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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. Fruit, a major evolutionary acquisition, are designed to execute a plant’s evolutionary plan of perpetuating the likeness of species for population persistence, and they do so by functioning as baits to frugivores whose predatory action mediates seed dispersal. This adaptive trait seems to be the underlying selective force in the evolution of fleshy fruit attractive to animals (Rodrıguez et al., 2013). Because humans are ancestrally derived from frugivorous primates (Dudley, 2004), these alluring organoleptic and nutritional communicative traits, in effect, intended for reproductive success, also appeal intuitively to their sense of aesthetics and liking, for instance berries of grapevine, grapes as fresh and dry fruit, and wine. Among all the sensorial ripening traits, the total soluble solids (TSS) are the most sought-after attributes as a result of their close relationship with organoleptic quality of fruit. The major components of TSS are soluble sugars, glucose (predominant substrate for fermentation), and fructose and organic acids such as tartaric and malic (Coombe, 1992; Kader, 1999). These compounds vary both spatially and temporally during the normal course of ripening to yield desirable fruit qualities. Because of their organoleptic values, TSS along with flavonoids and volatile aroma compounds have traditionally functioned as the universal set of criteria for judging fruit for commercial harvesting, especially grapes (Ribéreau-Gayon et al., 2000). For fruit to attain a morphocompositional aesthetic appeal through cytological and compositional modifications of the parenchymatous tissues for commercial use like in making wine from grapes, it is imperative that fruit undergo unhindered the highly organized events of ripening. Failure to do so results in numerous ripening disorders marked by a wide range of undesirable physical and quality attributes (Watkins, 2007). Some well-known examples of physiological disorders that reduce fresh market quality include blossom end rot of tomato [Solanum lycopersicum (Guichard et al., 2001; Ho et al., 2010)], split and shattered pits and double fruit of peach [Prunus persica (Ceponis et al., 1987)], albino and malformed fruit of strawberry [Fragaria · ananassa (Singh et al., 2007)], etc. Even the cultivated grapevines, the most ancient and widely known fruit crop of commercial importance (This et al., 2006), develops several physiological disorders. For instance, the bunch stem necrosis, also known as water berry, is the oldest known affliction (Bioletti, 1923). Other ripening physiopathies that render grapes qualitatively incompetent include sunburn, dehydration, and SOUR shrivel (Bondada and Keller, 2012a; Krasnow et al., 2010). Common to all these disorders is shriveling of the pericarp; however, each shrivel type is distinct (Bondada and Keller, 2012a). As yet, there are no known causes for any of these disorders. Among the many Received for publication 20 May 2014. Accepted for publication 23 June 2014. Financial support for this study was provided by the Wine Advisory Committee, the Washington Wine Commission. Corresponding author. E-mail: bbondada@wsu.edu. J. AMER. SOC. HORT. SCI. 139(5):567–581. 2014. 567 unexplained shrivel disorders that the grape and wine industry are grappling with today, none is more paradoxical and economically detrimental to fruit quality than SOUR shrivel (Bondada and Keller, 2012a, 2012b), also known as berry shrivel (Hall et al., 2011; Knoll et al., 2010), and sugar accumulation disorder (Krasnow et al., 2009) in viticulture parlance. This physiopathy is relatively a recent and lesser known oddity but has gained much notoriety for being the most perplexing ripening enigma of modern viticulture afflicting both red and white cultivars (Bondada and Keller, 2012b) and hybrids (Griesser et al., 2012) worldwide (Bachteler et al., 2013). The key aspect of SOUR shrivel is that it renders afflicted clusters unusable both by humans and the seed dispersers, the avian frugivores, who as humans adopted similar criteria for fruit choice, particularly of preferring hexoses over sucrose (Wilson and Downs, 2012). Typical symptoms of SOUR shrivel include flaccid berries caused by the loss of membrane competence in the mesocarp cells, high osmotic potential resulting from low accumulation of sugars and thus increased sourness, reduced levels of color, amino and oxalic acids, and very often the berries develop an off-flavor (Bondada and Keller, 2012b; Griesser et al., 2012; Knoll et al., 2010; Krasnow et al., 2009). In a given block, yield loss can be up to 50% (Bondada et al., 2009). What precisely causes such physiological, biochemical, and structural changes are not known. In the context of climate change scenarios (Jones et al., 2010), the incidence of SOUR shrivel is likely to exacerbate in the foreseeable future and with no known clues, the vexation will escalate among grape growers and viticulturists. Consequently, there is an urgent need for preventive measures by exploring its mechanistic basis before it blights the productivity of vineyards around the world. This article compares the structure and morphology between healthy and afflicted shoots including clusters by using techniques of light and scanning electron microscopy (SEM) concomitant with compositional analysis of fruit to determine whether a functional link exists between vine structure and the incidence of SOUR shrivel. The rationale for such a line of inquiry lay in the fact that success in understanding the underlying mechanisms with which they provoke any affliction requires histological analysis, a microscopic tool routinely used in examining physiological disorders of fruit including grapes (Agusti et al., 2001; Freeman, 1976; Miqueloto et al., 2014; Rogiers et al., 2004). This methodology will not only aid in assessing yield and quality losses of SOUR shrivel affliction, but also in providing clues to ripening disorders of other fruit that share analogous symptomatology and eventually in planning preventive measures to curb the overall rising incidence of fruit disorders. Fig. 1. Photographs of a (A) healthy ‘Cabernet Sauvignon’ grape cluster showing spherical berries attached to the rachis with healthy pedicels, (B) ‘Cabernet Sauvignon’ grape cluster wherein the berries are wholly afflicted with suppression of uniform ripening (SOUR) shrivel, but the cluster framework remained healthy (inset, a single SOUR shrivel-afflicted berry resembling a deflated soccer ball), stereomicrographs showing (C) longitudinal section of a healthy berry with a seed overlain by anthocyanins, and (D) longitudinal section of a SOUR shrivel berry with collapsed and nonviable mesocarp that disorganized the vascular bundles but the mesocarp within the vicinity of seeds remained healthy (inset). Scale bars: 10 mm (A–B), 1 mm (B inset), 1 mm (C–D). 568 J. AMER. SOC. HORT. SCI. 139(5):567–581. 2014. Materials and Methods PLANT MATERIAL. Commercial vineyards with mature ownrooted V. vinifera cultivars Cabernet Sauvignon and Grenache located near Benton City, WA (lat. 46 15#47.48$ N, long. 119 29#16.09$ W) were chosen for anatomizing SOUR shrivel disorder during the 2011–13 growing seasons. This vineyard was chosen because these vines consistently exhibited incidences of all physiological ripening disorders including SOUR shrivel. The vineyards had vine by row spacing of 1.83 · 2.74 m on a uniformly deep (greater than 1 m) loamy fine sand. Vines were trained to bilateral cordon, which entailed training the vines in both directions along the cordon (an extension of the trunk) wire from the trunk and were drip-irrigated during the growing season. Training in viticulture parlance refers to the design and development of a grapevine framework. The shoots emerging from the cordon were positioned vertically using catch wires. Vines were spur-pruned during winter; i.e., canes (a mature woody and lignified stem from

journal of the american society for horticultural science

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