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Control of plant development and gene expression by sugar signaling

Susan I Gibson
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.
Addresses Department of Plant Biology, University of Minnesota, 122 Cargill Building, 1500 Gortner Avenue, St. Paul, Minnesota 55108-1095, USA Corresponding author: Gibson, SI (gibso043@tc.umn.edu)

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 sugarresponse 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 [8–10]) 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 [3,4,9,10,16,17–21]. Although not a focus of this review, genetic loci that are believed to affect sugar response are summarized in Table 2.
Current Opinion in Plant Biology 2005, 8:93–102

Current Opinion in Plant Biology 2005, 8:93–102 This review comes from a themed issue on Growth and development Edited by Liam Dolan and Michael Freeling Available online 19th November 2004 1369-5266/$ – see front matter # 2005 Elsevier Ltd. All rights reserved. DOI 10.1016/j.pbi.2004.11.003

Abbreviations ABA ABI2 ATHB13 pho3 SnRK abscisic acid ABA INSENSITIVE2 Arabidopsis thaliana B13 transcription factor phosphate3 SNF1-RELATED PROTEIN KINASE

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
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particularly phytohormone response pathways. Barley plants expressing SnRK1 in an anti-sense orientation abort pollen development. Trehalose-6-phosphate synthase activity is required for the flowering of Arabidopsis. in part due to difficulties in measuring tissue-specific sucrose and hexose concentrations during the development of small seeds such as those produced by Brassica napus and Arabidopsis thaliana [25. Most studies suggest that increasing sucrose levels help to induce flowering. such as ATP. glucose and fructose. One of the most fascinating aspects of these findings is that they suggest that glucose and sucrose act in almost opposite fashions during legume seed development. Elevated CO2 levels can induce the formation of larger and thicker leaves. soluble sugars have been postulated to act as regulatory molecules that help to control seed and embryo development. has also been shown to be important in regulating response to sugars (reviewed in [9. On the basis of these findings. The mechanisms by which sugar gradients are generated. 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. Cross-talk with other response pathways. inhibit cotyledon expansion. Interestingly. sugars appear to affect these developmental processes via more than one pathway. as well as how they act to help regulate seed development. Elevated sucrose concentrations can lead to the formation of increased numbers of potato tubers. Sugars appear to exert a positive effect in some assays but negative effects in other assays. this complexity of control is probably not surprising given the complex nature of the many www. In some cases. but not mannose or sorbitol.24]. as well as low concentrations of mannose. with the roles of some loci not apparent when examining plants that carry mutations in only a single locus but becoming evident when plants carrying mutations in multiple loci are examined [30]. Induction of senescence Seed and embryo development The levels of soluble sugars. Exogenous sucrose allows Arabidopsis to flower in complete darkness. In fact. with higher ATP levels being found in regions in which storage starch is beginning to form [31]. Glucose stimulates senescence in combination with low concentrations of nitrogen. different concentrations of sugars may exert varying effects.22]). Tissue-specific and temporally regulated expression of hexose transporters and invertases might play a role in establishing and maintaining sugar gradients [27]. true leaf formation and root growth of young Arabidopsis seedlings. Glucose retards the rate of Arabidopsis seed germination but allows seeds to germinate on otherwise inhibitory concentrations of ABA. High concentrations of glucose and sucrose. The manner in which phytohormone and sugar signals are integrated appears to be complex. glucose concentrations were shown to be greatest in nondifferentiated mitotically active cells. 