Hydraulic connection of grape berries to the vine: varietal differences in water conductance into and out of berries, and potential for backflow
Joanne Tilbrook A B and Stephen D. Tyerman A B CA Cooperative Research Centre for Viticulture, PO Box 154, Glen Osmond, SA 5064, Australia.
B School of Agriculture, Food and Wine, University of Adelaide, Glen Osmond, SA 5064, Australia.
C Corresponding author. Email: steve.tyerman@adelaide.edu.au
Functional Plant Biology 36(6) 541-550 https://doi.org/10.1071/FP09019
Submitted: 20 January 2009 Accepted: 16 April 2009 Published: 1 June 2009
Abstract
Weight loss in Vitis vinifera L. cv. Shiraz berries occurs in the later stages of ripening from 90–100 days after anthesis (DAA). This rarely occurs in varieties such as Chardonnay and Thompson seedless. Flow rates of water under a constant pressure into berries on detached bunches of these varieties are similar until 90–100 DAA. Shiraz berries then maintain constant flow rates until harvest maturity, and Chardonnay inflow tapers to almost zero. Thompson seedless maintains high xylem inflows. Hydraulic conductance for flow in and out of individual Shiraz and Chardonnay berries was measured using a root pressure probe. From 105 DAA, during berry weight loss in Shiraz, there were significant varietal differences in xylem hydraulic conductance. Both varieties showed flow rectification such that conductance for inflow was higher than conductance for outflow. For flow into the berry, Chardonnay had 14% of the conductance of Shiraz. For flow out of the berry Chardonnay was 4% of the conductance of Shiraz. From conductance measurements for outflow from the berry and stem water potential measurements, it was calculated that Shiraz could loose ~7% of berry volume per day, consistent with rates of berry weight loss. A functional pathway for backflow from the berries to the vine via the xylem was visualised with Lucifer Yellow CH loaded at the cut stylar end of berries on potted vines. Transport of the dye out of the berry xylem ceased before 97 DAA in Chardonnay, but was still transported into the torus and pedicel xylem of Shiraz at 118 DAA. Xylem backflow could be responsible for a portion of the post-veraison weight loss in Shiraz berries. These data provide evidence of varietal differences in hydraulic connection of berries to the vine that we relate to cell vitality in the mesocarp. The key determinates of berry water relations appear to be maintenance or otherwise of semi permeable membranes in the mesocarp cells and control of flow to the xylem to give variable hydraulic connection back to the vine.
Additional keywords: berry ripening, berry shrivel, berry xylem, flow meter, hydraulic conductance, pressure probe, Vitis vinifera.
Bondada BR,
Matthews MA, Shackel KA
(2005) Functional xylem in the post-veraison grape berry. Journal of Experimental Botany 56, 2949–2957.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Brummell DA,
Dal Cin V,
Crisosto C, Labavitch J
(2004) Cell wall metabolism during maturation, ripening and senescence of peach fruit. Journal of Experimental Botany 55, 2029–2039.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Chatelet DS,
Rost TL,
Shackel KA, Matthews MA
(2008) The peripheral xylem of grapevine (Vitis vinifera). 1. Structural integrity in post-veraison berries. Journal of Experimental Botany 59, 1987–1996.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Cochard H,
Bodet C,
Améglio T, Cruiziat P
(2000) Cryo-scanning electron microscopy observations of vessel content during transpiration in walnut petioles. Facts or artefacts? Plant Physiology 124, 1191–1202.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Coombe BG, Bishop GR
(1980) Development of the grape berry. II. Changes in diameter and deformability during veraison. Australian Journal of Agricultural Research 31, 499–509.
| Crossref | GoogleScholarGoogle Scholar |
Creasy G,
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.
|
CAS |
Dreier LP,
Stoll GS, Ruffner HP
(2000) Berry ripening and evapotranspiration in Vitis vinifera L. American Journal of Enology and Viticulture 51, 340–346.
