Cuticle and skin cell walls have common and unique roles in grape berry splitting

Ben-Min Chang , Markus Keller

Horticulture Research ›› 2021, Vol. 8 ›› Issue (1) : 168

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Horticulture Research ›› 2021, Vol. 8 ›› Issue (1) :168 DOI: 10.1038/s41438-021-00602-2
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Cuticle and skin cell walls have common and unique roles in grape berry splitting
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Abstract

The skin protects a fruit from environmental stresses and supports the fruit’s structure. Failure of the skin leads to fruit splitting and may compromise commercial production for fruit growers. The mechanical properties of the cuticle and skin cell walls might influence the splitting susceptibility of fleshy fruits. Thin shell theory and fracture mechanics were utilized in this study to target the potential factors contributing to splitting susceptibility. The study analyzed the structure of the cuticle and epidermis in ripening grape berries and examined the temporal dynamics of berry splitting. Cuticular waxes were partially removed, and skin cell walls were manipulated using wall stiffening and loosening solutions that altered reactions involving hydrogen peroxide. A more than twofold difference in cuticle thickness among grape cultivars did not account for their differences in splitting resistance. However, while removing predominantly epicuticular wax did not alter the berries’ splitting resistance, their surface appearance and increasing yield strength following partial wax removal support the notion that cuticular waxes contribute to berry mechanical properties. Immersing berries in H2O2-based cell wall loosening solutions increased the splitting probability and accelerated berry splitting, whereas cell wall stiffening solutions decreased the splitting probability and delayed berry splitting. These results showed that both cuticle and skin cell walls contribute to the mechanical properties of grape berries and to their splitting resistance. The results also suggest that the two current explanations for fruit splitting, the critical turgor model and the zipper model, should be viewed as complementary rather than incompatible.

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Ben-Min Chang, Markus Keller. Cuticle and skin cell walls have common and unique roles in grape berry splitting. Horticulture Research, 2021, 8 (1) : 168 DOI:10.1038/s41438-021-00602-2

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References

[1]

Hardie, W. J., O’Brien, T. P. & Jaudzems, V. G. Morphology, anatomy and development of the pericarp after anthesis in grape, Vitis vinifera L. Aust. J. Grape Wine Res. 2, 97-142 (1996).

[2]

Ginzberg, I. & Stern, R. A. Strengthening fruit-skin resistance to growth strain by application of plant growth regulators. Sci. Hortic. 198, 150-153 (2016).

[3]

Martin, L. B. B. & Rose, J. K. C. There’s more than one way to skin a fruit: formation and functions of fruit cuticles. J. Exp. Bot. 65, 4639-4651 (2014).

[4]

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

[5]

Matthews, M. A., Cheng, G. & Weinbaum, S. A. Changes in water potential and dermal extensibility during grape berry development. J. Am. Soc. Hortic. Sci. 112, 314-319 (1987).

[6]

Knoche, M. & Lang, A. Ongoing growth challenges fruit skin integrity. Crit. Rev. Plant Sci. 36, 190-215 (2017).

[7]

Opara, L. U., Studman, C. J. & Banks, N. H. Fruit skin splitting and cracking. Hortic. Rev. 19, 217-262 (1997).

[8]

Keller, M., Zhang, Y., Shrestha, P. M., Biondi, M. & Bondada, B. R. Sugar demand of ripening grape berries leads to recycling of surplus phloem water via the xylem. Plant Cell Environ. 38, 1048-1059 (2015).

[9]

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

[10]

Chang, B.-M., Zhang, Y. & Keller, M. Softening at the onset of grape ripening alters fruit rheological properties and decreases splitting resistance. Planta 250, 1293-1305 (2019).

[11]

Clarke, S. J., Hardie, W. J. & Rogiers, S. Y. 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 (2010).

[12]

Tracey, J. P. & Saunders, G. R. A technique to estimate bird damage in wine grapes. Crop Prot. 29, 435-439 (2010).

[13]

Anderson, T. L. Fracture Mechanics: Fundamentals and Applications . (CRC Press, 2017).

[14]

Cosgrove, D. J. Diffuse growth of plant cell walls. Plant Physiol. 176, 16-27 (2018).

[15]

Vullo, V. Circular Cylinders and Pressure Vessels (Springer, 2014).

[16]

Considine, J. A. & Brown, K. 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 (1981).

[17]

Keller, M., Smith, J. R. & Bondada, B. R. Ripening grape berries remain hydraulically connected to the shoot. J. Exp. Bot. 57, 2577-2587 (2006).

[18]

Thomas, T. R., Matthews, M. A. & Shackel, K. A. 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 (2006).

[19]

Castellarin, S. D., Gambetta, G. A., Wada, H., Shackel, K. A. & Matthews, M. A. Fruit ripening in Vitis vinifera: spatiotemporal relationships among turgor, sugar accumulation, and anthocyanin biosynthesis. J. Exp. Bot. 62, 4345-4354 (2011).

[20]

Matas, A. J., Cobb, E. D., Paolillo, D. J. & Niklas, K. J. Crack resistance in cherry tomato fruit correlates with cuticular membrane thickness. HortScience 39, 1354-1358 (2004).

[21]

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

[22]

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

[23]

Khanal, B. P., Grimm, E., Finger, S., Blume, A. & Knoche, M. Intracuticular wax fixes and restricts strain in leaf and fruit cuticles. N. Phytol. 200, 134-143 (2013).

