EARLY FLOWERING 3 interactions with PHYTOCHROME B and PHOTOPERIOD1 are critical for the photoperiodic regulation of wheat heading time

Abstract

The 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 inPPD1upregulation 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.