8:93–102 to be induced by high sucrose concentrations or low glucose concentrations.26]. Seed germination and early seedling development The levels of glucose and other sugars have been shown to affect seed germination and early seedling development. such as glucose and sucrose. In these plants. stimulate the formation of adventitious roots on the hypocotyls of dark-grown Arabidopsis seedlings. Snf1related protein kinases (SnRKs) have been postulated Current Opinion in Plant Biology 2005. Sucrose. ATP levels have recently been shown to vary across developing barley seeds. with glucose promoting cell division and sucrose being associated with cell expansion and starch synthesis [23.sciencedirect. but the similar effects of sorbitol suggest that this is an osmotic response. whereas sucrose concentrations increase as cells mature and begin to accumulate starch storage reserves.10. With hindsight. suggesting that these proteins could act as part of a mechanism to allow differential responses to sucrose and glucose (reviewed in [28]).29]). Using bioluminescence and single-photon counting. Process Embryogenesis Seed germination Seedling development Hypocotyl elongation Leaf formation Nodule growth Pollen development Tuber formation Formation of adventitious root Juvenile-to-adult phase transition Flowering Sugar effects Glucose promotes cell division whereas sucrose promotes cell expansion and reserve deposition in legume cotyledons. Glucose and sucrose inhibit hypocotyl elongation of dark-grown Arabidopsis seedlings.com . Another type of complexity arises from the likelihood that some ‘sugar responses’ could actually be regulated by fluctuations in the levels of other metabolites that vary in concentration in parallel with changing sugar levels. development has been found to proceed in a wave-like fashion across the cotyledons. In addition. Exogenous glucose prolongs the juvenile growth phase of the moss Physcomitrella patens.94 Growth and development Table 1 Selected developmental processes postulated to be sugar regulated. alterations in sugar levels are also expected to affect the levels of other metabolites. The effects of sugars on these processes are proving to be complicated. Whether the seeds of other species respond to sugar gradients in a similar manner remains unclear. For example. Sucrose alleviates the negative effects of nitrate on the growth rates of soybean nodules. are currently being investigated.

1 expression prevents seed germination on sucrose. Glucose-hypersensitive early seedling development.com Current Opinion in Plant Biology 2005. sucrose-insensitive early seedling development Resistant to sugar-inducible expression of ADP-glucose pyrophosphorylase subunit ApL3. sugar-hypersensitive early seedling development Hypersensitive to sugar-inducible expression of ADP-glucose pyrophosphorylase subunit ApL3.1 hba1 hsr1 Protein kinase Membrane-anchored protein Histidine protein kinase.38. sugar-hypersensitive early seedling development Hypersensitive to sugar-inducible expression of ADP-glucose pyrophosphorylase subunit ApL3. Seedling growth defect partially rescued by glucose but not by sucrose. ethylene receptor Inhibitor of 1-aminocyclopropane1-carboxylic acid synthase Histidine protein kinase.sciencedirect.Control of plant development and gene expression by sugar signaling Gibson 95 Table 2 Selected loci postulated to affect plant sugar responses.84] abi5 Transcription factor [36. and overexpression confers sugar-hypersensitivity and early seedling development. Glucose-insensitive early seedling development Glucose-insensitive early seedling development Glucose-insensitive early seedling development Glucose-insensitive early seedling development Glucose-insensitive early seedling development Anti-sense AtGLR1. 