Cell wall integrity modulates a PHYTOCHROME-INTERACTING FACTOR (PIF) - HOOKLESS1 (HLS1) signalling module controlling apical hook formation in Arabidopsis.

Etiolated seedlings of dicots form an apical hook to protect the meristems during soil emergence. Hook formation is the result of differential growth on both sides of the hypocotyl apex and is tightly controlled by environmental cues and hormones, among which auxin and gibberellins (GAs) are the main contributors. Cell expansion is tightly regulated by the cell wall, but whether and how feedback from this structure contributes to hook development is still unclear. Here we show that etiolated seedlings of the Arabidopsis thaliana quasimodo2-1 (qua2) mutant, defective in pectin biosynthesis, display severe defects in apical hook formation and maintenance, accompanied by loss of asymmetric auxin maxima and differential cell expansion. Moreover, qua2 seedlings show reduced expression of HOOKLESS1 (HLS1) and PHYTOCHROME-INTERACTING FACTOR 4 and 5 (PIF4/5), positive regulators of hook formation, and accumulate reduced levels of the active gibberellin GA4. Treatment of wild-type seedlings with the cellulose inhibitor isoxaben (isx) also prevents hook development and represses HLS1 expression and PIF4 accumulation. Moreover, isx stabilizes the DELLA protein REPRESSOR OF ga1-3 (RGA), which inhibits HLS1 expression and hook formation. Exogenous GAs or HLS1 overexpression partially restore hook development in isx-treated seedlings. Notably, agar concentration in the medium restores, both in qua2 and isx-treated seedlings, hook development and WT-like levels of PIFs and HLS1. We propose that turgor-dependent signals link changes in cell wall integrity to the PIF4/5-HLS1 signalling module to repress differential cell elongation during hook formation. Significance statementCell wall integrity modulates apical hook development through poorly understood mechanisms. We show here that, in Arabidopsis, repression of hook formation by either mutations in pectin biosynthesis or by isoxaben treatment is at least partially mediated by the downregulation of a gibberellin-controlled signalling module that comprises PIF4/5 and HLS1. Our results indicate that the signals derived from changes in the cell wall can modulate hormone-mediated pathways to control asymmetric growth during plant development.