Long noncoding RNA‐mediated epigenetic regulation of auxin‐related genes controls shade avoidance syndrome in Arabidopsis

The long noncoding RNA (lncRNA) AUXIN‐REGULATED PROMOTER LOOP (APOLO) recognizes a subset of target loci across the Arabidopsis thaliana genome by forming RNA–DNA hybrids (R‐loops) and modulating local three‐dimensional chromatin conformation. Here, we show that APOLO regulates shade avoidance syndrome by dynamically modulating expression of key factors. In response to far‐red (FR) light, expression of APOLO anti‐correlates with that of its target BRANCHED1 (BRC1), a master regulator of shoot branching in Arabidopsis thaliana. APOLO deregulation results in BRC1 transcriptional repression and an increase in the number of branches. Accumulation of APOLO transcription fine‐tunes the formation of a repressive chromatin loop encompassing the BRC1 promoter, which normally occurs only in leaves and in a late response to far‐red light treatment in axillary buds. In addition, our data reveal that APOLO participates in leaf hyponasty, in agreement with its previously reported role in the control of auxin homeostasis through direct modulation of auxin synthesis gene YUCCA2, and auxin efflux genes PID and WAG2. We show that direct application of APOLO RNA to leaves results in a rapid increase in auxin signaling that is associated with changes in the plant response to far‐red light. Collectively, our data support the view that lncRNAs coordinate shade avoidance syndrome in A. thaliana, and reveal their potential as exogenous bioactive molecules. Deploying exogenous RNAs that modulate plant–environment interactions may therefore become a new tool for sustainable agriculture. Synopsis The Arabidopsis lncRNA APOLO influences chromatin architecture to regulate transcription of specific genes, including auxin‐responsive genes which are involved in the plant's response to shade avoidance. Here, APOLO is shown to respond to changes in light by influencing transcription and plant behavior. APOLO modulates the expression of BRANCHED1 (BRC1), a master regulator of shoot branching in Arabidopsis, through chromatin looping around the BRC1 promoter. APOLO‐mediated chromatin looping is influenced by changes in light exposure and regulates branching behavior. Low‐red/far‐red light ratio‐mediated leaf hyponasty depends on APOLO regulation of auxin‐related genes. In vitro‐transcribed APOLO directly sprayed onto plants is sufficient to alter plant auxin homeostasis in response to light conditions. APOLO lncRNA influences plant behavior in response to light conditions through chromatin c