Evidence for Hydraulic Vulnerability Segmentation and Lack of Xylem Refilling under Tension.
The vascular system of grapevine (Vitis spp.) has been reported as being highly vulnerable, even though grapevine regularly experiences seasonal drought. Consequently, stomata would remain open below water potentials that would generate a high loss of stem hydraulic conductivity via xylem embolism. This situation would necessitate daily cycles of embolism repair to restore hydraulic function. However, a more parsimonious explanation is that some hydraulic techniques are prone to artifacts in species with long vessels, leading to the overestimation of vulnerability. The aim of this study was to provide an unbiased assessment of (1) the vulnerability to drought-induced embolism in perennial and annual organs and (2) the ability to refill embolized vessels in two Vitis species X-ray micro-computed tomography observations of intact plants indicated that both Vitis vinifera and Vitis riparia were relatively vulnerable, with the pressure inducing 50% loss of stem hydraulic conductivity = -1.7 and -1.3 MPa, respectively. In V. vinifera, both the stem and petiole had similar sigmoidal vulnerability curves but differed in pressure inducing 50% loss of hydraulic conductivity (-1.7 and -1 MPa for stem and petiole, respectively). Refilling was not observed as long as bulk xylem pressure remained negative (e.g. at the apical part of the plants; -0.11 ± 0.02 MPa) and change in percentage loss of conductivity was 0.02% ± 0.01%. However, positive xylem pressure was observed at the basal part of the plant (0.04 ± 0.01 MPa), leading to a recovery of conductance (change in percentage loss of conductivity = -0.24% ± 0.12%). Our findings provide evidence that grapevine is unable to repair embolized xylem vessels under negative pressure, but its hydraulic vulnerability segmentation provides significant protection of the perennial stem.
Bordeaux Sciences Agro, Institut des Sciences de la Vigne et du Vin, Ecophysiologie et Génomique Fonctionnelle de la Vigne, Unité Mixte de Recherche 1287, F-33140 Villenave d'Ornon, France (G.C., G.A.G.); BIOGECO, INRA, Univ. Bordeaux, 33610 Cestas, France (G.C., J.M.T.-R., R.B., S.D.); PIAF, Institut National de la Recherche Agronomique, UCA, 63000 Clermont-Ferrand, France (E.B., H.C.); Hawkesbury Institute for the Environment, Western Sydney University, Richmond, New South Wales 2753, Australia (B.C.); Unité Mixte de Recherche SAVE, INRA, BSA, Univ. Bordeaux, 33882 Villenave d'Ornon, France (C.E.L.D.); Bordeaux Sciences Agro, Unité Mixte de Recherche 1391 ISPA, F-33882 Villenave d'Ornon, France (J.-C.D.); Nicholas School of the Environment, Duke University, Durham, North Carolina 27708 (J.-C.D.); Institute of Systematic Botany and Ecology, Ulm University, Ulm D-89081, Germany (S.J.); Synchrotron SOLEIL, L'Orme de Merisiers, Saint Aubin-BP48, 91192 Gif-sur-Yvette cedex, France (A.K.); Centre National de la Recherche Scientifique, Univ. Bordeaux, UMS 3626 Placamat F-33608 Pessac, France (N.L.); and INRA, UR629 Ecologie des Forêts Méditerranéennes, 84914 Avignon, France (N.M.-S.) guillaume.charrier@bordeaux.inra.fr.
