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Role of aquaporin activity in regulating deep and shallow root hydraulic conductance during extreme drought

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Deep root hydraulic conductance is upregulated during severe drought and is associated with upregulation in aquaporin activity.

Abstract

In 2011, Texas experienced the worst single-year drought in its recorded history and, based on tree-ring data, likely its worst in the past millennium. In the Edwards Plateau of Texas, rainfall was 58 % lower and the mean daily maximum temperatures were >5 °C higher than long-term means in June through September, resulting in extensive tree mortality. To better understand the balance of deep and shallow root functioning for water supply, we measured root hydraulic conductance (K R) in deep (~20 m) and shallow (5–10 cm) roots of Quercus fusiformis at four time points in the field in 2011. Deep roots of Q. fusiformis obtained water from a perennial underground (18–20 m) stream that was present even during the drought. As the drought progressed, deep root K R increased 2.6-fold from early season values and shallow root K R decreased by 50 % between April and September. Inhibitor studies revealed that aquaporin contribution to K R increased in deep roots and decreased in shallow roots as the drought progressed. Deep root aquaporin activity was upregulated during peak drought, likely driven by increased summer evaporative demand and the need to compensate for declining shallow root K R. A whole-tree hydraulic transport model predicted that trees with greater proportions of deep roots would have as much as five times greater transpiration during drought periods and could sustain transpiration during droughts without experiencing total hydraulic failure. Our results suggest that trees shift their dependence on deep roots versus shallow roots during drought periods, and that upregulation of aquaporin activity accounts for at least part of this increase.

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Author contribution statement

DMJ contributed to data collection and analysis, and writing and editing the manuscript. MES contributed to data collection and analysis, and writing and editing the manuscript. JCD contributed to data collection and analysis, and writing and editing the manuscript. RBJ contributed to data analysis, and writing and editing the manuscript.

Acknowledgments

This work was funded by NSF IOS-0920355, NSF IOS-1146746, and a grant from USDA-AFRI (#2012-00857). We thank Philip Fay, Anne Gibson and Kyle Tiner for assistance in coordination of field campaigns. The authors would also like to thank Josiah Strauss and Will Cook for field assistance.

Conflict of interest

The authors declare that they have no conflict of interest.

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Author notes

  1. Daniel M. Johnson

    Present address: Department of Forest, Ranglend and Fire Sciences, University of Idaho, Moscow, ID, 83844, USA

Authors and Affiliations

  1. Nicholas School of the Environment, Duke University, Durham, NC, 27708, USA

    Daniel M. Johnson, Jean-Christophe Domec & Robert B. Jackson

  2. Department of Biology, University of Northern Iowa, Cedar Falls, IA, 50614, USA

    Mark E. Sherrard

  3. Bordeaux Sciences Agro, UMR 1391 INRA-ISPA, University of Bordeaux, 33175, Gradignan Cedex, France

    Jean-Christophe Domec

  4. School of Earth Sciences, Woods Institute for the Environment, and Precourt Institute for Energy, Stanford University, Stanford, CA, 94305, USA

    Robert B. Jackson

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  1. Daniel M. Johnson
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Correspondence to Daniel M. Johnson.

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Communicated by A. Nardini.

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Johnson, D.M., Sherrard, M.E., Domec, JC. et al. Role of aquaporin activity in regulating deep and shallow root hydraulic conductance during extreme drought. Trees 28, 1323–1331 (2014). https://doi.org/10.1007/s00468-014-1036-8

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  • DOI: https://doi.org/10.1007/s00468-014-1036-8

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