PHYTOCHROME C regulation of photoperiodic flowering via PHOTOPERIOD1 is mediated by EARLY FLOWERING 3 in Brachypodium distachyon

Authors: WOODS, DANIEL - University Of California, Davis; LI, WEIYA - University Of Wisconsin; SIBOUT, RICHARD - Inrae; SHAO, MINGQIN - Department Of Energy Joint Genome; L Chingcuanco, Debbie; VOGEL, JOHN - Department Of Energy Joint Genome; DUBCOVSKY, JORGE - University Of California, Davis; AMASINO, RICHARD - University Of Wisconsin

Submitted to: PLoS Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/17/2023
Publication Date: 5/10/2023
Citation: Woods, D., Li, W., Sibout, R., Shao, M., Chingcuanco, D.L., Vogel, J., Dubcovsky, J., Amasino, R. 2023. PHYTOCHROME C regulation of photoperiodic flowering via PHOTOPERIOD1 is mediated by EARLY FLOWERING 3 in Brachypodium distachyon. PLoS Genetics. 19(5). Article e1010706. https://doi.org/10.1371/journal.pgen.1010706.
DOI: https://doi.org/10.1371/journal.pgen.1010706

Interpretive Summary: Daylength 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 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 called EARLY FLOWERING 3 (ELF3) and PHOTOPERIOD1 (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 model Brachypodium distachyon that the translation of the light signal perceived by phytochromes into a flowering response is mediated by ELF3, and that PPD1 is genetically downstream of ELF3 in 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.

Technical Abstract: Daylength sensing in many plants is critical for coinciding the timing of flowering with the appropriate season. Temperate-climate-adapted grasses such as Brachypodium distachyon flower during the spring when days are becoming longer. The photoreceptor PHYTOCHROME C is essential for long-day (LD) flowering in B. distachyon. PHYC is required for the LD activation of a suite of genes in the photoperiod pathway including PHOTOPERIOD1 (PPD1) that, in turn, result in the activation of FLOWERING LOCUS T (FT1)/FLORIGEN, which causes flowering. Thus, phyC mutants are extremely delayed in flowering. Here we show that PHYC-mediated activation of PPD1 occurs via EARLY FLOWERING 3 (ELF3), a component of the evening complex in the circadian clock. The extreme delay of flowering of the phyC mutant disappears when combined with an elf3 loss-of-function mutation. Moreover, the dampened PPD1 expression in phyC mutant plants is elevated in phyC/elf3 mutant plants consistent with the rapid flowering of the double mutant. We show that loss of PPD1 function also results in reduced FT1 expression levels and extremely delayed flowering consistent with reports from wheat and barley. Additionally, elf3 mutant plants have elevated expression levels of PPD1 and we show that overexpression of ELF3 results in delayed flowering, which is associated with a reduction of PPD1 and FT1, demonstrating ELF3 represses PPD1 transcription, consistent with previous studies showing that ELF3 binds to the PPD1 promoter. Indeed, PPD1 is the main target of ELF3-mediated flowering as elf3/ppd1 double mutant plants are delayed flowering. Our results indicate that ELF3 operates downstream from PHYC and acts as a direct repressor of PPD1 in the photoperiod flowering pathway of B. distachyon.