title: Easy Come, Easy Go: Capillary Forces Enable Rapid Refilling of Embolized Primary Xylem Vessels.
abstract: Protoxylem plays an important role in the hydraulic function of vascular systems of both herbaceous and woody plants, but relatively little is known about the processes underlying the maintenance of protoxylem function in long-lived tissues. In this study, embolism repair was investigated in relation to xylem structure in two cushion plant species, Azorella macquariensis and Colobanthus muscoides, in which vascular water transport depends on protoxylem. Their protoxylem vessels consisted of a primary wall with helical thickenings that effectively formed a pit channel, with the primary wall being the pit channel membrane. Stem protoxylem was organized such that the pit channel membranes connected vessels with paratracheal parenchyma or other protoxylem vessels and were not exposed directly to air spaces. Embolism was experimentally induced in excised vascular tissue and detached shoots by exposing them briefly to air. When water was resupplied, embolized vessels refilled within tens of seconds (excised tissue) to a few minutes (detached shoots) with water sourced from either adjacent parenchyma or water-filled vessels. Refilling occurred in two phases: (1) water refilled xylem pit channels, simplifying bubble shape to a rod with two menisci; and (2) the bubble contracted as the resorption front advanced, dissolving air along the way. Physical properties of the protoxylem vessels (namely pit channel membrane porosity, hydrophilic walls, vessel dimensions, and helical thickenings) promoted rapid refilling of embolized conduits independent of root pressure. These results have implications for the maintenance of vascular function in both herbaceous and woody species, because protoxylem plays a major role in the hydraulic systems of leaves, elongating stems, and roots.
authors.affiliation: Plant Science Division, Research School of Biology (V.R., T.L., D.E.S., M.C.B.), and Centre for Advanced Microscopy (H.C.), Australian National University, Acton, Australian Capital Territory 2601, Australia;Australian Antarctic Division, Department of Environment, Kingston, Tasmania 7050, Australia (D.M.B.);Center for Molecular and Nanoscale Physics, School of Applied Sciences, RMIT University, Melbourne, Victoria 3001, Australia (G.B.);School of Physics, University of New South Wales, Sydney, New South Wales 2052, Australia (J.W.); andDepartment of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts 02138 (N.M.H.) vivien.rolland@anu.edu.au.
authors.forename: Vivien
authors.identifier: http://orcid.org/0000-0002-9232-1287
authors.initials: V
authors.lastname: Rolland
authors.affiliation: Plant Science Division, Research School of Biology (V.R., T.L., D.E.S., M.C.B.), and Centre for Advanced Microscopy (H.C.), Australian National University, Acton, Australian Capital Territory 2601, Australia;Australian Antarctic Division, Department of Environment, Kingston, Tasmania 7050, Australia (D.M.B.);Center for Molecular and Nanoscale Physics, School of Applied Sciences, RMIT University, Melbourne, Victoria 3001, Australia (G.B.);School of Physics, University of New South Wales, Sydney, New South Wales 2052, Australia (J.W.); andDepartment of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts 02138 (N.M.H.).
authors.forename: Dana M
authors.identifier: http://orcid.org/0000-0001-8484-8954
authors.initials: DM
authors.lastname: Bergstrom
authors.affiliation: Plant Science Division, Research School of Biology (V.R., T.L., D.E.S., M.C.B.), and Centre for Advanced Microscopy (H.C.), Australian National University, Acton, Australian Capital Territory 2601, Australia;Australian Antarctic Division, Department of Environment, Kingston, Tasmania 7050, Australia (D.M.B.);Center for Molecular and Nanoscale Physics, School of Applied Sciences, RMIT University, Melbourne, Victoria 3001, Australia (G.B.);School of Physics, University of New South Wales, Sydney, New South Wales 2052, Australia (J.W.); andDepartment of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts 02138 (N.M.H.).
authors.forename: Thomas
authors.initials: T
authors.lastname: Lenné
authors.affiliation: Plant Science Division, Research School of Biology (V.R., T.L., D.E.S., M.C.B.), and Centre for Advanced Microscopy (H.C.), Australian National University, Acton, Australian Capital Territory 2601, Australia;Australian Antarctic Division, Department of Environment, Kingston, Tasmania 7050, Australia (D.M.B.);Center for Molecular and Nanoscale Physics, School of Applied Sciences, RMIT University, Melbourne, Victoria 3001, Australia (G.B.);School of Physics, University of New South Wales, Sydney, New South Wales 2052, Australia (J.W.); andDepartment of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts 02138 (N.M.H.).
