title: Outside-Xylem Vulnerability, Not Xylem Embolism, Controls Leaf Hydraulic Decline during Dehydration.
abstract: Leaf hydraulic supply is crucial to maintaining open stomata for CO2capture and plant growth. During drought-induced dehydration, the leaf hydraulic conductance (Kleaf) declines, which contributes to stomatal closure and, eventually, to leaf death. Previous studies have tended to attribute the decline of Kleafto embolism in the leaf vein xylem. We visualized at high resolution and quantified experimentally the hydraulic vulnerability of xylem and outside-xylem pathways and modeled their respective influences on plant water transport. Evidence from all approaches indicated that the decline of Kleafduring dehydration arose first and foremost due to the vulnerability of outside-xylem tissues. In vivo x-ray microcomputed tomography of dehydrating leaves of four diverse angiosperm species showed that, at the turgor loss point, only small fractions of leaf vein xylem conduits were embolized, and substantial xylem embolism arose only under severe dehydration. Experiments on an expanded set of eight angiosperm species showed that outside-xylem hydraulic vulnerability explained 75% to 100% of Kleafdecline across the range of dehydration from mild water stress to beyond turgor loss point. Spatially explicit modeling of leaf water transport pointed to a role for reduced membrane conductivity consistent with published data for cells and tissues. Plant-scale modeling suggested that outside-xylem hydraulic vulnerability can protect the xylem from tensions that would induce embolism and disruption of water transport under mild to moderate soil and atmospheric droughts. These findings pinpoint outside-xylem tissues as a central locus for the control of leaf and plant water transport during progressive drought.
authors.affiliation: Department of Ecology and Evolutionary Biology, University of California, Los Angeles, California, 90095 (C.S., S.V.T., G.P.J., M.K.B., L.S.); cscoffoni@ucla.edu.|Department of Biology, Utah State University, Logan, Utah 84322 (C.S.); cscoffoni@ucla.edu.|Department of Viticulture and Enology, University of California, Davis, California 95616 (C.A., A.J.M.); cscoffoni@ucla.edu.|School of Forestry and Environmental Studies, Yale University, New Haven, Connecticut 06511 (C.R.B.); cscoffoni@ucla.edu.|IA Watson Grains Research Centre, Plant Breeding Institute, Sydney Institute of Agriculture, University of Sydney, Narrabri, New South Wales 2390, Australia (T.N.B.); and cscoffoni@ucla.edu.|United States Department of Agriculture-Agricultural Research Service, Davis, California 95616 (A.J.M.) cscoffoni@ucla.edu.
authors.forename: Christine
authors.identifier: 0000-0002-2680-3608
authors.initials: C
authors.lastname: Scoffoni
authors.affiliation: Department of Ecology and Evolutionary Biology, University of California, Los Angeles, California, 90095 (C.S., S.V.T., G.P.J., M.K.B., L.S.).|Department of Biology, Utah State University, Logan, Utah 84322 (C.S.).|Department of Viticulture and Enology, University of California, Davis, California 95616 (C.A., A.J.M.).|School of Forestry and Environmental Studies, Yale University, New Haven, Connecticut 06511 (C.R.B.).|IA Watson Grains Research Centre, Plant Breeding Institute, Sydney Institute of Agriculture, University of Sydney, Narrabri, New South Wales 2390, Australia (T.N.B.); and.|United States Department of Agriculture-Agricultural Research Service, Davis, California 95616 (A.J.M.).
authors.forename: Caetano
authors.identifier: 0000-0001-6222-3996
authors.initials: C
authors.lastname: Albuquerque
authors.affiliation: Department of Ecology and Evolutionary Biology, University of California, Los Angeles, California, 90095 (C.S., S.V.T., G.P.J., M.K.B., L.S.).|Department of Biology, Utah State University, Logan, Utah 84322 (C.S.).|Department of Viticulture and Enology, University of California, Davis, California 95616 (C.A., A.J.M.).|School of Forestry and Environmental Studies, Yale University, New Haven, Connecticut 06511 (C.R.B.).|IA Watson Grains Research Centre, Plant Breeding Institute, Sydney Institute of Agriculture, University of Sydney, Narrabri, New South Wales 2390, Australia (T.N.B.); and.|United States Department of Agriculture-Agricultural Research Service, Davis, California 95616 (A.J.M.).
authors.forename: Craig R
authors.identifier: 0000-0002-0924-2570
authors.initials: CR
authors.lastname: Brodersen
authors.affiliation: Department of Ecology and Evolutionary Biology, University of California, Los Angeles, California, 90095 (C.S., S.V.T., G.P.J., M.K.B., L.S.).|Department of Biology, Utah State University, Logan, Utah 84322 (C.S.).|Department of Viticulture and Enology, University of California, Davis, California 95616 (C.A., A.J.M.).|School of Forestry and Environmental Studies, Yale University, New Haven, Connecticut 06511 (C.R.B.).|IA Watson Grains Research Centre, Plant Breeding Institute, Sydney Institute of Agriculture, University of Sydney, Narrabri, New South Wales 2390, Australia (T.N.B.); and.|United States Department of Agriculture-Agricultural Research Service, Davis, California 95616 (A.J.M.).
