Increasing water use efficiency along the C3 to C4 evolutionary pathway: a stomatal optimization perspective

Way, Danielle A.; Katul, Gabriel G.; Manzoni, Stefano; Vico, Giulia

doi:10.1093/jxb/eru205

Increasing water use efficiency along the C3 to C4 evolutionary pathway: a stomatal optimization perspective

Journal Article · Fri May 23 00:00:00 EDT 2014 · Journal of Experimental Botany

DOI:https://doi.org/10.1093/jxb/eru205· OSTI ID:1625386

Way, Danielle A. ^[1]; Katul, Gabriel G. ^[2]; Manzoni, Stefano ^[3]; Vico, Giulia ^[4]

Western Univ., London, ON (Canada). Dept. of Biology; Duke Univ., Durham, NC (United States). Nicholas School of the Environment; DOE/OSTI
Duke Univ., Durham, NC (United States). Nicholas School of the Environment; Duke Univ., Durham, NC (United States). Dept. of Civil and Environmental Engineering
Swedish Univ. of Agricultural Sciences, Uppsala (Sweden). Dept. of Crop Production Ecology; Swedish Univ. of Agricultural Sciences, Uppsala (Sweden). Dept. of Ecology; Stockholm Univ. (Sweden). Dept. of Physical Geography and Quaternary Geology
Swedish Univ. of Agricultural Sciences, Uppsala (Sweden). Dept. of Crop Production Ecology

C4 photosynthesis evolved independently numerous times, probably in response to declining atmospheric CO2 concentrations, but also to high temperatures and aridity, which enhance water losses through transpiration. Here, the environmental factors controlling stomatal behaviour of leaf-level carbon and water exchange were examined across the evolutionary continuum from C3 to C4 photosynthesis at current (400 μmol mol–1) and low (280 μmol mol–1) atmospheric CO2 conditions. To this aim, a stomatal optimization model was further developed to describe the evolutionary continuum from C3 to C4 species within a unified framework. Data on C3, three categories of C3–C4 intermediates, and C4 Flaveria species were used to parameterize the stomatal model, including parameters for the marginal water use efficiency and the efficiency of the CO2-concentrating mechanism (or C4 pump); these two parameters are interpreted as traits reflecting the stomatal and photosynthetic adjustments during the C3 to C4 transformation. Neither the marginal water use efficiency nor the C4 pump strength changed significantly from C3 to early C3–C4 intermediate stages, but both traits significantly increased between early C3–C4 intermediates and the C4-like intermediates with an operational C4 cycle. At low CO2, net photosynthetic rates showed continuous increases from a C3 state, across the intermediates and towards C4 photosynthesis, but only C4-like intermediates and C4 species (with an operational C4 cycle) had higher water use efficiencies than C3 Flaveria. The results demonstrate that both the marginal water use efficiency and the C4 pump strength increase in C4 Flaveria to improve their photosynthesis and water use efficiency compared with C3 species. These findings emphasize that the advantage of the early intermediate stages is predominantly carbon based, not water related.

View Accepted Manuscript (DOE)

Research Organization:: Duke Univ., Durham, NC (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER). Earth and Environmental Systems Science Division

Grant/Contract Number:: SC0006967

OSTI ID:: 1625386

Journal Information:: Journal of Experimental Botany, Journal Name: Journal of Experimental Botany Journal Issue: 13 Vol. 65; ISSN 0022-0957

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United States

Language:: English

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