A Novel Small Heat Shock Protein Gene,vis1, Contributes to Pectin Depolymerization and Juice Viscosity in Tomato Fruit

Abstract

We have characterized a novel small heat shock protein gene, viscosity 1 (vis1) from tomato (Lycopersicon esculentum) and provide evidence that it plays a role in pectin depolymerization and juice viscosity in ripening fruits. Expression of vis1 is negatively associated with juice viscosity in diverse tomato genotypes. vis1 exhibits DNA polymorphism among tomato genotypes, and the alleles vis1-hta (high-transcript accumulator; accession no. AY128101) and vis1-lta (low transcript accumulator; accession no. AY128102) are associated with thinner and thicker juice, respectively. Segregation of tomato lines heterogeneous for vis1 alleles indicates that vis1 influences pectin depolymerization and juice viscosity in ripening fruits. vis1 is regulated by fruit ripening and high temperature and exhibits a typical heat shock protein chaperone function when expressed in bacterial cells. We propose that VIS1 contributes to physiochemical properties of juice, including pectin depolymerization, by reducing thermal denaturation of depolymerizing enzymes during daytime elevated temperatures.Ripening of fleshy fruits is a dynamic transitional period that encompasses a myriad of biochemical and physiological changes leading to easily perceivable alterations in fruit texture, firmness, pigmentation, aroma, and sweetness (Tucker, 1993;Grierson and Fray, 1994). Significant progress has been made in characterizing the molecular components of fruitripening process, including ethylene biosynthesis and perception, cell wall depolymerization, light signal transduction, and carotenoid accumulation (Giovannoni, 2001). Fruit ripening-related cell wall depolymerization has been investigated in tomato (Lycopersicon esculentum) pericarp to understand the molecular components that regulate the physiochemical properties of cell walls during plant growth and development in general and fruit textural changes in particular (Brownleader et al., 1999). These studies have provided evidence that depolymerization of polyuronides (Huber and O'Donoghue, 1993; Brummell and Labavitch, 1997) and hemicelluloses (Maclachlan and Brady, 1994; Brummell et al., 1999b) and the loss of Gal (Tong and Gross, 1988) are the most prominent changes that occur in cell walls during fruit ripening. Reverse genetics has been used to delineate effects of several cell wall polymer modifying and depolymerizing enzymes that show coordinated increases during the fruit-ripening process (Giovannoni, 2001). Characterization of the effects of polygalacturonase (Giovannoni et al., 1989;Smith et al., 1990;Kramer et al., 1992; Brummell et al., 1997) and pectin methylesterase in transgenic plants over-or underexpressing these enzymes (Tieman et al., 1992;Tieman and Handa, 1994) showed that they play roles in pectin degradation but do not significantly effect pericarp texture. Impaired expression of two tomato ␤-glucanases by antisense technology suggested that these enzymes affect fruit metabolism but do not change fruit phenotype (Lashbrook et al., 1998; Brummell et al., 1999a). How...

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