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Hydraulic basis for the evolution of photosynthetic productivity

Nature Plants volume 2, Article number: 16072 (2016) Cite this article

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Abstract

Clarifying the evolution and mechanisms for photosynthetic productivity is a key to both improving crops and understanding plant evolution and habitat distributions. Current theory recognizes a role for the hydraulics of water transport as a potential determinant of photosynthetic productivity based on comparative data across disparate species. However, there has never been rigorous support for the maintenance of this relationship during an evolutionary radiation. We tested this theory for 30 species of Viburnum, diverse in leaf shape and photosynthetic anatomy, grown in a common garden. We found strong support for a fundamental requirement for leaf hydraulic capacity (Kleaf) in determining photosynthetic capacity (Amax), as these traits diversified across this lineage in tight coordination, with their proportionality modulated by the climate experienced in the species' range. Variation in Kleaf arose from differences in venation architecture that influenced xylem and especially outside-xylem flow pathways. These findings substantiate an evolutionary basis for the coordination of hydraulic and photosynthetic physiology across species, and their co-dependence on climate, establishing a fundamental role for water transport in the evolution of the photosynthetic rate.

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Figure 1: Description of the hydraulic theory as a driver of leaf gas exchange.
Figure 2: Estimated ancestral states for Kleaf and Amax showing their co-evolution across the phylogenetic tree for Viburnum species.
Figure 3: Testing hydraulic theory in an evolutionary context across Viburnum species.
Figure 4: Drivers of leaf hydraulic conductance for Viburnum species.
Figure 5: Coordination of hydraulics and gas exchange with leaf venation.
Figure 6: Diversity of leaf size, shape and venation architecture in the model genus Viburnum.

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Acknowledgements

We thank the staff at the Arnold Arboretum of Harvard University, Erin Riordan for help with climate data, and M. Alfaro, M. Bartlett, M. Caringella, J. Chang and G. John for helpful comments on the manuscript. We would like to thank T. Givnish and two anonymous reviewers for their constructive comments. This work was funded by the Department of Ecology and Evolutionary Biology at UCLA, a UCLA Dissertation Year Fellowship and NSF grants IOS-0842771 to L.S., IOS-0843231 to E.J.E., and IOS-0842800 to M.J.D.

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Authors and Affiliations

  1. Department of Ecology and Evolutionary Biology, University of California Los Angeles, 621 Charles E. Young Drive South, Los Angeles, 90095, California, USA

    Christine Scoffoni, Jessica Pasquet-kok, Michael Rawls & Lawren Sack

  2. Department of Ecology and Evolutionary Biology, Brown University, Box G-W, 80 Waterman St., Providence, Rhode Island, 02912, USA

    David S. Chatelet & Erika J. Edwards

  3. Department of Ecology and Evolutionary Biology, Yale University, PO Box 208106, New Haven, 06520-8106, Connecticut, USA

    David S. Chatelet & Michael J. Donoghue

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  1. Christine Scoffoni
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Contributions

C.S., D.S.C., M.J.D., E.J.E. and L.S. designed experiments. C.S., D.S.C., J.P.K. and M.R. performed experiments. C.S. and D.S.C. analysed data. C.S. and L.S. wrote the paper with inputs from all authors.

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Correspondence to Christine Scoffoni.

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Appendices 1 and 2, Supplementary Figs 1 and 2, Supplementary Table 1 and Supplementary References. (PDF 1116 kb)

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Scoffoni, C., Chatelet, D., Pasquet-kok, J. et al. Hydraulic basis for the evolution of photosynthetic productivity. Nature Plants 2, 16072 (2016). https://doi.org/10.1038/nplants.2016.72

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