8:93–102 . Loss-of-function mutations confer sugar-insensitivity. sugar-hypersensitive early seedling development Glucose-hypersensitive early seedling development Anti-sense AtHXK1 expression confers glucose-insensitivity. sugar-hypersensitive early seedling development Hypersensitive to sugar-inducible expression of ADP-glucose pyrophosphorylase subunit ApL3. sorbitol or mannitol Hypersensitive to sugar-inducible expression of b-amylase Hypersensitive to sugar-inducible expression of ADP-glucose pyrophosphorylase subunit ApL3. Sucrose-hypersensitive early seedling development. but not on glucose.87] [72] [76] [38. Glucose-hypersensitive early seedling development.41] [88] [40. overexpression confers glucose-hypersensitive early seedling development. ethylene receptor Plastid 30S ribosomal protein S21 Short chain dehydrogenase/ reductase (= ABA2) Hexokinase (= HXK1) Protein kinase (= CTR1) Molybdenum cofactor sulphurase (= ABA3) Transcription factor (= ABI4) Putative glutamate receptor Gene product not identified Gene product not identified (locus maps to chromosome 1) Gene product not identified (locus maps to chromosome 4) Gene product not identified (locus maps to chromosome 1) Gene product not identified (locus maps to chromosome 1) Putative nuclear-localized membrane protein Hexokinase [40.76] [87] [41] [40] [40.and sucrose-hypersensitive early seedling development. and overexpression confers sugar-hypersensitivity and early seedling development.83. and overexpression confers glucose-hypersensitivity and early seedling development Resistant to sugar-inducible expression of ADP-glucose pyrophosphorylase subunit ApL3 Resistant to sugar-inducible expression of ADP-glucose pyrophosphorylase subunit ApL3 Resistant to sugar-inducible expression of ADP-glucose pyrophosphorylase subunit ApL3.81.85] abi8 acn3 ATHB13 Protein function unknown Protein function unknown Transcription factor [44] [86] [45] ctr1 ein2 ein4 eto1 etr1 ghs1 gin1 gin2 gin4 gin5 gin6 GLR1.76] [38] [89] [90] [91] hsr2 [91] hsr3 [91] hsr4 [91] hys1 HXK1 [70] [37. sucrose insensitive early seedling development Resistant to sugar-inducible expression of b-amylase Predicted gene products Transcription factor Reference(s) [81.82] abi4 Transcription factor [36.81.38.72] isi1 isi2 isi3 Gene product not identified (locus maps to chromosome 4) Gene product not identified (locus maps to chromosome 1) Transcription factor (= ABI4) [84] [84] [84] isi4 Short chain dehydrogenase/ reductase (= ABA2) Gene product not identified (locus maps to chromosome 5) [84] lba1 [92] www. Loci/genes abi3 Selected sugar-response defects Some loss-of-function mutations confer resistance to the combined inhibitory effects of glucose and ABA on early seedling development. Loss-of-function mutations confer slight sugar-insensitivity. Glucose.41.and sucrose-insensitive early seedling development. Glucose-hypersensitive early seedling development and chlorophyll accumulation. ATHB13 overexpression inhibits the expansion of cotyledon cells in sucrose-grown plants and leads to hypersensitive sucrose induction of b-amylase and vegetative storage protein expression. Sensitive to sucrose-induced chlorosis. Glucose.

Together. HXK1. more recent studies suggest that exogenous glucose retards the rate at which endogenous ABA is broken down in germinating seeds [13]. ethylene overproducer1. GLUTAMATE RECEPTOR 1. whereas 10 mM 3-O-methylglucose has no significant effects on rates of seed germination.30]. In earlier studies.35].96 Growth and development Table 2 Continued Loci/genes lba2 MYB10 prl1 ram1 rgs1 rsr1 rsr4 sis1 sis4 sis5 SnRK1 sun1 sun6 sun7 Selected sugar-response defects Resistant to sugar-inducible expression of b-amylase CpMYB10 overexpression confers glucose-insensitive early seedling development Sugar-hypersensitive early seedling development Resistant to sugar-inducible b-amylase expression Overexpression confers glucose-hypersensitivity.and sucrose-insensitive early seedling development Glucose. is able to retard seed germination significantly at concentrations of 5–10 mM. GLR1. Interactions between sugar.94.15].13.13]. ethylene receptor1. and that the concentration of sugar necessary to exert a noticeable effect varies between different sugar species. these studies Current Opinion in Plant Biology 2005. By contrast. reduced b-amylase1. ram1. sis1. this result has been interpreted as suggesting that the delay of seed germination by relatively low concentrations of exogenous glucose and 3-Omethylglucose may occur via a