Letter

Recovery of trees from drought depends on belowground sink control

  • Nature Plants 2, Article number: 16111 (2016)
  • doi:10.1038/nplants.2016.111
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Abstract

Climate projections predict higher precipitation variability with more frequent dry extremes1. CO2 assimilation of forests decreases during drought, either by stomatal closure2 or by direct environmental control of sink tissue activities3. Ultimately, drought effects on forests depend on the ability of forests to recover, but the mechanisms controlling ecosystem resilience are uncertain4. Here, we have investigated the effects of drought and drought release on the carbon balances in beech trees by combining CO2 flux measurements, metabolomics and 13CO2 pulse labelling. During drought, net photosynthesis (AN), soil respiration (RS) and the allocation of recent assimilates below ground were reduced. Carbohydrates accumulated in metabolically resting roots but not in leaves, indicating sink control of the tree carbon balance. After drought release, RS recovered faster than AN and CO2 fluxes exceeded those in continuously watered trees for months. This stimulation was related to greater assimilate allocation to and metabolization in the rhizosphere. These findings show that trees prioritize the investment of assimilates below ground, probably to regain root functions after drought. We propose that root restoration plays a key role in ecosystem resilience to drought, in that the increased sink activity controls the recovery of carbon balances.

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Acknowledgements

We thank P. Bleuler for technical assistance and for maintaining the model ecosystem facility. We also thank B. Meier, R. Appenzeller, Y. Bicker, D. Brödlin, D. Christen, N. Hajjar, R. Köchli, F. Schreyer and A. Zürcher for their help with sampling and measurements, and F. Buegger, L. Schmidt and A. Schlumpf for completing the isotope analysis. We are grateful to M. Dawes for critically reading and providing helpful comments on the manuscript. This work was supported by funding from the Swiss Federal Institute for Forest, Snow and Landscape Research WSL and the Swiss Federal Office for the Environment FOEN.

Author information

Author notes

    • Frank Hagedorn
    • , Jobin Joseph
    • , Arthur Gessler
    •  & Matthias Arend

    These authors contributed equally to the work.

Affiliations

  1. Swiss Federal Institute for Forest, Snow and Landscape Research (WSL), Zürcherstrasse 111, 8903 Birmensdorf, Switzerland

    • Frank Hagedorn
    • , Jobin Joseph
    • , Martina Peter
    • , Jörg Luster
    • , Virginie Molinier
    • , Simon Egli
    • , Marcus Schaub
    • , Maihe Li
    • , Arthur Gessler
    •  & Matthias Arend
  2. Chair of Hydrology, Faculty of Environment and Natural Resources, University of Freiburg, Fahnenbergplatz, 79098 Freiburg, Germany

    • Jobin Joseph
    •  & Markus Weiler
  3. Institute of Biochemical Plant Pathology, Helmholtz Zentrum München, German Research Centre for Environmental Health (GmbH), Ingolstaedter Landstrasse 1, 85764 Neuherberg, Germany

    • Karin Pritsch
    • , Uwe Geppert
    •  & Rene Kerner
  4. Research Institute of Forestry, Chinese Academy of Forestry, Xiangshan Road, 100091 Beijing, China

    • Jian-Feng Liu
  5. Department of Forest Genetics, Dendrology and Botany, Faculty of Forestry, University of Zagreb, Svetošimunska 25, HR-10000 Zagreb, Croatia

    • Krunoslav Sever
  6. Laboratory of Atmospheric Chemistry, Ecosystem Fluxes Group, Paul Scherrer Institute (PSI), 5232 Villigen, Switzerland

    • Rolf T. W. Siegwolf
  7. Institute for Landscape Biogeochemistry, Leibnitz Centre for Agricultural Landscape Research (ZALF), Eberswalder Strasse 84, 15374 Müncheberg, Germany

    • Arthur Gessler
  8. Berlin-Brandenburg Institute of Advanced Biodiversity Research (BBIB), Altensteinstrasse 6, 14195 Berlin, Germany

    • Arthur Gessler
  9. School of Forest Science and Resource Management, Technical University of Munich, Hans-Carl-von-Carlowitz-Platz 2, 85354 Freising, Germany

    • Matthias Arend

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Contributions

M.A., R.S., F.H., M.S. and A.G. designed the experiments; R.S., F.H., J.J. and M.A. performed the 13C pulse labelling; F.H., K.S. and M.A. measured seasonal CO2 fluxes and chlorophyll fluorescence; M.A., M.P., K.P., U.G., R.K., V.M., S.E. J.L., J.J., M.W., R.S. and F.H. analysed 13C allocation patterns; A.G., J-F.L. and M.L. analysed metabolites; J.J. and F.H. performed statistical analysis; A.G., J.J., F.H. and M.A. wrote the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Matthias Arend.

Supplementary information

PDF files

  1. 1.

    Supplementary Information

    Supplementary Figs 1-4, Supplementary Tables 1-4 and Supplementary Methods.