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Recovery of trees from drought depends on belowground sink control

Nature Plants volume 2, Article number: 16111 (2016) Cite this article

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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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Figure 1: Hypothetical trajectories of metabolic activity and metabolite concentration in leaves and roots as a consequence of drought onset and drought release.
Figure 2: Reduction of net photosynthesis (AN) and soil respiration (RS) in the model ecosystem experiment during drought (dry season), and during recovery and stimulation after drought release (wet season).
Figure 3: Suppressed uptake and allocation of 13C assimilates in the model ecosystem experiment under drought (dry season) and increased transfer to and metabolization in the belowground compartment after drought release (wet season).
Figure 4: Decreased net photosynthesis (AN) in the pot experiment during drought but unchanged metabolite concentrations in leaves and increased concentrations in roots.

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References

  1. IPCC Managing the Risks of Extreme Events and Disasters to Advance Climate Change Adaptation Vol. 582 (Cambridge Univ. Press, 2012).

  2. McDowell, N. et al. Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytol. 178, 719–739 (2008).

    Article  Google Scholar 

  3. Körner, C. Carbon limitation in trees. J. Ecol. 91, 4–17 (2003).

    Article  Google Scholar 

  4. Reichstein, M. et al. Climate extremes and the carbon cycle. Nature 500, 287–295 (2013).

    Article  CAS  Google Scholar 

  5. Pan, Y. et al. A large and persistent carbon sink in the world's forests. Science 333, 988–993 (2011).

    Article  CAS  Google Scholar 

  6. Ciais, P. et al. Europe-wide reduction in primary productivity caused by the heat and drought in 2003. Nature 437, 529–533 (2005).

    Article  CAS  Google Scholar 

  7. Zha, T. S. et al. Gross and aboveground net primary production at Canadian forest carbon flux sites. Agr. Forest Meteorol. 174–175, 54–64 (2013).

    Article  Google Scholar 

  8. Guillemot, J. et al. The dynamic of the annual carbon allocation to wood in European tree species is consistent with a combined source–sink limitation of growth: implications for modelling. Biogeosciences 12, 2773–2790 (2015).

    Article  Google Scholar 

  9. Fatichi, S., Leuzinger, S. & Körner, C. Moving beyond photosynthesis: from carbon source to sink-driven vegetation modeling. New Phytol. 201, 1086–1095 (2014).

    Article  CAS  Google Scholar 

  10. Klein, T. & Hoch, G. Tree carbon allocation dynamics determined using a carbon mass balance approach. New Phytol. 205, 147–159 (2015).

    Article  CAS  Google Scholar 

  11. Ruehr, N. et al. Effects of drought on allocation of recent carbon: from beech leaves to soil respiration. New Phytol. 184, 950–961 (2009).

    Article  CAS  Google Scholar 

  12. Arndt, S. K., Clifford, S. C., Wanek, W., Jones, H. G. & Popp, M. Physiological and morphological adaptations of the fruit tree Ziziphus rotundifolia in response to progressive drought stress. Tree Physiol. 21, 705–715 (2001).

    Article  CAS  Google Scholar 

  13. Galvez, D. A., Landhausser, S. M. & Tyree, M. T. Root carbon reserve dynamics in aspen seedlings: does simulated drought induce reserve limitation? Tree Physiol. 31, 250–257 (2011).

    Article  Google Scholar 

  14. Sala, A., Woodruff, D. R. & Meinzer, F. C. Carbon dynamics in trees: feast or famine? Tree Physiol. 32, 764–775 (2012).

    Article  CAS  Google Scholar 

  15. Hasibeder, R., Fuchslueger, L., Richter, A. & Bahn, M. Summer drought alters carbon allocation to roots and root respiration in mountain grassland. New Phytol. 205, 1117–1127 (2015).

    Article  CAS  Google Scholar 

  16. Ashraf, M. & Foolad, M. R. Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ. Exp. Bot. 59, 206–216 (2007).

    Article  CAS  Google Scholar 

  17. Wiley, E. & Helliker, B. A re-evaluation of carbon storage in trees lends greater support for carbon limitation to growth. New Phytol. 195, 285–289 (2012).

    Article  CAS  Google Scholar 

  18. Unger, S., Máguas, C., Pereira, J. S., David, T. S. & Werner, C. The influence of precipitation pulses on soil respiration – assessing the “Birch effect” by stable carbon isotopes. Soil Biol. Biochem. 42, 1800–1810 (2010).

    Article  CAS  Google Scholar 

  19. Birch, H. F. Mineralisation of plant nitrogen following alternate wet and dry conditions. Plant Soil 20, 43–49 (1964).

    Article  Google Scholar 

  20. Ogle, K. et al. Quantifying ecological memory in plant and ecosystem processes. Ecol. Lett. 18, 221–235 (2015).

    Article  Google Scholar 

  21. Kuzyakov, Y. & Gavrichkova, O. Review: Time lag between photosynthesis and carbon dioxide efflux from soil: a review of mechanisms and controls. Glob. Change Biol. 16, 3386–3406 (2010).

