Journal of Experimental Botany, Vol. 51, No. 90001, pp. 407-416,
February 2000
© 2000 Oxford University Press
Photosynthesis, sugars and the regulation of gene expression
Molecular Plant Physiology, University of Utrecht, Padualaan 8, 3584 CH Utrecht, The Netherlands
Received 26 March 1999; Accepted 30 September 1999
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Abstract |
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 Top Abstract IntroductionCarbon metabolite-mediated...Screening strategies for mutants...The mig mutant screenThe mig screen and...ConclusionsReferences |
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Sugar-mediated regulation of gene expression is a mechanism controlling the expression of many different plant genes. In this review, a compilation of the genes encoding photosynthetic proteins, subject to this mode of regulation, is presented. Several groups have devised different screening strategies to obtain Arabidopsis mutants in sugar sensing and signalling. An overview of these strategies has been included. Sugar-mediated regulation of gene expression is thought to require the hexokinase (HXK) protein. It has previously been shown that one such sugar, mannose, is capable of blocking germination in Arabidopsis. This inhibition is also mediated by HXK and occurs in the low millimolar concentration range. Here, the use of germination on mannose as an effective screening strategy for putative sugar sensing and signalling mutants is reported. T-DNA- and EMS-mutagenized collections were used to isolate 31 mannose-insensitive germination (mig) mutants. With the use of these mutants, a comparison between this screen and other existing sugar-sensing screens is presented.
Key words: Photosynthesis, sugars, mannose, Arabidopsis, mutants.
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Introduction |
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TopAbstractIntroductionCarbon metabolite-mediated...Screening strategies for mutants...The mig mutant screenThe mig screen and...ConclusionsReferences |
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In the 1770s Joseph Priestley performed experiments showing that plants release a type of air that allows combustion and, since then, photosynthesis has been the subject of a broad and intensive research effort. As a result, the pathways of photosynthesis are well established and the enzymatic properties of individual enzymes are well understood. The underlying mode of regulation, however, remains an area of relative ignorance. How are the synthesis and assembly of the multimeric protein complexes involved in photosynthesis regulated? And how is net photosynthetic activity regulated as the plant encounters a wide range of environmental conditions each day and throughout its life cycle? These questions are of great interest since this knowledge would eventually allow control and manipulation of the entire photosynthetic process. Progress in this area has been impressive and this review shows how molecular genetic techniques are contributing to a new understanding of these issues.
Although photosynthesis may be partly regulated at the enzyme or translation level (‘fine control’), bulk regulation (‘coarse control’) seems to take place at the level of transcript accumulation. In most cases patterns of protein accumulation reflect those of mRNA (Monroy and Schwartzbach, 1983; Nelson and Langdale, 1989; Kuhlemeier, 1992; Van Oosten and Besford, 1995).
Light-regulation of photosynthesis and expression of genes encoding proteins of photosynthesis are well-documented processes and several Arabidopsis mutant screens have begun to resolve the mode of regulation (Staub and Deng, 1996; Wei and Deng, 1996). Light, however, cannot account for the regulation that must take place as the plant encounters variations in other environmental and developmental factors and processes throughout its life cycle. Lately, a fundamental regulatory mechanism has been discovered which is capable of detecting the end-product of photosynthesis, sugars, and enhances or represses the photosynthetic apparatus by regulating transcription of the genes involved. This carbon metabolite-mediated regulatory mechanism is not only capable of regulating photosynthesis, but also of providing the necessary integration with plant metabolism as a whole.
Global atmospheric CO2 has risen from 27 Pa before the industrial revolution to 36 Pa 200 years later (Griffin and Seemann, 1996) due to human activity and is expected to double during the 21st century (McElroy, 1994). This dramatic increase is occurring much faster than the natural genetic adaptation of plants and is expected to alter the functional balance of photosynthesis reactions. In this context the study and understanding of photosynthesis function and regulation gain increasing importance.
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Carbon metabolite-mediated repression of genes involved in photosynthesis |
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TopAbstractIntroductionCarbon metabolite-mediated...Screening strategies for mutants...The mig mutant screenThe mig screen and...ConclusionsReferences |
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Carbon metabolite concentrations may affect the expression of genes encoding photosynthetic components in two different ways. The depletion of sugars leads to activation of gene expression and to an increase in photosynthetic capacity. When output exceeds the plant's capacity to metabolize or export sugars, the subsequent increase in sugar concentrations in the leaf triggers repression of genes for photosynthetic components and ultimately photosynthesis itself (Stitt, 1991; Krapp et al., 1993; Van Oosten and Besford, 1994, 1995). These two distinct effects, however, are probably the result of a single regulatory mechanism, as enhanced expression following sugar depletion seems to be largely the result of de-repression of sugar controls on transcription (Koch, 1996). mRNA stability and translation may, in some cases, also contribute to carbon metabolite modulation in vivo (Sheu et al., 1994; Rook et al., 1998). The putative advantage in sugar-mediated regulation of genes encoding photosynthetic components is that, in times of sugar deficiency, reserves will be mobilized to increase photosynthesis and sugar output, whereas valuable resources (e.g. reduced N) need not be committed to the processes if carbohydrate supplies are already sufficient.
