PHYTOCHROME C regulation ofPHOTOPERIOD1is mediated byEARLY FLOWERING 3inBrachypodium distachyon

Abstract

ABSTRACTDaylength sensing in many plants is critical for coinciding the timing of flowering with the appropriate season. Temperate-climate-adapted grasses such asBrachypodium distachyonflower during the spring when days are becoming longer. The photoreceptor PHYTOCHROME C is essential for long-day (LD) flowering inB. distachyon. PHYCis required for the LD activation of a suite of genes in the photoperiod pathway includingPHOTOPERIOD1(PPD1) that, in turn, result in the activation ofFLOWERING LOCUS T(FT1)/FLORIGEN, which causes flowering. Thus,phyCmutants are extremely delayed in flowering. Here we show that PHYC-mediated activation of PPD1 occurs viaEARLY FLOWERING 3(ELF3), a component of the evening complex in the circadian clock. The extreme delay of flowering of thephyCmutant disappears when combined with anelf3loss-of-function mutation. Moreover, the dampenedPPD1expression inphyCmutant plants is elevated inphyC/elf3mutant plants consistent with the rapid flowering of the double mutant. We show that loss ofPPD1function also results in reducedFT1expression levels and extremely delayed flowering consistent with reports from wheat and barley. Additionally,elf3mutant plants have elevated expression levels ofPPD1and we show that overexpression ofELF3results in delayed flowering, which is associated with a reduction ofPPD1andFT1, demonstrating ELF3 repressesPPD1transcription, consistent with previous studies showing that ELF3 binds to thePPD1promoter. Indeed,PPD1is the main target of ELF3-mediated flowering aself3/ppd1double mutant plants are delayed flowering. Our results indicate thatELF3operates downstream fromPHYCand acts as a repressor ofPPD1in the photoperiod flowering pathway ofB. distachyon.AUTHOR SUMMARYDaylength is an important environmental cue that plants and animals use to coincide important life history events with a proper season. In plants, timing of flowering to a particular season is an essential adaptation to many ecological niches. Perceiving changes in daylength starts with the perception of light via specific photoreceptors such as phytochromes. In temperate grasses, how daylength perception is integrated into downstream pathways to trigger flowering is not fully understood. However, some of the components involved in the translation of daylength perception into the induction of flowering in temperate grasses have been identified from studies of natural variation. For example, specific alleles of two genes calledEARLY FLOWERING 3(ELF3) andPHOTOPERIOD1(PPD1) have been selected during breeding of different wheat and barley varieties to modulate the photoperiodic response to maximize reproduction in different environments. Here, we show in the temperate grass modelBrachypodium distachyonthat the translation of the light signal perceived by phytochromes into a flowering response is mediated byELF3, and thatPPD1is genetically downstream ofELF3in the photoperiodic flowering pathway. These results provide a genetic framework for understanding the photoperiodic response in temperate grasses that include agronomically important crops such as wheat, oats, barley, and rye.