In the absence of light signals, Arabidopsis plants fail to develop the rosette habit typical for this species. Instead, plants display caulescent growth due to elongation of rosette internodes. This aspect of photomorphogenic development has been paid little attention and molecular events involved, downstream of photoreceptor signaling, remain to be identified.Using a combination of genetic and molecular approaches, we show that Arabidopsis rosette habit is a photomorphogenic trait controlled by induction of ARABIDOPSIS THALI-ANA HOMEOBOX GENE1 (ATH1) as downstream target of multiple photoreceptors.ATH1 induction prevents rosette internode elongation by maintaining the shoot apical meristem (SAM) rib zone area inactive and requires inactivation of photomorphogenesis inhibitors, including PHYTOCHROME INTERACTING FACTOR (PIF) proteins. ATH1 activity results in tissue-specific inhibition of PIF expression, establishing double-negative feedbackregulation at the SAM. Light-requirement for ATH1 expression can be overcome by high sugar availability to the SAM. Both sugar and light signals that induce ATH1 and, subsequently, rosette habit are mediated by TOR kinase.Collectively, our data reveal a SAM-specific, double-negative ATH1-PIF feedback loop at the basis of rosette habit. Upstream, TOR kinase functions as central hub integrating light and energy signals that control this for Arabidopsis quintessential trait.

Here, we demonstrate that Arabidopsis rosette habit is a bona fide photomorphogenic trait controlled by the homeodomain protein ATH1. In light, ATH1 expression at the SAM is induced by broad wavelengths, mediated through multiple photoreceptors, and requires inactivation of COP1 and PIF photomorphogenesis inhibitors. Such induced ATH1 prevents elongation of rosette internodes by maintaining the rib zone area of the SAM in an inactive state. In the absence of light, Arabidopsis plants cannot complete seedling establishment after germination due to inactivity of the shoot apical meristem (SAM). Light requirement for SAM activation can be overcome by availability to the meristem of metabolizable sugars, such as sucrose. However, under these conditions plants fail to establish a typical compact rosette and display a caulescent growth habit. We show that this is due to insufficient expression of ATH1 at the SAM. ATH1 induction restores rosette habit in dark-grown plants through inhibition of PIF gene expression. Together, this suggests that a SAM-specific, double-negative ATH1-PIF feedback loop is at the basis of Arabidopsis rosette habit. Induction of ATH1 expression and restoration of rosette habit in darkness also occurs at increased levels of sucrose. Both sugar and light signals that induce ATH1 are mediated by TOR kinase. Overall, these results support a fundamental role for ATH1 in Arabidopsis rosette habit and further strengthen a role for TOR kinase as a central hub for integration of energy and light signals controlling organogenesis at the SAM.