Findlay N,
Oliver KJ,
Nii N, Coombe BG
(1987) Solute accumulation by grape pericarp cells. Journal of Experimental Botany 38, 668–679.
| Crossref | GoogleScholarGoogle Scholar |
Greenspan MD,
Shackel KD, Matthews MA
(1994) Developmental changes in the diurnal water budget of the grape berry exposed to water deficits. Plant, Cell & Environment 17, 811–820.
| Crossref | GoogleScholarGoogle Scholar |
Greenspan MD,
Schultz HR, Matthews MA
(1996) Field evaluation of water transport in grape berries during water deficits. Physiologia Plantarum 97, 55–62.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Keller M,
Smith JP, Bondada BR
(2006) Ripening grape berries remain hydraulically connected to the shoot. Journal of Experimental Botany 57, 2577–2587.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Krasnow M,
Matthews M, Shackel K
(2008) Evidence for substantial maintenance of membrane integrity and cell viability in normally developing grape (Vitis vinifera L.) berries throughout development. Journal of Experimental Botany 59, 849–859.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Lang A, Thorpe M
(1986) Water potential, translocation and assimilate partitioning. Journal of Experimental Botany 37, 495–503.
| Crossref | GoogleScholarGoogle Scholar |
Lang A, Thorpe MR
(1989) Xylem, phloem and transpiration flows in a grape: application of a technique for measuring the volume of attached fruits to high resolution using Archimedes’ principle. Journal of Experimental Botany 40, 1069–1078.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar |
Nunan KJ,
Sims IM,
Bacic A,
Robinson SP, Fincher GB
(1998) Changes in cell wall composition during ripening of grape berries. Plant Physiology 118, 783–792.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Patrick JW
(1997) Phloem unloading: sieve element unloading and post-sieve element transport. Annual Review of Plant Physiology and Plant Molecular Biology 48, 191–222.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Picaud S,
Becq F, Dédaldéchamp F
(2003) Cloning and expression of two plasma membrane aquaporins expressed during the ripening of grape berry. Functional Plant Biology 30, 621–630.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Rogiers S,
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.
| Crossref | GoogleScholarGoogle Scholar |
Rogiers S,
Hatfield J,
Gunta Jaudzems V,
White R, 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 S,
Greer D,
Hatfield J,
Orchard B, Keller M
(2006) Solute transport into Shiraz berries during development and late-ripening shrinkage. American Journal of Enology and Viticulture 57, 73–80.
|
CAS |
Sadras V, McCarthy MG
(2007) Quantifying the dynamics of sugar concentration in berries of ‘Vitis vinifera’ cv. Shiraz: a novel approach based on allometric analysis. Australian Journal of Grape and Wine Research 13, 66–71.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Shackel KA,
Greve C,
Labavitch JM, Hahmadi H
(1991) Cell turgor changes associated with ripening in tomato pericarp tissue. Plant Physiology 97, 814–816.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Steudle E,
Murrmann M, Peterson CA
(1993) Transport of water and solutes across maize roots modified by puncturing the endodermis. Plant Physiology 103, 335–349.
|
CAS |
PubMed |
Thomas RT,
Matthews MA, Shackel KA
(2006) Direct in situ measurement of cell turgor in grape (Vitis vinifera L.) berries during development and in response to plant water deficits. Plant, Cell and Environment 29, 993–1001.
| 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.
| Crossref | GoogleScholarGoogle Scholar |
Tyerman SD,
Niemietz CM, Bramley H
(2002) Plant aquaporins: multifunctional water and solute channels with expanding roles. Plant, Cell & Environment 25, 173–194.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
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.
van Bel A
(2003) The phloem, a miracle of ingenuity. Plant, Cell & Environment 26, 125–149.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Wada H,
Shackel K, Matthews M
(2008) Fruit ripening in Vitis vinifera: apoplastic solute accumulation accounts for pre-veraison turgor loss in berries. Planta 227, 1351–1361.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Zhang X-Y,
Wang X-L,
Wang X,
Xia G-H,
Pan Q-H,
Fan R-C,
Wu F-Q,
Yu X-C, Zhang D-P
(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.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
