Flowering time regulation: photoperiod- and temperature-sensing in leaves

doi:10.1016/j.tplants.2013.05.003

Trends in Plant Science

Volume 18, Issue 10, October 2013, Pages 575-583

https://doi.org/10.1016/j.tplants.2013.05.003 Get rights and content

Highlights

•
Photoperiod and developmental stages converge to regulate the expression of FT, a major component of florigen, in leaves.
•
The photoperiodic photoreceptor, FKF1, for time-dependent CO stabilization was revealed recently.
•
Lower temperature-dependent flowering regulation, has been characterized recently and temperature also regulates FT in leaves.
•
The phytohormone, GA, also participates in flowering time regulation in long days by regulating FT.
•
Multiple external and internal factors are integrated into FT transcriptional regulation in leaves.

Plants monitor changes in photoperiod and temperature to synchronize their flowering with seasonal changes to maximize fitness. In the Arabidopsis photoperiodic flowering pathway, the circadian clock-regulated components, such as FLAVIN-BINDING, KELCH REPEAT, F-BOX 1 and CONSTANS, both of which have light-controlled functions, are crucial to induce the day-length specific expression of the FLOWERING LOCUS T (FT) gene in leaves. Recent advances indicate that FT transcriptional regulation is central for integrating the information derived from other important internal and external factors, such as developmental age, amount of gibberellic acid, and the ambient temperature. In this review, we describe how these factors interactively regulate the expression of FT, the main component of florigen, in leaves.

Section snippets

Photoperiodic flowering mechanism in Arabidopsis

Seasonal changes in day length (photoperiod) are consistent from year to year. Therefore, many plants use photoperiod information to predict upcoming environmental changes and precisely align the timing of flowering with favorable conditions [1]. Another important environmental factor that influences flowering is surrounding temperature. Ambient temperature changes arising from global climate change have already altered the phenology of plants, including the timing of flowering [2]. Therefore,

Interaction between photoperiodic and gibberellic acid pathways

GA affects diverse biological processes, including flowering time. Recent studies have reported that interactions occur between photoperiodic and GA pathways to regulate FT expression under both LD and SD conditions 29, 64, 65, 66 (Figure 4). The bioactive GA₄ is synthesized through multiple oxidation steps catalyzed by GA 20-oxidase (GA20ox) and GA 3-oxidase (GA3ox) [64]. The amount of active GA₄ is tightly regulated through synthesis as well as through deactivation catalyzed by GA 2-oxidase

Effects of temperature changes on flowering regulation

In addition to day-length changes, leaves sense information about temperature fluctuation. Studies on the effects of temperature changes on flowering time have mostly focused on vernalization responses [72]. The key regulator of the vernalization response in Arabidopsis is the FLC gene, which encodes a transcription repressor of FT. Vernalization represses the expression of FLC by regulating the chromatin status of the FLC locus; therefore, FLC repression is removed in the spring. In contrast

Concluding remarks

Recently there have been large advances in our understanding of flowering time regulation, which have clarified how several exogenous and endogenous factors regulate flowering time at the molecular level, and how these signaling pathways are integrated to control the expression of a major floral regulator, FT, in leaves (Figure 1). Although not covered in this review, a complex picture has also emerged in recent years of the dynamic interactions among floral integrators, including FT, and

Acknowledgments

We thank Hannah Kinmonth-Shultz, Greg Golembeski, and Lesley Pettigrew for critical reading. This work was supported by funding from the Next-Generation BioGreen 21 Program (SSAC, PJ009495) to Y.H.S., JSPS KAKENHI Grant-in-Aid for Young Scientists (B) (25840104) to S.I., and the National Institutes of Health (GM079712) and the University of Washington Royalty Research Fund to T.I.

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^*: These authors contributed equally.

View full text

Trends in Plant Science

ReviewFlowering time regulation: photoperiod- and temperature-sensing in leaves

Highlights

Section snippets

Photoperiodic flowering mechanism in Arabidopsis

Interaction between photoperiodic and gibberellic acid pathways

Effects of temperature changes on flowering regulation

Concluding remarks

Acknowledgments

Photoperiodism in Plants

Rapid changes in flowering time in British plants

Science

The multifaceted roles of FLOWERING LOCUS T in plant development

Plant Cell Environ.

