Comparison of isohydric and anisohydric Vitis vinifera L. cultivars reveals a fine balance between hydraulic resistances, driving forces and transpiration in ripening berries
Johannes Daniel Scharwies A and Stephen Donald Tyerman A B
+ Author Affiliations
- Author Affiliations
A Australian Research Council Centre of Excellence in Plant Energy Biology, School of Agriculture, Food and Wine, Waite Research Institute, University of Adelaide, Glen Osmond, SA 5064, Australia.
B Corresponding author. Email: steve.tyerman@adelaide.edu.au
Functional Plant Biology 44(3) 324-338 https://doi.org/10.1071/FP16010
Submitted: 11 January 2016 Accepted: 1 November 2016 Published: 13 December 2016
Abstract
The degree to which isohydric or anisohydric behaviour extends to the water balance of developing fruits has not previously been explored. Here, we examine the water relations and hydraulic behaviour of Vitis vinifera L. berries during development from two contrasting cultivars that display isohydric (cv. Grenache) or anisohydric (cv. Shiraz) behaviour. Hydraulic resistance normalised to the berry surface area of Grenache clusters was significantly lower and more constant during development, whereas that of Shiraz increased. Lower rachis hydraulic resistance in Grenache compared with Shiraz was inversely related to xylem vessel diameter. Berry transpiration and xylem water uptake measured on detached berries decreased alike during development. From veraison, detached berries of both cultivars showed a transition to a net imbalance between xylem water uptake and transpiration, with Shiraz showing a larger imbalance and berry dehydration towards the end of ripening. In planta, this imbalance must be counterbalanced by a larger phloem water influx in post-veraison berries. Concurrently, the calculated pressure gradients for xylem water uptake showed a decline, which broadly agreed with the measured values. Higher suction for xylem water uptake in pre-veraison berries was mainly generated by transpiration. We conclude that isohydric or anisohydric behaviour is reflected in the contrasting behaviour of fruit hydraulics and that a change from xylem water uptake to phloem import is correlated with the loss of the propensity to generate negative apoplastic pressure in the berry.
Additional keywords: berry shrivel, berry water relations, fruit hydraulic conductance, fruit transpiration, grapevine.
References
Bondada BR, Matthews MA, Shackel KA (2005) Functional xylem in the post-veraison grape berry. Journal of Experimental Botany 56, 2949–2957.| Functional xylem in the post-veraison grape berry.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFCjt7jF&md5=0e8e1569c4842a965a772f0570885c5aCAS |
Chaumont F, Tyerman SD (2014) Aquaporins: highly regulated channels controlling plant water relations. Plant Physiology 164, 1600–1618.
| Aquaporins: highly regulated channels controlling plant water relations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXmsV2jsr4%3D&md5=9280679c4bdf33a07e273d0c68e480d4CAS |
Choat B, Gambetta GA, Shackel KA, Matthews MA (2009) Vascular function in grape berries across development and its relevance to apparent hydraulic isolation. Plant Physiology 151, 1677–1687.
| Vascular function in grape berries across development and its relevance to apparent hydraulic isolation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsVCjsbfJ&md5=fb70ad05415b8f4969160cc93eece8dfCAS |
Clearwater MJ, Luo Z, Ong SE, Blattmann P, Thorp TG (2012) Vascular functioning and the water balance of ripening kiwifruit (Actinidia chinensis) berries. Journal of Experimental Botany 63, 1835–1847.
| Vascular functioning and the water balance of ripening kiwifruit (Actinidia chinensis) berries.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xjslehtrk%3D&md5=9cbbff5aa541dfc5b598c12bac07f275CAS |
Considine JA, Kriedemann PE (1972) Fruit splitting in grapes – determination of critical turgor pressure. Australian Journal of Agricultural Research 23, 17–23.
| Fruit splitting in grapes – determination of critical turgor pressure.Crossref | GoogleScholarGoogle Scholar |
Coombe BG, McCarthy MG (2000) Dynamics of grape berry growth and physiology of ripening. Australian Journal of Grape and Wine Research 6, 131–135.
| Dynamics of grape berry growth and physiology of ripening.Crossref | GoogleScholarGoogle Scholar |
Coupel-Ledru A, Lebon É, Christophe A, Doligez A, Cabrera-Bosquet L, Péchier P, Hamard P, This P, Simonneau T (2014) Genetic variation in a grapevine progeny (Vitis vinifera L. cvs Grenache × Syrah) reveals inconsistencies between maintenance of daytime leaf water potential and response of transpiration rate under drought. Journal of Experimental Botany 65, 6205–6218.
