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Mesocarp cell turgor in Vitis vinifera L. berries throughout development and its relation to firmness, growth, and the onset of ripening

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Abstract

Vitis vinifera L. berries are non-climacteric fruit that exhibit a double sigmoid growth pattern and dynamic changes in gene expression, cell metabolism, and water relations at the onset of ripening. The cell-pressure probe was utilized to examine the relationships of turgor pressure (P) in mesocarp cells to growth, sugar accumulation, and fruit softening during development. In replications utilizing three different varieties, mesocarp cell P demonstrated a consistent pattern of a relative mid-range P early in development, followed by an increase to a maximum of about 0.35 MPa, and a subsequent rapid decline before ripening to less than 0.1 MPa. Fruit “apparent elastic modulus” (E, units of MPa), was introduced as a standard measure to describe ripening-related softening. E changed dynamically and synchronously with P during development and in response to water deficits for fruit grown in greenhouse and field conditions. Thus, E and P were positively and linearly related. Sugar accumulation did not increase significantly until P had declined to less than 0.1 MPa. The results suggest that P is an important determinant of fruit softening and that P decreases in conjunction with many of the physiological and gene expression changes that are known to occur at the onset of ripening.

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References

  • Aloni B, Karni L, Moreshet S, Yao C, Stanghellini C (1999) Cuticular cracking in bell pepper fruit: II. Effects of fruit water relations and fruit expansion. J Hort Sci and Biotech 74:1–5

    Google Scholar 

  • Amerine MA, Ough CS (1980) Methods for analysis of musts and wines. Wiley, New York

    Google Scholar 

  • ASAE (2003) Compression Test of Food Materials of Convex Shape. ASAE standard S368.4 DEC00. Am Soc Agr Eng, St. Joseph, MI

  • Baiges I, Schaffner AR, Affenzuller MJ (2002) Plant aquaporins. Physiol Plant 115:175–182

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Boyer JS (1995) Measuring the water status of plants and soils. Academic Press, Inc, New York

    Google Scholar 

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

    Article  Google Scholar 

  • Brummell DA, Harpster MH (2001) Cell wall metabolism in fruit softening and quality and its manipulation in transgenic plants. Plant Mol Biol 47:311–339

    Article  PubMed  CAS  Google Scholar 

  • Cakir B, Agasse A, Gaillard C, Saumonneau A, Delrot S, Atanassova R (2003) A grape ASR protein involved in sugar and abscisic acid signaling. Plant Cell 15:2165–2180

    Article  PubMed  CAS  Google Scholar 

  • Chatelet D, Rost T, Shackel K, Matthews M (2008) The peripheral xylem of grapevine (Vitis vinifera): 1. Structural integrity in postveraison berries. J Exp Bot 59:1987–1996

    Article  PubMed  CAS  Google Scholar 

  • Coombe BG (1976) The development of fleshy fruits. Ann Rev Plant Physiol 27:507–528

    Article  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 Agric Res 31:499–509

    Article  Google Scholar 

  • Coombe BG, Hale CR (1973) The hormone content of ripening grape berries and the effects of growth substance treatments. Plant Physiol 51:629–634

    PubMed  CAS  Google Scholar 

  • Coombe BG, Phillips PE (1980) Development of the grape berry. III. Compostional changes during veraison measured by sequential hypodermic sampling. UCD Grape and Wine Continental Symposium. University of California, Davis

    Google Scholar 

  • 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. Am J Enol Vitic 44:187–192

    CAS  Google Scholar 

  • Davies C, Robinson SP (2000a) Differential screening indicates a dramatic change in mRNA profiles during grape berry ripening. Cloning and characterization of cDNAs encoding putative cell wall and stress response proteins. Plant Physiol 122:803–812

    Article  PubMed  CAS  Google Scholar 

  • Davies C, Robinson SP (2000b) Molecular biology of ripening. Aust J Grape Wine Res 6:175–188

    Article  Google Scholar 

  • Davies C, Boss PK, Robinson SP (1997) Treatment of grape berries, a nonclimacteric fruit with a synthetic auxin, retards ripening and alters the expression of developmentally regulated genes. Plant Physiol 115:1155–1161

    PubMed  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 

  • Deluc LG, Grimplet J, Wheatley MD, Tillett RL, Quilici DR, Osborne C, Schooley DA, Schlauch KA, Cushman JC, Cramer GR (2007) Transcriptomic and metabolite analyses of Cabernet Sauvignon grape berry development. BMC Genomics 8:429

    Article  PubMed  Google Scholar 

  • Düring H, Lang A, Oggionni F (1987) Patterns of water flow in Riesling berries in relation to developmental changes in their xylem morphology. Vitis 26:123–131

    Google Scholar 

  • Famiani F, Walker RP, Tecsi L, Chen ZH, Proietti P, Leegood RC (2000) An immunohistochemical study of the compartmentation of metabolism during the development of grape (Vitis vinifera L.) berries. J Exp Bot 51:675

