Integration of photoperiod and cold temperature signals into flowering genetic pathways in Arabidopsis

Abstract

Appropriate timing of flowering is critical for propagation and reproductive success in plants. Therefore, flowering time is coordinately regulated by endogenous developmental programs and external signals, such as changes in photoperiod and temperature. Flowering is delayed by a transient shift to cold temperatures that frequently occurs during early spring in the temperate zones. It is known that the delayed flowering by short-term cold stress is mediated primarily by the floral repressor FLOWERING LOCUS C (FLC). However, how the FLC-mediated cold signals are integrated into flowering genetic pathways is not fully understood. We have recently reported that the INDUCER OF CBF EXPRESSION 1 (ICE1), which is a master regulator of cold responses, FLC, and the floral integrator SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 (SOC1) constitute an elaborated feedforward-feedback loop that integrates photoperiod and cold temperature signals to regulate seasonal flowering in Arabidopsis. Cold temperatures promote the binding of ICE1 to FLC promoter to induce its expression, resulting in delayed flowering. However, under floral inductive conditions, SOC1 induces flowering by blocking the ICE1 activity. We propose that the ICE1-FLC-SOC1 signaling network fine-tunes the timing of photoperiodic flowering during changing seasons.

Plants pass through a series of developmental transitions during their life cycle, among which the vegetative-to-reproductive transition or flowering induction is most important for their reproductive success. The onset of flowering is coordinately regulated by endogenous developmental programs, such as gibberellic acid and plant aging, and a variety of environmental factors, such as photoperiod and temperature.^1-3 Flowering time is also affected profoundly by environmental stresses, including temperature extremes and nutrient deficiency.^4-6 The flowering signals are integrated into flowering genetic pathways via the floral integrators FLOWERING LOCUS T (FT) and SOC1.⁷

Arabidopsis flowering is promoted through the photoperiod flowering pathway, in which CONSTANS and GIGANTEA activate the expression of FT gene, thereby inducing flowering initiation under long day conditions. Photoperiodic flowering is also influenced by temperature. The effects of temperature on flowering time are categorized into 3 clades, such as those of ambient temperatures and long-term and short-term cold conditions.^8-11 Ambient temperatures regulate flowering time through the thermosensory flowering pathways.⁸ Low but non-freezing temperatures differentially affect flowering time, depending on the duration of cold exposure.⁹ Prolonged exposure to cold temperatures or vernalization accelerates flowering by silencing FLC.^10,11 In contrast, short-term cold conditions, which are frequently encountered during changing seasons, delays flowering by inducing FLC.

In the temperate zones, plants acquire tolerance to freezing shock after exposure to non-freezing, cold temperatures. The master cold signaling mediator ICE1 transcription factor activates a set of cold-responsive C-REPEAT BINDING FACTOR (CBF) and COLD REGULATED (COR) genes to induce freezing tolerance. The ICE1-CBF-COR regulon has been extensively studied in terms of its regulatory schemes and underlying molecular events.¹²

Cold responses are intimately associated with flowering time control. For example, FVE, which encodes a homolog of the mammalian retinoblastoma-associated protein, is involved in the regulation of flowering time by short-term cold. It has been found that FVE-defective mutants, which exhibit delayed flowering, display enhanced freezing tolerance and CBF and COR genes are up-regulated in the mutants.¹³ Recent studies provide a better understanding of the interplay between flowering timing and cold responses. The floral integrator SOC1 negatively regulates CBF gene expression.⁵ In addition, HIGH EXPRESSION OF OSMOTICALLY RESPONSIVE GENES1 (HOS1), a E3 ubiquitin ligase that attenuates cold signaling by degrading ICE1,₁₄ represses flowering by inducing FLC transcription under short-term cold conditions.¹⁵

We have recently reported that the ICE1 transcription factor integrates cold temperature signals into FLC-mediated flowering pathways to determine the optimal timing of flowering during changing seasons. Exposure to cold temperatures triggers the binding of ICE1 to FLC gene promoter to induce its expression, causing delayed flowering. In contrast, under floral promotive long day conditions, SOC1 interacts with ICE1 to inhibit its activity in inducing FLC and CBF3 genes, accelerating flowering but reducing the capacity of cold acclimation. These observations indicate that the ICE1-FLC-SOC1 signaling module constitutes a feedforward-feedback loop that balances between flowering induction and cold responses.

It is notable that the integration of photoperiod and cold temperature signals by the ICE1/SOC1-mediated feedforward-feedback control contributes to optimization of plant developments, while minimizing the damages caused by cold stress, depending on the external conditions during changing seasons (Fig. 1). Under cold temperature conditions, rapid activation of CBF genes by ICE1 enhances freezing tolerance. The CBF transcription factors also activate FLC gene expression, suppressing SOC1 gene expression and thus causing delayed flowering. On the other hand, the SOC1-mediated feedback inhibition of ICE1 activity minimizes freezing tolerance response under floral inductive conditions. Our findings provide a seminal example of signaling networks that harmonizes external signals to optimize plant development under fluctuating environmental conditions.

Figure 1.

An intricate feedforward-feedback signaling network integrates photoperiod and cold signals to modulate the timing of flowering under cold temperature conditions. During changing seasons, such as early spring and late fall, the ICE1-FLC-SOC1 signaling module integrates photoperiod and cold signals to regulate seasonal flowering.

The previous and our own data demonstrate that ICE1, which is otherwise a cold signaling mediator, plays developmental roles, such as stomatal development, endosperm breakdown, and photoperiodic flowering.^16,17 It is also known that ICE1 is involved in various osmotic stress responses.¹⁸ Given the diverse roles in perceiving environmental signals during plant development, it is likely that ICE1 acts as a molecular knob that integrates environmental cues into plant development.

Accumulating evidence support that the floral repressor FLC gene is regulated by cold signaling mediators belonging to cold acclimation pathways. The E3 ubiquitin ligase HOS1 activates FLC transcription via chromatin remodeling, providing an additional layer of gene expression regulation.¹⁵ In addition, the SUMO E3 ligase SIZ1, which facilitates SUMO-mediated modification of ICE1 during cold acclimation, induces FLC transcription by inhibiting FLOWERING LOCUS D activity.¹⁹ It will be interesting to examine whether ICE1 functionally interacts with the regulators of flowering induction other than FLC and SOC1.

Funding

This work was supported by the Leaping Research (NRF-20151A2A1A05001636) and Global Research Lab (NRF-2012K1A1A2055546) Programs provided by the National Research Foundation of Korea and the Next-Generation BioGreen 21 Program (PJO111532015) provided by the Rural Development Administration of Korea.

Disclosure of Potential Conflicts of Interest

No potential conflicts of interest were disclosed.