hexokinase-independent mechanism [12]. Interestingly.100] [100] Abbreviations: acn3. sun1. eto1. Given the number of dramatic developmental and metabolic shifts www. in the presence of exogenous ABA. 30–60 mM) have been shown to cause measurable delays in seed germination [12. rsr1. earlier studies examining the effects of lower concentrations of glucose analogs found that mannose. impaired sucrose induction1. More recently. in which glucose and other sugars were found to exert negative effects on seed germination. Resolution of some of these apparent discrepancies will require more information about the mechanisms by which sugars. suggested that glucose retards seed germination via a pathway that does not involve the ABA-response pathway components ABI2. phytohormones and other factors regulate seed germination. As 3-O-methylglucose is a poor substrate for hexokinase. hba1. regulator of G-protein signaling1. these concentrations of sugars delay germination significantly.1. On the basis of these findings. glucose was found to allow wildtype seeds to germinate on otherwise inhibitory concentrations of abscisic acid (ABA) [34.com . Furthermore.and phytohormone-response pathways during seed germination are similarly complex. however. hypersenescence1. the glucose analog 3-Omethylglucose at concentrations of about 84 mM was also shown to delay seed germination [12]. the authors concluded that inhibition of seed germination by mannose occurs via a hexokinase-dependent pathway [33]. hsr1. glucose might be expected to exacerbate rather than to alleviate the negative effects of ABA on seed germination. These findings indicate that.and sucrose-insensitive early seedling development Glucose. sucrose-insensitive early seedling development Resistant to sucrose repression of plastocyanin expression Predicted gene products Gene product not identified Transcription factor WD-40 protein b-amylase G-protein coupled receptor Gene product not identified (locus maps to chromosome 1) Gene product not identified (locus maps to chromosome 5) Protein kinase (= CTR1) Short chain dehydrogenase/ reductase (= ABA2) Transcription factor (= ABI4) Protein kinase Gene product not identified Transcription factor (= ABI4) Gene product not identified Reference(s) [92] [93] [39. gin1. reduced sucrose responses1. low b-amylase1. much lower glucose concentrations (e. etr1. ein2. hys1. high b-amylase1. isi1. pleiotropic regulatory locus1. 0. glucose hypersensitive1.and sucrose-insensitive early seedling development Anti-sense PKIN1 expression confers sucrose-insensitive expression of sucrose synthase Resistant to sucrose repression of plastocyanin expression Resistant to sucrose repression of plastocyanin expression. rgs1. ghs1.1. Characterization of the effects of exogenous glucose on the seed germination rates of different ABA-metabolic and ABA-response mutants has. which is a much better substrate than 3-O-methylglucose for hexokinase [32].g. indicating that the effects of high sugar concentrations on seed germination rates are not solely due to osmotic stress [14. HEXOKINASE1. By contrast. developmental and metabolic changes that take place during these developmental stages. These findings are in contrast to the results described above. glucose is able either to stimulate seed germination or to alleviate the inhibitory effects of ABA on seed germination. prl1. equi-molar concentrations of sorbitol do not exert similar effects. sugar insensitive1. high sugar response1. acetate non-utilization3. ethylene insensitive2. lba1. glucose insensitive1.95] [96] [97] [98] [98] [41] [36] [36] [99] [100] [83. 8:93–102 suggest that different sugars may delay seed germination via different pathways.g. and loss-of-function confers sugar-insensitivity and early seedling development Resistant to sugar-inducible patatin expression Resistant to sugar-inducible patatin expression Glucose.3 M) of exogenous glucose and sucrose do not prevent seed germination. with a catalytic efficiency rate that is five orders of magnitude lower than that for glucose [32].sciencedirect. sucrose uncoupled1. ABI4 and ABI5 [12. Although high concentrations (e. On the basis of these results.