    Article  PubMed  CAS  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 

  • Findlay N, Oliver KJ, Nil N, Coombe BG (1987) Solute accumulation by grape pericarp cells: IV. Perfusion of pericarp apoplast via the pedicel and evidence for xylem malfunction in ripening berries. J Exp Bot 38:668

    Article  Google Scholar 

  • Fougere-Rifot M, Park HS, Bouard J (1997) Berry pericarp ontogenesis from fertilization to maturity of Vitis vinifera L. var. Merlot. J Int des Sci de la Vigne et du Vin 31:109–118

    Google Scholar 

  • Franke KE, Liu Y, Adams DO (1995) Yield and quality of RNA from grape berries at different developmental stages. Am J Enol Vitic 46:315–318

    CAS  Google Scholar 

  • Goes da Silva F, Iandolino A, Al-Kayal F, Bohlmann MC, Cushman MA, Lim H, Ergul A, Figueroa R, Kabuloglu EK, Osborne C (2005) Characterizing the grape transcriptome. Analysis of expressed sequence tags from multiple Vitis species and development of a compendium of gene expression during berry development. Plant Physiol 139:574–597

    Article  CAS  Google Scholar 

  • Grange RI (1995) Water relations and growth of tomato fruit pericarp tissue. Plant Cell Environ 18:1311–1318

    Article  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 

  • Greenspan MD, Schultz HR, Matthews MA (1996) Field evaluation of water transport in grape berries during water deficits. Physiol Plant 97:55–62

    Article  CAS  Google Scholar 

  • Greve LC, Shackel KA, Ahmadi H, McArdle RN, Gohlke JR, Labavitch JM (1994) Impact of heating on carrot firmness: contribution of cellular turgor. J Agric Food Chem 42:2896–2899

    Article  CAS  Google Scholar 

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

    PubMed  Google Scholar 

  • Jones JT, Mullet JE (1995) Developmental expression of a turgor-responsive gene that encodes an intrinsic membrane protein. Plant Mol Biol 28:983–996

    Article  PubMed  CAS  Google Scholar 

  • Keller M, Smith JP, Bondada BR (2006) Ripening grape berries remain hydraulically connected to the shoot. J Exp Bot 57:2577

    Article  PubMed  CAS  Google Scholar 

  • 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. J Exp Bot 59:849–859

    Article  PubMed  CAS  Google Scholar 

  • Kutschera U (2004) The biophysical basis of cell elongation and organ maturation in coleoptiles of rye seedlings: Implications for shoot development. Plant Biol 6:158–164

    Article  PubMed  CAS  Google Scholar 

  • Lalonde S, Tegeder M, Throne-Holst M, Frommer WB, Patrick JW (2003) Phloem loading and unloading of sugars and amino acids. Plant Cell Environ 26:37–56

    Article  CAS  Google Scholar 

  • Lang A (1983) Turgor-regulated translocation. Plant Cell Environ 6:683–689

    Google Scholar 

  • Lang A, During 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 (1986) Water potential, translocation and assimilate partitioning. J Exp Bot 37:495

    Article  Google Scholar 

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

    Google Scholar 

  • Matthews MA, Van Volkenburgh E, Boyer JS (1984) Acclimation of leaf growth to low water potentials in sunflower. Plant Cell Environ 7:199–206

    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 

  • McCutchan H, Shackel KA (1992) Stem-water potential as a sensitive indicator of water stress in prune trees (prunus domestica l. Cv. French). J Am Soc Hort Sci 117:607–611

    Google Scholar 

  • Neill SJ, Burnett EC (1999) Regulation of gene expression during water deficit stress. Plant Growth Regul 29:23–33

    Article  CAS  Google Scholar 

  • Nonami H, Boyer JS (1993) Direct demonstration of a growth-induced water potential gradient. Plant Physiol 102:13–19

    PubMed  CAS  Google Scholar 

  • Nonami H, Schulze ED (1989) Cell water potential, osmotic potential, and turgor in the epidermis and mesophyll of transpiring leaves. Planta 177:35–46

    Article  Google Scholar 

  • Nonami H, Boyer JS, Steudle E (1987) Pressure probe and isopiestic psychrometer measure similar turgor. Plant Physiol 83:592–595

    PubMed  Google Scholar 

  • Nunan KJ, Sims IM, Bacic A, Robinson SP, Fincher GB (1998) Changes in cell wall composition during ripening of grape berries. Plant Physiol 118:783–792

    Article  PubMed  CAS  Google Scholar 

  • Nunan KJ, Davies C, Robinson SP, Fincher GB (2001) Expression patterns of cell wall-modifying enzymes during grape berry development. Planta 214:257–264

    PubMed  CAS  Google Scholar 

  • Ohnishi S, Fujii T, Miyawaki O (2003) Freezing injury and rheological properties of agricultural products. Food Sci Technol Res 9:367–371

    Article  Google Scholar 

  • Ollat N, Diakou-Verdin P, Carde JP, Barrieu F, Gaudillere JP, Moing A (2002) Grape berry development: A review. J Int des Sci de la Vigne et du Vin 36:109–131

    CAS  Google Scholar 

  • Patrick JW (1997) Phloem unloading: Sieve element unloading and post-sieve element transport. Annu Rev Plant Physiol Plant Mol Biol 48:191–222

