Skip to main content

Advertisement

Log in

Fruit ripening in Vitis vinifera: apoplastic solute accumulation accounts for pre-veraison turgor loss in berries

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

In Vitis vinifera L. berries, the onset of ripening (known as “veraison”) involves loss of turgor (P) in the mesocarp cells. We hypothesized that P loss was associated with an accumulation of apoplastic solutes in mesocarp tissue prior to veraison. Apoplastic sap was extracted from the mesocarp by centrifugation at the appropriate gravity to measure the apoplast solute potential (Ψ As ) and assay the sap composition. The Ψ As was about −0.2 MPa early in development, decreased about 1.0 MPa by veraison, and continued to decrease during ripening to almost −4.0 MPa by the end of berry development. Potassium, malate, tartrate, proline, glucose, fructose, and sucrose were quantified in apoplastic sap. The calculated contribution of these solutes was about 50% of the total Ψ As preveraison, but increased to about 75% as fructose and glucose accumulated during ripening. The contribution of the estimated matric potential to apoplast water potential decreased during development and was only 1.5% postveraison. We conclude that high concentrations of solutes accumulated in the mesocarp apoplast prior to veraison, and that P loss was a direct result of decreased Ψ As . Because Ψ As decreased before veraison, our findings suggest that apoplast solutes play an important role in the events of cellular metabolism that lead to the onset of ripening.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

F:

Firmness

P:

Turgor

PostV:

Postveraison

PreV:

Preveraison

Ψm :

Matric potential

Ψs :

Solute potential

Ψ As :

Apoplast solute potential

Ψ Ps :

Protoplast (symplast) solute potential

Ψ Ts :

Tissue solute potential

Ψw :

Total water potential

Ψ Aw :

Apoplast total water potential

Ψ Pw :

Protoplast (symplast) total water potential

References

  • Bernstein L (1971) Method for determining solutes in the cell walls of leaves. Plant Physiol 47:361–365

    PubMed  CAS  Google Scholar 

  • Bondada BR, Matthews MA, Shackel KA (2005) Functional xylem in the post-veraison grape berry. J Exp Bot 56:2949–2957

    Article  PubMed  CAS  Google Scholar 

  • Boyer JS (1967) Leaf water potentials measured with a pressure chamber. Plant Physiol 42:133–137

    PubMed  CAS  Google Scholar 

  • Boyer JS, Nonami H (1990) Water potential and its components in growing tissues. In: Hashimoto Y, Kramer PJ, Nonami H, Strain BR (eds) Measurement techniques in plant science. Academic Press, San Diego, pp 101–112

    Google Scholar 

  • Bruce DM (2003) Mathematical modelling of the cellular mechanics of plants. Philos Trans R Soc Lond B Biol Sci 358:1437–1444

    Article  PubMed  Google Scholar 

  • Brummell DA, Harpster MH (2001) Cell wall metabolism in fruit softening and quality and its manipulation in transgenic plants. Plant Mol Biol 47:311–340

    Article  PubMed  CAS  Google Scholar 

  • Cochrane TT (1994) A new equation for calculating osmotic potential. Plant Cell Environ 17:427–433

    Article  Google Scholar 

  • Cochrane TT, Cochrane TA (2005) Osmotic potential properties of solutes common in the soil-plant solution continuum. Soil Sci 170:433–444

    Article  CAS  Google Scholar 

  • Considine J, Brown K (1981) Physical aspects of fruit growth: theoretical analysis of distribution of surface growth forces in fruit in relation to cracking and splitting. Plant Physiol 68:371–376

    Article  PubMed  CAS  Google Scholar 

  • Coombe BG (1976) Development of fleshy fruits. Annu Rev Plant Physiol Plant Mol Biol 27:207–228

    CAS  Google Scholar 

  • Coombe BG (1992) Research on development and ripening of the grape berry. Am J Enol Vitic 43:101–110

    Google Scholar 

  • Coombe BG, Bishop GR (1980) Development of the grape berry. II: Changes in diameter and deformability during veraison. Aust J Agri Res 31:499–509

    Article  Google Scholar 

  • Cosgrove DJ, Cleland RE (1983) Solutes in the free space of growing stem tissues. Plant Physiol 72:326–331

    PubMed  CAS  Google Scholar 

  • Dannel F, Pfeffer H, Marschner H (1995) Isolation of apoplasmic fluid from sunflower leaves and its use for studies on influence of nitrogen supply on apoplasmic pH. J Plant Physiol 146:273–278

    CAS  Google Scholar 

  • Davies C, Wolf T, Robinson SP (1999) Three putative sucrose transporters are differentially expressed in grapevine tissues. Plant Sci 147:93–100

    Article  CAS  Google Scholar 

  • Delrot S, Picaud S, Gaudillere JP (2001) Water transport and aquaporins in grapevine. In: Roubelakis-Angelakis KA (ed) Molecular biology and biotechnology of the grapevine. Kluwer, London, pp 241–262