| Genetic variation in a grapevine progeny (Vitis vinifera L. cvs Grenache × Syrah) reveals inconsistencies between maintenance of daytime leaf water potential and response of transpiration rate under drought.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXitl2gsbg%3D&md5=798e3474305aa65992c8c8e6a96dc1ddCAS |
Creasy GL, Price SF, Lombard PB (1993) Evidence for xylem discontinuity in Pinot Noir and Merlot grapes: dye uptake and mineral composition during berry maturation. American Journal of Enology and Viticulture 44, 187–192.
Dai ZW, Vivin P, Barrieu F, Ollat N, Delrot S (2010) Physiological and modelling approaches to understand water and carbon fluxes during grape berry growth and quality development: a review. Australian Journal of Grape and Wine Research 16, 70–85.
| Physiological and modelling approaches to understand water and carbon fluxes during grape berry growth and quality development: a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXislart78%3D&md5=e64fab8b5d650aed28781e2d873bae34CAS |
Edwards WRN, Jarvis PG (1981) A new method of measuring water potential in tree stems by water injection. Plant, Cell & Environment 4, 463–465.
Fuentes S, Sullivan W, Tilbrook J, Tyerman S (2010) A novel analysis of grapevine berry tissue demonstrates a variety-dependent correlation between tissue vitality and berry shrivel. Australian Journal of Grape and Wine Research 16, 327–336.
| A novel analysis of grapevine berry tissue demonstrates a variety-dependent correlation between tissue vitality and berry shrivel.Crossref | GoogleScholarGoogle Scholar |
Gerzon E, Biton I, Yaniv Y, Zemach H, Netzer Y, Schwartz A, Fait A, Ben-Ari G (2015) Grapevine anatomy as a possible determinant of isohydric or anisohydric behavior. American Journal of Enology and Viticulture 66, 340–347.
| Grapevine anatomy as a possible determinant of isohydric or anisohydric behavior.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XnsFeqsbc%3D&md5=7b36185d6f102b9cf8170ad525699e92CAS |
Greenspan MD, Shackel KA, Matthews MA (1994) Developmental changes in the diurnal water budget of the grape berry exposed to water deficits. Plant, Cell & Environment 17, 811–820.
| Developmental changes in the diurnal water budget of the grape berry exposed to water deficits.Crossref | GoogleScholarGoogle Scholar |
Greer DH, Rogiers SY (2009) Water flux of Vitis vinifera L. cv. Shiraz bunches throughout development and in relation to late-season weight loss. American Journal of Enology and Viticulture 60, 155–163.
Hocking B, Tyerman SD, Burton RA, Gilliham M (2016) Fruit calcium: transport and physiology. Frontiers in Plant Science 7,
| Fruit calcium: transport and physiology.Crossref | GoogleScholarGoogle Scholar |
Keller M, Smith JP, Bondada BR (2006) Ripening grape berries remain hydraulically connected to the shoot. Journal of Experimental Botany 57, 2577–2587.
| Ripening grape berries remain hydraulically connected to the shoot.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xotl2mt70%3D&md5=06291a68656ecc18eea5c1926cbb3965CAS |
Keller M, Zhang YUN, Shrestha PM, Biondi M, Bondada BR (2015) Sugar demand of ripening grape berries leads to recycling of surplus phloem water via the xylem. Plant, Cell & Environment 38, 1048–1059.
| Sugar demand of ripening grape berries leads to recycling of surplus phloem water via the xylem.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXotVSmsLg%3D&md5=bf13142d31f41a8d6f3aa3199652bc69CAS |
Knipfer T, Fei J, Gambetta GA, McElrone AJ, Shackel KA, Matthews MA (2015) Water transport properties of the grape pedicel during fruit development: insights into xylem anatomy and function using microtomography. Plant Physiology 168, 1590–1602.
| Water transport properties of the grape pedicel during fruit development: insights into xylem anatomy and function using microtomography.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhsVSrtL%2FI&md5=7ba8753440ad4a4ae79be132a80e8accCAS |
Knoche M, Peschel S, Hinz M, Bukovac MJ (2001) Studies on water transport through the sweet cherry fruit surface: II. Conductance of the cuticle in relation to fruit development. Planta 213, 927–936.
