title: How Does Leaf Anatomy Influence Water Transport outside the Xylem?
abstract: Leaves are arguably the most complex and important physicobiological systems in the ecosphere. Yet, water transport outside the leaf xylem remains poorly understood, despite its impacts on stomatal function and photosynthesis. We applied anatomical measurements from 14 diverse species to a novel model of water flow in an areole (the smallest region bounded by minor veins) to predict the impact of anatomical variation across species on outside-xylem hydraulic conductance (Kox). Several predictions verified previous correlational studies: (1) vein length per unit area is the strongest anatomical determinant of Kox, due to effects on hydraulic pathlength and bundle sheath (BS) surface area; (2) palisade mesophyll remains well hydrated in hypostomatous species, which may benefit photosynthesis, (3) BS extensions enhance Kox; and (4) the upper and lower epidermis are hydraulically sequestered from one another despite their proximity. Our findings also provided novel insights: (5) the BS contributes a minority of outside-xylem resistance; (6) vapor transport contributes up to two-thirds of Kox; (7) Kox is strongly enhanced by the proximity of veins to lower epidermis; and (8) Kox is strongly influenced by spongy mesophyll anatomy, decreasing with protoplast size and increasing with airspace fraction and cell wall thickness. Correlations between anatomy and Kox across species sometimes diverged from predicted causal effects, demonstrating the need for integrative models to resolve causation. For example, (9) Kox was enhanced far more in heterobaric species than predicted by their having BS extensions. Our approach provides detailed insights into the role of anatomical variation in leaf function.
authors.affiliation: I.A. Watson Grains Research Centre, Faculty of Agriculture and Environment, University of Sydney, Narrabri, New South Wales 2390, Australia (T.N.B.); andDepartment of Ecology and Evolutionary Biology, University of California, Los Angeles, California 90095 (G.P.J., C.S., L.S.) t.buckley@sydney.edu.au.
authors.forename: Thomas N
authors.initials: TN
authors.lastname: Buckley
authors.affiliation: I.A. Watson Grains Research Centre, Faculty of Agriculture and Environment, University of Sydney, Narrabri, New South Wales 2390, Australia (T.N.B.); andDepartment of Ecology and Evolutionary Biology, University of California, Los Angeles, California 90095 (G.P.J., C.S., L.S.).
authors.forename: Grace P
authors.identifier: http://orcid.org/0000-0002-8045-5982
authors.initials: GP
authors.lastname: John
authors.affiliation: I.A. Watson Grains Research Centre, Faculty of Agriculture and Environment, University of Sydney, Narrabri, New South Wales 2390, Australia (T.N.B.); andDepartment of Ecology and Evolutionary Biology, University of California, Los Angeles, California 90095 (G.P.J., C.S., L.S.).
authors.forename: Christine
authors.initials: C
authors.lastname: Scoffoni
authors.affiliation: I.A. Watson Grains Research Centre, Faculty of Agriculture and Environment, University of Sydney, Narrabri, New South Wales 2390, Australia (T.N.B.); andDepartment of Ecology and Evolutionary Biology, University of California, Los Angeles, California 90095 (G.P.J., C.S., L.S.).
authors.forename: Lawren
authors.initials: L
authors.lastname: Sack
mesh_terms: D000465:Algorithms; D001692:Biological Transport / Q000502:physiology; D005740:Gases / Q000378:metabolism; D057446:Hydrodynamics; D008954:Models, Biological; D018515:Plant Leaves / Q000166:cytology / Q000502:physiology*; D018521:Plant Physiological Phenomena / Q000502:physiology; D018526:Plant Transpiration / Q000502:physiology; D010944:Plants / Q000033:anatomy & histology / Q000145:classification / Q000378:metabolism; D013045:Species Specificity; D014867:Water / Q000378:metabolism*; D052584:Xylem / Q000033:anatomy & histology / Q000502:physiology*
chemical_list: D005740:Gases; D014867:Water