Overexpression of Arabidopsis Hexokinase in Tomato Plants Inhibits Growth, Reduces Photosynthesis, and Induces Rapid Senescence

Abstract

Sugars are key regulatory molecules that affect diverse processes in higher plants. Hexokinase is the first enzyme in hexose metabolism and may be a sugar sensor that mediates sugar regulation. We present evidence that hexokinase is involved in sensing endogenous levels of sugars in photosynthetic tissues and that it participates in the regulation of senescence, photosynthesis, and growth in seedlings as well as in mature plants. Transgenic tomato plants overexpressing the Arabidopsis hexokinase-encoding gene AtHXK1 were produced. Independent transgenic plants carrying single copies of AtHXK1 were characterized by growth inhibition, the degree of which was found to correlate directly to the expression and activity of AtHXK1 . Reciprocal grafting experiments suggested that the inhibitory effect occurred when AtHXK1 was expressed in photosynthetic tissues. Accordingly, plants with increased AtHXK1 activity had reduced chlorophyll content in their leaves, reduced photosynthesis rates, and reduced photochemical quantum efficiency of photosystem II reaction centers compared with plants without increased AtHXK1 activity. In addition, the transgenic plants underwent rapid senescence, suggesting that hexokinase is also involved in senescence regulation. Fruit weight, starch content in young fruits, and total soluble solids in mature fruits were also reduced in the transgenic plants. The results indicate that endogenous hexokinase activity is not rate limiting for growth; rather, they support the role of hexokinase as a regulatory enzyme in photosynthetic tissues, in which it regulates photosynthesis, growth, and senescence. INTRODUCTIONSugars are central compounds in nature that serve as essential metabolic nutrients and structural components for most organisms. They are also major regulatory molecules that control gene expression, metabolism, physiology, cell cycle, and development in prokaryotes and eukaryotes (Newgard and McGarry, 1995;Ronne, 1995;Saier et al., 1995). In plants, it has been shown that sugars regulate the expression of a broad spectrum of genes involved in many essential processes (e.g., Sheen, 1990;Thomas and Rodriguez, 1994;Stitt and Sonnewald, 1995; Graham, 1996; Koch, 1996;Smeekens, 1998). Furthermore, sugars affect developmental and metabolic processes throughout the life cycle of the plant. These processes include germination, growth, flowering, senescence, sugar metabolism, and photosynthesis (von Schaewen et al., 1990;Dickinson et al., 1991;Stitt et al., 1991; Goldschmidt and Huber, 1992; Huber and Hanson, 1992; Bernier et al., 1993; Ding et al., 1993; Yang et al., 1993;Thomas and Rodriguez, 1994; Dangl et al., 1995; Kovtun and Daie, 1995; Jang and Sheen, 1997;Perata et al., 1997;Prata et al., 1997;Smeekens and Rook, 1997; Wingler et al., 1998).Photosynthesis is regulated by sugar levels, and this regulation overrides that of light, tissue type, and developmental stage (Sheen, 1990;von Schaewen et al., 1990; Krapp et al., 1993). Increased concentrations of externally supplemented sugar o...

Large‐scale identification of leaf senescence‐associated genes

“…It has been hypothesized that sugars, in addition to their important role in energy supply, might act as signal molecules triggering the senescence program (Yoshida, 2003). The hexokinase-mediated sugar signaling pathway has been suggested to regulate the initiation of senescence (Dai et al, 1999). Lipid degradation also accompanies the other characteristic catabolic processes of leaf senescence (Thompson et al, 1998), and is re¯ected by an increase in the expression of a lipase (At2g42690) and Phospholipase Da (Fan et al, 1997).…”

Ethylene Insensitivity Results in Down-Regulation of Rubisco Expression and Photosynthetic Capacity in Tobacco

“…Also, in these cases, genes related to photosynthesis were repressed, including those for chlorophyllbinding protein and Rubisco (Sheen, 1990;Krapp and Stitt, 1995;. The regulation of photosynthetic gene expression by sugars is thought to be mediated by the enzyme hexokinase, a sensor of endogenous Glc levels (Jang et al, 1997;Dai et al, 1999;Moore et al, 2003). However, a complete understanding of photosynthetic acclimation in response to high CO 2 or sugars is still lacking.…”

Novel Gene Encoding a Ca2+-Binding Protein and under Hexokinase-dependent Sugar Regulation

“…35) In the transduction of sugar signals, hexokinase can act as a sensor for both sugar-repressible and sugar-inducible gene expression. 3) Sugar-inducible, down-regulation mediated by hexokinase occurs for genes linked to a role of sugar in plant functions such as photosynthesis, 3) starch degradation, 18) and adaptation in leaf cells in the dark.…”