| Studies on water transport through the sweet cherry fruit surface: II. Conductance of the cuticle in relation to fruit development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXotVait7s%3D&md5=2dd7e2063f86c4d24ecb55acf480a75fCAS |
Mazzeo M, Dichio B, Clearwater MJ, Montanaro G, Xiloyannis C (2013) Hydraulic resistance of developing Actinidia fruit. Annals of Botany 112, 197–205.
| Hydraulic resistance of developing Actinidia fruit.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtVCqu7vN&md5=1e1a909f5e4cb247f7b47a9546ba5c5eCAS |
McCarthy MG (1999) Weight loss from ripening berries of Shiraz grapevines (Vitis vinifera L. cv. Shiraz). Australian Journal of Grape and Wine Research 5, 10–16.
| Weight loss from ripening berries of Shiraz grapevines (Vitis vinifera L. cv. Shiraz).Crossref | GoogleScholarGoogle Scholar |
Niimi Y, Torikata H (1979) Changes in photosynthesis and respiration during berry development in relation to the ripening of Delaware grapes. Journal of the Japanese Society for Horticultural Science 47, 448–453.
| Changes in photosynthesis and respiration during berry development in relation to the ripening of Delaware grapes.Crossref | GoogleScholarGoogle Scholar |
Peet MM (1992) Fruit cracking in tomato. HortTechnology 2, 216–219, 222–223.
Rogiers SY, Smith JA, White R, Keller M, Holzapfel BP, Virgona JM (2001) Vascular function in berries of Vitis vinifera (L) cv. Shiraz. Australian Journal of Grape and Wine Research 7, 47–51.
| Vascular function in berries of Vitis vinifera (L) cv. Shiraz.Crossref | GoogleScholarGoogle Scholar |
Rogiers SY, Hatfield JM, Jaudzems VG, White RG, Keller M (2004) Grape berry cv. Shiraz epicuticular wax and transpiration during ripening and preharvest weight loss. American Journal of Enology and Viticulture 55, 121–127.
Rogiers SY, Greer DH, Hatfield JM, Orchard BA, Keller M (2006) Solute transport into Shiraz berries during development and late-ripening shrinkage. American Journal of Enology and Viticulture 57, 73–80.
Sack L, Holbrook NM (2006) Leaf hydraulics. Annual Review of Plant Biology 57, 361–381.
| Leaf hydraulics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XosVKhtrs%3D&md5=f7445993b3921033fee6db1a9edd7ae6CAS |
Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nature Methods 9, 671–675.
| NIH Image to ImageJ: 25 years of image analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVKntb7P&md5=71447d5ca15dc8993428944031d55206CAS |
Schultz HR (2003) Differences in hydraulic architecture account for near-isohydric and anisohydric behaviour of two field-grown Vitis vinifera L. cultivars during drought. Plant, Cell & Environment 26, 1393–1405.
| Differences in hydraulic architecture account for near-isohydric and anisohydric behaviour of two field-grown Vitis vinifera L. cultivars during drought.Crossref | GoogleScholarGoogle Scholar |
Sperry JS, Nichols KL, Sullivan JEM, Eastlack SE (1994) Xylem embolism in ring-porous, diffuse-porous, and coniferous trees of northern Utah and interior Alaska. Ecology 75, 1736–1752.
| Xylem embolism in ring-porous, diffuse-porous, and coniferous trees of northern Utah and interior Alaska.Crossref | GoogleScholarGoogle Scholar |
Thomas TR, Shackel KA, Matthews MA (2008) Mesocarp cell turgor in Vitis vinifera L. berries throughout development and its relation to firmness, growth, and the onset of ripening. Planta 228, 1067–1076.
| Mesocarp cell turgor in Vitis vinifera L. berries throughout development and its relation to firmness, growth, and the onset of ripening.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlCkt73M&md5=a1da0aec8db6c5701ce5a688a0d7ad42CAS |
Thorp TG, Clearwater MJ, Barnett AM, Martin PJ, Blattmann PJ, Currie MB (2007) ‘Hort16A’ fruit beak end softening and shrivelling in California. Acta Horticulturae 753, 389–396.
