Rapid dehydration of grape berries dampens the post-ripening transcriptomic program and the metabolite profile evolution

Abstract

The postharvest dehydration of grape berries allows the concentration of sugars and other solutes and promotes the synthesis of metabolites and aroma compounds unique to high-quality raisin wines such as the passito wines made in Italy. These dynamic changes are dependent on environmental parameters such as temperature and relative humidity, as well as endogenous factors such as berry morphology and genotype, but the contribution of each variable is not well understood. Here, we compared berries subjected to natural or accelerated dehydration, the latter driven by forced air flow. We followed the evolution of transcript and metabolite profiles and found that accelerated dehydration clearly dampened the natural transcriptomic and metabolomic programs of postharvest berries. We found that slow dehydration over a prolonged duration is necessary to induce gene expression and metabolite accumulation associated with the final quality traits of dehydrated berries. The accumulation of key metabolites (particularly stilbenoids) during postharvest dehydration is inhibited by rapid dehydration conditions that shorten the berry life time.

References

[1] Coombe, B. G. & McCarthy, M. G. Dynamics of grape berry growth and physiology of ripening. Aust. J. Grape Wine Res. 6, 4 (2000).

[2] Paronetto, L. & Dellaglio, F. Amarone: a modern wine coming from an ancient production technology. Adv. Food Nutr. 63, 21 (2011).

[3] Barbanti, D., Mora, B., Ferrarini, R., Tornielli, G. B. & Cipriani, M. Effect of various thermo-hygrometric conditions on the withering kinetics of grapes used for the production of “Amarone” and “Recioto” wines. J. Food Eng. 85, 350-358 (2008).

[4] Mencarelli, F. & Bellincontro, A. Sweet, Reinforced and Fortified Wines: Grape Biochemistry, Technology and Vinification (eds F. Mencarelli & P. Tonutti) 25 (Wiley-Blackwell, 2013).

[5] Zamboni, A. et al. Molecular analysis of post-harvest withering in grape by AFLP transcriptional profiling. J. Exp. Bot. 59, 4145-4159 (2008).

[6] Fasoli, M. et al. The grapevine expression atlas reveals a deep transcriptome shift driving the entire plant into a maturation program. Plant Cell 24, 3489-3505 (2012).

[7] Zenoni, S. et al. Disclosing the molecular basis of the postharvest life of berry in different grapevine genotypes. Plant Physiol. 172, 1821-1843 (2016).

[8] Costantini, V., Bellincontro, A., De Santis, D., Botondi, R. & Mencarelli, F. Metabolic changes of Malvasia grapes for wine production during postharvest drying. J. Agr. Food Chem. 54, 3334-3340 (2006).

[9] Bellincontro, A., De Santis, D., Botondi, R., Villa, I. & Mencarelli, F. Different postharvest dehydration rates affect quality characteristics and volatile compounds of Malvasia, Trebbiano and Sangiovese grapes for wine production. J. Sci. Food Agr. 84, 1791-1800 (2004).

[10] Versari, A., Parpinello, G. P., Tornielli, G. B., Ferrarini, R. & Giulivo, C. Stilbene compounds and stilbene synthase expression during ripening, wilting, and UV treatment in grape cv. Corvina. J. Agr. Food Chem. 49, 5531-5536 (2001).

[11] Rizzini, F. M., Bonghi, C. & Tonutti, P. Postharvest water loss induces marked changes in transcript profiling in skins of wine grape berries. Postharvest Biol. Technol. 52, 247-253 (2009).

[12] Bellincontro, A., Fardelli, A., De Santis, D., Botondi, R. & Mencarelli, F. Postharvest ethylene and 1-MCP treatments both affect phenols, anthocyanins, and aromatic quality of Aleatico grapes and wine. Aust. J. Grape Wine Res. 12, 141-149 (2006).

[13] Zoccatelli, G. et al. Skin pectin metabolism during the postharvest dehydration of berries from three distinct grapevine cultivars. Aust. J. Grape Wine Res. 19, 171-179 (2013).

[14] Salvetti, E. et al. Whole-metagenome-sequencing-based community profiles of vitis vinifera L. cv. corvina berries withered in two post-harvest conditions. Front. Microbiol. 7, 937 (2016).

[15] Seymour, G. B., Østergaard, L., Chapman, N. H., Knapp, S. & Martin, C. Fruit development and ripening. Annu. Rev. Plant Biol. 64, 219-241 (2013).

[16] Ding, Y. et al. Network analysis of postharvest senescence process in citrus fruits revealed by transcriptomic and metabolomic profiling. Plant Physiol. 168, 357-376 (2015).

[17] Tonutti P. & Bonghi C. in Sweet, Reinforced and Fortified Wines: Biochemistry and Physiology of Dehydrating Berries. (eds. F. Mencarelli, & P. Tonutti ) 25 (Wiley-Blackwell, 2013).

