Arabidopsis hypocotyl growth in darkness requires the phosphorylation of a microtubule-associated protein

Rapid hypocotyl elongation allows buried seedlings to emerge, where light triggers de-etiolation and inhibits hypocotyl growth mainly by photoreceptors. Phosphorylation/dephosphorylation events regulate many aspects of plant development. Only recently we have begun to uncover the earliest phospho-signaling responders to light. Here, we reported a large-scale phosphoproteomic analysis and identified 20 proteins that changed their phosphorylation pattern following a 20 min light pulse compared to darkness. Microtubule-associated proteins were highly overrepresented in this group. Among them, we studied CIP7 (COP1-INTERACTING-PROTEIN 7), which presented microtubule (MT) localization in contrast to the previous description. An isoform of CIP7 phosphorylated at Serine915 was detected in etiolated seedlings but was undetectable after a light pulse in the presence of photoreceptors, while CIP7 transcript expression decays with long light exposure. The short hypocotyl phenotype and rearrangement of MTs in etiolated cip7 mutants are complemented by CIP7-YFP and the phospho-mimetic CIP7S915D-YFP, but not the phospho-null CIP7S915A-YFP suggesting that the phosphorylated S915CIP7 isoform promotes hypocotyl elongation through MT reorganization in darkness. Our evidence on Serine915 of CIP7 unveils phospho-regulation of MT-based processes during skotomorphogenic hypocotyl growth. In our large-scale phosphoproteome assay to elucidate the initial phospho-signaling components triggered by a short light pulse, we found an enrichment of microtubule (MTs)-associated proteins. Among these proteins, CIP7 (COP1-INTERATING-PROTEIN-7) localizes to MTs and affects hypocotyl growth and MT orientation in dark hypocotyls. Serine915 of CIP7 is dephosphorylated by a brief light pulse. Phosphorylation status of Serine915 regulates this response. Our work establishes a link among skotomorphogenic development, phosphorylation dynamics and MTs-based processes.