Direct attenuation of Arabidopsis ERECTA signaling by a pair of U-box E3 ligases

Abstract

Plants sense a myriad of signals through cell-surface receptors to coordinate their development and environmental response. The Arabidopsis ERECTA receptor kinase regulates diverse developmental processes via perceiving multiple EPIDERMAL PATTERNING FACTOR (EPF)/EPF-LIKE peptide ligands. How the activated ERECTA protein is turned over is unknown. Here we identify two closely-related Plant U-box ubiquitin E3 ligases, PUB30 and PUB31, as key attenuators of ERECTA signaling for two distinct developmental processes: inflorescence/pedicel growth and stomatal development. Loss-of-function pub30 pub31 mutant plants exhibit extreme inflorescence/pedicel elongation and reduced stomatal numbers owing to excessive ERECTA protein accumulation. Ligand-activation of ERECTA leads to phosphorylation of PUB30/31 by the co-receptor BRI1 ASSOCIATED KINASE1 (BAK1), which then promotes PUB30/31 to associate with and ubiquitinate ERECTA for eventual degradation. We further show that the PUB30 and PUB31 phosphorylation by BAK1 and their ubiquitination activities are critical for the proper in vivo developmental outputs. Our work highlights PUB30 and PUB31 as integral components of the ERECTA regulatory circuit that ensures optimal signaling strengths upon ligand activation, thereby enabling proper growth and development.