title: Increasing water use efficiency along the C3 to C4 evolutionary pathway: a stomatal optimization perspective.
abstract: 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.
authors.affiliation: Department of Biology, Western University, London, ON, Canada Nicholas School of the Environment, Duke University, Durham, NC, USA dway4@uwo.ca.
authors.forename: Danielle A
authors.initials: DA
authors.lastname: Way
authors.affiliation: Nicholas School of the Environment, Duke University, Durham, NC, USA Department of Civil and Environmental Engineering, Duke University, Durham, NC, USA.
authors.forename: Gabriel G
authors.initials: GG
authors.lastname: Katul
authors.affiliation: Department of Crop Production Ecology, Swedish University of Agricultural Sciences, Uppsala, Sweden Department of Ecology, Swedish University of Agricultural Sciences, Uppsala, Sweden Department of Physical Geography and Quaternary Geology, Stockholm University, Stockholm, Sweden.
authors.forename: Stefano
authors.initials: S
authors.lastname: Manzoni
authors.affiliation: Department of Crop Production Ecology, Swedish University of Agricultural Sciences, Uppsala, Sweden.
authors.forename: Giulia
authors.initials: G
authors.lastname: Vico
mesh_terms: D005075:Biological Evolution; D002245:Carbon Dioxide / Q000378:metabolism*; D037142:Flaveria / Q000235:genetics / Q000502:physiology*; D008962:Models, Theoretical; D010788:Photosynthesis; D018515:Plant Leaves / Q000235:genetics / Q000502:physiology; D054046:Plant Stomata / Q000235:genetics / Q000502:physiology; D018526:Plant Transpiration; D014867:Water / Q000378:metabolism*
chemical_list: D014867:Water; D002245:Carbon Dioxide
keywords: C3 photosynthesis; C3–C4 intermediates; leaf gas exchange; photosynthetic model; stomatal conductance; water use efficiency.