Guillaume
G
Charrier
Bordeaux Sciences Agro, Institut des Sciences de la Vigne et du Vin, Ecophysiologie et Génomique Fonctionnelle de la Vigne, Unité Mixte de Recherche 1287, F-33140 Villenave d'Ornon, France (G.C., G.A.G.); BIOGECO, INRA, Univ. Bordeaux, 33610 Cestas, France (G.C., J.M.T.-R., R.B., S.D.); PIAF, Institut National de la Recherche Agronomique, UCA, 63000 Clermont-Ferrand, France (E.B., H.C.); Hawkesbury Institute for the Environment, Western Sydney University, Richmond, New South Wales 2753, Australia (B.C.); Unité Mixte de Recherche SAVE, INRA, BSA, Univ. Bordeaux, 33882 Villenave d'Ornon, France (C.E.L.D.); Bordeaux Sciences Agro, Unité Mixte de Recherche 1391 ISPA, F-33882 Villenave d'Ornon, France (J.-C.D.); Nicholas School of the Environment, Duke University, Durham, North Carolina 27708 (J.-C.D.); Institute of Systematic Botany and Ecology, Ulm University, Ulm D-89081, Germany (S.J.); Synchrotron SOLEIL, L'Orme de Merisiers, Saint Aubin-BP48, 91192 Gif-sur-Yvette cedex, France (A.K.); Centre National de la Recherche Scientifique, Univ. Bordeaux, UMS 3626 Placamat F-33608 Pessac, France (N.L.); and INRA, UR629 Ecologie des Forêts Méditerranéennes, 84914 Avignon, France (N.M.-S.).
José M
0000-0003-1367-7056
JM
Torres-Ruiz
Bordeaux Sciences Agro, Institut des Sciences de la Vigne et du Vin, Ecophysiologie et Génomique Fonctionnelle de la Vigne, Unité Mixte de Recherche 1287, F-33140 Villenave d'Ornon, France (G.C., G.A.G.); BIOGECO, INRA, Univ. Bordeaux, 33610 Cestas, France (G.C., J.M.T.-R., R.B., S.D.); PIAF, Institut National de la Recherche Agronomique, UCA, 63000 Clermont-Ferrand, France (E.B., H.C.); Hawkesbury Institute for the Environment, Western Sydney University, Richmond, New South Wales 2753, Australia (B.C.); Unité Mixte de Recherche SAVE, INRA, BSA, Univ. Bordeaux, 33882 Villenave d'Ornon, France (C.E.L.D.); Bordeaux Sciences Agro, Unité Mixte de Recherche 1391 ISPA, F-33882 Villenave d'Ornon, France (J.-C.D.); Nicholas School of the Environment, Duke University, Durham, North Carolina 27708 (J.-C.D.); Institute of Systematic Botany and Ecology, Ulm University, Ulm D-89081, Germany (S.J.); Synchrotron SOLEIL, L'Orme de Merisiers, Saint Aubin-BP48, 91192 Gif-sur-Yvette cedex, France (A.K.); Centre National de la Recherche Scientifique, Univ. Bordeaux, UMS 3626 Placamat F-33608 Pessac, France (N.L.); and INRA, UR629 Ecologie des Forêts Méditerranéennes, 84914 Avignon, France (N.M.-S.).
Eric
0000-0003-2282-7554
E
Badel
Bordeaux Sciences Agro, Institut des Sciences de la Vigne et du Vin, Ecophysiologie et Génomique Fonctionnelle de la Vigne, Unité Mixte de Recherche 1287, F-33140 Villenave d'Ornon, France (G.C., G.A.G.); BIOGECO, INRA, Univ. Bordeaux, 33610 Cestas, France (G.C., J.M.T.-R., R.B., S.D.); PIAF, Institut National de la Recherche Agronomique, UCA, 63000 Clermont-Ferrand, France (E.B., H.C.); Hawkesbury Institute for the Environment, Western Sydney University, Richmond, New South Wales 2753, Australia (B.C.); Unité Mixte de Recherche SAVE, INRA, BSA, Univ. Bordeaux, 33882 Villenave d'Ornon, France (C.E.L.D.); Bordeaux Sciences Agro, Unité Mixte de Recherche 1391 ISPA, F-33882 Villenave d'Ornon, France (J.-C.D.); Nicholas School of the Environment, Duke University, Durham, North Carolina 27708 (J.-C.D.); Institute of Systematic Botany and Ecology, Ulm University, Ulm D-89081, Germany (S.J.); Synchrotron SOLEIL, L'Orme de Merisiers, Saint Aubin-BP48, 91192 Gif-sur-Yvette cedex, France (A.K.); Centre National de la Recherche Scientifique, Univ. Bordeaux, UMS 3626 Placamat F-33608 Pessac, France (N.L.); and INRA, UR629 Ecologie des Forêts Méditerranéennes, 84914 Avignon, France (N.M.-S.).
