The receptor kinase OsWAK11 monitors cell wall pectin changes to fine-tune brassinosteroid signaling and regulate cell elongation in rice

Rates of plant cell elongation change with day-night alternation, reflecting differences in metabolism related to cell wall remodeling. Information from cell wall surveillance pathways must be integrated with growth regulation pathways to provide feedback regulation of cell wall modification; such feedback regulation is important to ensure sufficient strength and prevent rupture of the cell wall during growth. Several lines of evidence suggest that cell wall perturbations often influence phytohormone signaling, but the identity of the nexus between these two processes remained elusive. Here, we show that wall-associated kinase11 (OsWAK11) acts as a linker connecting cell wall pectin methyl-esterification changes and brassinosteroid (BR) signaling in rice. Our data show that OsWAK11 controls several important agronomical traits by regulating cell elongation in rice. OsWAK11 directly binds and phosphorylates the BR receptor OsBRI1 at residue Thr752, within a motif conserved across most monocot graminaceous crops, thus hindering OsBRI1 interaction with its co-receptor OsSERK1/OsBAK1 and inhibiting BR signaling. The extracellular domain of OsWAK11 shows a much stronger interaction toward methyl-esterified pectin as compared with de-methyl-esterified pectin. OsWAK11 is stabilized in light but is degraded in darkness, in a process triggered by changes in the ratio of methyl-esterified to de-methyl-esterified pectin, creating fluctuations in plant BR signaling in response to day and night alternation. We conclude that OsWAK11 is a cell wall monitor that regulates cell elongation rates to adapt to the environment from the outside in, which complements the well-established inside-out signaling pathway affecting cell elongation in plants.