[24]

Airianah, O. B., Vreeburg, R. A. M. & Fry, S. C. Pectic polysaccharides are attacked by hydroxyl radicals in ripening fruit: evidence from a fluorescent fingerprinting method. Ann. Bot. 117, 441-455 (2016).

[25]

Andrews, J ., Adams, S. R., Burton, K. S. & Edmondson, R. N. Partial purification of tomato fruit peroxidase and its effect on the mechanical properties of tomato fruit skin. J. Exp. Bot. 53, 2393-2399 (2002).

[26]

Andrews, J., Adams, S. R., Burton, K. S. & Evered, C. E. Subcellular localization of peroxidase in tomato fruit skin and the possible implications for the regulation of fruit growth. J. Exp. Bot. 53, 2185-2191 (2002).

[27]

Barceló, A. R., Pomar, F., López-Serrano, M. & Pedreño, M. A. Peroxidase: a multifunctional enzyme in grapevines. Funct. Plant Biol. 30, 577-591 (2003).

[28]

Ribeiro, J. et al. The contribution of extensin network formation to rapid, hydrogen peroxide-mediated increases in grapevine callus wall resistance to fungal lytic enzymes. J. Exp. Bot. 57, 2025-2035 (2006).

[29]

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

[30]

Gao, Y., Fangel, J. U., Willats, W. G. T., Vivier, M. A. & Moore, J. P. Dissecting the polysaccharide-rich grape cell wall matrix using recombinant pectinases during winemaking. Carbohyd. Polym. 152, 510-519 (2016).

[31]

Pinelo, M., Arnous, A. & Meyer, A. S. Upgrading of grape skins: Significance of plant cell-wall structural components and extraction techniques for phenol release. Trends Food Sci. Technol. 17, 579-590 (2006).

[32]

Agudelo-Romero, P., Bortolloti, C., Pais, M. S., Tiburcio, A. F. & Fortes, A. M. Study of polyamines during grape ripening indicate an important role of polyamine catabolism. Plant Physiol. Biochem. 67, 105-119 (2013).

[33]

Pottosin, I. et al. Cross-talk between reactive oxygen species and polyamines in regulation of ion transport across the plasma membrane: implications of plant adaptive responses. J. Exp. Bot. 65, 1271-1283 (2014).

[34]

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

[35]

Lai, X., Khanal, B. P. & Knoche, M. Mismatch between cuticle deposition and area expansion in fruit skins allows potentially catastrophic buildup of elastic strain. Planta 244, 1145-1156 (2016).

[36]

Khanal, B. P. & Knoche, M. Mechanical properties of cuticles and their primary determinants. J. Exp. Bot. 68, 5351-5367 (2017).

[37]

Keller, M., Viret, O. & Cole, F. M. Botrytis cinerea infection in grape flowers: defense reaction, latency, and disease expression . Phytopathology 93, 316-322 (2003).

[38]

Viret, O., Keller, M., Jaudzems, V. G. & Cole, F. M. Botrytis cinerea infection of grape flowers: light and electron microscopical studies of infection sites . Phytopathology 94, 850-857 (2004).

[39]

Grimm, E. et al. Localized bursting of mesocarp cells triggers catastrophic fruit cracking. Hortic. Res. 6, 79-88 (2019).

[40]

Keller, M. & Shrestha, P. M. Solute accumulation differs in the vacuoles and apoplast of ripening grape berries. Planta 239, 633-642 (2014).

[41]

Castellarin, S. D. et al. 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 (2015).

[42]

Calderón, A. A., Zapata, J. M. & Ros Barceló, A. Peroxidase isoenzymes as markers of cell de-differentiation in grapevines (Vitis vinifera) . Vitis 34, 207-210 (1995).

[43]

Pereira, C. S. et al. Extensin network formation in Vitis vinifera callus cells is an essential and causal event in rapid and H2O2-induced reduction in primary cell wall hydration. BMC Plant Biol. 11, 106 (2011).

[44]

Thomas, T., Shackel, K. & Matthews, M. 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).

[45]

Winkler, A., Peschel, S., Kohrs, K. & Knoche, M. 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 (2016).

[46]

Hernández-Montes, E., Zhang, Y., Chang, B.-M., Shcherbatyuk, N. & Keller, M. Soft, sweet and colorful: stratified sampling reveals sequence of events at the onset of grape ripening. Am. J. Enol. Vitic. 72, 137-151 (2021).

[47]

Buda, G. J., Isaacson, T., Matas, A. J., Paolillo, D. J. & Rose, J. K. C. Three-dimensional imaging of plant cuticle architecture using confocal scanning laser microscopy. Plant J. 60, 378-385 (2009).

[48]

Ficke, A., Gadoury, D. M., Seem, R. C., Godfrey, D. & Dry, I. B. Host barriers and responses to Uncinula necator in developing grape berries. Phytopathology 94, 438-445 (2004).

[49]

Rogiers, S. Y., Hatfield, J. M., Jaudzems, V. G., White, R. G. & Keller, M. Grape berry cv. Shiraz epicuticular wax and transpiration during ripening and preharvest weight loss. Am. J. Enol. Vitic. 55, 121-127 (2004).

[50]

Liszkay, A., van der Zalm, E. & Schopfer, P. Production of reactive oxygen intermediates (O2.-, H2O2, and .OH) by maize roots and their role in wall loosening and elongation growth . Plant Physiol. 136, 3114-3123 (2004).

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