Interestingly. Pollen carrying the transgene cease development at the binucleate stage. Exogenous sugars also stimulate the formation of adventitious roots under certain conditions [57].and sucrose-mediated developmental arrest has been used to screen for sugar hypersensitive and insensitive mutants. increasing sucrose concentrations do not always correlate with the formation of greater numbers of tubers.48.49]). nodules. In addition to affecting the growth or development of organs that would normally form on a plant. pollen. Antisense expression of ADP-glucose pyrophosphorylase and overexpression of invertase have also been used to manipulate sugar levels.sciencedirect. The reason that these experiments. Characterization of these mutants has revealed that many of them are also defective in phytohormone metabolism or response (reviewed in [9. Ovule development may also be affected by the presence of the SnRK1 antisense transgene. These results suggest that some. tubers and roots. with concomitant alterations in tuber size and number [52.53]. 8:93–102 Effects of sugars on the formation of adult organs and tissues In addition to mediating early developmental events. sometimes leads to the formation of larger and thicker leaves (reviewed in [2]). which presumably increases sugar production. The negative effects of nitrate on nodule growth rates can be reduced by the addition of sucrose to the media. growth at elevated CO2 concentrations. When nitrate is added to the media of hydroponically grown soybeans. higher concentrations of sorbitol (0. Constitutive overexpression of a spinach sucrose transporter in transgenic potatoes led to elevated sugar levels in the tubers but no significant alterations in tuber size or total yield [54]. In addition. When Current Opinion in Plant Biology 2005. almost 100% of wildtype Arabidopsis seeds of the Columbia ecotype germinate in the presence of 300 mM glucose or sucrose [36].51]. The homeodomain leucine zipper transcription factor ATHB13 of Arabidopsis has been implicated in regulation of leaf shape in response to sugar levels [45]. Although equi-molar concentrations of mannitol and sorbitol do not exert the same effects. as none of the progeny of the transgenic plants inherit a copy of the transgene [47]. these results suggest that pollen and ovule development are dependent on normal metabolic response. As SnRK1 is believed to function in metabolic response pathways (reviewed in [16]). the possibility that sugars and phytohormones may affect different processes in different ways and via multiple mechanisms seems not unlikely. For example. Similarly. indicating that the effects of glucose and sucrose are not due to alterations in osmotic potential.18. such as extra tubers and adventitious roots. Overexpression of this gene in transgenic Arabidopsis leads to the formation of narrow cotyledons and leaves when plants are grown in the presence of exogenous sugars such as glucose and sucrose.29]). mutations in the ABI8 gene of Arabidopsis were found to confer resistance to both ABA inhibition of seed germination and glucose inhibition of early seedling development [44]. Although exogenous sugars do retard seed germination.5 M) do exert similar effects. However. true leaves or extensive root systems [36–41].43].4–0.com .Control of plant development and gene expression by sugar signaling Gibson 97 that occur during germination. of the inhibitory effects of exogenous glucose and sucrose on early seedling development are due to osmotic stress [36]. these seedlings fail to develop chloroplasts [42] and do not mobilize the majority of their seed storage lipid [14. These results were interpreted as indicating that ATHB13 modulates www. underand overexpression of hexokinases 1 and 2 also failed to alter tuber yield. sugar levels can cause the formation of extra organs. Further examination of these transgenic plants revealed that sucrose inhibits lateral expansion of cotyledonary cells in plants overexpressing ATHB13. However. Sugar levels also influence the normal growth and development of nodules and pollen. the majority of seedlings formed on these media fail to form expanded cotyledons. soluble sugars also effect the formation of more adult structures. However.10. given sufficient time the majority of wildtype seeds will germinate on even very high concentrations of sugars. These experiments suggest that hexokinases do not play a major role in the regulation of tuber formation [55. showed no correlation between sugar levels and tuber formation remains unclear. no significant differences in the leaves or cotyledons of wildtype and ATHB13-overexpressing plants were observed when the plants were grown in the presence of the non-metabolizable sugar analogs mannose and 3-O-methylglucose. leaf and cotyledon shape only in response to metabolizable sugars [45]. unlike the experiments described above. such as leaves. the rate of nodule growth is significantly reduced. For example. Several lines of evidence have led to the hypothesis that increasing sucrose concentrations correlate with formation of greater numbers of tubers (reviewed in [9. as the concentrations of mannose and 3-O-methylglucose used in these experiments were much lower than those of glucose and sucrose. Sorbitol and mannitol do not exert similar effects. suggesting that nodule growth rates are partially dependent on carbon availability:nitrogen availability [46]. Evidence that sugar-response pathways may play a role in pollen development is provided by experiments on transgenic barley expressing the protein kinase SnRK1 in an anti-sense orientation [47]. but not all. Most recently. This glucose. This effect has been shown relatively directly by in-vitro experiments in which the application of exogenous sucrose resulted in the formation of increased numbers of tubers [50. interpretation of the results of these experiments is complicated.56].

