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Systematic analysis of how phytochrome B dimerization determines its specificity

Nature Plants volume 1, Article number: 15090 (2015) Cite this article

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A Corrigendum to this article was published on 17 October 2016

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Abstract

Phytochromes are red/far-red-light detecting photoreceptors that regulate plant growth and development. They photo-interconvert between an inactive Pr (red-light absorbing) and a physiologically active Pfr (far-red-light absorbing) form, acting as light-controlled molecular switches. Although the two major plant phytochromes A (phyA) and B (phyB) share similar absorption properties, they exhibit dramatic differences in their action spectra. Since both phytochromes antagonistically regulate seedling development under vegetative shade, it is essential for plants to clearly distinguish between phyA and phyB action. This discrimination is not comprehensible solely by the molecular properties of the phytochromes, but is evidently due to the dynamics of the phytochrome system. Using an integrated experimental and mathematical modelling approach we show that phytochrome dimerization is an essential element for phyB function. Our findings reveal that light-independent Pfr to Pr relaxation (dark reversion) and association/dissociation to nuclear bodies (NBs) severely depend on the conformational state of the phyB dimer. We conclude that only Pfr–Pfr homodimers of phyB can be responsible for triggering physiological responses, leading to a suppression of phyB function in the far-red range of the light spectrum.

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Figure 1: Discrepancy between model predictions and experimental results.
Figure 2: Reaction scheme describing phyB dimer dynamics.
Figure 3: In vivo phyB dark reversion kinetics.
Figure 4: Calibration of the kinetic phyB model.
Figure 5: Model prediction of fluence rate responses identifies the nuclear Pfr–Pfr homodimer pool as physiologically relevant.

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Acknowledgements

We thank Andreas Hiltbrunner, Jens Timmer and Robert Smith for helpful comments on the manuscript and Michael Volpers and Milad Adibi for helpful discussions and support. F.V. acknowledges funding from the LGFG/International Graduate Academy, University of Freiburg. C.K. was supported by DFG grant (SCHA 303/16-1) to E.S., S.K. acknowledges support by a DFG grant (KI 1077/2). C.F. was supported by the Human Frontier Science Program (HFSP Research Grant RGP0025/2013).

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Author notes

  1. Cornelia Klose and Filippo Venezia: These authors contributed equally to this work.

Authors and Affiliations

  1. Institute of Biology II, University of Freiburg, Schänzlestrasse 1, 79104, Freiburg, Germany

    Cornelia Klose, Filippo Venezia, Andrea Hussong, Stefan Kircher & Eberhard Schäfer

  2. Centre for Biological Systems Analysis, University of Freiburg, Habsburgerstr. 49, 79104, Freiburg, Germany

    Filippo Venezia

  3. BIOSS Centre for Biological Signalling Studies, University of Freiburg, Schänzlestr. 18, 79104, Freiburg, Germany

    Eberhard Schäfer

  4. Laboratory for Systems and Synthetic Biology, Wageningen UR, Dreijenplein 10, 6703 HB, Wageningen, The Netherlands

    Christian Fleck

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  1. Cornelia Klose
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Contributions

C.F. and E.S. devised this project. C.K. designed and performed the experiments, except the nuclear body experiments and the hypocotyl measurements (Fig. 1). F.V. analysed the experimental data, performed all mathematical calculations, designed the nuclear body study and performed and analysed the nuclear body experiments. S.K. supervised the nuclear body study and performed some of these experiments (Supplementary Fig. 11). A.H. performed hypocotyl measurement (Fig. 1). E.S. supervised all other experiments; C.F. supervised the mathematical modelling. F.V., C.K., S.K., E.S. and C.F. wrote the manuscript.

Corresponding authors

Correspondence to Eberhard Schäfer or Christian Fleck.

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The authors declare no competing interests.

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Klose, C., Venezia, F., Hussong, A. et al. Systematic analysis of how phytochrome B dimerization determines its specificity. Nature Plants 1, 15090 (2015). https://doi.org/10.1038/nplants.2015.90

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