Sugar Sensing and Signaling in Plants

Abstract

In addition to their essential roles as substrates in carbon and energy metabolism and in polymer biosynthesis, sugars have important hormone-like functions as primary messengers in signal transduction. The pivotal role of sugars as signaling molecules is well illustrated by the variety of sugar sensing and signaling mechanisms discovered in free-living microorganisms such as bacteria and yeast (Stulke and Hillen, 1999; Rolland et al., 2001). For such unicellular organisms, nutrient availability is the main extracellular factor controlling growth and metabolism. The role of nutrients as regulatory molecules has come to be appreciated only recently in mammals despite extensive previous research on Glc homeostasis and diabetes (Hanson, 2000; Rolland et al., 2001). In plants, sugar production through photosynthesis is a vital process, and sugar status modulates and coordinates internal regulators and environmental cues that govern growth and development (Koch, 1996; Sheen et al., 1999; Smeekens, 2000). Although the regulatory effect of sugars on photosynthetic activity and plant metabolism has long been recognized, the concept of sugars as central signaling molecules is relatively novel. Recent progress has begun to reveal the molecular mechanisms underlying sugar sensing and signaling in plants, including the demonstration of hexokinase (HXK) as a Glc sensor that modulates gene expression and multiple plant hormone-signaling pathways (Sheen et al., 1999; Smeekens, 2000). Analyses of HXK mutants will provide new evidence for distinct signaling and metabolic activities. Diverse roles of Snf1-related protein kinases (SnRKs) in carbon metabolism and sugar signaling also are emerging (Halford and Hardie, 1998; Hardie et al., 1998). In addition, Suc, trehalose, and other HXK-independent sugar sensing and signaling pathways add more complexity in plants (Goddijn and Smeekens, 1998; Lalonde et al., 1999; Smeekens, 2000). Biochemical, molecular, and genetic experiments have supported a central role of sugars in the control of plant metabolism, growth, and development and have revealed interactions that integrate light, stress, and hormone signaling (Roitsch, 1999; Sheen et al., 1999; Smeekens, 2000; Gazzarrini and McCourt, 2001; Finkelstein and Gibson, 2002) and coordinate carbon and nitrogen metabolism (Stitt and Krapp, 1999; Coruzzi and Bush, 2001; Coruzzi and Zhou, 2001). A number of reviews have appeared in the past few years emphasizing different aspects of sugar signaling and its interactions with other plant signal transduction pathways. In this review, the extent and impact of the sugar signaling network on plant life is illustrated. We explore diverse sugar responses, summarize biochemical and genetic evidence for different sugar sensing and signaling mechanisms, consider the extensive regulatory web that mediates sugar and hormone signaling, and suggest possible directions for future research. Differential Effects of Sugars on Plant Source and Sink Activities. Suc is transported from photosynthesizing source leaves to sink organs such as roots, meristems, young leaves, flowers, fruit, and developing seed. Lowered (L) sugar levels can increase source activities, including photosynthesis, nutrient mobilization, and export. In contrast, higher (H) sugar levels in sink tissues stimulate growth and storage. Accumulation of higher (H) sugar levels in source tissues, however, is believed to downregulate photosynthesis, ensuring the maintenance of sugar homeostasis. The differential source-sink effects allow the adaptation of carbon metabolism to changing environmental conditions and to the availability of other nutrients. The effect of carbon allocation on organ and whole plant architecture is illustrated most dramatically by carbohydrate storage and the concomitant cell expansion in reserve organs such as roots, fruit, seed, and tubers. However, cell division and differentiation can be ascribed to both changes in metabolic activity and sophisticated developmental switches (Jackson, 1999; Wobus and Weber, 1999a; Hajirezaei et al., 2000; White et al., 2000; Giovannoni, 2001). In Vicia faba embryos, gradients of sugars have been reported to correlate spatially with mitotic activity (Borisjuk et al., 1998). Consistently, Arabidopsis D-type cyclin gene expression is regulated differentially by sugars (Riou-Khamlichi et al., 2000). Therefore, sugars also could act as morphogens, providing positional information to the cell cycle machinery and different developmental programs. Remarkably, differential display analysis using portions of tomato meristems destined to form leaves revealed spatially regulated carbohydrate metabolism within the meristem and suggested the involvement of carbohydrate metabolism in organogenesis (Pien et al., 2001). Sugar sensing and signaling are involved in the control of growth and development during the entire plant life cycle. During germination and early seedling development, sugars can rep