Regis
0000-0001-8289-5757
R
Burlett
Bordeaux Sciences Agro, Institut des Sciences de la Vigne et du Vin, Ecophysiologie et Génomique Fonctionnelle de la Vigne, Unité Mixte de Recherche 1287, F-33140 Villenave d'Ornon, France (G.C., G.A.G.); BIOGECO, INRA, Univ. Bordeaux, 33610 Cestas, France (G.C., J.M.T.-R., R.B., S.D.); PIAF, Institut National de la Recherche Agronomique, UCA, 63000 Clermont-Ferrand, France (E.B., H.C.); Hawkesbury Institute for the Environment, Western Sydney University, Richmond, New South Wales 2753, Australia (B.C.); Unité Mixte de Recherche SAVE, INRA, BSA, Univ. Bordeaux, 33882 Villenave d'Ornon, France (C.E.L.D.); Bordeaux Sciences Agro, Unité Mixte de Recherche 1391 ISPA, F-33882 Villenave d'Ornon, France (J.-C.D.); Nicholas School of the Environment, Duke University, Durham, North Carolina 27708 (J.-C.D.); Institute of Systematic Botany and Ecology, Ulm University, Ulm D-89081, Germany (S.J.); Synchrotron SOLEIL, L'Orme de Merisiers, Saint Aubin-BP48, 91192 Gif-sur-Yvette cedex, France (A.K.); Centre National de la Recherche Scientifique, Univ. Bordeaux, UMS 3626 Placamat F-33608 Pessac, France (N.L.); and INRA, UR629 Ecologie des Forêts Méditerranéennes, 84914 Avignon, France (N.M.-S.).
Brendan
B
Choat
Bordeaux Sciences Agro, Institut des Sciences de la Vigne et du Vin, Ecophysiologie et Génomique Fonctionnelle de la Vigne, Unité Mixte de Recherche 1287, F-33140 Villenave d'Ornon, France (G.C., G.A.G.); BIOGECO, INRA, Univ. Bordeaux, 33610 Cestas, France (G.C., J.M.T.-R., R.B., S.D.); PIAF, Institut National de la Recherche Agronomique, UCA, 63000 Clermont-Ferrand, France (E.B., H.C.); Hawkesbury Institute for the Environment, Western Sydney University, Richmond, New South Wales 2753, Australia (B.C.); Unité Mixte de Recherche SAVE, INRA, BSA, Univ. Bordeaux, 33882 Villenave d'Ornon, France (C.E.L.D.); Bordeaux Sciences Agro, Unité Mixte de Recherche 1391 ISPA, F-33882 Villenave d'Ornon, France (J.-C.D.); Nicholas School of the Environment, Duke University, Durham, North Carolina 27708 (J.-C.D.); Institute of Systematic Botany and Ecology, Ulm University, Ulm D-89081, Germany (S.J.); Synchrotron SOLEIL, L'Orme de Merisiers, Saint Aubin-BP48, 91192 Gif-sur-Yvette cedex, France (A.K.); Centre National de la Recherche Scientifique, Univ. Bordeaux, UMS 3626 Placamat F-33608 Pessac, France (N.L.); and INRA, UR629 Ecologie des Forêts Méditerranéennes, 84914 Avignon, France (N.M.-S.).
Herve
0000-0002-2727-7072
H
Cochard
Bordeaux Sciences Agro, Institut des Sciences de la Vigne et du Vin, Ecophysiologie et Génomique Fonctionnelle de la Vigne, Unité Mixte de Recherche 1287, F-33140 Villenave d'Ornon, France (G.C., G.A.G.); BIOGECO, INRA, Univ. Bordeaux, 33610 Cestas, France (G.C., J.M.T.-R., R.B., S.D.); PIAF, Institut National de la Recherche Agronomique, UCA, 63000 Clermont-Ferrand, France (E.B., H.C.); Hawkesbury Institute for the Environment, Western Sydney University, Richmond, New South Wales 2753, Australia (B.C.); Unité Mixte de Recherche SAVE, INRA, BSA, Univ. Bordeaux, 33882 Villenave d'Ornon, France (C.E.L.D.); Bordeaux Sciences Agro, Unité Mixte de Recherche 1391 ISPA, F-33882 Villenave d'Ornon, France (J.-C.D.); Nicholas School of the Environment, Duke University, Durham, North Carolina 27708 (J.-C.D.); Institute of Systematic Botany and Ecology, Ulm University, Ulm D-89081, Germany (S.J.); Synchrotron SOLEIL, L'Orme de Merisiers, Saint Aubin-BP48, 91192 Gif-sur-Yvette cedex, France (A.K.); Centre National de la Recherche Scientifique, Univ. Bordeaux, UMS 3626 Placamat F-33608 Pessac, France (N.L.); and INRA, UR629 Ecologie des Forêts Méditerranéennes, 84914 Avignon, France (N.M.-S.).
