Root-derived GA12 contributes to temperature-induced shoot growth in Arabidopsis

Abstract

Plants are able to sense a rise in temperature of several degrees, and appropriately adapt their metabolic and growth processes. To this end, plants produce various signalling molecules that act throughout the plant body. Here, we report that root-derived GA12, a precursor of the bioactive gibberellins, mediates thermo-responsive shoot growth in Arabidopsis. Our data suggest that root-to-shoot translocation of GA12 enables a flexible growth response to ambient temperature changes.

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Fig. 1: Root-derived GA are essential for the thermal induction of shoot growth.
Fig. 2: Root-borne GA12 enhances hypocotyl elongation at 28 °C via a DELLA-dependent mechanism.

Data availability

All data generated or analysed during this study are included in the published article and its Supplementary Information.

References

  1. 1.

    Quint, M. et al. Molecular and genetic control of plant thermomorphogenesis. Nat. Plants 2, 15190 (2016).

  2. 2.

    Martins, S. et al. Brassinosteroid signaling-dependent root responses to prolonged elevated ambient temperature. Nat. Commun. 8, 309 (2017).

  3. 3.

    Kumar, S. V. et al. Transcription factor PIF4 controls the thermosensory activation of flowering. Nature 484, 242–245 (2012).

  4. 4.

    Davière, J.-M. & Achard, P. Gibberellin signaling in plants. Development 140, 1147–1151 (2013).

  5. 5.

    Achard, P. et al. Integration of plant responses to environmentally activated phytohormonal signals. Science 311, 91–94 (2006).

  6. 6.

    Colebrook, E. H., Thomas, S. G., Phillips, A. L. & Hedden, P. The role of gibberellin signaling in plant responses to abiotic stress. J. Exp. Bot. 217, 67–75 (2014).

  7. 7.

    Stavang, J. A. et al. Hormonal regulation of temperature-induced growth in Arabidopsis. Plant J. 60, 589–601 (2009).

  8. 8.

    Bai, L., Deng, H., Zhang, X., Yu, X. & Li, Y. Gibberellin is involved in inhibition of cucumber growth and nitrogen uptake at suboptimal root-zone temperature. PLoS ONE 11, e0156188 (2016).

  9. 9.

    Regnault, T. et al. The gibberellin precursor GA12 acts as a long-distance growth signal in Arabidopsis. Nat. Plants 1, 15073 (2015).

  10. 10.

    Binenbaum, J., Weinstain, R. & Shani, E. Gibberellin localization and transport in plants. Trends Plant Sci. 23, 410–421 (2018).

  11. 11.

    Hedden, P. & Thomas, S. G. Gibberellin biosynthesis and its regulation. Biochem. J. 444, 11–25 (2012).

  12. 12.

    Gaymard, F. et al. Identification and disruption of a plant shaker-like outward channel involved in K+ release into the xylem sap. Cell 94, 647–655 (1998).

  13. 13.

    de Lucas, M. et al. A molecular framework for light and gibberellin control of cell elongation. Nature 451, 480–484 (2008).

  14. 14.

    Regnault, T., Davière, J.-M., Heintz, D., Lange, T. & Achard, P. The gibberellin biosynthetic genes AtKAO1 and AtKAO2 have overlapping roles throughout Arabidopsis development. Plant J. 80, 462–474 (2014).

  15. 15.

    Hwang, I. & Goodman, H. M. An Arabidopsis thaliana root-specific kinase homolog is induced by dehydration, ABA, and NaCl. Plant J. 8, 37–43 (1995).

  16. 16.

    Osugi, A. et al. Systemic transport of trans-zeatin and its precursor have differing roles in Arabidopsis shoots. Nat. Plants 3, 17112 (2017).

  17. 17.

    Saito, H. et al. The jasmonate-responsive GTR1 transporter is required for gibberellin-mediated stamen development in Arabidopsis. Nat. Commun. 6, 6095 (2015).

  18. 18.

    Tal, I. et al. The Arabidopsis NPF3 protein is a GA transporter. Nat. Commun. 7, 11486 (2016).

  19. 19.

    Reid, D. M., Crozier, A. & Harvey, B. M. The effects of flooding on the export of gibberellins from the root to the shoot. Planta 89, 346–379 (1969).

  20. 20.

    Lavender, D. P., Sweet, G. B., Zaerr, J. B. & Hermann, R. K. Spring shoot growth in Douglas fir may be initiated by gibberellins exported from the roots. Science 182, 838–839 (1973).

  21. 21.

    Nakamura, S. et al. Gateway binary vectors with the bialaphos resistance gene, bar, as a selection marker for plant transformation. Biosci. Biotechnol. Biochem. 74, 1315–1319 (2010).

  22. 22.

    Karimi, M., Inzé, D. & Depicker, A. GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 7, 193–195 (2002).

  23. 23.

    Turnbull, C. G. N., Booker, J. P. & Leyser, O. Micrografting techniques for testing long-distance signalling in Arabidopsis. Plant J. 32, 255–262 (2002).

  24. 24.

    Lange, T. et al. Gibberellin biosynthesis in developing pumpkin seedlings. Plant Physiol. 139, 213–223 (2005).

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Acknowledgements

We thank T.P. Sun for providing seeds of ga1-3 (Col-0 background) and P. Hedden for providing ga20ox1-2-3. This work was supported by the Centre National de la Recherche Scientifique and the French Ministry of Research and Higher Education.

Author information

L.C., T.R., L.S.-A., E.C., J.Z., D.H., N.L., M.J.P.L., T.L., J.-M.D. and P.A. performed experimental work. L.C., T.R., D.H., N.L., M.J.P.L., T.L., J.-M.D. and P.A. designed the experiments. M.S., M.J.P.L., T.L., J.-M.D. and P.A. realised the figures and wrote the paper.

Correspondence to Patrick Achard.

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Supplementary information

Supplementary Information

Supplementary Discussion and Supplementary Figures 1–5.

Reporting Summary

Supplementary Tables

Supplementary Tables 1–5.

Supplementary Dataset 1

Statistics (ANOVA and t-test), P values.

Source data

Source Data Fig. 1

Statistical source data.

Source Data Fig. 2

Statistical source data.

Source Data Supplementary Fig. 1

Statistical source data.

Source Data Supplementary Fig. 2

Statistical source data.

Source Data Supplementary Fig. 3

Statistical source data.

Source Data Supplementary Fig. 4

Statistical source data.

Source Data Fig. 2d

Unprocessed blots.

Source Data Supplementary Fig. 4b

Unprocessed blots.

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Camut, L., Regnault, T., Sirlin-Josserand, M. et al. Root-derived GA12 contributes to temperature-induced shoot growth in Arabidopsis. Nat. Plants 5, 1216–1221 (2019). https://doi.org/10.1038/s41477-019-0568-8

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