Long noncoding RNA-mediated epigenetic regulation of auxin-related genes controlling shade avoidance syndrome inArabidopsis thaliana

The long noncoding RNA (lncRNA)AUXIN-REGULATED PROMOTER LOOP(APOLO) recognizes a subset of target loci across theArabidopsis thalianagenome by forming RNA-DNA hybrids (R-loop) and modulating local three-dimensional chromatin conformation. Here we show thatAPOLOis involved in regulating the shade avoidance syndrome (SAS) by dynamically modulating the expression of key factors. In response to far-red (FR) light, the expression ofAPOLOanticorrelates with its targetBRANCHED1(BRC1), a master regulator of shoot branching inArabidopsis thaliana.APOLOderegulation results inBRC1transcriptional repression and an increase in the number of branches.APOLOtranscriptional accumulation fine-tunes the formation of a repressive chromatin loop encompassing theBRC1promoter, which normally occurs only in leaves as well as in a late response to FR treatment in axillary buds. In addition, our data reveal thatAPOLOparticipates in leaf hyponasty, in agreement with its previously reported role in the control of auxin homeostasis through direct modulation ofYUCCA2(auxin synthesis),PIDandWAG2(auxin efflux). We found that direct application ofAPOLORNA to leaves results in a rapid increase in auxin accumulation that is associated with changes in the response of the plants to FR light. Collectively, our data support the view that lncRNAs coordinate the shade avoidance syndrome inArabidopsis thalianaand shed light on the potential of lncRNAs as bioactive exogenous molecules. Deploying exogenous RNAs that modulate plant-environment interactions are important new tools for sustainable agriculture.