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  • Review Article
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The genetic basis of flowering responses to seasonal cues

Key Points

  • Day length and temperature are the major seasonal cues that regulate flowering, and molecular pathways conferring these responses have been defined in Arabidopsis thaliana and several other species.

  • Day length is measured in the leaves, and in all species examined it causes expression of highly conserved genes similar to FT of A. thaliana.

  • In many species, a graft-transmissible signal that includes the FT protein is made in the leaves in response to day length and is transported to the shoot apical meristem, where it induces the floral transition.

  • Seasonal flowering is also controlled by extended exposure to low winter temperatures (vernalization) that confers competence to flower in response to day length the following summer and spring.

  • Genetic networks that confer vernalization appear to have evolved independently in different plant families and are therefore an example of convergent evolution.

  • In contrast to annual plants, perennial plants flower multiple times during their lifespan. Recently developed genetic models for perennial species have identified floral repressors that are regulated by environmental signals and differentially expressed compared with closely related annual species.

Abstract

Plants respond to the changing seasons to initiate developmental programmes precisely at particular times of year. Flowering is the best characterized of these seasonal responses, and in temperate climates it often occurs in spring. Genetic approaches in Arabidopsis thaliana have shown how the underlying responses to changes in day length (photoperiod) or winter temperature (vernalization) are conferred and how these converge to create a robust seasonal response. Recent advances in plant genome analysis have demonstrated the diversity in these regulatory systems in many plant species, including several crops and perennials, such as poplar trees. Here, we report progress in defining the diverse genetic mechanisms that enable plants to recognize winter, spring and autumn to initiate flower development.

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Figure 1: Transcriptional and post-translational regulation of CONSTANS controls photoperiodic flowering of Arabidopsis thaliana.
Figure 2: Comparison of flowering time regulation by day length and vernalization in different species.
Figure 3: Seasonal control of flowering in perennial species.

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Acknowledgements

We thank the members of the Coupland group and the three independent reviewers for their comments on the manuscript. F.A. was funded by a Marie Curie postdoctoral fellowship from the European Union. The laboratory of G.C. is funded by a core grant from the Max Planck Society.

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Glossary

Photoperiod

The duration of light that a plant is exposed to.

Vernalization

Prolonged exposure to low winter temperatures that in many plant species is required to accelerate flowering.

Floral integrator genes

A set of genes that regulate the floral transition and are the convergence point of diverse flowering pathways.

Life histories

A variety of strategies related to key biological events in the lifetime of an organism, such as juvenile-to-adult transition, reproduction and senescence. These strategies have been adopted by different species during evolution in order to maximize the number of viable offspring they produce.

Circadian clock

An endogenous time-keeping mechanism with a cycle time of approximately 24 hours that regulates the transcription of many plant genes.

Phytochrome

Phytochrome proteins are red- and far-red-light-absorbing photoreceptors. They covalently bind to light-absorbing linear tetrapyrrole chromophore, photochromobilin, which is able to absorb light of wavelengths between 650nm (red) and 740nm (far red). Activated phytochromes are imported into the nucleus and directly interact with transcription factors.

Photoreceptors

Proteins with attached chromophores that absorb light changing the conformation of the protein and initiating photoreceptor signalling.

Cryptochrome

A blue-light-absorbing photoreceptor. Cryptochromes contain two noncovalently bound chromophores (pterin and flavin). Studies in Arabidopsis thaliana suggest that pterin absorbs at a wavelength of 380nm and flavin at 450nm. Flavin photoreduction and autophosphorylation of conserved tryptophans appear to be important steps of the cryptochrome signalling pathway.

Raf-kinase inhibitor proteins

Proteins that are present in diverse organisms. In mammals, they participate in cell differentiation, the cell cycle, apoptosis and cell migration by affecting different signalling pathways.

Polycomb-repressive complex 2

A protein complex that is highly conserved between plants and animals and includes methylase enzymes that cause trimethylation of lysine 27 on histone H3 leading to repression of gene transcription.

Polycomb-repressive complex 1

A protein complex found in animals that is only weakly conserved in plants and is required for repression of gene transcription by recognition of trimethylated lysine 27 on histone H3.

14-3-3 proteins

A family of acidic proteins present in all eukaryotes and involved in a wide range of biological processes. 14-3-3 proteins directly interact with many other proteins containing phospho-serine and phospho-threonine residues and thereby affect their activity. Interestingly, 14-3-3 proteins can mediate the nuclear-cytoplasmic shuttling of some of their targets.

B-type response regulator

Transcription factors that contain an aminoterminal receiver domain and a long carboxyterminal extension with a MYB-like DNA-binding domain. In Arabidopsis thaliana, these genes participate in the two-component cytokinin signal transduction pathway.

Summer annuals and winter annuals

Summer-annual plants typically complete a full life cycle very rapidly during spring and summer because they do not require vernalization to induce flowering. Winter-annual plants usually live for longer because flowering is not induced until they experience vernalization in winter and then flower the following spring.

Biennial

Flowering requires exposure to vernalization and the plant must reach a certain size before being sensitive to vernalization.

Polycarpic

A plant that flowers and produces fruit more than once during its lifetime.

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Andrés, F., Coupland, G. The genetic basis of flowering responses to seasonal cues. Nat Rev Genet 13, 627–639 (2012). https://doi.org/10.1038/nrg3291

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