| ‘Hort16A’ fruit beak end softening and shrivelling in California.Crossref | GoogleScholarGoogle Scholar |
Tilbrook J, Tyerman SD (2008) Cell death in grape berries: varietal differences linked to xylem pressure and berry weight loss. Functional Plant Biology 35, 173–184.
| Cell death in grape berries: varietal differences linked to xylem pressure and berry weight loss.Crossref | GoogleScholarGoogle Scholar |
Tilbrook J, Tyerman SD (2009) Hydraulic connection of grape berries to the vine: varietal differences in water conductance into and out of berries, and potential for backflow. Functional Plant Biology 36, 541–550.
| Hydraulic connection of grape berries to the vine: varietal differences in water conductance into and out of berries, and potential for backflow.Crossref | GoogleScholarGoogle Scholar |
Tsuda M, Tyree MT (2000) Plant hydraulic conductance measured by the high pressure flow meter in crop plants. Journal of Experimental Botany 51, 823–828.
| Plant hydraulic conductance measured by the high pressure flow meter in crop plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjtF2jsLY%3D&md5=5138420ea55ee4809de1eb365b369e4cCAS |
Tyerman SD, Tilbrook J, Pardo C, Kotula L, Sullivan W, Steudle E (2004) Direct measurement of hydraulic properties in developing berries of Vitis vinifera L. cv Shiraz and Chardonnay. Australian Journal of Grape and Wine Research 10, 170–181.
| Direct measurement of hydraulic properties in developing berries of Vitis vinifera L. cv Shiraz and Chardonnay.Crossref | GoogleScholarGoogle Scholar |
Tyree MT, Patiño S, Bennink J, Alexander J (1995) Dynamic measurements of roots hydraulic conductance using a high-pressure flowmeter in the laboratory and field. Journal of Experimental Botany 46, 83–94.
| Dynamic measurements of roots hydraulic conductance using a high-pressure flowmeter in the laboratory and field.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXjslKiu7o%3D&md5=d1ecc9646026c2b7bfd0df4458971fb4CAS |
Van Ieperen W, Volkov VS, Van Meeteren U (2003) Distribution of xylem hydraulic resistance in fruiting truss of tomato influenced by water stress. Journal of Experimental Botany 54, 317–324.
| Distribution of xylem hydraulic resistance in fruiting truss of tomato influenced by water stress.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3s%2FksFOqsA%3D%3D&md5=e236707267d6dd33af347e33fdf6b7e5CAS |
Vandeleur RK, Mayo G, Shelden MC, Gilliham M, Kaiser BN, Tyerman SD (2009) The role of plasma membrane intrinsic protein aquaporins in water transport through roots: diurnal and drought stress responses reveal different strategies between isohydric and anisohydric cultivars of grapevine. Plant Physiology 149, 445–460.
| The role of plasma membrane intrinsic protein aquaporins in water transport through roots: diurnal and drought stress responses reveal different strategies between isohydric and anisohydric cultivars of grapevine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjt1WqtL8%3D&md5=b8f574eecf3f1de919d4134424cc6732CAS |
Windt CW, Gerkema E, Van As H (2009) Most water in the tomato truss is imported through the xylem, not the phloem: a nuclear magnetic resonance flow imaging study. Plant Physiology 151, 830–842.
| Most water in the tomato truss is imported through the xylem, not the phloem: a nuclear magnetic resonance flow imaging study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlSjsr%2FP&md5=0c83cdd790551d0398ed19ac95cbd97aCAS |
Zhang Y, Keller M (2015) Grape berry transpiration is determined by vapor pressure deficit, cuticular conductance, and berry size. American Journal of Enology and Viticulture 66, 454–462.
| Grape berry transpiration is determined by vapor pressure deficit, cuticular conductance, and berry size.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XnvVOluro%3D&md5=230cc9373a63ccb7647cb73c9ba12346CAS |
Zhang DP, Zhang XY, Wang XL, Wang XF, Xia GH, Pan QH, Fan RC, Wu FQ, Yu XC (2006) A shift of phloem unloading from symplasmic to apoplasmic pathway is involved in developmental onset of ripening in grape berry. Plant Physiology 142, 220–232.
| A shift of phloem unloading from symplasmic to apoplasmic pathway is involved in developmental onset of ripening in grape berry.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XpvVKhsrc%3D&md5=f516e5c44060dc522dd0371b5466d31cCAS |
