Structural and Compositional Characterization of Suppression of Uniform Ripening in Grapevine: A Paradoxical Ripening Disorder of Grape Berries with No Known Causative Clues

Abstract

Grapes (Vitis vinifera) have been used as a model system for understanding ripening and ripening-related physiological disorders in fleshy fruit; hence, a comparative analysis was undertaken to explore the mechanistic basis of a paradoxical ripening phenomenon of grape berries known as suppression of uniform ripening (SOUR) shrivel. Fruit organoleptic attributes coupled with morphology and structure, and tissue organization in various organs of healthy and afflicted field-grown grapevines were examined using a range of microscopy techniques. As opposed to healthy berries, SOUR shrivel berries were flaccid and had the lowest pH and lowest levels of sugars, potassium (K), and malic acid that paralleled with a significant reduction in the synthesis of anthocyanin. On the other hand, titratable acidity, tartaric acids, and tannins were much higher than perfectly healthy berries. The SOUR shrivel cluster tinged its rachis red but held no relationship with flaccidity of the berries because healthy vines totally devoid of SOUR shrivel clusters also displayed same coloration. Furthermore, although the phloem sieve tubes in both cases were plugged with callose, a carbohydrate generally implicated in impeding translocation in phloem, the afflicted grapevines exhibited relatively more plugged sieve tubes. The study revealed that the spatiotemporal configuration of cell and tissue communities determining the structure–function relationship remained intact in afflicted vines throughout the growing season. However, the functionality, especially of flows in phloem sieve tubes, started to decelerate after veraison (initiation of ripening) most likely as a result of early activation of callose synthesis and subsequently plugging of sieve plates during the remaining course of ripening. Hence, in future studies, a broader analysis of phloem sieve tubes entailing its flows and ultrastructure in phloem-girdled grapevines simulating symptoms of SOUR shrivel is needed to characterize the mechanistic basis of SOUR shrivel.