Cell death in grape berries: varietal differences linked to xylem pressure and berry weight loss

Abstract

Abstract. Some varieties of Vitis vinifera L. can undergo berry weight loss during later stages of ripening. This defines a third phase of development in addition to berry formation and berry expansion. Berry weight loss is due to net water loss, but the component water flows through different pathways have remained obscure. Because of the very negative osmotic potential of the cell sap, the maintenance of semipermeable membranes in the berry is required for the berry to counter xylem and apoplast tensions that may be transferred from the vine. The transfer of tension is determined by the hydraulic connection through the xylem from the berry to the vine, which changes during development. Here we assess the membrane integrity of three varieties of V. vinifera berries (cvv. Shiraz, Chardonnay and Thompson seedless) throughout development using the vitality stains, fluorescein diacetate and propidium iodide, on fresh longitudinal sections of whole berries. We also measured the xylem pressure using a pressure probe connected to the pedicel of detached berries. The wine grapes, Chardonnay and Shiraz, maintained fully vital cells after veraison and during berry expansion, but began to show cell death in the mesocarp and endocarp at or near the time that the berries attain maximum weight. This corresponded to a change in rate of accumulation of solutes in the berry and the beginning of weight loss in Shiraz, but not in Chardonnay. Continuous decline in mesocarp and endocarp cell vitality occurred for both varieties until normal harvest dates. Shiraz grapes classified as high quality and sourced from a different vineyard also showed the same death response at the same time after anthesis, but they displayed a more consistent pattern of pericarp cell death. The table grape, Thompson seedless, showed near to 100% vitality for all cells throughout development and well past normal harvest date, except for berries with noticeable berry collapse that were treated with giberellic acid. The high cell vitality in Thompson seedless berries corresponded to negative xylem pressures that contrasted to the slightly positive pressures for Shiraz and Chardonnay. We hypothesise that two variety dependent strategies exist for grapevine berries late in development: (1) programmed cell death in the pericarp and loss of osmotically competent membranes that requires concomitant reduction in the hydraulic conductance via the xylem to the vine; (2) continued cell vitality and osmotically competent membranes that can allow high hydraulic conductance to the vine.Additional keywords: berry shrivel, berry weight loss, cell death, grape berry development.

Understanding Differential Responses of Grapevine (Vitis vinifera L.) Leaf and Fruit to Water Stress and Recovery Following Re-Watering

“…Consequently, the berries were spherical (Figure 6(B)) caused by turgid mesocarp cells with semipermeable plasmalemma and a very low osmotic potential as evidenced by a thin fluorescence emitting from their cytoplasm (Figure 5(C)). A low osmotic potential of the mesocarp cells is expected to balance the negative pressure in the apoplast and the tension generated in vine xylem by leaf transpiration allowing high hydraulic conductance to the vine [58]. This crafts an ideal setting for backflow to occur especially in the event of water stress [49] causing shriveling of berries as observed with un-ripened (no or less color) berries, not with ripened berries of the present study.…”

Not All Shrivels Are Created Equal—Morpho-Anatomical and Compositional Characteristics Differ among Different Shrivel Types That Develop during Ripening of Grape (<i>Vitis vinifera</i> L.) Berries

“…A similar scenario occurs in pears afflicted with internal browning, a physiological disorder wherein the leaking of cell liquid into the intercellular space following membrane damage reduced the gas diffusivity [108]. In grape berries such as Chardonnay and Shiraz, leakiness of cell membranes in the mesocarp and breaking down of cell compartmentation have been reported but this generally occurs at or near the time when the berries attain maximum weight and continue to decline until normal harvest dates, not at the inception of ripening [38]. What may trigger BS is not known at this time.…”

“…For instance, as evident in this study, the mesocarp represented about 75% -85% of the weight of which water accumulation accounts for about 70% -80% of the weight [37]. Collectively, the growth of mesocarp and its water balance determined by supply of sap through peripheral vascular bundles, back flow to other organs, and by cuticular transpiration has dominant effect on the overall growth of the berry [13,31,38,39]. The same is true for apricots, peach, and apple and hence could be regarded as the general feature of the growth of many fleshy fruits [40] with a minor variation in grape berry in that the mesocarp is separated by the dorsal vascular bundles into inner and outer zones, the inner and outer mesocarp [41][42][43].…”

Integrative Effects of Vine Water Relations and Grape Ripeness Level of Vitis vinifera L. cv. Shiraz/Richter 99. I. Physiological Changes and Vegetative-Reproductive Growth Balances

“…The osmotic potential of the berry is also not determined solely by sugar, but an array of compounds, including amino acids, organic acids, inorganic cations and anions, and other taste and flavour compounds, all contributing to the soluble solid/ osmotic status of the berry. Although partial degeneration seems more evident (Krasnow et al, 2008;Fontes et al, 2011), the viability of the internal structure of the berry (mesocarp cell integrity) changes during this time, be it because of compartmentation/membrane breakdown and/or cell death (Dreier et al, 1998;Tilbrook & Tyerman, 2008), hence the decrease in firmness and observed shrivelling (Krasnow et al, 2008). According to Thomas et al (2006), cell membranes (assumed plasmalemma and tonoplast) remain intact post-véraison [the difficulty is that few studies dealing with phloem transport, unloading, berry/cell integrity, etc.…”