth and in the FER pathway for root hair tip growth (35). It is yet to be determined whether MARIS, like RIPK, can directly interact with FER or ANX1.…”

“…S4E). It is likely that FER works together with multiple RLCK partner proteins (such as MARIS) to control its multiple downstream responses (35). As a result, mutation of one of these partners (such as in the ripk mutant) disrupts only part of these responses, leading to weaker phenotypes compared with those in fer-4.…”

ROS Regulation of Polar Growth in Plant Cells

“…Recently, it was postulated that OXI1 activates MRI, a receptor-like cytoplasmic kinase of the VIII subfamily. MRI present in growing root hairs and pollen tubes is postulated to act downstream of the Catharanthus roseus RLKs FERONIA (FER) and ANXUR1 (ANX1)/ANX2 (Boisson-Dernier et al, 2015). Recently, it was shown that MRI interacts with OXI1, and in an vitro assay it was phosphorylated by OXI1 (Liao et al, 2016).…”

Bound by Fate: The Role of Reactive Oxygen Species in Receptor-Like Kinase Signaling

“…A suppressor mutant screen for male sterility in the anx1 anx2 double mutant identified a mutation in the RLCK MARIS (MRI) that stimulates its kinase activity. Hyperactive (but not wild type) MRI partially rescued the male sterility of anx1 anx2 and rbohH rbohJ double mutants (Boisson-Dernier et al, 2015), suggesting that MRI is capable of activating other RBOHs. This hypothesis is in line with the ability of hyperactive MRI to rescue RBOHC/RHD2-dependent root hair growth defects in fer (Boisson-Dernier et al, 2015).…”

“…Hyperactive (but not wild type) MRI partially rescued the male sterility of anx1 anx2 and rbohH rbohJ double mutants (Boisson-Dernier et al, 2015), suggesting that MRI is capable of activating other RBOHs. This hypothesis is in line with the ability of hyperactive MRI to rescue RBOHC/RHD2-dependent root hair growth defects in fer (Boisson-Dernier et al, 2015). To gain more insight into the integration of MRI into CrRLK1L signaling, it would be interesting to assess ROS accumulation in plants with hyperactive and kinase-dead MRI.…”