sugar levels have been postulated to affect the timing of flowering in at least some plant species (reviewed in [1]). Hexokinase has been implicated in the regulation of senescence because transgenic tomato plants that overexpress Arabidopsis HEXOKINASE1 senesce earlier [71]. also increase the formation of adventitious roots.sciencedirect. indicating that the effect is not due to alterations in the osmotic potential of the media and suggesting that only metabolizable sugars are effective in inducing adventitious root formation. More recently. direct contact of the hypocotyls with the sugar-containing media is necessary for the stimulation of adventitious root formation. acts in the sugarmediated regulation of senescence [73]. higher concentrations of sucrose (e.18. but only if nitrogen levels are low [69]. Recently.98 Growth and development wildtype Arabidopsis seedlings are grown in the dark on media containing around 15–60 mM sucrose. the roles of several components of the ABAresponse pathway in sugar-mediated regulation of senescence have been investigated. the knockout strain is insensitive to this glucose-mediated developmental delay [60]. the C:N ratios of leaf exudates from Arabidopsis and Sinapis alba increase under flowering-inductive conditions [62]. suggesting that senescence may be regulated more by C:N ratios than by absolute sugar levels. than wildtype plants. Similarly. In studies on Arabidopsis. Affymetrix GeneChips have been used to investigate sugar-regulated gene www. application of exogenous sugars stimulates the early stages of senescence. knockouts of a cyclin D gene in the moss Physcomitrella patens have suggested that cyclin D helps to integrate metabolism and development in this organism.67]). In this case. leaf source strength decreased with a concomitant extension in the length of an early phase of shoot development [59]. Application of sucrose to the apical part of the plant has also been shown to allow flowering of Arabidopsis in complete darkness [64]. As sugars and ABA have been shown to interact in the regulation of other developmental programs.76]). In addition. When the RUBISCO small subunit was expressed in an antisense orientation in tobacco. such as tomato. application of moderate (111 mM) concentrations of glucose stimulates the senescence of Arabidopsis. a correlation was found between greater export of carbohydrates from the leaves and increased flower induction [61].com . high (e.g. In addition. flowering of wildtype Arabidopsis [65]. such as the progression from juvenile to adult phases.9. An extracellular invertase is required for the cytokinin-mediated delay of senescence: cytokinins no longer delay senescence in the presence of an inhibitor of that invertase [74]. however. fructose and maltose did not exert similar effects [58]. but can inhibit the expression of some senescence-associated genes in the later stages of senescence (reviewed in [2. A role for sugar metabolism in the regulation of senescence by cytokinin has also been identified. Glucose and fructose. The effects of sugar levels on leaf senescence are complex. flowering by raising sugar concentrations above optimal levels. Endogenous leaf sugar levels tend to increase during senescence. Senescence can also be stimulated by low nitrogen concentrations [68]. but not mannose or sorbitol. The effects of sugars on the formation of adventitious roots are concentration dependent. lending further support to the hypothesis that sugars promote flowering. hexokinase-independent and sucrose-specific signaling pathways (reviewed in [6. Arabidopsis plants carrying mutations in the trehalose-6-phosphate synthase gene were shown to be unable to flower.g. 10. the formation of adventitious roots on the hypocotyls is stimulated. the finding that 30 mM sucrose also inhibits flowering is in contrast to previous reports and will require further experimentation to explain. Whereas wildtype Physcomitrella patens exhibits a prolonged juvenile phase when grown in the presence of glucose.7. The roles of other sugars and sugar metabolites in flowering are also being investigated. however.75. a species that flowers earlier under long-day conditions. Similarly. 150 mM) suppress rather than stimulate induction [57]. Similarly. 