    Google Scholar 

  • Fillion L, Ageorges A, Picaud S, Coutos-Thevenot P, Lemoine R, Romieu C, Delrot S (1999) Cloning and expression of a hexose transporter gene expressed during the ripening of grape berry. Plant Physiol 120:1083–1094

    Article  PubMed  CAS  Google Scholar 

  • Greenspan MD, Shackel KA, Matthews MA (1994) Developmental changes in the diurnal water budget of the grape berry exposed to water deficits. Plant Cell Environ 17:811–820

    Article  Google Scholar 

  • Gutiérrez-Granda MJ, Morrison JC (1992) Solute distribution and malic enzyme activity in developing grape berries. Am J Enol Vitic 43:323–328

    Google Scholar 

  • Hiwasa K, Nakano R, Hashimoto A, Matsuzaki M, Murayama H, Inaba A, Kubo Y (2004) European, Chinese and Japanese pear fruits exhibit differential softening characteristics during ripening. J Exp Bot 55:2281–2290

    Article  PubMed  CAS  Google Scholar 

  • Hüsken D, Steudle E, Zimmermann U (1978) Pressure probe technique for measuring water relations of cells in higher plants. Plant Physiol 61:158–163

    PubMed  Google Scholar 

  • Jachetta JJ, Appleby AP, Boersma L (1986) Use of the pressure-vessel to measure concentrations of solutes in apoplastic and membrane-filtered symplastic sap in sunflower leaves. Plant Physiol 82:995–999

    PubMed  CAS  Google Scholar 

  • Krasnow MN, Matthews MA, Shackel KA (2008) Evidence for substantial maintenance of membrane integrity and cell viability in normally developing grape (Vitis vinifera L.) berries throughout development. J Exp Bot (in press)

  • Lang A, Düring H (1991) Partitioning control by water potential gradient: Evidence for compartmentation breakdown in grape berries. J Exp Bot 42:1117–1122

    Article  Google 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. J Exp Bot 40:1069–1078

    Article  Google Scholar 

  • Livingston DP, Henson CA (1998) Apoplastic sugars, fructans, fructan exohydrolase, and invertase in winter oat: responses to second-phase cold hardening. Plant Physiol 116:403–408

    Article  CAS  Google Scholar 

  • Lohaus G, Pennewiss K, Sattelmacher B, Hussmann M, Muehling KH (2001) Is the infiltration–centrifugation technique appropriate for the isolation of apoplastic fluid?: a critical evaluation with different plant species. Physiol Plant 111:457–465

    Article  PubMed  CAS  Google Scholar 

  • Matthews MA, Shackel KA (2005) Growth and water transport in fleshy fruit. In: Holbrook MN, Zwieniecki MA (eds) Vascular transport in plants. Elsevier, Boston, pp 189–197

    Google Scholar 

  • Matthews MA, Anderson MM (1988) Fruit ripening in Vitis vinifera L.: responses to seasonal water deficits. Am J Enol Vitic 39:313–320

    Google Scholar 

  • Matthews MA, Cheng G, Weinbaum SA (1987) Changes in water potential and dermal extensibility during grape berry development. J Am Soc Hort Sci 112:314–319

    Google Scholar 

  • Meinzer FC, Moore PH (1988) Effect of apoplastic solutes on water potential in elongating sugarcane leaves. Plant Physiol 86:873–879

    PubMed  CAS  Google Scholar 

  • Mignani I, Greve LC, Benarie R, Stotz HU, Li CY, Shackel KA, Labavitch JM (1995) The effects of GA3 and divalent-cations on aspects of pectin metabolism and tissue softening in ripening tomato pericarp. Physiol Plant 93:108–115

    Article  CAS  Google Scholar 

  • Nonami H, Boyer JS (1987) Origin of growth-induced water potential: solute concentration is low in apoplast of enlarging tissues. Plant Physiol 83:596–601

    PubMed  CAS  Google Scholar 

  • Ogden TE, Citron MC, Pierantoni R (1978) The jet stream microbeveler: an inexpensive way to bevel ultrafine glass micropipettes. Science 201:469–470

    Article  PubMed  CAS  Google Scholar 

  • Picaud S, Becq F, Dedaldechamp F, Ageorges A, Delrot S (2003) Cloning and expression of two plasma membrane aquaporins expressed during the ripening of grape berry. Funct Plant Biol 30:621–630

    Article  CAS  Google Scholar 

  • Pomper KW, Breen PJ (1995) Levels of apoplastic solutes in developing strawberry fruit. J Exp Bot 46:743–752

    Article  CAS  Google Scholar 

  • Rose JKC, Lee HH, Bennett AB (1997) Expression of a divergent expansin gene is fruit-specific and ripening-regulated. Proc Natl Acad Sci USA 94:5955–5960

    Article  PubMed  CAS  Google Scholar 

  • Sakurai N (1998) Dynamic function and regulation of apoplast in the plant body. J Plant Res 111:133–148

    Article  CAS  Google Scholar 

  • Saladié M, Matas AJ, Isaacson T, Jenks MA, Goodwin SM, Niklas KJ, Ren XL, Labavitch JM, Shackel KA, Fernie AR, Lytovchenko A, O’Neill MA, Watkins CB, Rose JKC (2007) A reevaluation of the key factors that influence tomato fruit softening and integrity. Plant Physiol 144:1012–1028

