Genetic and Epigenetic Understanding of the Seasonal Timing of Flowering

Abstract

The developmental transition to flowering in many plants is timed by changing seasons, which enables plants to flower at a season that is favorable for seed production. Many plants grown at high latitudes perceive the seasonal cues of changing day length and/or winter cold (prolonged cold exposure), to regulate the expression of flowering-regulatory genes through the photoperiod pathway and/or vernalization pathway, and thus align flowering with a particular season. Recent studies in the model flowering plant Arabidopsis thaliana have revealed that diverse transcription factors engage various chromatin modifiers to regulate several key flowering-regulatory genes including FLOWERING LOCUS C (FLC) and FLOWERING LOCUS T (FT) in response to seasonal signals. Here, we summarize the current understanding of molecular and chromatin-regulatory or epigenetic mechanisms underlying the vernalization response and photoperiodic control of flowering in Arabidopsis. Moreover, the conservation and divergence of regulatory mechanisms for seasonal flowering in crops and other plants are briefly discussed.

Keywords: FLOWERING LOCUS C; FLOWERING LOCUS T; chromatin modification; flowering time; photoperiodism; vernalization.

Figure 1

Seasonal Timing of Flowering in Arabidopsis thaliana. (A) A winter annual Arabidopsis line without prolonged cold exposure. FRIGIDA activates the expression of the floral repressor FLC (for FLOWERING LOCUS C), which directly represses the expression of the florigenic FT (for FLOWERING LOCUS T) gene to inhibit flowering. (B) After experiencing winter cold, Arabidopsis winter annuals in temperate regions flower in late spring in response to increasing day length. Winter cold, through the vernalization pathway, represses FLC expression and thus relieves FT repression. This enables long-day induction of FT expression by the photoperiod pathway to promote flowering. FT feedback represses FLC expression.

Figure 2

Dynamic Epigenetic Regulation of FLC Expression throughout the Arabidopsis Life Cycle. In early embryogenesis, FLC is re-activated or reset by the embryonic LEC pathway consisting of three transcription factors (TFs): the pioneer TF LEC1 (for LEAFY COTYLEDON 1) and two B3 domain TFs including LEC2 and FUSCA 3 (FUS3). These TFs function together with the FRI supercomplex (FRIsc) containing active chromatin modifiers (e.g., the EFS H3K36 methyltransferase) to establish an active chromatin state at FLC, which is transmitted to young seedlings following seed germination (often in autumn under field conditions). The LEC pathway is developmentally silenced during post-seed development. When seedlings encounter winter cold, the B3 domain proteins VIVIPAROUS1/ABI3-LIKE 1 (VAL1)/VAL2 bind to the Cold Memory Element (CME) to mediate FLC repression by PcG proteins (e.g., LHP1 and PRC2). This results in a silenced state that is subsequently maintained upon return to warmth in the following spring, enabling long-day induction of flowering in late spring in temperate regions.

Figure 3

Long-Day Induction of FT Expression by CO in Arabidopsis under Controlled Growth Conditions. (A) Transcriptional regulation of CO mRNA expression in LDs. The morning-expressed MYB TFs CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) and LATE ELONGATED HYPOCOTYL (LHY) activate the expression of CYCLING DOF FACTORs (CDFs), which directly repress CO expression in the morning. In the afternoon, upon perception of blue light FLAVIN-BINDING, KELCH REPEAT, F-BOX 1 (FKF1) forms a dimeric ubiquitin ligase complex with GIGANTEA (GI) to degrade CDFs; subsequently, the FLOWERING BHLH (FBH) family TFs bind to a CO promoter region to promote CO transcription. (B) Control of CO protein accumulation in the leaf vasculature in LDs. The E3 ubiquitin ligase HOS1 (for HIGH EXPRESSION OF OSMOTICALLY RESPONSIVE GENES 1) and the red-light photoreceptor Phytochrome B (PHYB) function to destabilize the CO protein in the morning. In the afternoon, CO is stabilized by the blue light photoreceptors FKF1 and Cryptochrome 2 (CRY2), and the far-red light photoreceptor Phytochrome A (PHYA). The blue light-dependent association of FKF1 with CO functions to stabilize the CO protein. In addition, the blue-light activated CRY2 physically associates with the E3 ubiquitin ligase complex CONSTITUTIVE PHOTOMORPHOGENIC 1 (COP1)-SPA1 (for SUPPRESSOR OF PHYA-105 1), to inhibit it from degrading CO. The coincidence of light exposure with a high level of CO mRNA in the afternoon results in CO protein accumulation toward dusk. At night, the COP1-SPA1complex targets CO for degradation by the proteasome. (C) Transcriptional regulation of FT expression in leaf veins in LDs. FT expression is largely constitutively repressed by PcG proteins together with repressive TFs (e.g., the FLC family), over a 24-h LD cycle except around dusk. Upon CO protein accumulation toward dusk, the DNA-binding CO associates with a dimer of NF-YB2/3 and NF-YC3/4/9 to form a trimeric NF-CO complex. NF-CO and the trimeric NF-Y complex (NF-YA with an NF-YB and NF-YC dimer) bind to proximal and distal FT promoter regions, respectively, to disrupt PcG enrichment on FT chromatin. The chromatin-remodeler PICKLE (PKL) physically associates with CO to facilitate its binding to the FT promoter, and PKL-CO recruits the H3K4 methyltransferase ATX1 (for ARABIDOPSIS HOMOLOG OF TRITHORAX 1) and H3K4me3/H3K36me3 readers including MORF RELATED GENE 1 (MRG1) and MRG2 to promote deposition of the active H3K4me3 mark on FT chromatin specifically at dusk. In addition, CO directly interacts with CIB1 (for CRY2-INTERACTING bHLH 1, a bHLH TF), which physically associates with CRY2 under blue light, and the CO-CIB1-CRY2 complex promotes FT expression at dusk, likely by facilitating active chromatin modifications on FT chromatin. CO-mediated disruption of Polycomb silencing at FT, together with the active chromatin modifications made by CO partners, results in FT de-repression/activation specifically at dusk in LDs. Upon FT de-repression at dusk, the histone deacetylase complex AFR-HDAC dampens the level of FT expression to prevent precocious flowering.