The phytochromes are a family of plant photoreceptor proteins that control several adaptive developmental strategies1,2. For example, the phytochromes perceive far-red light (wavelengths between 700 and 800 nm) reflected or scattered from the leaves of nearby vegetation. This provides an early warning of potential shading, and triggers a series of ‘shade-avoidance’ responses, such as a rapid increase in elongation3, by which the plant attempts to overgrow its neighbours3. Other, less immediate, responses include accelerated flowering and early production of seeds. However, little is known about the molecular events that connect light perception with increased growth in shade avoidance. Here we show that the circadian clock gates this rapid shade-avoidance response. It is most apparent around dusk and is accompanied by altered expression of several genes. One of these rapidly responsive genes encodes a basic helix–loop–helix protein, PIL1, previously shown to interact with the clock protein TOC1 (ref. 4). Furthermore PIL1 and TOC1 are both required for the accelerated growth associated with the shade-avoidance response.
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Quail, P. H. et al. Phytochromes: Photosensory perception and signal transduction. Science 268, 675–680 (1995)
Kendrick, R. E. & Kronenberg, G. H. M. Photomorphogenesis in Plants 2nd edn (Kluwer Academic, Dordrecht, The Netherlands, 1999)
Smith, H. & Whitelam, G. C. The shade avoidance syndrome: multiple responses mediated by multiple phytochromes. Plant Cell Environ. 20, 840–844 (1997)
Makino, S., Matsushika, A., Kojima, M., Yamashino, T. & Mizuno, T. The APRR1/TOC1 quintet implicated in circadian rhythms of Arabidopsis thaliana. I. Characterization with APRR1-overexpressing plants. Plant Cell Physiol. 43, 58–69 (2002)
Franklin, K. A. et al. Phytochromes B, D and E act redundantly to control multiple physiological responses in Arabidopsis. Plant Physiol. 131, 1340–1346 (2003)
Morgan, D. C., O'Brien, T. & Smith, H. Rapid photomodulation of stem extension in light-grown Sinapis alba L. studies on kinetics, site of perception and photoreceptor. Planta 150, 95–101 (1980)
Cerdan, P. & Chory, J. Regulation of flowering time by light quality. Nature 423, 881–885 (2003)
Carabelli, M., Morelli, G., Whitelam, G. & Ruberti, I. Twilight-zone and canopy shade induction of the Athb-2 homeobox gene in green plants. Proc. Natl Acad. Sci. USA 93, 3530–3535 (1996)
Yamashino, T. et al. A link between circadian-controlled bHLH factors and the APPR1/TOC1 quintet in Arabidopsis thaliana. Plant Cell Physiol. 44, 619–629 (2003)
Tepperman, J. M., Zhu, T., Chang, H.-S., Wang, X. & Quail, P. H. Multiple transcription-factor genes are early targets of phytochrome A signaling. Proc. Natl Acad. Sci. USA 98, 9437–9442
Botto, J. F. & Smith, H. Differential genetic variation in adaptive strategies to a common environmental signal in Arabidopsis accessions: phytochrome-mediated shade avoidance. Plant Cell Environ. 25, 53–63 (2002)
Tóth, R. et al. Circadian clock-regulated expression of phytochrome and cryptochrome genes in Arabidopsis. Plant Physiol. 127, 1607–1616 (2001)
Hall, A., Kozma-Bognár, L., Tóth, R., Nagy, F. & Millar, A. J. Conditional circadian regulation of PHYTOCHROME A gene expression. Plant Physiol. 127, 1808–1818 (2001)
Sharrock, R. A. & Clack, T. Patterns of expression and normalized levels of the five Arabidopsis phytochromes. Plant Physiol. 130, 442–456 (2002)
Mas, P., Alabadi, D., Yanovsky, M. J., Oyama, T. & Kay, S. A. Dual role of TOC1 in the control of circadian and photomorphogenic responses in Arabidopsis. Plant Cell 15, 233–236 (2003)
Harmer, S. L. et al. Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science 290, 2110–2113 (2000)
Dowson-Day, M. J. & Millar, A. J. Circadian dysfunction causes aberrant hypocotyl elongation patterns in Arabidopsis. Plant J. 17, 63–71 (1999)
Johnson, E., Bradley, J. M., Harberd, N. H. & Whitelam, G. C. Photoresponses of light-grown phyA mutants of Arabidopsis. Phytochrome A is required for the perception of daylength extensions. Plant Physiol. 105, 141–149 (1994)
Smith, H. Phytochromes and light signal perception by plants—an emerging synthesis. Nature 407, 585–591 (2000)
Halliday, K. J., Salter, M. G., Thingnaes, E. & Whitelam, G. C. The phyB-controlled flowering pathway is temperature sensitive and is mediated by the floral integrator FT. Plant J. 33, 875–885 (2003)
We thank E. Halligan, D. Lowes and J. Lunec for assistance with the Affymetrix microarrays, T. Ingles for assistance in creating transgenic lines, and A. Millar for providing toc1 alleles. This work was supported by grants from the Biotechnology and Biological Research Council, UK.
The authors declare that they have no competing financial interests.
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Salter, M., Franklin, K. & Whitelam, G. Gating of the rapid shade-avoidance response by the circadian clock in plants. Nature 426, 680–683 (2003). https://doi.org/10.1038/nature02174
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