authors.forename: Gary
authors.identifier: http://orcid.org/0000-0001-5483-7592
authors.initials: G
authors.lastname: Bryant
authors.affiliation: Plant Science Division, Research School of Biology (V.R., T.L., D.E.S., M.C.B.), and Centre for Advanced Microscopy (H.C.), Australian National University, Acton, Australian Capital Territory 2601, Australia;Australian Antarctic Division, Department of Environment, Kingston, Tasmania 7050, Australia (D.M.B.);Center for Molecular and Nanoscale Physics, School of Applied Sciences, RMIT University, Melbourne, Victoria 3001, Australia (G.B.);School of Physics, University of New South Wales, Sydney, New South Wales 2052, Australia (J.W.); andDepartment of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts 02138 (N.M.H.).
authors.forename: Hua
authors.identifier: http://orcid.org/0000-0001-6573-517X
authors.initials: H
authors.lastname: Chen
authors.affiliation: Plant Science Division, Research School of Biology (V.R., T.L., D.E.S., M.C.B.), and Centre for Advanced Microscopy (H.C.), Australian National University, Acton, Australian Capital Territory 2601, Australia;Australian Antarctic Division, Department of Environment, Kingston, Tasmania 7050, Australia (D.M.B.);Center for Molecular and Nanoscale Physics, School of Applied Sciences, RMIT University, Melbourne, Victoria 3001, Australia (G.B.);School of Physics, University of New South Wales, Sydney, New South Wales 2052, Australia (J.W.); andDepartment of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts 02138 (N.M.H.).
authors.forename: Joe
authors.initials: J
authors.lastname: Wolfe
authors.affiliation: Plant Science Division, Research School of Biology (V.R., T.L., D.E.S., M.C.B.), and Centre for Advanced Microscopy (H.C.), Australian National University, Acton, Australian Capital Territory 2601, Australia;Australian Antarctic Division, Department of Environment, Kingston, Tasmania 7050, Australia (D.M.B.);Center for Molecular and Nanoscale Physics, School of Applied Sciences, RMIT University, Melbourne, Victoria 3001, Australia (G.B.);School of Physics, University of New South Wales, Sydney, New South Wales 2052, Australia (J.W.); andDepartment of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts 02138 (N.M.H.).
authors.forename: N Michele
authors.initials: NM
authors.lastname: Holbrook
authors.affiliation: Plant Science Division, Research School of Biology (V.R., T.L., D.E.S., M.C.B.), and Centre for Advanced Microscopy (H.C.), Australian National University, Acton, Australian Capital Territory 2601, Australia;Australian Antarctic Division, Department of Environment, Kingston, Tasmania 7050, Australia (D.M.B.);Center for Molecular and Nanoscale Physics, School of Applied Sciences, RMIT University, Melbourne, Victoria 3001, Australia (G.B.);School of Physics, University of New South Wales, Sydney, New South Wales 2052, Australia (J.W.); andDepartment of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts 02138 (N.M.H.).
authors.forename: Daniel E
authors.identifier: http://orcid.org/0000-0002-6713-9328
authors.initials: DE
authors.lastname: Stanton
authors.affiliation: Plant Science Division, Research School of Biology (V.R., T.L., D.E.S., M.C.B.), and Centre for Advanced Microscopy (H.C.), Australian National University, Acton, Australian Capital Territory 2601, Australia;Australian Antarctic Division, Department of Environment, Kingston, Tasmania 7050, Australia (D.M.B.);Center for Molecular and Nanoscale Physics, School of Applied Sciences, RMIT University, Melbourne, Victoria 3001, Australia (G.B.);School of Physics, University of New South Wales, Sydney, New South Wales 2052, Australia (J.W.); andDepartment of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts 02138 (N.M.H.).
authors.forename: Marilyn C
authors.identifier: http://orcid.org/0000-0001-9170-940X
authors.initials: MC
authors.lastname: Ball
mesh_terms: D019661:Apiaceae / Q000033:anatomy & histology / Q000502:physiology* / Q000648:ultrastructure; D001692:Biological Transport / Q000502:physiology; D029748:Caryophyllaceae / Q000033:anatomy & histology / Q000502:physiology* / Q000648:ultrastructure; D002473:Cell Wall / Q000502:physiology / Q000648:ultrastructure; D020285:Cryoelectron Microscopy; D057446:Hydrodynamics; D018613:Microscopy, Confocal; D008855:Microscopy, Electron, Scanning; D018517:Plant Roots / Q000033:anatomy & histology / Q000502:physiology / Q000648:ultrastructure; D018520:Plant Shoots / Q000033:anatomy & histology / Q000502:physiology / Q000648:ultrastructure; D018547:Plant Stems / Q000033:anatomy & histology / Q000502:physiology / Q000648:ultrastructure; D013045:Species Specificity; D014867:Water / Q000378:metabolism*; D052584:Xylem / Q000033:anatomy & histology / Q000502:physiology* / Q000648:ultrastructure
chemical_list: D014867:Water