authors.forename: Shatara V
authors.initials: SV
authors.lastname: Townes
authors.affiliation: Department of Ecology and Evolutionary Biology, University of California, Los Angeles, California, 90095 (C.S., S.V.T., G.P.J., M.K.B., L.S.).|Department of Biology, Utah State University, Logan, Utah 84322 (C.S.).|Department of Viticulture and Enology, University of California, Davis, California 95616 (C.A., A.J.M.).|School of Forestry and Environmental Studies, Yale University, New Haven, Connecticut 06511 (C.R.B.).|IA Watson Grains Research Centre, Plant Breeding Institute, Sydney Institute of Agriculture, University of Sydney, Narrabri, New South Wales 2390, Australia (T.N.B.); and.|United States Department of Agriculture-Agricultural Research Service, Davis, California 95616 (A.J.M.).
authors.forename: Grace P
authors.identifier: 0000-0002-8045-5982
authors.initials: GP
authors.lastname: John
authors.affiliation: Department of Ecology and Evolutionary Biology, University of California, Los Angeles, California, 90095 (C.S., S.V.T., G.P.J., M.K.B., L.S.).|Department of Biology, Utah State University, Logan, Utah 84322 (C.S.).|Department of Viticulture and Enology, University of California, Davis, California 95616 (C.A., A.J.M.).|School of Forestry and Environmental Studies, Yale University, New Haven, Connecticut 06511 (C.R.B.).|IA Watson Grains Research Centre, Plant Breeding Institute, Sydney Institute of Agriculture, University of Sydney, Narrabri, New South Wales 2390, Australia (T.N.B.); and.|United States Department of Agriculture-Agricultural Research Service, Davis, California 95616 (A.J.M.).
authors.forename: Megan K
authors.initials: MK
authors.lastname: Bartlett
authors.affiliation: Department of Ecology and Evolutionary Biology, University of California, Los Angeles, California, 90095 (C.S., S.V.T., G.P.J., M.K.B., L.S.).|Department of Biology, Utah State University, Logan, Utah 84322 (C.S.).|Department of Viticulture and Enology, University of California, Davis, California 95616 (C.A., A.J.M.).|School of Forestry and Environmental Studies, Yale University, New Haven, Connecticut 06511 (C.R.B.).|IA Watson Grains Research Centre, Plant Breeding Institute, Sydney Institute of Agriculture, University of Sydney, Narrabri, New South Wales 2390, Australia (T.N.B.); and.|United States Department of Agriculture-Agricultural Research Service, Davis, California 95616 (A.J.M.).
authors.forename: Thomas N
authors.initials: TN
authors.lastname: Buckley
authors.affiliation: Department of Ecology and Evolutionary Biology, University of California, Los Angeles, California, 90095 (C.S., S.V.T., G.P.J., M.K.B., L.S.).|Department of Biology, Utah State University, Logan, Utah 84322 (C.S.).|Department of Viticulture and Enology, University of California, Davis, California 95616 (C.A., A.J.M.).|School of Forestry and Environmental Studies, Yale University, New Haven, Connecticut 06511 (C.R.B.).|IA Watson Grains Research Centre, Plant Breeding Institute, Sydney Institute of Agriculture, University of Sydney, Narrabri, New South Wales 2390, Australia (T.N.B.); and.|United States Department of Agriculture-Agricultural Research Service, Davis, California 95616 (A.J.M.).
authors.forename: Andrew J
authors.initials: AJ
authors.lastname: McElrone
authors.affiliation: Department of Ecology and Evolutionary Biology, University of California, Los Angeles, California, 90095 (C.S., S.V.T., G.P.J., M.K.B., L.S.).|Department of Biology, Utah State University, Logan, Utah 84322 (C.S.).|Department of Viticulture and Enology, University of California, Davis, California 95616 (C.A., A.J.M.).|School of Forestry and Environmental Studies, Yale University, New Haven, Connecticut 06511 (C.R.B.).|IA Watson Grains Research Centre, Plant Breeding Institute, Sydney Institute of Agriculture, University of Sydney, Narrabri, New South Wales 2390, Australia (T.N.B.); and.|United States Department of Agriculture-Agricultural Research Service, Davis, California 95616 (A.J.M.).
authors.forename: Lawren
authors.initials: L
authors.lastname: Sack
mesh_terms: D001692:Biological Transport; D003198:Computer Simulation; D003681:Dehydration; D055864:Droughts; D019684:Magnoliopsida / Q000502:physiology*; D008954:Models, Biological; D018515:Plant Leaves / Q000502:physiology*; D013045:Species Specificity; D014867:Water / Q000502:physiology*; D055114:X-Ray Microtomography; D052584:Xylem / Q000502:physiology*
chemical_list: D014867:Water