    Article  PubMed  CAS  Google Scholar 

  • Shackel KA, Greve C, Labavitch JM, Ahmadi H (1991) Cell turgor changes associated with ripening in tomato pericarp tissue. Plant Physiol 97:814–816

    PubMed  CAS  Google Scholar 

  • Shackel KA, Matthews MA, Morrison JC (1987) Dynamic relation between expansion and cellular turgor in growing grape (Vitis vinifera L.) leaves. Plant Physiol 84:1166–1171

    PubMed  CAS  Google Scholar 

  • Soga T, Imaizumi M (2001) Capillary electrophoresis method for the analysis of inorganic anions, organic acids, amino acids, nucleotides, carbohydrates and other anionic compounds. Electrophoresis 22:3418–3425

    Article  PubMed  CAS  Google Scholar 

  • Speer M, Kaiser WM (1991) Ion relations of symplastic and apoplastic space in leaves from Spinacia oleracea L. and Pisum sativum L. under salinity. Plant Physiol 97:990–997

    Article  PubMed  CAS  Google Scholar 

  • Tang AC, Boyer JS (2002) Growth-induced water potentials and the growth of maize leaves. J Exp Bot 53:489–503

    Article  PubMed  CAS  Google Scholar 

  • Terry ME, Bonner BA (1980) An examination of centrifugation as a method of extracting an extracellular solution from peas, and its use for the study of indoleacetic acid-induced growth. Plant Physiol 66:321–325

    PubMed  CAS  Google Scholar 

  • Tetlow IJ, Farrar JF (1993) Apoplastic sugar concentration and pH in barley leaves infected with brown rust. J Exp Bot 44:929–936

    Article  CAS  Google Scholar 

  • Thomas TR (2004) Grape berry cellular turgor: responses to water deficits, relation to fruit firmness, and changes throughout development in Cabernet Sauvignon, Chardonnay, and Pinot noir. MS thesis, University of California, Davis

  • Thomas TR, 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 Environ 29:993–1001

    Article  PubMed  Google Scholar 

  • Tong C, Krueger D, Vickers Z, Bedford D, Luby J, El-Shiekh A, Shackel K, Ahmadi H (1999) Comparison of softening-related changes during storage of ‘Honeycrisp’ apple, its parents, and ‘Delicious’. J Am Soc Hort Sci 124:407–415

    Google Scholar 

  • 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. Aust J Grape Wine Res 10:170–181

    Article  Google Scholar 

  • Wada H, Iwaya-Inoue M, Akita M, Nonami H (2005) Hydraulic conductance in tepal growth and extension of vase life with trehalose in cut tulip flowers. J Am Soc Hort Sci 130:275–286

    Google Scholar 

  • Wakabayashi K (2000) Changes in cell wall polysaccharides during fruit ripening. J Plant Res 113:231–237

    Article  CAS  Google Scholar 

  • Welbaum GE, Meinzer FC (1990) Compartmentation of solutes and water in developing sugarcane stalk tissue. Plant Physiol 93:1147–1153

    Article  PubMed  CAS  Google Scholar 

  • Yu Q, Tang C, Kuo J (2000) A critical review on methods to measure apoplastic pH in plants. Plant Soil 219:29–40

    Article  CAS  Google Scholar 

  • Zhang WH, Atwell BJ, Patrick JW, Walker NA (1996) Turgor-dependent efflux of assimilates from coats of developing seed of Phaseolus vulgaris L.: water relations of the cells involved in efflux. Planta 199:25–33

    CAS  Google Scholar 

  • Zhang XY, Wang XL, Wang XF, Xia GH, Pan QH, Fan RC, Wu FQ, Yu XC, Zhang DP (2006) A shift of phloem unloading from symplasmic to apoplasmic pathway is involved in developmental onset of ripening in grape berry. Plant Physiol 142:220–232

    Article  PubMed  CAS  Google Scholar 

  • Zhu J, Chen S, Alvarez S, Asirvatham VS, Schachtman DP, Wu Y, Sharp RE (2006) Cell wall proteome in the maize primary root elongation zone. I. Extraction and identification of water-soluble and lightly ionically bound proteins. Plant Physiol 140:311–325

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Dr. Kentaro Inoue of the Department of Plant Sciences, University of California, Davis, for use of his centrifuge. We gratefully acknowledge Dr. Thomas T. Cochrane of Department of Civil Engineering, University of Canterbury, for providing us with his valuable data sheet for solute potential calculations. The authors also thank Cal-Western Nurseries, Visalia, CA, USA for providing Chardonnay grapevines.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mark A. Matthews.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wada, H., Shackel, K.A. & Matthews, M.A. Fruit ripening in Vitis vinifera: apoplastic solute accumulation accounts for pre-veraison turgor loss in berries. Planta 227, 1351–1361 (2008). https://doi.org/10.1007/s00425-008-0707-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-008-0707-3

Keywords

Navigation