8:93–102 Sugar-regulation of gene expression Analyses of limited sets of genes suggested that significant numbers of plant genes are regulated at the steadystate mRNA level in response to sugar levels. 30 mM) concentrations of sucrose slightly inhibited. Recent studies are beginning to provide clues as to some of the molecular mechanisms by which sugars and other factors regulate senescence.21. More recently. several lines of evidence have suggested the existence of hexokinase-dependent. Genetic evidence for a link between sugar response and senescence is provided by findings that Arabidopsis hypersenescence1 (hys1) mutants senesce early and are hypersensitive to the inhibitory effects of exogenous sugars on early seedling development [70]. Sugar levels have also been shown to affect flowering in autonomously flowering species. and low (e. In-vitro studies on tomato revealed that optimal sucrose and nitrogen levels are necessary to promote flowering [63]. and Arabidopsis mutants with decreased HEXOKINASE1 activity senesce later [72]. 150 mM) concentrations of exogenous sucrose significantly inhibited. High concentrations (300 mM) of sucrose also inhibit the elongation of carrot radicles. Effects of sugars on timing of developmental events Sugars also help to regulate the timing of developmental phase changes. but not ABI4. flowering and senescence. indicating that this gene is essential for the transition to flowering in Arabidopsis [66]. Although it is possible that 150 mM sucrose could inhibit Current Opinion in Plant Biology 2005. glucose. For example. These studies suggest that Arabidopsis ABI5. In other studies.20.g.

Weber H: Seed development and differentiation: a role for metabolic regulation. 54:533-537. Petitjean A. Scha expression of rbcS and other photosynthetic genes by carbohydrates: a mechanism for the ‘sink regulation’ of photosynthesis?. GeneChips have also been used to examine interactions between sugar. Eastmond PJ.and light-regulated gene expression. have been shown to affect developmental programs ranging from embryogenesis to senescence. Six-day-old Arabidopsis seedlings were induced for three hours by treatment with glucose. Gene expression was analyzed using Affymetrix AG GeneChips. published within the annual period of review. Coruzzi G. sugar levels or flux appear to determine whether an event occurs (e. 125:61-64.  . Pellny TK: Carbon metabolite feedback regulation of leaf photosynthesis and development. References and recommended reading Papers of particular interest. the number of developmental processes postulated to be affected by sugar levels is expected to grow in the future. Rosette leaves were then harvested and gene expression analyzed using Affymetrix ATH1 Arabidopsis GeneChips. Zhou L: Carbon and nitrogen sensing and signaling in plants: emerging ‘matrix effects’. 8:93–102 2. A better understanding of the nature of the signals that are associated with different sugar responses will be useful in characterizing sugarresponse pathways. and that genes that are involved in metabolism are over-represented within this group [78]. J Exp Bot 2003. the possibility that different concentrations of glucose or nitrogen might affect the relative magnitudes of the observed effects should be considered. These experiments indicate that many genes are regulated by interactions between light and sugar signaling. The Arabidopsis phosphate3 (pho3) mutant was used to examine gene expression in adult plants in response to alterations in endogenous sugar levels. which encodes a sucrose transporter that functions in phloem loading. glucose and fructose. 