Control of plant development and gene expression by sugar signaling
Introduction
Plants, like other organisms, need to coordinate development with the availability of crucial nutrients, such as soluble sugars. For example, it may be beneficial for plants to adjust the timing with which nutrient-intensive events occur to ensure an adequate supply of materials and energy for successful completion of those events. Levels of sugars, such as sucrose, have been postulated to affect the timing with which at least some plant species flower (reviewed in [1]). Soluble sugar levels have also been shown to affect other phase changes, such as the onset of senescence (reviewed in [2]). Besides affecting the timing with which developmental events occur, soluble sugar levels can also affect organ number and shape. Higher sugar levels may lead to the formation of plants that produce larger and thicker leaves, and increased numbers of tubers and adventitious roots. Some of the most well-characterized examples of developmental processes that are affected by soluble sugar levels are discussed in more detail below and are summarized in Table 1.
The mechanisms by which sugars act to influence plant development and gene expression are just beginning to be deciphered. Understanding of sugar response is complicated by the fact that plants have multiple sugar-response pathways and that the molecules actually being sensed are not known in all cases. Although glucose and sucrose appear to be sensed directly, in some cases, different sugars or sugar metabolites might sometimes act as the actual signal molecules. For example, recent evidence has implicated trehalose-6-phosphate in the control of some sugar responses (reviewed in 3., 4.). In addition, many sugar responses may actually be regulated by alterations in sugar flux [5] or in C:N ratios (reviewed in 6., 7.) rather than by absolute sugar or sugar-metabolite levels. Sugar response pathways also ‘interact’ or exhibit ‘cross-talk’ with numerous other pathways, including those for phytohormone (reviewed in 8.•, 9.•, 10.•) and light responses (reviewed in 2., 11.).
An additional factor that complicates our understanding of sugar responses is that sugars can act by affecting osmotic potentials as well as by functioning as signaling molecules. For example, the inhibitory effects of glucose and sucrose on Arabidopsis hypocotyl elongation in the dark can be mimicked by osmoticum such as sorbitol (L Sommerlad, SI Gibson, unpublished). By contrast, osmoticum cannot completely mimic the effects of sugars on the rate of germination of Arabidopsis seeds 12.•, 13.•, 14., 15.. Consequently, appropriate osmotic controls are essential in distinguishing between events that are mediated by sugars acting as osmotica and events in which sugars act via other mechanisms.
A better understanding of sugar-response pathways will require the identification and characterization of more of their components. Information regarding sugar-response pathways can be obtained from recent reviews 3., 4., 9.•, 10.•, 16.•, 17., 18., 19., 20., 21.. Although not a focus of this review, genetic loci that are believed to affect sugar response are summarized in Table 2.
Section snippets
Seed and embryo development
The levels of soluble sugars, such as glucose and sucrose, are known or postulated to regulate developmental processes spanning from embryo development to senescence. The role of soluble sugars in embryo development has predominantly been studied using large-seeded legumes as models (reviewed in 8.•, 22.). In these plants, development has been found to proceed in a wave-like fashion across the cotyledons. Using bioluminescence and single-photon counting, glucose concentrations were shown to be
Seed germination and early seedling development
The levels of glucose and other sugars have been shown to affect seed germination and early seedling development. The effects of sugars on these processes are proving to be complicated. Sugars appear to exert a positive effect in some assays but negative effects in other assays. In some cases, different concentrations of sugars may exert varying effects. In addition, sugars appear to affect these developmental processes via more than one pathway. With hindsight, this complexity of control is
Effects of sugars on the formation of adult organs and tissues
In addition to mediating early developmental events, soluble sugars also effect the formation of more adult structures, such as leaves, nodules, pollen, tubers and roots. For example, growth at elevated CO2 concentrations, which presumably increases sugar production, sometimes leads to the formation of larger and thicker leaves (reviewed in [2]). The homeodomain leucine zipper transcription factor ATHB13 of Arabidopsis has been implicated in regulation of leaf shape in response to sugar levels
Effects of sugars on timing of developmental events
Sugars also help to regulate the timing of developmental phase changes, such as the progression from juvenile to adult phases, flowering and senescence. When the RUBISCO small subunit was expressed in an antisense orientation in tobacco, leaf source strength decreased with a concomitant extension in the length of an early phase of shoot development [59]. More recently, knockouts of a cyclin D gene in the moss Physcomitrella patens have suggested that cyclin D helps to integrate metabolism and
Sugar-regulation of gene expression
Analyses of limited sets of genes suggested that significant numbers of plant genes are regulated at the steady-state mRNA level in response to sugar levels. In addition, several lines of evidence have suggested the existence of hexokinase-dependent, hexokinase-independent and sucrose-specific signaling pathways (reviewed in 6., 7., 9.•, 10.•, 18., 20., 21., 75., 76.). More recently, Affymetrix GeneChips have been used to investigate sugar-regulated gene expression in Arabidopsis on a more
Conclusions
Alterations in the levels of soluble sugars, such as glucose and sucrose, have been shown to affect developmental programs ranging from embryogenesis to senescence. In some cases, sugar levels or flux appear to determine whether an event occurs (e.g. whether additional tubers or adventitious roots are formed) or the timing with which an event occurs (e.g. the timing of flowering and senescence). As the role of sugar levels in many developmental processes has not yet been examined, the number of
References and recommended reading
Papers of particular interest, published within the annual period of review, have been highlighted as:
• of special interest
•• of outstanding interest
Acknowledgements
Research in the author's laboratory in this area is supported by the Energy Biosciences Program of the US Department of Energy.
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