Pierdona, F. G.; Silva, A. J. M.; Vicente, M. H.; Taylor, L.; Pedmale, U. V.; Nogueira, F. T. S.

Auxin coordinates cell growth by promoting or inhibiting cell expansion during etiolated seedling development, but whether and how microRNA modules participate in this process remains unclear. Here, we show the miRNA156/SQUAMOSA PROMOTER-BINDING-PROTEIN-LIKE9 (miR156/SPL9) module is critical for skotomorphogenesis. Perturbation of the miR156/SPL9 module affected skotomorphogenesis, as the loss of miR156 function or SPL9 de-repression led to shorter hypocotyl, higher hook angle, and delayed hook opening. Opposing phenotypes were observed in dark-grown spl9 and miR156-overexpressing seedlings. Importantly, loss of miR156-dependent SPL9 regulation triggered apical hook formation even under reduced levels of endogenous auxin. miR156-targeted SPL9 arrested cell expansion by repressing small auxin-up RNA19 (SAUR19) gene in a FRUITFULL (FUL)-dependent and independent manner. The conserved miR156/SPL9/15 module also affects skotomorphogenesis in tomato, impacting its successful soil emergence. Our findings unravel how the miR156/SPL9 module plays a pivotal role in the auxin network coordinating apical hook development to enable appropriate seedling emergence.