Chloe E L
CE
Delmas
Bordeaux Sciences Agro, Institut des Sciences de la Vigne et du Vin, Ecophysiologie et Génomique Fonctionnelle de la Vigne, Unité Mixte de Recherche 1287, F-33140 Villenave d'Ornon, France (G.C., G.A.G.); BIOGECO, INRA, Univ. Bordeaux, 33610 Cestas, France (G.C., J.M.T.-R., R.B., S.D.); PIAF, Institut National de la Recherche Agronomique, UCA, 63000 Clermont-Ferrand, France (E.B., H.C.); Hawkesbury Institute for the Environment, Western Sydney University, Richmond, New South Wales 2753, Australia (B.C.); Unité Mixte de Recherche SAVE, INRA, BSA, Univ. Bordeaux, 33882 Villenave d'Ornon, France (C.E.L.D.); Bordeaux Sciences Agro, Unité Mixte de Recherche 1391 ISPA, F-33882 Villenave d'Ornon, France (J.-C.D.); Nicholas School of the Environment, Duke University, Durham, North Carolina 27708 (J.-C.D.); Institute of Systematic Botany and Ecology, Ulm University, Ulm D-89081, Germany (S.J.); Synchrotron SOLEIL, L'Orme de Merisiers, Saint Aubin-BP48, 91192 Gif-sur-Yvette cedex, France (A.K.); Centre National de la Recherche Scientifique, Univ. Bordeaux, UMS 3626 Placamat F-33608 Pessac, France (N.L.); and INRA, UR629 Ecologie des Forêts Méditerranéennes, 84914 Avignon, France (N.M.-S.).
Jean-Christophe
JC
Domec
Bordeaux Sciences Agro, Institut des Sciences de la Vigne et du Vin, Ecophysiologie et Génomique Fonctionnelle de la Vigne, Unité Mixte de Recherche 1287, F-33140 Villenave d'Ornon, France (G.C., G.A.G.); BIOGECO, INRA, Univ. Bordeaux, 33610 Cestas, France (G.C., J.M.T.-R., R.B., S.D.); PIAF, Institut National de la Recherche Agronomique, UCA, 63000 Clermont-Ferrand, France (E.B., H.C.); Hawkesbury Institute for the Environment, Western Sydney University, Richmond, New South Wales 2753, Australia (B.C.); Unité Mixte de Recherche SAVE, INRA, BSA, Univ. Bordeaux, 33882 Villenave d'Ornon, France (C.E.L.D.); Bordeaux Sciences Agro, Unité Mixte de Recherche 1391 ISPA, F-33882 Villenave d'Ornon, France (J.-C.D.); Nicholas School of the Environment, Duke University, Durham, North Carolina 27708 (J.-C.D.); Institute of Systematic Botany and Ecology, Ulm University, Ulm D-89081, Germany (S.J.); Synchrotron SOLEIL, L'Orme de Merisiers, Saint Aubin-BP48, 91192 Gif-sur-Yvette cedex, France (A.K.); Centre National de la Recherche Scientifique, Univ. Bordeaux, UMS 3626 Placamat F-33608 Pessac, France (N.L.); and INRA, UR629 Ecologie des Forêts Méditerranéennes, 84914 Avignon, France (N.M.-S.).
