Transcription factor-mediated activities of enhancer lincRNAs in flower development

Genome-wide efforts revealed have identified a large number of long non-coding RNAs (lncRNAs), though their potential functions remain largely enigmatic. The floral meristem identity factor APETALA1 (AP1) controls the initiation of flower morphogenesis. Here, we used the AP1-based system for synchronized floral induction in Arabidopsis to identify 4106 flower-related long intergenic RNAs (lincRNAs) with distinct features compared to protein coding genes. Flower-related lincRNAs are typically associated with functional enhancers which are bi-directionally transcribed and are associated with diverse functional gene modules related to floral organ development based on co-expression network analysis. The master regulatory transcription factors (TFs) AP1 and SEPALLATA3 (SEP3) bind to lincRNA-associated enhancers. Binding of these TFs is correlated with increase in lincRNA transcription and chromatin accessibility at enhancers, presumably followed by activation of target genes. For example, the lincRNA Aralnc.19175 (designated previously as LINC-AP2) spanning two enhancers bound by AP1 and SEP3 shows increasing activity during flower development. The enhanced expression of the lincRNA is coupled to increasing accessibility of the two corresponding enhancers, thereby potentially contributing to activation of the neighboring AP2 gene. We hypothesize that enhancer-associated lincRNA expression is functionally linked with TF activity in floral gene regulation.