Arabidopsis noncoding RNA mediates control of photomorphogenesis by red light

Seedling photomorphogenesis is a sophisticated developmental process that is controlled by both the transcriptional and post-transcriptional regulation of gene expression. Here, we identify an Arabidopsis noncoding RNA, designated HIDDEN TREASURE 1 (HID1), as a factor promoting photomorphogenesis in continuous red light (cR). We show that HID1 acts through PHYTOCHROME-INTERACTING FACTOR 3 (PIF3), which encodes a basic helix-loop-helix transcription factor known to be a key repressor of photomorphogenesis. Knockdown of HID1 in hid1 mutants leads to a significant increase in the expression of PIF3, which in turn drives the development of elongated hypocotyls in cR. We identified two major stem-loops in HID1 that are essential for its modulation of hypocotyl growth in cR-grown seedlings. Furthermore, our data reveal that HID1 is assembled into large nuclear protein-RNA complex(es) and that it associates with the chromatin of the first intron of PIF3 to repress its transcription. Strikingly, phylogenetic analysis reveals that many land plants have conserved homologs of HID1 and that its rice homolog can rescue the mutant phenotype when expressed in Arabidopsis hid1 mutants. We thus concluded that HID1 is a previously uncharacterized noncoding RNA whose function represents another layer of regulation in the precise control of seedling photomorphogenesis.