Control of plant development and gene expression by sugar signaling

Coordination of development with the availability of nutrients, such as soluble sugars, may help ensure an adequate supply of building materials and energy with which to carry out specific developmental programs. For example, in-vivo and in-vitro experiments suggest that increasing sugar levels delay seed germination and stimulate the induction of flowering and senescence in at least some plant species. Higher sugar concentrations can also increase the number of tubers formed by potatoes and can stimulate the formation of adventitious roots by Arabidopsis. New insights into the mechanisms by which sugar-response pathways interact with other response pathways have been provided by microarray experiments examining sugar-regulated gene expression under different light and nitrogen conditions.

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.