Steven
0000-0002-4476-5334
S
Jansen
Bordeaux Sciences Agro, Institut des Sciences de la Vigne et du Vin, Ecophysiologie et Génomique Fonctionnelle de la Vigne, Unité Mixte de Recherche 1287, F-33140 Villenave d'Ornon, France (G.C., G.A.G.); BIOGECO, INRA, Univ. Bordeaux, 33610 Cestas, France (G.C., J.M.T.-R., R.B., S.D.); PIAF, Institut National de la Recherche Agronomique, UCA, 63000 Clermont-Ferrand, France (E.B., H.C.); Hawkesbury Institute for the Environment, Western Sydney University, Richmond, New South Wales 2753, Australia (B.C.); Unité Mixte de Recherche SAVE, INRA, BSA, Univ. Bordeaux, 33882 Villenave d'Ornon, France (C.E.L.D.); Bordeaux Sciences Agro, Unité Mixte de Recherche 1391 ISPA, F-33882 Villenave d'Ornon, France (J.-C.D.); Nicholas School of the Environment, Duke University, Durham, North Carolina 27708 (J.-C.D.); Institute of Systematic Botany and Ecology, Ulm University, Ulm D-89081, Germany (S.J.); Synchrotron SOLEIL, L'Orme de Merisiers, Saint Aubin-BP48, 91192 Gif-sur-Yvette cedex, France (A.K.); Centre National de la Recherche Scientifique, Univ. Bordeaux, UMS 3626 Placamat F-33608 Pessac, France (N.L.); and INRA, UR629 Ecologie des Forêts Méditerranéennes, 84914 Avignon, France (N.M.-S.).
Andrew
A
King
Bordeaux Sciences Agro, Institut des Sciences de la Vigne et du Vin, Ecophysiologie et Génomique Fonctionnelle de la Vigne, Unité Mixte de Recherche 1287, F-33140 Villenave d'Ornon, France (G.C., G.A.G.); BIOGECO, INRA, Univ. Bordeaux, 33610 Cestas, France (G.C., J.M.T.-R., R.B., S.D.); PIAF, Institut National de la Recherche Agronomique, UCA, 63000 Clermont-Ferrand, France (E.B., H.C.); Hawkesbury Institute for the Environment, Western Sydney University, Richmond, New South Wales 2753, Australia (B.C.); Unité Mixte de Recherche SAVE, INRA, BSA, Univ. Bordeaux, 33882 Villenave d'Ornon, France (C.E.L.D.); Bordeaux Sciences Agro, Unité Mixte de Recherche 1391 ISPA, F-33882 Villenave d'Ornon, France (J.-C.D.); Nicholas School of the Environment, Duke University, Durham, North Carolina 27708 (J.-C.D.); Institute of Systematic Botany and Ecology, Ulm University, Ulm D-89081, Germany (S.J.); Synchrotron SOLEIL, L'Orme de Merisiers, Saint Aubin-BP48, 91192 Gif-sur-Yvette cedex, France (A.K.); Centre National de la Recherche Scientifique, Univ. Bordeaux, UMS 3626 Placamat F-33608 Pessac, France (N.L.); and INRA, UR629 Ecologie des Forêts Méditerranéennes, 84914 Avignon, France (N.M.-S.).
Nicolas
N
Lenoir
Bordeaux Sciences Agro, Institut des Sciences de la Vigne et du Vin, Ecophysiologie et Génomique Fonctionnelle de la Vigne, Unité Mixte de Recherche 1287, F-33140 Villenave d'Ornon, France (G.C., G.A.G.); BIOGECO, INRA, Univ. Bordeaux, 33610 Cestas, France (G.C., J.M.T.-R., R.B., S.D.); PIAF, Institut National de la Recherche Agronomique, UCA, 63000 Clermont-Ferrand, France (E.B., H.C.); Hawkesbury Institute for the Environment, Western Sydney University, Richmond, New South Wales 2753, Australia (B.C.); Unité Mixte de Recherche SAVE, INRA, BSA, Univ. Bordeaux, 33882 Villenave d'Ornon, France (C.E.L.D.); Bordeaux Sciences Agro, Unité Mixte de Recherche 1391 ISPA, F-33882 Villenave d'Ornon, France (J.-C.D.); Nicholas School of the Environment, Duke University, Durham, North Carolina 27708 (J.-C.D.); Institute of Systematic Botany and Ecology, Ulm University, Ulm D-89081, Germany (S.J.); Synchrotron SOLEIL, L'Orme de Merisiers, Saint Aubin-BP48, 91192 Gif-sur-Yvette cedex, France (A.K.); Centre National de la Recherche Scientifique, Univ. Bordeaux, UMS 3626 Placamat F-33608 Pessac, France (N.L.); and INRA, UR629 Ecologie des Forêts Méditerranéennes, 84914 Avignon, France (N.M.-S.).
