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Softening at the onset of grape ripening alters fruit rheological properties and decreases splitting resistance

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Abstract

Main conclusion

Applying principles of shell theory, we found that grape berries rapidly change their behavior from thick-walled spheres to pressurized thin-walled spheres and become susceptible to splitting during berry softening.

Abstract

Knowledge of the rheological properties of the skin of berry fruits is needed to make decisions concerning berry splitting prevention. However, how these properties and splitting resistance respond to varietal differences and developmental changes is poorly understood. In a customized injection test, pressurized water was injected into the berries of four grape varieties until they split. In a compression test, the deformation of berries in response to berry softening or dehydration was measured. Shell theory was applied to estimate how the internal pressure translates to tensile stress on the skin. The results suggested that berry softening at the onset of ripening drastically alters berry rheological properties; berries rapidly changed from brittle to ductile materials. The skin became the major stress-bearing structure during berry softening and became vulnerable to tensile stress, which was associated with a rapid decline in splitting resistance. The rate of decline and the absolute extent of the skin’s ability to bear stress varied by variety. Dehydration of overripe or water-stressed berries did not alter the skin properties but reduced the risk of berry splitting. These results indicate that the vulnerability to berry splitting is closely related to developmentally regulated changes in fruit rheological properties and water relations.

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Abbreviations

σ :

Applied stress

E :

Elastic modulus

ɛ c :

Compressive strain

ɛ s :

Strain at splitting

OYP:

Offset yield point

P i :

Internal pressure

P sf :

Interface pressure

R p0.2 :

Offset yield strength at 0.2% strain

R s :

Splitting resistance

T cs :

Critical shell tension

V i :

Injected water volume

References

  • Anderson TL (2017) Fracture mechanics: fundamentals and applications. CRC Press, Boca Raton

    Book  Google Scholar 

  • Becker T, Knoche M (2012) Deposition, strain, and microcracking of the cuticle in developing ‘Riesling’ grape berries. Vitis 51:1–6

    Google Scholar 

  • Boudaoud A (2010) An introduction to the mechanics of morphogenesis for plant biologists. Trends Plant Sci 15:353–360

    Article  CAS  PubMed  Google Scholar 

  • Brown K, Considine J (1982) Physical aspects of fruit growth stress distribution around lenticels. Plant Physiol 69:585–590

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brüggenwirth M, Knoche M (2016) Factors affecting mechanical properties of the skin of sweet cherry fruit. J Am Soc Hortic Sci 141:45–53

    Article  Google Scholar 

  • Brüggenwirth M, Fricke H, Knoche M (2014) Biaxial tensile tests identify epidermis and hypodermis as the main structural elements of sweet cherry skin. AoB Plants 6:1–13

    Article  Google Scholar 

  • Castellarin SD, Gambetta GA, Wada H, Shackel KA, Matthews MA (2011) Fruit ripening in Vitis vinifera: spatiotemporal relationships among turgor, sugar accumulation, and anthocyanin biosynthesis. J Exp Bot 62:4345–4354

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Castellarin SD, Gambetta GA, Wada H, Krasnow MN, Cramer GR, Peterlunger E, Shackel KA, Matthews MA (2015) Characterization of major ripening events during softening in grape: turgor, sugar accumulation, abscisic acid metabolism, colour development, and their relationship with growth. J Exp Bot 67:709–722

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clarke SJ, Hardie WJ, Rogiers SY (2010) Changes in susceptibility of grape berries to splitting are related to impaired osmotic water uptake associated with losses in cell vitality. Aust J Grape Wine Res 16:469–476

    Article  Google Scholar 

  • Considine JA, Kriedemann PE (1972) Fruit splitting in grapes: determination of the critical turgor pressure. Aust J Agric Res 23:17–24

    Article  Google Scholar 

  • Dean RJ, Bobek G, Stait-Gardner T, Clarke SJ, Rogiers SY, Price WS (2016) Time-course study of grape berry split using diffusion magnetic resonance imaging. Aust J Grape Wine Res 22:240–244

