Regulation of the stability of RGF1 receptor by the ubiquitin-specific proteases UBP12/UBP13 is critical for root meristem maintenance

ROOT MERISTEM GROWTH FACTOR (RGF) 1 is an important peptide hormone that regulates root growth. Upon binding to its receptor, RGFR1, RGF1 regulates the expression of two transcription factors, PLETHORA 1 and 2 (PLT1/2), to influence root meristem development. Here, we show that the ubiquitin-specific proteases UBP12 and UBP13 are positive regulators of root meristem development and that UBP13 interacts directly with RGF1 receptor (RGFR1) and its close homolog RGFR2. The ubp12,13 double-mutant root is completely insensitive to exogenous applied RGF1. Consistent with this result, RGF1-induced ubiquitination and turnover of RGFR1 protein were accelerated in ubp12,13-mutant plants but were delayed in transgenic plants overexpressing UBP13. Genetic analysis showed that PLT2 or RGFR1 overexpression partially rescued the short-root phenotype and the reduced cortical root meristem cell number in ubp12,13 plants. Together, our results demonstrate that UBP12/13 are regulators of the RGF1–RGFR1–PLT1/2 signaling pathway and that UBP12/13 can counteract RGF1-induced RGFR1 ubiquitination, stabilize RGFR1, and maintain root cell sensitivity to RGF1.