Nicolas
0000-0001-7574-0108
N
Martin-StPaul
Bordeaux Sciences Agro, Institut des Sciences de la Vigne et du Vin, Ecophysiologie et Génomique Fonctionnelle de la Vigne, Unité Mixte de Recherche 1287, F-33140 Villenave d'Ornon, France (G.C., G.A.G.); BIOGECO, INRA, Univ. Bordeaux, 33610 Cestas, France (G.C., J.M.T.-R., R.B., S.D.); PIAF, Institut National de la Recherche Agronomique, UCA, 63000 Clermont-Ferrand, France (E.B., H.C.); Hawkesbury Institute for the Environment, Western Sydney University, Richmond, New South Wales 2753, Australia (B.C.); Unité Mixte de Recherche SAVE, INRA, BSA, Univ. Bordeaux, 33882 Villenave d'Ornon, France (C.E.L.D.); Bordeaux Sciences Agro, Unité Mixte de Recherche 1391 ISPA, F-33882 Villenave d'Ornon, France (J.-C.D.); Nicholas School of the Environment, Duke University, Durham, North Carolina 27708 (J.-C.D.); Institute of Systematic Botany and Ecology, Ulm University, Ulm D-89081, Germany (S.J.); Synchrotron SOLEIL, L'Orme de Merisiers, Saint Aubin-BP48, 91192 Gif-sur-Yvette cedex, France (A.K.); Centre National de la Recherche Scientifique, Univ. Bordeaux, UMS 3626 Placamat F-33608 Pessac, France (N.L.); and INRA, UR629 Ecologie des Forêts Méditerranéennes, 84914 Avignon, France (N.M.-S.).
Gregory Alan
0000-0002-8838-5050
GA
Gambetta
Bordeaux Sciences Agro, Institut des Sciences de la Vigne et du Vin, Ecophysiologie et Génomique Fonctionnelle de la Vigne, Unité Mixte de Recherche 1287, F-33140 Villenave d'Ornon, France (G.C., G.A.G.); BIOGECO, INRA, Univ. Bordeaux, 33610 Cestas, France (G.C., J.M.T.-R., R.B., S.D.); PIAF, Institut National de la Recherche Agronomique, UCA, 63000 Clermont-Ferrand, France (E.B., H.C.); Hawkesbury Institute for the Environment, Western Sydney University, Richmond, New South Wales 2753, Australia (B.C.); Unité Mixte de Recherche SAVE, INRA, BSA, Univ. Bordeaux, 33882 Villenave d'Ornon, France (C.E.L.D.); Bordeaux Sciences Agro, Unité Mixte de Recherche 1391 ISPA, F-33882 Villenave d'Ornon, France (J.-C.D.); Nicholas School of the Environment, Duke University, Durham, North Carolina 27708 (J.-C.D.); Institute of Systematic Botany and Ecology, Ulm University, Ulm D-89081, Germany (S.J.); Synchrotron SOLEIL, L'Orme de Merisiers, Saint Aubin-BP48, 91192 Gif-sur-Yvette cedex, France (A.K.); Centre National de la Recherche Scientifique, Univ. Bordeaux, UMS 3626 Placamat F-33608 Pessac, France (N.L.); and INRA, UR629 Ecologie des Forêts Méditerranéennes, 84914 Avignon, France (N.M.-S.).
Sylvain
0000-0003-3442-1711
S
Delzon
D001696:Biomechanical Phenomena; D005740:Gases / Q000378:metabolism; D018515:Plant Leaves / Q000502:physiology; D018547:Plant Stems / Q000502:physiology; D027843:Vitis / Q000166:cytology / Q000502:physiology*; D014867:Water / Q000502:physiology*; D055114:X-Ray Microtomography; D052584:Xylem / Q000502:physiology*
D005740:Gases; D014867:Water