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Coordinated circadian timing through the integration of local inputs in Arabidopsis thaliana

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  • Mark Greenwood
  • Mirela Domijan
  • Peter D Gould
  • Anthony J W Hall
  • James C W Locke

Abstract

Individual plant cells have a genetic circuit, the circadian clock, that times key processes to the day-night cycle. These clocks are aligned to the day-night cycle by multiple environmental signals that vary across the plant. How does the plant integrate clock rhythms, both within and between organs, to ensure coordinated timing? To address this question, we examined the clock at the sub-tissue level across Arabidopsis thaliana seedlings under multiple environmental conditions and genetic backgrounds. Our results show that the clock runs at different speeds (periods) in each organ, which causes the clock to peak at different times across the plant in both constant environmental conditions and light-dark (LD) cycles. Closer examination reveals that spatial waves of clock gene expression propagate both within and between organs. Using a combination of modeling and experiment, we reveal that these spatial waves are the result of the period differences between organs and local coupling, rather than long-distance signaling. With further experiments we show that the endogenous period differences, and thus the spatial waves, can be generated by the organ specificity of inputs into the clock. We demonstrate this by modulating periods using light and metabolic signals, as well as with genetic perturbations. Our results reveal that plant clocks can be set locally by organ-specific inputs but coordinated globally via spatial waves of clock gene expression.Computational modeling and experiments with Arabidopsis thaliana reveal a new mechanism for the coordination of circadian timing across an organism, acting through a combination of organ-specific sensitivity to environmental inputs and local cell-cell coupling.

Suggested Citation

  • Mark Greenwood & Mirela Domijan & Peter D Gould & Anthony J W Hall & James C W Locke, 2019. "Coordinated circadian timing through the integration of local inputs in Arabidopsis thaliana," PLOS Biology, Public Library of Science, vol. 17(8), pages 1-31, August.
  • Handle: RePEc:plo:pbio00:3000407
    DOI: 10.1371/journal.pbio.3000407
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    References listed on IDEAS

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    1. Ilka Schultheiß Araújo & Jessica Magdalena Pietsch & Emma Mathilde Keizer & Bettina Greese & Rachappa Balkunde & Christian Fleck & Martin Hülskamp, 2017. "Stochastic gene expression in Arabidopsis thaliana," Nature Communications, Nature, vol. 8(1), pages 1-9, December.
    2. Motomu Endo & Hanako Shimizu & Maria A. Nohales & Takashi Araki & Steve A. Kay, 2014. "Tissue-specific clocks in Arabidopsis show asymmetric coupling," Nature, Nature, vol. 515(7527), pages 419-422, November.
    3. Michael J. Haydon & Olga Mielczarek & Fiona C. Robertson & Katharine E. Hubbard & Alex A. R. Webb, 2013. "Photosynthetic entrainment of the Arabidopsis thaliana circadian clock," Nature, Nature, vol. 502(7473), pages 689-692, October.
    4. Mark R. Doyle & Seth J. Davis & Ruth M. Bastow & Harriet G. McWatters & László Kozma-Bognár & Ferenc Nagy & Andrew J. Millar & Richard M. Amasino, 2002. "The ELF4 gene controls circadian rhythms and flowering time in Arabidopsis thaliana," Nature, Nature, vol. 419(6902), pages 74-77, September.
    5. Tomasz Zielinski & Anne M Moore & Eilidh Troup & Karen J Halliday & Andrew J Millar, 2014. "Strengths and Limitations of Period Estimation Methods for Circadian Data," PLOS ONE, Public Library of Science, vol. 9(5), pages 1-26, May.
    6. Alex A. R. Webb & Motohide Seki & Akiko Satake & Camila Caldana, 2019. "Continuous dynamic adjustment of the plant circadian oscillator," Nature Communications, Nature, vol. 10(1), pages 1-9, December.
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