Maintenance of carbohydrate transport in tall trees/631/449/1736/631/449/1870 article

Jessica A. Savage, Sierra D. Beecher, Laura Clerx, Jessica T. Gersony, Jan Knoblauch, Juan M. Losada, Kaare H. Jensen, Michael Knoblauch, N. Michele Holbrook

Research output: Contribution to journalArticlepeer-review

20 Scopus citations

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.

Original languageEnglish (US)
Pages (from-to)965-972
Number of pages8
JournalNature plants
Volume3
Issue number12
DOIs
StatePublished - Dec 1 2017

Bibliographical note

Funding Information:
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.

Funding Information:
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).

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