    Article  PubMed  CAS  Google Scholar 

  • Pomper KW, Breen PJ (1996) The effect of cell turgor on sugar uptake in strawberry fruit cortex tissue. Physiol Plant 96:324–332

    Article  CAS  Google Scholar 

  • Preston CE (1901) Structural studies on southwestern cactaceae. Bot Gaz 32:35–55

    Article  Google Scholar 

  • Ravi N, Wan KT, Swindle K, Hamilton PD, Duan G (2006) Development of techniques to compare mechanical properties of reversible hydrogels with spherical, square columnar and ocular lens geometry. Polymer 47:4203–4209

    Article  CAS  Google Scholar 

  • van de Rhee MD, Linthorst HJM, Bol JF (1994) Pathogen-induced gene expression. Stress-induced gene expression in plants Lausanne. Harwood Academic Publishers, New York, pp 249–284

  • Rose JKC, Bennett AB (1999) Cooperative disassembly of the cellulose-xyloglucan network of plant cell walls: parallels between cell expansion and fruit ripening. Trends Plant Sci 4:176–183

    Article  PubMed  Google Scholar 

  • Sajnin C, Gamba G, Gerschenson LN, Rojas AM (2003) Textural, histological and biochemical changes in cucumber (Cucumis sativus L) due to immersion and variations in turgor pressure. J Sci Food Agric 83:731–740

    Article  CAS  Google Scholar 

  • Schultz HR, Matthews MA (1993) Growth, osmotic, adjustment, and cell-wall mechanics of expanding grape leaves during water deficits. Crop Sci 33:287–294

    Google Scholar 

  • Serpe MD, Matthews MA (1994) Growth, pressure, and wall stress in epidermal cells of Begonia argenteo-guttata L. leaves during development. Int J Plant Sci 155:291–301

    Article  Google Scholar 

  • Serpe MD, Matthews MA (2000) Turgor and cell wall yielding in dicot leaf growth in response to changes in relative humidity. Aust J Plant Physiol 27:1131–1140

    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  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  Google Scholar 

  • Silacci MW, Morrison JC (1990) Changes in pectin content of Cabernet sauvignon grape berries during maturation. Am J Enol Vitic 41:111–115

    CAS  Google Scholar 

  • Spollen WG, Sharp RE (1991) Spatial distribution of turgor and root growth at low water potentials. Plant Physiol 96:438–443

    PubMed  Google Scholar 

  • Tattersall DB, van Heeswijck R, Hoj PB (1997) Identification and characterization of a fruit-specific, thaumatin-like protein that accumulates at very high levels in conjunction with the onset of sugar accumulation and berry softening in grapes. Plant Physiol 114:759–769

    Article  PubMed  CAS  Google Scholar 

  • Terrier N, Glissant D, Grimplet J, Barrieu F, Abbal P, Couture C, Ageorges A, Atanassova R, Léon C, Renaudin JP (2005) Isogene specific oligo arrays reveal multifaceted changes in gene expression during grape berry (Vitis vinifera L.) development. Planta 222:832–847

    Article  PubMed  CAS  Google Scholar 

  • Thomas TR, Matthews MA, Shackel K (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

    Google Scholar 

  • Wada H, Shackel KA, Matthews MA (2008) Fruit ripening in Vitis vinifera: apoplastic solute accumulation accounts for pre-veraison turgor loss in berries. Planta 227:1351–1361

    Article  PubMed  CAS  Google Scholar 

  • Wang ZP, Deloire A, Carbonneau A, Federspiel B, Lopez F (2003) An in vivo experimental system to study sugar phloem unloading in ripening grape berries during water deficiency stress. Ann Bot 92:523–528

    Article  PubMed  Google Scholar 

  • Welbaum GE, Bradford KJ (1988) Water relations of seed development and germination in muskmelon (Cucumis melo L.): I. Water relations of seed and fruit development. Plant Physiol 86:406–411

    Article  PubMed  Google Scholar 

  • Yakushiji H, Nonami H, Fukuyama T, Ono S, Takagi N, Hashimoto Y (1996) Sugar accumulation enhanced by osmoregulation in Satsuma mandarin fruit. J Am Soc Hort Sci 121:466–472

    CAS  Google Scholar 

  • Yakushiji H, Sakurai N, Morinaga K (2001) Changes in cell-wall polysaccharides from the mesocarp of grape berries during veraison. Physiol Plant 111:188–195

    Article  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

    Article  PubMed  CAS  Google Scholar 

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  1. Department of Viticulture and Enology, University of California, One Shields Ave, Davis, CA, 95616, USA

    Tyler R. Thomas & Mark A. Matthews

  2. Department of Plant Sciences, University of California, Davis, CA, USA

    Ken A. Shackel & Mark A. Matthews

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  1. Tyler R. Thomas
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Correspondence to Mark A. Matthews.

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Thomas, T.R., Shackel, K.A. & Matthews, M.A. 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 (2008). https://doi.org/10.1007/s00425-008-0808-z

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