Arabidopsis thaliana EARLY FLOWERING 3 (ELF3) as a zeitnehmer (time taker) is responsible for generation of circadian rhythm and regulation of photoperiodic flowering. There are two orthologs (OsELF3-1 and OsELF3-2) of ELF3 in rice (Oryza sativa), but their roles have not yet been fully identified. Here, we performed a functional characterization of OsELF3-1 and revealed it plays a more predominant role than OsELF3-2 in rice heading. Our results suggest OsELF3-1 can affect rice circadian systems via positive regulation of OsLHY expression and negative regulation of OsPRR1, OsPRR37, OsPRR73 and OsPRR95 expression. In addition, OsELF3-1 is involved in blue light signaling by activating EARLY HEADING DATE 1 (Ehd1) expression to promote rice flowering under short-day (SD) conditions. Moreover, OsELF3-1 suppresses a flowering repressor GRAIN NUMBER, PLANT HEIGHT AND HEADING DATE 7 (Ghd7) to indirectly accelerate flowering under long-day (LD) conditions. Taken together, our results indicate OsELF3-1 is essential for circadian regulation and photoperiodic flowering in rice.

Photoperiodic flowering is one of the most important pathways to govern flowering in rice (Oryza sativa), in which Heading date 1 (Hd1), an ortholog of the Arabidopsis CONSTANS gene, encodes a pivotal regulator. Hd1 promotes flowering under short-day conditions (SD) but represses flowering under long-day conditions (LD) by regulating the expression of Heading date 3a (Hd3a), the FLOWERING LOCUS T (FT) ortholog in rice. However, the molecular mechanism of how Hd1 changes its regulatory activity in response to day length remains largely unknown. In this study, we demonstrated that the repression of flowering in LD by Hd1 is dependent on the transcription factor DAYS TO HEADING 8 (DTH8). Loss of DTH8 function results in the activation of Hd3a by Hd1, leading to early flowering. We found that Hd1 directly interacts with DTH8 and that the formation of the DTH8-Hd1 complex is necessary for the transcriptional repression of Hd3a by Hd1 in LD, implicating that the switch of Hd1 function is mediated by DTH8 in LD rather than in SD. Furthermore, we revealed that DTH8 associates with the Hd3a promoter to modulate the level of H3K27 trimethylation (H3K27me3) at the Hd3a locus. In the presence of the DTH8-Hd1 complex, the H3K27me3 level was increased at Hd3a, whereas loss of DTH8 function resulted in decreased H3K27me3 level at Hd3a. Taken together, our findings indicate that, in response to day length, DTH8 plays a critical role in mediating the transcriptional regulation of Hd3a by Hd1 through the DTH8-Hd1 module to shape epigenetic modifications in photoperiodic flowering.