    Article  Google Scholar 

  22. Volkmann, T., Haberer, K., Gessler, A. & Weiler, M. High-resolution isotope measurements resolve rapid ecohydrological dynamics at the soil-plant interface. New Phytol. 210, 839–849 (2016).

    Article  Google Scholar 

  23. Lehto, T. & Zwiazek, J. J. Ectomycorrhizas and water relations of trees: a review. Mycorrhiza 21, 71–90 (2011).

    Article  Google Scholar 

  24. Anderegg, W. R. L. et al. Pervasive drought legacies in forest ecosystems and their implications for carbon models. Science 349, 528–532 (2015).

    Article  CAS  Google Scholar 

  25. Hill, P. W. et al. Living roots magnify the response of soil organic carbon decomposition to temperature in temperate grassland. Glob. Change Biol. 21, 1368–1375 (2015).

    Article  Google Scholar 

  26. Tognetti, R., Michelozzi, M. & Borghetti, M. The response of European beech seedlings from two Italian populations to drought and recovery. Trees Struct. Funct. 9, 348–354 (1995).

    Article  Google Scholar 

  27. Gallé, A. & Feller, U. Changes of photosynthetic traits in beech under severe drought stress and during recovery. Physiol. Plant. 131, 412–421 (2007).

    Article  Google Scholar 

  28. Albert, K. R., Mikkelsen, T. N., Michelsen, A., Ro-Poulsen, H. & van der Linden, L. Interactive effects of drought, elevated CO2 and warming on photosynthetic capacity and photosystem performance in temperate heath plants. J. Plant Physiol. 168, 1550–1561 (2011).

    Article  CAS  Google Scholar 

  29. Bader, M. K. F. & Körner, C. No overall stimulation of soil respiration under mature deciduous forest trees after 7 years of CO2 enrichment. Glob. Change Biol. 16, 2830–2843 (2010).

    Article  Google Scholar 

  30. Lang, S. Q., Bernasconi, S. M. & Früh-Green, G. L. Stable isotope analysis of organic carbon in small (µg C) samples and dissolved organic matter using a GasBench preparation device. Rapid. Comm. Mass Spectrom. 26, 9–16 (2012).

    Article  CAS  Google Scholar 

  31. Högberg, P. et al. High temporal resolution tracing of photosynthate carbon from the tree canopy to forest soil microorganisms. New Phytol. 177, 220–228 (2008).

    PubMed  Google Scholar 

  32. Ohlsson, K. E. A. et al. Uncertainties in static closed chamber measurements of the carbon isotopic ratio of soil-respired CO2 . Soil Biol. Biochem. 37, 2273–2276 (2005).

    Article  CAS  Google Scholar 

  33. Subke, J. A. et al. Feedback interactions between needle litter decomposition and rhizosphere activity. Oecologia 139, 551–559 (2004).

    Article  Google Scholar 

  34. Erxleben, A., Gessler, A., Vervliet-Scheebaum, M. & Reski, R. Metabolite profiling of the moss Physcomitrella patens reveals evolutionary conservation of osmoprotective substances. Plant Cell Rep. 31, 427–436 (2012).

    Article  CAS  Google Scholar 

  35. Gessler, A. et al. On the metabolic origin of the carbon isotope composition of CO2 evolved from darkened light-acclimated leaves in Ricinus communis. New Phytol. 181, 374–386 (2009).

    Article  CAS  Google Scholar 

  36. Schneider, S. et al. Soluble N compounds in trees exposed to high loads of N: a comparison of spruce (Picea abies) and beech (Fagus sylvatica) grown under field conditions. New Phytol. 134, 103–114 (1996).

    Article  CAS  Google Scholar 

  37. Pinheiro, J., Bates, D., Debroy, S. & Sarkar, D., the R Core Team Nlme: Linear and Nonlinear Mixed Effects Models R package version 3.1–118 (CRAN, 2014); http://CRAN.Rproject.org/package=nlme

  38. van Bel, A. The phloem, a miracle of ingenuity. Plant Cell Environ. 26, 125–149 (2003).

    Article  CAS  Google Scholar 

Download references

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.

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Author notes

  1. Frank Hagedorn, Jobin Joseph, Arthur Gessler and Matthias Arend: These authors contributed equally to the work.

Authors and 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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  1. Frank Hagedorn
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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.

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Correspondence to Matthias Arend.

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The authors declare no competing financial interests.

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Supplementary Figs 1-4, Supplementary Tables 1-4 and Supplementary Methods. (PDF 510 kb)

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Hagedorn, F., Joseph, J., Peter, M. et al. Recovery of trees from drought depends on belowground sink control. Nature Plants 2, 16111 (2016). https://doi.org/10.1038/nplants.2016.111

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