    Article  Google Scholar 

  • Deytieux-Belleau C, Vallet A, Donèche B, Geny L (2008) Pectin methylesterase and polygalacturonase in the developing grape skin. Plant Physiol Biochem 46:638–646

    Article  CAS  PubMed  Google Scholar 

  • Di Matteo M, Cinquanta L, Galiero G, Crescitelli S (2000) Effect of a novel physical pretreatment process on the drying kinetics of seedless grapes. J Food Eng 46:83–89

    Article  Google Scholar 

  • 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. Aust J Grape Wine Res 16:327–336

    Article  Google Scholar 

  • Hardie WJ, O’Brien TP, Jaudzems VG (1996) Morphology, anatomy and development of the pericarp after anthesis in grape, Vitis vinifera L. Aust J Grape Wine Res 2:97–142

    Article  Google Scholar 

  • Hetzroni A, Vana A, Mizrach A (2011) Biomechanical characteristics of tomato fruit peels. Postharvest Biol Technol 59:80–84

    Article  Google Scholar 

  • Huang X-M, Huang H-B (2001) Early post-veraison growth in grapes: evidence for a two-step mode of berry enlargement. Aust J Grape Wine Res 7:132–136

    Article  Google Scholar 

  • Huang X-M, Huang H-B, Wang H-C (2005) Cell walls of loosening skin in post-veraison grape berries lose structural polysaccharides and calcium while accumulate structural proteins. Sci Hortic 104:249–263

    Article  CAS  Google Scholar 

  • Huber F, Röckel F, Schwander F, Maul E, Eibach R, Cousins P, Töpfer R (2016) A view into American grapevine history: Vitis vinifera cv. ‘Sémillon’ is an ancestor of ‘Catawba’ and ‘Concord’. Vitis 55:53–56

    Google Scholar 

  • Jáuregui-Riquelme F, Kremer-Morales MS, Alcalde JA, Pérez-Donoso AG (2017) Pre-anthesis CPPU treatment modifies quality and susceptibility to post-harvest berry cracking of Vitis vinifera cv. ‘Thompson seedless’. J Plant Growth Regul 36:413–423

    Article  CAS  Google Scholar 

  • Keller M, Shrestha PM (2014) Solute accumulation differs in the vacuoles and apoplast of ripening grape berries. Planta 239:633–642

    Article  CAS  PubMed  Google Scholar 

  • Keller M, Smith JR, Bondada BR (2006) Ripening grape berries remain hydraulically connected to the shoot. J Exp Bot 57:2577–2587

    Article  CAS  PubMed  Google Scholar 

  • Keller M, Zhang Y, 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 Environ 38:1048–1059

    Article  CAS  Google Scholar 

  • Keller M, Shrestha PM, Hall GE, Bondada BR, Davenport JR (2016) Arrested sugar accumulation and altered organic acid metabolism in grape berries affected by berry shrivel syndrome. Am J Enol Vitic 67:398–406

    Article  CAS  Google Scholar 

  • Lang A, Düring H (1990) Grape berry splitting and some mechanical properties of the skin. Vitis 29:61–70

    Google Scholar 

  • Leong S-L, Hocking AD, Pitt JI (2004) Occurrence of fruit rot fungi (Aspergillus section Nigri) on some drying varieties of irrigated grapes. Aust J Grape Wine Res 10:83–88

    Article  Google Scholar 

  • Lim H-K, Son I-C, Oh S-I, Shin H, Oh Y-J, Park S-J, Kim D (2014) Characteristics of berry growth in cracking susceptible tetraploid grapevines. Acta Hortic 1046:511–516

    Google Scholar 

  • Lustig I, Bernstein Z (1985) Determination of the mechanical properties of the grape berry skin by hydraulic measurements. Sci Hortic 25:279–285

    Article  Google Scholar 

  • Marshall DA, Spiers JM, Stringer SJ, Curry KJ (2007) Laboratory method to estimate rain-induced splitting in cultivated blueberries. HortScience 42:1551–1553

    Article  Google Scholar 

  • Martin LBB, Rose JKC (2014) There’s more than one way to skin a fruit: formation and functions of fruit cuticles. J Exp Bot 65:4639–4651

