Rhythmic growth explained by coincidence between internal and external cues

Abstract

Most organisms use circadian oscillators to coordinate physiological and developmental processes such as growth with predictable daily environmental changes like sunrise and sunset. The importance of such coordination is highlighted by studies showing that circadian dysfunction causes reduced fitness in bacteria1 and plants2, as well as sleep and psychological disorders in humans3. Plant cell growth requires energy and water—factors that oscillate owing to diurnal environmental changes. Indeed, two important factors controlling stem growth are the internal circadian oscillator4,5,6 and external light levels7. However, most circadian studies have been performed in constant conditions, precluding mechanistic study of interactions between the clock and diurnal variation in the environment. Studies of stem elongation in diurnal conditions have revealed complex growth patterns, but no mechanism has been described8,9,10. Here we show that the growth phase of Arabidopsis seedlings in diurnal light conditions is shifted 8–12 h relative to plants in continuous light, and we describe a mechanism underlying this environmental response. We find that the clock regulates transcript levels of two basic helix–loop–helix genes, phytochrome-interacting factor 4 (PIF4) and PIF5, whereas light regulates their protein abundance. These genes function as positive growth regulators; the coincidence of high transcript levels (by the clock) and protein accumulation (in the dark) allows them to promote plant growth at the end of the night. Thus, these two genes integrate clock and light signalling, and their coordinated regulation explains the observed diurnal growth rhythms. This interaction may serve as a paradigm for understanding how endogenous and environmental signals cooperate to control other processes.

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Figure 1: Diurnal rhythms of hypocotyl elongation require light and the circadian clock.
Figure 2: Transcript and protein level regulation of light-signalling components in hypocotyl growth control.

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Acknowledgements

We thank A. Wallace for technical assistance; J. C. Lagarias, N. Sinha and C. Wessinger for critical reading and comments on the manuscript; E. Tobin, S. Kay, A. Millar, J. C. Lagarias, T. Mizuno, P. Quail and the Arabidopsis Biological Resources Centre for seeds; and J. C. Lagarias for the loan of computer equipment. This work was supported by grants from the NSF (to J.N.M. and C. Weinig), the Swiss National Science foundation (to C.F.), the HFSP (to C.F., J.N.M. and U. Genick), the NRI of the USDA CSREES (to M.F.C.) and the NIH (to S.L.H.). The microarray data have been deposited in the GEOdatabase (http://www.ncbi.nlm.nih.gov/projects/geo/) under accession number GSE6906.

Author Contributions K.N. performed all experiments. Statistical analysis of growth and microarray data was done by J.N.M. K.N. and J.N.M. wrote the paper. P.D.D., S.L. and C.F. contributed HA-tagged protein overexpressing plants, western blot protocols, and pif4 pif5 double-mutant seed. M.F.C. contributed microarray experimental design. K.N., J.N.M. and S.L.H. contributed to project design. All authors discussed the results and commented on the manuscript.

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Correspondence to Julin N. Maloof.

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The microarray data have been deposited in the GEO database (http://www.ncbi.nlm.nih.gov/projects/geo/) under accession number GSE6906. Reprints and permissions information is available at www.nature.com/reprints. The authors declare no competing financial interests.

Supplementary information

Supplementary Information

This file contains Supplementary Discussion of growth pattern shifts between LL and SD, of additional circadian mutants, and of the microarray data; Supplementary Figures 1-8 with Legends; Supplementary Tables 1 -2 and additional references. (PDF 1290 kb)

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Nozue, K., Covington, M., Duek, P. et al. Rhythmic growth explained by coincidence between internal and external cues. Nature 448, 358–361 (2007). https://doi.org/10.1038/nature05946

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