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Living by the calendar: how plants know when to flower

Nature Reviews Molecular Cell Biology volume 4, pages 265–276 (2003)Cite this article

Key Points

  • The ability of organisms to anticipate daily and seasonal changes in their environment is crucial for survival and reproductive success. During the early and mid 1920s, it was shown that plants and animals time developmental and behavioural processes throughout the year by responding to daylength, or photoperiod, which is an environmental cue that is associated with seasonal progression. In 1936, Erwin Bünning proposed that daylength was measured through the coincidence of light with a rhythm of sensitivity to this environmental signal that was driven by an endogenous circadian clock.

  • Arabidopsis thaliana, the model organism for plant biologists, flowers earlier under long-day conditions than short-day conditions. The molecular-genetic dissection of flowering time, circadian rhythms and light signalling in Arabidopsis has provided strong support for Bünning's hypothesis and, more importantly, is helping us to understand the molecular basis of daylength measurement in this species.

  • The acceleration of flowering time by long days in Arabidopsis results in part from the direct effects of light, perceived by cryptochrome 2 and phytochrome A, on the expression of FLOWERING LOCUS T (FT), a gene that triggers the transition from vegetative to reproductive development when expressed above a certain threshold level. This direct effect of light on FT expression requires CONSTANS (CO) — a transcriptional regulator the expression of which is regulated by the clock such that the overlap between high levels of CO mRNA and the illuminated part of the day is minimal on short days and maximal on long days. So, FT mRNA levels accumulate to levels that are sufficient to promote flowering only under the latter condition.

  • Other plants, such as rice, flower earlier on short days than long days. Several genes that affect the photoperiodic regulation of flowering time in rice have been identified recently. Remarkably, all of them encode genes that are known to mediate the photoperiodic regulation of flowering time in Arabidopsis, which indicates that these two species measure daylength by similar mechanisms. The contrasting effect of photoperiod on flowering time in Arabidopsis and rice is due to the fact that FT expression in Arabidopsis is activated when there is a coincidence of light with high levels of CO, whereas in rice the expression of FT-like genes is activated by a CO-like gene in the dark and is repressed by light perceived through phytochromes.

  • Finally, many cereals grown in temperate regions of the world, as well as several Arabidopsis ecotypes, flower more rapidly in response to long days when these are preceded by a prolonged exposure to cold — a phenomenon known as vernalization. This ensures that flowering takes place during the optimal environmental conditions of the spring. Recent studies indicate that the interaction between photoperiodic and temperature signalling pathways in the regulation of flowering time is mediated by the antagonistic effects of CO and FLC (a MADS-box transcription factor) on the expression of floral-inductive genes.

Abstract

Reproductive processes in plants and animals are usually synchronized with favourable seasons of the year. It has been known for 80 years that organisms anticipate seasonal changes by adjusting developmental programmes in response to daylength. Recent studies indicate that plants perceive daylength through the degree of coincidence of light with the expression of CONSTANS, which encodes a clock-regulated transcription factor that controls the expression of floral-inductive genes in a light-dependent manner.

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Figure 1: Physiological models of photoperiodic time measurement.
Figure 2: Molecular interactions that shape the plant circadian oscillator.
Figure 3: Photoperiodic regulation of CO and FT expression.
Figure 4: The regulation of flowering time by photoperiod in Arabidopsis and rice.
Figure 5: The Arabidopsis calendar.

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Acknowledgements

Our thanks to C. Dean, J.J. Casal, F. Harmon, P. Mas and S. Harmer for their critical reading of this review. We apologize to those colleagues whose work is not discussed here because of space limitations.

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Authors and Affiliations

  1. Department of Cell Biology, The Scripps Research Institute, 10550 North Torrey Pines Road, La Jolla, 92037, California, USA

    Marcelo J. Yanovsky & Steve A. Kay

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  1. Marcelo J. Yanovsky
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  2. Steve A. Kay
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Correspondence to Steve A. Kay.

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DATABASES

Entrez

Hd3a

Hd1

Interpro

F-box

kelch

PAS

Swiss-Prot

cry2

phyA

The Arabidopsis Information Resource

CCA1

CO

ELF4

FT

LHY

TOC1

FURTHER INFORMATION

Steve A. Kay's laboratory

The Flowering Web

Tutorials on Biological Clocks

Glossary

DAYLENGTH

(photoperiod). The duration of the illuminated phase of a daily light/dark cycle.

PHOTOPERIODIC RESPONSE

The biological response to changes in daylength, or photoperiod, that are associated with seasonal adaptations.

CIRCADIAN RHYTHM

A rhythm with an approximate 24-h period.

ENTRAINMENT

The synchronization or adjustment of a rhythm to another cycle of similar periodicity. In the case of circadian rhythms, it refers to their synchronization to the 24-h solar cycle in response to changes in environmental cues such as light and temperature that normally occur at dawn and dusk.

TEMPERATURE COMPENSATION

The ability of circadian clocks to maintain a relatively constant pace over a wide temperature range.

PHOTOMORPHOGENIC RESPONSE

The morphological and physiological adaptation of plants to changes in the quality and quantity of their light environment.

PSEUDO-RESPONSE REGULATOR

A protein that shares strong sequence similarity to response regulators of bacterial two-component signalling systems, but that lacks the conserved residues that are phosphorylated by a sensor kinase, which modulates its activity.

CHROMOPROTEIN

A protein that is linked to a chromophore, which allows the holoprotein (protein plus chromophore) to work as a photoreceptor.

SHORT-/LONG-DAY CONDITIONS

In Arabidopsis, short-day conditions usually consist of 8–10-h photoperiods, and long-day conditions of 14–16-h photoperiods. The length of the day that, when exceeded, promotes or inhibits flowering varies for each species.

CHROMOPHORE

A molecule that selectively absorbs certain wavelengths.

PAS/LOV

PAS is a signalling domain that was identified initially in period circadian protein, Ah receptor nuclear translocator protein and single-minded protein. It mediates protein–protein interactions and/or binds small ligands. LOV domains are a subset of PAS domains that are found in signalling proteins that are activated by light, oxygen or voltage.

MERISTEM-IDENTITY GENE

A gene, such as LEAFY and APETALA1, that triggers the initiation of flowers, instead of leaves, from the shoot apical meristem.

MERISTEM

A small group of undifferentiated cells from which plant organs are formed.

QUANTITATIVE TRAIT LOCUS

(QTL). A genetic locus that is identified through the statistical analysis of complex traits (such as plant height or body weight). These traits are typically influenced by more than one gene and also by the environment.

MADS BOX

A conserved DNA-binding domain that is found in a family of transcriptional regulators that are present in animals, fungi and plants.

EPIGENETIC

A heritable change in gene expression that is controlled by modifications in DNA methylation and/or chromatin structure.

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Yanovsky, M., Kay, S. Living by the calendar: how plants know when to flower. Nat Rev Mol Cell Biol 4, 265–276 (2003). https://doi.org/10.1038/nrm1077

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