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PMID: 27613852 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Evidence for Hydraulic Vulnerability Segmentation and Lack of Xylem Refilling under Tension.

Plant physiology ·Vol. 172 ·No. 3 ·2016-00-00 ·Pages 1657-1668

Charrier G, Torres-Ruiz JM, Badel E, Burlett R, Choat B, Cochard H, Delmas CE, Domec JC, Jansen S, King A, Lenoir N, Martin-StPaul N, Gambetta GA, Delzon S

Abstract

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.

MeSH Terms
Biomechanical Phenomena Gases/metabolism Plant Leaves/physiology Plant Stems/physiology Vitis/cytology,physiology Water/physiology X-Ray Microtomography Xylem/physiology
Chemicals
Gases Water
Authors & Affiliations
14 authors, click to expand affiliations / ORCID
Charrier Guillaume
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.
Torres-Ruiz José M ORCID
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.).
Badel Eric ORCID
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.).
Burlett Regis ORCID
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.).
Choat Brendan
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.).
Cochard Herve ORCID
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.).
Delmas Chloe E L
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.).
Domec Jean-Christophe
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.).
Jansen Steven ORCID
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.).
King Andrew
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.).
Lenoir Nicolas
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.).
Martin-StPaul Nicolas ORCID
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.).
Gambetta Gregory Alan ORCID
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.).
Delzon Sylvain ORCID
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.).
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Article Info
Journal
Plant physiology
Abbr.
Plant Physiol
ISSN
1532-2548
DOI
10.1104/pp.16.01079
Email
guillaume.charrier@bordeaux.inra.fr
Published
2016-00-00
Epub
2016-00-09
Pages
1657-1668
Language
English
Region
United States
NLM ID
0401224
PMCID
PMC5100766
Subset
IM
External Links
PubMed source DOI: 10.1104/pp.16.01079 PMC Full Text View journal details
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