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Title: Weak tradeoff between xylem safety and xylem-specific hydraulic efficiency across the world’s woody plant species

Author
item Gleason, Sean
item WESTOBY, MARK - Macquarie University
item JANSEN, STEVEN - Ulm University
item CHOAT, BRENDAN - Western Sydney University
item HACKE, UWE - University Of Alberta
item PRATT, ROBERT - California State University
item BHASKAR, RADIKA - Haverford College
item BRODRIBB, TIM - University Of Tasmania
item BUCCI, SANDRA - The National University Of The Pagagonia San Juan Bosco
item CAO, KUN-FANG - Guangxi University
item COCHARD, HERVE - Centre National De La Recherche Scientifique
item DELZON, SYLVAIN - University Of Bordeaux
item DOMEC, CHRISTOPHE - Duke University
item FAN, ZE-XIN - Chinese Academy Of Sciences
item FIELD, TAYLOR - James Cook University
item JACOBSEN, ANNA - California State University
item JOHNSON, DAN - University Of Idaho
item LENS, FREDERIC - Leiden University
item MAHERALI, HAFIZ - University Of Guelph
item MARTINEZ-VILALTA, JORDI - Autonomous University Of Barcelona
item MAYR, STEFAN - University Of Innsbruck
item MCCULLOH, KATHERINE - University Of Wisconsin
item MENCUCCIN, MAURIZIO - University Of Edinburgh
item MITCHELL, PATRICK - Commonwealth Scientific And Industrial Research Organisation (CSIRO)
item MORRIS, HUGH - Ulm University
item NARDINA, ANDREA - University Of Trieste
item PITTERMANN, JARMILA - University Of California
item PLAVOCA, LENKA - University Of Alberta
item SCHREIBER, STEFAN - University Of Alberta
item SPERRY, JOHN - University Of Utah
item WRIGHT, IAN - Macquarie University
item ZANNE, AMY - George Washington University

Submitted to: New Phytologist
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/13/2015
Publication Date: 1/8/2016
Citation: Gleason, S.M., Westoby, M., Jansen, S., Choat, B., Hacke, U.G., Pratt, R.B., Bhaskar, R., Brodribb, T.J., Bucci, S.J., Cao, K., Cochard, H., Delzon, S., Domec, C., Fan, Z., Field, T.S., Jacobsen, A.L., Johnson, D.M., Lens, F., Maherali, H., Martinez-Vilalta, J., Mayr, S., Mcculloh, K.A., Mencuccin, M., Mitchell, P.J., Morris, H., Nardina, A., Pittermann, J., Plavoca, L., Schreiber, S.G., Sperry, J.S., Wright, I.J., Zanne, A.E. 2016. Weak tradeoff between xylem safety and xylem-specific hydraulic efficiency across the world’s woody plant species. New Phytologist. doi:10.1111/nph.13646.

Interpretive Summary: • The evolution of xylem (wood tissue) in plant species allowed for the transport of water under negative tension. This means water could be “drawn up” through the xylem, driven by the energy of the sun. However, drawing water through xylem using negative tension also exposes xylem to the risk of spontaneous bubble formation (gas embolism) and the subsequent spread of this gas between xylem conduits. If emboli occur in sufficient quantity, water transport to the leaves is slowed down and, in severe cases, stopped, thus also arresting plant growth. A well-known hypothesis proposes that the safety of xylem (its ability to resist embolism formation and spread) should trade off against xylem efficiency (its capacity to transport water). • We tested this safety-efficiency hypothesis in branch xylem across 335 angiosperm (flowering seed plants) and 89 gymnosperm species (non-flowering seed plants). • Although associations between safety and efficiency were weak, no species had high both efficiency and high safety, supporting the idea for a safety-efficiency tradeoff. However, many species had low efficiency and low safety. Species with low efficiency and low safety were weakly associated with higher wood density, lower leaf-area to sapwood-area, and shorter stature. • There appears to be no persuasive explanation for the considerable number of species with both low efficiency and low safety. These species represent a real challenge for understanding the evolution of xylem.

Technical Abstract: • The evolution of lignified xylem allowed for the efficient transport of water under tension, but also exposed the vascular network to the risk of gas emboli and the spread of gas between xylem conduits, thus impeding sap transport to the leaves. A well-known hypothesis proposes that the safety of xylem (its ability to resist embolism formation and spread) should trade off against xylem efficiency (its capacity to transport water). • We tested this safety-efficiency hypothesis in branch xylem across 335 angiosperm and 89 gymnosperm species. Safety was considered at three levels: the xylem water potentials where 12, 50, and 88% of maximal conductivity are lost. • Although correlations between safety and efficiency were weak (r2 < 0.086), no species had high efficiency and high safety, supporting the idea for a safety-efficiency tradeoff. However, many species had low efficiency and low safety. Species with low efficiency and low safety were weakly associated (r2 < 0.02 in most cases) with higher wood density, lower leaf-area to sapwood-area, and shorter stature. • There appears to be no persuasive explanation for the considerable number of species with both low efficiency and low safety. These species represent a real challenge for understanding the evolution of xylem.