The end of innocence: flowering networks explode in complexity

Curr. Opin. Plant Biol.

The genetic basis of flowering responses to seasonal cues

Nat. Rev. Genet.

FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis

Science

Regulation of flowering time: all roads lead to Rome

Cell. Mol. Life Sci.

Arabidopsis circadian clock and photoperiodism: time to think about location

Curr. Opin. Plant Biol.

The genetic basis of flowering responses to seasonal cues

Nat. Rev. Genet.

FKF1 F-box protein mediates cyclic degradation of a repressor of CONSTANS in Arabidopsis

Science

FKF1 and GIGANTEA complex formation is required for day-length measurement in Arabidopsis

Science

Arabidopsis DOF transcription factors act redundantly to reduce CONSTANS expression and are essential for a photoperiodic flowering response

Dev. Cell

FKF1 is essential for photoperiodic-specific light signalling in Arabidopsis

Nature

Distinct roles of GIGANTEA in promoting flowering and regulating circadian rhythms in Arabidopsis

Plant Cell

ELF4 regulates GIGANTEA chromatin access through subnuclear sequestration

Cell Rep.

DAY NEUTRAL FLOWERING represses CONSTANS to prevent Arabidopsis flowering early in short days

Plant Cell

EDL3 is an F-box protein involved in the regulation of abscisic acid signalling in Arabidopsis thaliana

J. Exp. Bot.

FLOWERING BHLH transcriptional activators control expression of the photoperiodic flowering regulator CONSTANS in Arabidopsis

Proc. Natl. Acad. Sci. U.S.A.

Functional importance of conserved domains in the flowering-time gene CONSTANS demonstrated by analysis of mutant alleles and transgenic plants

Plant J.

The flowering time regulator CONSTANS is recruited to the FLOWERING LOCUS T promoter via a unique cis-element

New Phytol.

FKF1 conveys timing information for CONSTANS stabilization in photoperiodic flowering

Science

CONSTANS and the CCAAT box binding complex share a functionally important domain and interact to regulate flowering of Arabidopsis

Plant Cell

The CCAAT binding factor can mediate interactions between CONSTANS-like proteins and DNA

Plant J.

A putative CCAAT-binding transcription factor is a regulator of flowering timing in Arabidopsis

Plant Physiol.

AtHAP3b plays a crucial role in the regulation of flowering time in Arabidopsis during osmotic stress

J. Biochem. Mol. Biol.

The Nuclear Factor Y subunits NF-YB2 and NF-YB3 play additive roles in the promotion of flowering by inductive long-day photoperiods in Arabidopsis

Planta

NF-YC3, NF-YC4 and NF-YC9 are required for CONSTANS-mediated, photoperiod-dependent flowering in Arabidopsis thaliana

Plant J.

Isolation of CONSTANS as a TGA4/OBF4 interacting protein

Mol. Cells

CONSTANS and ASYMMETRIC LEAVES 1 complex is involved in the induction of FLOWERING LOCUS T in photoperiodic flowering in Arabidopsis

Plant J.

Photoreceptor regulation of CONSTANS protein in photoperiodic flowering

Science

Blue light-dependent interaction of CRY2 with SPA1 regulates COP1 activity and floral initiation in Arabidopsis

Curr. Biol.

Arabidopsis SPA proteins regulate photoperiodic flowering and interact with the floral inducer CONSTANS to regulate its stability

Development

Arabidopsis COP1 shapes the temporal pattern of CO accumulation conferring a photoperiodic flowering response

EMBO J.

COP1-mediated ubiquitination of CONSTANS is implicated in cryptochrome regulation of flowering in Arabidopsis

Plant Cell

Blue-light-dependent interaction of cryptochrome 1 with SPA1 defines a dynamic signaling mechanism

Genes Dev.

Arabidopsis cryptochrome 1 interacts with SPA1 to suppress COP1 activity in response to blue light

Genes Dev.

Review
Flowering time regulation: photoperiod- and temperature-sensing in leaves