A TOR-YAK1 signaling axis controls cell cycle, meristem activity and plant growth in Arabidopsis

International audienceTARGET OF RAPAMYCIN (TOR) is a conserved eukaryotic phosphatidylinositol-3-kinase-related kinase that plays a major role in regulating growth and metabolism in response to environment in plants. We performed a genetic screen for Arabidopsis ethylmethane sulfonate mutants resistant to the ATP-competitive TOR inhibitor AZD-8055 to identify new components of the plant TOR pathway. We found that loss-of-function mutants of the DYRK (dual specificity tyrosine phosphorylation regulated kinase)/YAK1 kinase are resistant to AZD-8055 and, reciprocally, that YAK1 overexpressors are hypersensitive to AZD-8055. Significantly, these phenotypes were conditional on TOR inhibition, positioning YAK1 activity downstream of TOR. We further show that the ATP-competitive DYRK1A inhibitor pINDY phenocopies YAK1 loss of function. Microscopy analysis revealed that YAK1 functions to repress meristem size and induce differentiation. We show that YAK1 represses cyclin expression in the different zones of the root meristem and that YAK1 is essential for TOR-dependent transcriptional regulation of the plant-specific SIAMESE-RELATED (SMR) cyclin-dependent kinase inhibitors in both meristematic and differentiating root cells. Thus, YAK1 is a major regulator of meristem activity and cell differentiation downstream of TOR