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Maintenance of carbohydrate transport in tall trees

Nature Plants volume 3, pages 965–972 (2017)Cite this article

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Abstract

Trees present a critical challenge to long-distance transport because as a tree grows in height and the transport pathway increases in length, the hydraulic resistance of the vascular tissue should increase. This has led many to question whether trees can rely on a passive transport mechanism to move carbohydrates from their leaves to their roots. Although species that actively load sugars into their phloem, such as vines and herbs, can increase the driving force for transport as they elongate, it is possible that many trees cannot generate high turgor pressures because they do not use transporters to load sugar into the phloem. Here, we examine how trees can maintain efficient carbohydrate transport as they grow taller by analysing sieve tube anatomy, including sieve plate geometry, using recently developed preparation and imaging techniques, and by measuring the turgor pressures in the leaves of a tall tree in situ. Across nine deciduous species, we find that hydraulic resistance in the phloem scales inversely with plant height because of a shift in sieve element structure along the length of individual trees. This scaling relationship seems robust across multiple species despite large differences in plate anatomy. The importance of this scaling becomes clear when phloem transport is modelled using turgor pressures measured in the leaves of a mature red oak tree. These pressures are of sufficient magnitude to drive phloem transport only in concert with structural changes in the phloem that reduce transport resistance. As a result, the key to the long-standing mystery of how trees maintain phloem transport as they increase in size lies in the structure of the phloem and its ability to change hydraulic properties with plant height.

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Fig. 1: Diagram of sieve tube anatomy and structural parameters that contribute to hydraulic resistance in angiosperms.
Fig. 2: Relationship between phloem anatomical parameters and height.
Fig. 3: Model of pressure differential required to drive phloem transport with increasing tree height under three different scenarios.
Fig. 4: Parameterization of carbohydrate transport in a 120-year-old red oak tree.
Fig. 5: Structural changes in sieve plate anatomy that affect sieve tube resistance.
Fig. 6: Comparison of xylem and phloem anatomy.

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Acknowledgements

Funding was provided by the National Science Foundation (IOS 1021779 and 1456682 to N.M.H. and M.K.), a Katharine H. Putnam Fellowship in Plant Science (J.A.S.), a Harvard Bullard Fellowship (M.K.), and the University of Minnesota Duluth (J.A.S.). Samples were collected at the Arnold Arboretum of Harvard University (permit no. 22-2013), the Harvard Forest and the main campus of Harvard University. Imaging was completed at the Harvard Center for Biological Imaging, Franceschi Microscopy and Imaging Center at WSU, the Center for Nanoscale Systems (Harvard University) and the Weld Hill Microscopy Lab at the Arnold Arboretum.

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Authors and Affiliations

  1. Department of Biology, University of Minnesota, Duluth, MN, USA

    Jessica A. Savage

  2. Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA, USA

    Jessica A. Savage, Laura Clerx, Jessica T. Gersony, Juan M. Losada & N. Michele Holbrook

  3. School of Biological Sciences, Washington State University, Pullman, WA, USA

    Sierra D. Beecher, Jan Knoblauch & Michael Knoblauch

  4. Department of Physics, Technical University of Denmark, Lyngby, Denmark

    Kaare H. Jensen

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  1. Jessica A. Savage
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Contributions

J.A.S., K.H.J., M.K. and N.M.H. designed the research. J.A.S., S.D.B., L.C., J.T.G., J.K., M.K. and J.M.L. collected the data and standardized protocols. J.A.S. and K.H.J. analysed the data. J.A.S., N.M.H., K.H.J. and M.K. wrote the paper.

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Correspondence to Jessica A. Savage.

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Savage, J.A., Beecher, S.D., Clerx, L. et al. Maintenance of carbohydrate transport in tall trees. Nature Plants 3, 965–972 (2017). https://doi.org/10.1038/s41477-017-0064-y

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