The role of lipids as molecular sentinels in grape ripening

Abstract

Grape berry growth and ripening involve continuous physical, biochemical, and physiological changes driven by a dynamic genetic program. Traditional models of berry development often rely on population averages, but recent single-berry studies [1-2] have shown that these models can be substantially biased by the asynchrony of ripening phases and developmental kinetics. This highlights the need for higher-resolution analyses. Building on this, single-berry metabolomics [3] has revealed previously unrecognized transient stages and metabolic switches during fruit development, including distinct metabolic clusters. Increasing temporal resolution enabled detection of metabolite groups that signal the onset of ripening, notably transient lipid changes that coincide with the rise in ABA, the key hormone of non-climacteric ripening.

Under climate-change-related abiotic stresses, such as drought, grapevines activate adaptive mechanisms that reshape their metabolism. Lipids are essential constituents of the cellular membrane, ensuring integrity and fluidity, and they also form the fruit cuticle, which limits water loss and protects against external damage. Polyunsaturated fatty acids (PUFAs) arise through desaturase activity, which introduces double bonds into acyl chains; in grapevine, linoleic (C18:2) and linolenic (C18:3) acids are the most abundant. Drought during fruit development can affect PUFAbiosynthesis and alter the saturated-to-unsaturated fatty acid ratio, with significant implications for membrane properties. At veraison, lipid peroxidation—driven by LOX—modifies membrane lipids [3]. These oxidative processes are tightly linked to the controlled accumulation of reactive oxygen species (ROS), including hydrogen peroxide (H₂O₂), which may act as signals that initiate the regulatory network of fruit development.

Here, severe and prolonged drought stress applied to potted Barbera vines, starting 23 days after flowering, resulted in ripe fruits with a significant increase in total fatty acids, indicating a potential resilience response to water stress, with long-chain fatty acids possibly stabilizing cell membranes under stress. The reduction in C18:2 at the onset of ripening with several active VviLOX, VviHPL and VviADH suggests that PUFAdegradation due to oxidative stress is enhancing fruit ripening, with more enphasis under stress.

References

Savoi S, Torregrosa L, Romieu C. 2021. Transcripts switched off at the stop of phloem unloading highlight the energy efficiency of sugar import in the ripening V. vinifera fruit. Horticulture Research 8, 1–15.

Savoi S, Shi M, Sarah G, Weber A, Torregrosa L, Romieu C. 2025 Time-resolved transcriptomics of single Vitis vinifera fruits: membrane transporters as switches of the double sigmoidal growth, Journal of Experimental Botany.

Tavernier F, Savoi S, Torregrosa L, Hugueney P, Baltenweck R, Segura V, Romieu C. 2025. The single-berry metabolomic clock paradigm reveals new stages and metabolic switches during grapevine berry development. Journal of Experimental Botany

Pilati S, Brazzale D, Guella G, Milli A, Ruberti C, Biasioli F, Zottini M, Moser C. 2014. The onset of grapevine berry ripening is characterized by ROS accumulation and lipoxygenase-mediated membrane peroxidation in the skin. BMC Plant Biology 14, 87.

Acknowledgements

We would like to thank Danilo Caruso for his work during the field experiment and analysis.