[18] Barkan, A. & Small, I. Pentatricopeptide repeat proteins in plants. Annu Rev. Plant Biol. 65, 415 (2014).

[19] Xing, H. T. et al. Genome-wide investigation of pentatricopeptide repeat gene family in poplar and their expression analysis in response to biotic and abiotic stresses. Sci. Rep. 8, 2817 (2018).

[20] Tilbrook, J. & Tyerman, S. D. Cell death in grape berries: varietal differences linked to xylem pressure and berry weight loss. Funct. Plant Biol. 35, 1-12 (2008).

[21] Krasnow, M., Matthews, M. & Shackel, K. 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 (2008).

[22] Fontes, N., Côrte-Real, M. & Gerós, H. New observations on the integrity, structure, and physiology of flesh cells from fully ripened grape berry. Am. J. Enol. Vitic. 62, 279-284 (2011).

[23] Clarke, S. J. & Rogiers, S. Y. The role of fruit exposure in the late season decline of grape berry mesocarp cell vitality. Plant Physiol. Biochem 135, 69-76 (2019).

[24] Jeandet, P. et al. Biosynthesis, metabolism, molecular engineering and biological functions of stilbene phytoalexins in plants. Biofactors 36, 331-341 (2010).

[25] Dal Santo, S. et al. The plasticity of the grapevine berry transcriptome. Genome Biol. 14, r54 (2013).

[26] Anesi, A. et al. Towards a scientific interpretation of the terroir concept: plasticity of the grape berry metabolome. BMC Plant Biol. 15, 191 (2015).

[27] Dal Santo, S. et al. Grapevine field experiments reveal the contribution of genotype, the influence of environment and the effect of their interaction (GxE) on the berry transcriptome. Plant J. 93, 1143-1159 (2018).

[28] Gatto, P. et al. Ripening and genotype control stilbene accumulation in healthy grapes. J. Agr. Food Chem. 56, 11773-11785 (2008).

[29] Massonnet, M. et al. Ripening transcriptomic program in red and white grapevine varieties correlates with berry skin anthocyanin accumulation. Plant Physiol. 174, 2376-2396 (2017).

[30] Fasoli, M. et al. Timing and order of the molecular events marking the onset of berry ripening in grapevine. Plant Physiol. 178, 1187-1206 (2018).

[31] Rienth, M. et al. Day and night heat stress trigger different transcriptomic responses in green and ripening grapevine (vitis vinifera) fruit. BMC Plant Biol. 14, 108 (2014).

[32] Pastore, C. et al. Whole plant temperature manipulation affects flavonoid metabolism and the transcriptome of grapevine berries. Front. Plant Sci. 8, 929 (2017).

[33] Sterjiades, R., Dean, J. F. D. & Eriksson, K. E. L. Laccase from Sycamore Maple (Acer-Pseudoplatanus) polymerizes monolignols. Plant Physiol. 99, 1162-1168 (1992).

[34] Bao, W., O’Malley, D. M., Whetten, R. & Sederoff, R. R. A laccase associated with lignification in loblolly pine xylem. Science 260, 672-674 (1993).

[35] Berthet, S. et al. Disruption of LACCASE4 and 17 results in tissue-specific alterations to lignification of Arabidopsis thaliana stems. Plant Cell 23, 1124-1137 (2011).

[36] Zhang, Y. C. et al. Overexpression of microRNA OsmiR397 improves rice yield by increasing grain size and promoting panicle branching. Nat. Biotechnol. 31, 848 (2013).

[37] Wang, Y. et al. LACCASE5 is required for lignification of the Brachypodium distachyon Culm. Plant Physiol. 168, 192-U951 (2015).

[38] Wang, G. D., Li, Q. J., Luo, B. & Chen, X. Y. Ex planta phytoremediation of trichlorophenol and phenolic allelochemicals via an engineered secretory laccase. Nat. Biotechnol. 22, 893-897 (2004).

[39] Pourcel, L. et al. TRANSPARENT TESTA10 encodes a laccase-like enzyme involved in oxidative polymerization of flavonoids in Arabidopsis seed coat. Plant Cell 17, 2966-2980 (2005).

[40] Hu, Q. et al. Laccase GhLac1 modulates broad-spectrum biotic stress tolerance via manipulating phenylpropanoid pathway and jasmonic acid synthesis. Plant Physiol. 176, 1808-1823 (2018).

[41] Ramakers, C., Ruijter, J. M., Deprez, R. H. L. & Moorman, A. F. M. Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci. Lett. 339, 62-66 (2003).

[42] Pfaffl, M. W., Horgan, G. W. & Dempfle, L. Relative expression software tool (REST (c)) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 30, e36 (2002).