4:247-253. suggesting the presence of mechanisms to coordinate nitrogen and carbon metabolism [80]. Houssa C. A potential mechanism for identifying additional sugar-regulated developmental events will be to scan lists of sugar-regulated genes that are identified by microarray experiments for genes known to be involved in different developmental events. whether additional tubers or adventitious roots are formed) or the timing with which an event occurs (e. Curr Opin Plant Biol 2001.Control of plant development and gene expression by sugar signaling Gibson 99 expression in Arabidopsis on a more global scale. Stitt M: Regulation of the Krapp A. Plant Cell 1993. Eastmond PJ. 6:231-235. Hofmann B. In some cases. Wobus U. Borisjuk L. 54:539-547. have been highlighted as:  of special interest  of outstanding interest 1. Also of future interest will be more precise information regarding the natures of the signals that trigger different sugar responses. ¨ fer C. 5.com Conclusions Alterations in the levels of soluble sugars. Bernier G. Additional experiments have investigated interactions between sugar and nitrogen signaling. Mutant plants accumulate high concentrations of sucrose. Many genes that are involved in glucose and trehalose metabolism were shown to be nitrate regulated. Li Y. 6:375-386. Interactions between carbon and nitrogen signaling were also suggested by studies examining nitrate response. Coruzzi GM. As the role of sugar levels in many developmental processes has not yet been examined. which contain information from approximately 8000 Arabidopsis genes. 3.g. 8. Plant Physiol 2001. such as glucose and sucrose. Radchuk R. Lejeune P: Physiological signals that induce flowering. 6. including some that are involved in carbon metabolism [77]. Bush DR: Nitrogen and carbon nutrient and metabolite signaling in plants. Weschke W. Graham IA: Is trehalose-6-phosphate a regulator of sugar metabolism in plants? J Exp Bot 2003. 7. Rolletschek H. Plant J 1993. glucose + nitrogen. The pho3 mutant carries a mutation in SUC2. www. Current Opinion in Plant Biology 2005. nitrogen. However. Paul MJ. Graham IA: Trehalose metabolism: a regulatory role for trehalose-6-phosphate? Curr Opin Plant Biol 2003. 3-O-methylglucose or nothing in the presence or absence of the protein synthesis inhibitor cycloheximide. Plant Biol 2004. suggesting that de novo protein synthesis is more typically required for glucose induction than for repression [79]. Havelange A. 4. Acknowledgements Research in the author’s laboratory in this area is supported by the Energy Biosciences Program of the US Department of Energy. In these experiments. Gene expression was monitored in whole seedlings using Affymetrix ATH1 GeneChips.g. Mutant and wildtype plants were grown in soil under long-day (16 h light) conditions until the first flowers began to open. Sixteen-day-old Arabidopsis plants were induced for eight hours by treatment with 0 mM or 30 mM sucrose in continuous light or the dark before harvesting whole seedlings. ten-day-old Arabidopsis seedlings were induced for 20 min with nitrate or a negative control. whether sugar levels or C:N ratios are being measured and whether absolute sugar levels or flux are being sensed. Questions that need to be answered include which sugars or sugar metabolites are actually being sensed. 3:817-828. which carry 22 500 probe sets. Small changes were detected in the expression of many genes. These experiments also indicate that cycloheximide affects the expression of glucose-induced genes more than that of glucose-repressed genes. 5:1147-1155. These experiments indicate that glucose treatment has stronger effects on gene expression than nitrogen treatment [79]. the timing of flowering and senescence). Shoot and root tissue were harvested and analyzed separately using Affymetrix ATH1 GeneChips.sciencedirect.

Brouquisse RM: In plants. light. Planta 2004. Koncz-Ka ´ lma ´ n Z. a nuclear WD protein. Smeekens SCM: Photosynthesis. Roby C. Wobus U. The authors include a good description of metabolic imaging studies that have led to the hypothesis that glucose and sucrose form gradients that help to regulate the development of legume cotyledons. 9. Leo sensor in higher plants. Zhou L. abscisic acid. www. Panitz R. Weber H. 23. Trends Plant 10. Garciarrubio A. Edited by Francis D. 9:5-19. physiologically relevant. 36. The work described in this paper demonstrates that low. 24. 40:151-160. 203:182-187. 29:521-530. The finding that glucose and sucrose play very different roles in the regulation of legume cotyledon development is of particular interest. Heyraud A. Gibson SI: Mobilization of seed storage lipid by Arabidopsis seedlings is retarded in the presence of exogenous sugars. Schuurmans JAMJ. 51:49-81. 19. Planta 1997. Salchert K. 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