EARLY FLOWERING 3interactions withPHYTOCHROME BandPHOTOPERIOD1are critical for the photoperiodic regulation of wheat heading time

AbstractThe photoperiodic response is critical for plants to adjust their reproductive phase to the most favorable season. Wheat heads earlier under long days (LD) than under short days (SD) and this difference is mainly regulated by thePHOTOPERIOD1(PPD1) gene. Tetraploid wheat plants carrying thePpd-A1aallele with a large deletion in the promoter head earlier under SD than plants carrying the wildtypePpd-A1ballele with an intact promoter. PhytochromesPHYBandPHYCare necessary for the light activation ofPPD1, and mutations in either of these genes result in the downregulation ofPPD1and very late heading time. We show here that both effects are reverted when thephyBmutant is combined with loss-of-function mutations inEARLY FLOWERING 3(ELF3), a component of the Evening Complex (EC) in the circadian clock. We also show that the wheat ELF3 protein interacts with PHYB and PHYC, is rapidly modified by light, and binds to thePPD1promoterin planta(likely as part of the EC). Deletion of the ELF3 binding region in thePpd-A1apromoter results in its upregulation at dawn, similar toPPD1alleles with intact promoters in theelf3mutant background. The upregulation ofPPD1is correlated with the upregulation of the florigen geneFLOWERING LOCUS T1(FT1) and early heading time. Loss-of-function mutations inppd1result in the downregulation ofFT1and delayed heading, even when combined with theelf3mutation. Taken together, these results indicate that ELF3 operates downstream ofPHYBas a direct transcriptional repressor ofPPD1, and that this repression is relaxed both by light and by the deletion of the ELF3 binding region in thePpd-A1apromoter. In summary, the regulation of the light mediated activation ofPPD1by ELF3 is critical for the photoperiodic regulation of wheat heading time.Author SummaryThe coordination of reproductive development with the optimal season for seed production is critical to maximize grain yield in crop species. Plants can perceive the length of the day or night (photoperiod) and use this information to anticipate seasonal changes. In most eudicot plants,CONSTANSplays a central role in the perception of photoperiod, but in wheat the main photoperiod gene isPHOROPERIOD1(PPD1). In this study, we show that the clock geneEARLY FLOWERING 3(ELF3) regulates the phytochrome-mediated light activation ofPPD1. Loss-of-function mutations inELF3result in the upregulation ofPPD1at and dawn, and in early heading under both long and short days, even in the absence ofPHYB. A deletion in thePPD1promoter including an ELF3 binding region also results in earlier heading under short days, indicating that ELF3 acts as a direct transcriptional repressor ofPPD1. This study shows thatELF3plays a critical role in the wheat photoperiod pathway by regulating the light signal between the phytochromes andPPD1. ELF3 provides an additional entry point to engineer heading time in wheat, an important trait for the development of better adapted varieties to a changing environment.