Hydraulic isolation of ripening grape berries: the end of a dogma

Abstract

It has long been believed that ripening grape berries become dependent upon phloem water supply because xylem flow into the berries ceases at veraison due to rupture of vessels during rapid berry expansion. We provide evidence that this hydraulic isolation dogma should be replaced by a new model. We monitored berry diameter on grapevines during drydown and rewatering at veraison and measured berry solutes and leaf gas exchange. We also pressurized roots or shoots with or without adding xylem-mobile dye to probe xylem functionality. Using field-grown vines, we conducted a mass balance analysis on ripening berries to estimate rates of berry growth, transpiration, and phloem flow. Finally, using a modified pressure-chamber technique, we extracted apoplast sap from ripening berries and compared its composition with that of cell sap. Measurements indicated a sudden rise in phloem inflow into berries undergoing veraison on drought-stressed vines. Rewatering accelerated berry expansion by stimulating leaf photosynthesis, but girdling the cluster peduncle prevented this effect. Pressurizing the roots or shoots increased expansion only in preveraison berries, but led to cracking of postveraison berries. Pressurization also restored the normally impeded dye movement into ripening berries. Our results showed that the phloem generally supplied more water than was needed for berry growth and transpiration. Solute accumulation and changes in pH and osmotic pressure in the berry apoplast differed from that inside the cells and were under developmental control. These results demonstrated that phloem inflow is controlled by sugar demand in the ripening berries and that these berries do not become hydraulically isolated. While xylem flow remains reversible, it is usually from berry to shoot during ripening. We propose a model in which surplus phloem water that osmotically follows the unloaded sugar to the berry apoplast is recycled directly to the xylem or transpired across the skin. Xylem backflow and transpiration may serve as ‘overflow valves’ for excess phloem water, thus facilitating sugar accumulation and protecting berries from cracking.