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Mesejo C, Reig C, Martínez-Fuentes A, Gambetta G, Gravina A, Agustí M (2016) Tree water status influences fruit splitting in Citrus. Sci Hortic 209:96–104

    Article  Google Scholar 

  • Mohsenin NN (1986) Physical properties of plant and animal materials: structure, physical characteristics and mechanical properties. Gordon and Breach Science Publishers, New York

    Google Scholar 

  • Opara LU, Studman CJ, Banks NH (1997) Fruit skin splitting and cracking. Hortic Rev 19:217–262

    Google Scholar 

  • Pratt C (1971) Reproductive anatomy in cultivated grapes—a review. Am J Enol Vitic 22:92–109

    Google Scholar 

  • Segado P, Domínguez E, Heredia A (2016) Ultrastructure of the epidermal cell wall and cuticle of tomato fruit (Solanum lycopersicum L.) during development. Plant Physiol 170:935–946

    Article  CAS  PubMed  Google Scholar 

  • Swift JG, May P, Lawton EA (1974) Concentric cracking of grape berries. Vitis 13:30–35

    Google Scholar 

  • 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 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Viret O, Keller M, Gunta Jaudzems V, Mary Cole F (2004) Botrytis cinerea infection of grape flowers: light and electron microscopical studies of infection sites. Phytopathol 94:850–857

    Article  Google Scholar 

  • Vullo V (2014) Circular cylinders and pressure vessels. Springer, Berlin

    Book  Google Scholar 

  • Wada H, Matthews MA, Shackel KA (2009) Seasonal pattern of apoplastic solute accumulation and loss of cell turgor during ripening of Vitis vinifera fruit under field conditions. J Exp Bot 60:1773–1781

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Long LE (2015) Physiological and biochemical changes relating to postharvest splitting of sweet cherries affected by calcium application in hydrocooling water. Food Chem 181:241–247

    Article  CAS  PubMed  Google Scholar 

  • Winkler A, Peschel S, Kohrs K, Knoche M (2016) Rain cracking in sweet cherries is not due to excess water uptake but to localized skin phenomena. J Am Soc Hortic Sci 141:653–660

    Article  CAS  Google Scholar 

  • Yamamoto T, Satoh H (1994) Relationship among berry cracking susceptibility, berry morphology and skin stress distribution in several grape cultivars. J Jpn Soc Hortic Sci 63:247–256

    Article  Google Scholar 

  • Yamamura H, Naito R, Tamura H (1986) Effects of light intensity and humidity around clusters on the formation of surface wax and the resistance to berry splitting in ‘Delaware’ grapes. J Jpn Soc Hortic Sci 55:138–144

    Article  Google Scholar 

  • Zhang Y, Keller M (2015) Grape berry transpiration is determined by vapor pressure deficit, cuticular conductance, and berry size. Am J Enol Vitic 66:454–462

    Article  CAS  Google Scholar 

  • Zhang Y, Keller M (2017) Discharge of surplus phloem water may be required for normal grape ripening. J Exp Bot 68:585–595

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zoffoli JP, Latorre BA, Naranjo P (2008) Hairline, a postharvest cracking disorder in table grapes induced by sulfur dioxide. Postharvest Biol Technol 47:90–97

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the USDA National Institute of Food and Agriculture, Hatch project 1000186, the Chateau Ste. Michelle Distinguished Professorship, and the Graduate School of Washington State University. We thank Lynn Mills and Alan Kawakami for technical assistance.

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Correspondence to Markus Keller.

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425_2019_3226_MOESM1_ESM.pdf

Supplementary material 1 Radius measurements on a grape berry in a perspective view, b front view, and c side view. The width is 2ra, the depth is 2rb, and the height is 2rc (PDF 52 kb)

Supplementary material 2 (DOCX 23 kb)

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Chang, BM., Zhang, Y. & Keller, M. Softening at the onset of grape ripening alters fruit rheological properties and decreases splitting resistance. Planta 250, 1293–1305 (2019). https://doi.org/10.1007/s00425-019-03226-y

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