The repression of both nuclear and plastidic genes for photosynthetic components (Table 1
) by elevated sugar concentrations has been demonstrated in several different ways. Many groups have shown that the addition of sugars to the external medium down-regulates the expression of such genes (Krapp et al., 1993; Dijkwel et al., 1996). Leaf discs have been cut and floated on a solution containing 175 mM sucrose or glucose and repression of the chloroplastic ribulose-1,5-bisphosphate carboxylase/oxygenase (RBCS) gene was observed (Van Oosten and Besford, 1994). Similar experiments, using detached, single leaves with the cut petioles placed in a sugar-containing solution, examined the expression of the triose phosphate translocator gene, with similar results (Knight and Gray, 1994). A maize protoplast suspension was used and the expression of seven different promoters of genes encoding photosynthetic components was measured when various sugars were supplied to the external media (Jang and Sheen, 1994). All of the metabolizable sugars tested were able to repress expression. Sugar uptake was not involved, as the same effect was observed with sugars directly electroporated into the protoplasts. The low concentrations of sugars used for electroporation demonstrated the physiological relevance of the sugar-mediated regulation of expression of genes coding for photosynthesis proteins. This was later confirmed in Chenopodium rubrum cell-suspension cultures where 1 mM glucose sufficed to inhibit expression of RBCS (Klein and Stitt, 1998).
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A second strategy to observe down-regulation of genes coding for photosynthesis proteins is cold-girdling. Temperature-controlled aluminium blocks are placed around petioles of photosynthetically active source leaves of whole plants. The lowering of the temperature in the petiole inhibits the export of sugars and other metabolites, resulting in a rise in sugar concentrations in the leaf to a point where repression of gene expression occurs (Krapp et al., 1993). These strategies, while useful in the study of sugar-regulated gene expression, should be viewed with caution as they may, in some instances, lead to high, physiologically non-relevant, internal sugar concentrations.
A third means of triggering repression of photosynthesis through repression of the genes involved is by placing plants in a carbon dioxide-rich atmosphere. The increase in pCO2 leads initially to increased photosynthesis rates (reviewed in Stitt, 1991) and to increased intracellular sugar concentrations (Arp, 1991; Wullschleger et al., 1992). However, over a period of days, photosynthetic rates decline (Curtis et al., 1995; Van Oosten and Besford, 1995) due, probably, to an accumulation of sugars in the leaves (Von Schaewen et al., 1990; Krapp et al., 1993; Van Oosten and Besford, 1994, 1995; Webber et al., 1994; Drake et al., 1997), or to the consequent increase in flux through hexokinase (Jang and Sheen, 1994; Koch, 1996). Remarkably, this is apparently not a cell-autonomous response, but is controlled at the whole plant level (Sims et al., 1998).
Yet another approach to altering internal sugar concentrations has been taken by producing transgenic tobacco plants expressing invertase derived from yeast in the cytosol, vacuole or apoplast (Von Schaewen et al., 1990; Sonnewald et al., 1991). Although direct measurements of gene expression were not carried out in these plants, increased carbohydrate accumulation and inhibition of photosynthesis was observed in all three cases. The increase in carbohydrate concentrations was proposed as the cause for the inhibition of photosynthesis (Heineke et al., 1994).
Apart from photosynthesis, carbon metabolites have been shown to control the expression of genes involved in processes as diverse as pathogen attack, environmental stress, storage protein accumulation, and starch, lipid and nitrogen metabolism (Hattori et al., 1990; Nakamura et al., 1991; Cheng et al., 1992; Karrer and Rodriguez, 1992; Koch et al., 1992; McLaughlin and Smith, 1994; Chevalier et al., 1996; Herbers et al., 1996; Prata et al., 1997). In general, it can be said that when sugar concentrations in the plant increase, there is repression of genes involved in mobilization of stored reserves and photosynthesis. At the same time, genes required for metabolism and storage of carbon metabolites for future use are induced. There are many genes whose expression is regulated by this mechanism (for reviews, see Koch, 1996; Quick and Schaffer, 1996; Jang and Sheen, 1997; Smeekens and Rook, 1997), and carbon metabolite-mediated regulation of gene expression seems to be a central and basic process, probably common to all higher plants.
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Screening strategies for mutants in sugar-mediated regulation of photosynthesis genes |
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TopAbstractIntroductionCarbon metabolite-mediated...Screening strategies for mutants...The mig mutant screenThe mig screen and...ConclusionsReferences |
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Biochemical and physiological approaches have delivered limited progress in unravelling the cascade of events by which sugars regulate gene expression. The foreseeable complexity of the mechanism, by analogy with the yeast system (Thevelein, 1994; Ronne, 1995; Gancedo, 1998), and the probable interactions with other plant regulatory and biosynthetic pathways (e.g. of hormones) and the environment (e.g. light, osmotic stress, nitrogen, phosphate supply, etc), make it impracticable to dissect the pathway based solely on such approaches. Genetic and molecular techniques, especially in Arabidopsis, provide powerful tools for dissecting complex pathways. The relative ease by which Arabidopsis mutants can be generated, the more recent ready availability of tagged mutant collections (Feldmann, 1991; Bancroft et al., 1992; Long et al., 1993; Aarts et al., 1995; Klimyuk et al., 1995; Wisman et al., 1998), and the development of efficient techniques for cloning the genes tagged (Ochman et al., 1988; Liu et al., 1995; Souer et al., 1995) further highlight the potential of a molecular approach. Several groups have, therefore, isolated putative Arabidopsis mutants in carbon metabolite-mediated gene regulation.
Arabidopsis seeds can be exposed to high concentrations of widely occurring metabolizable sugars that allow germination, but inhibit further seedling development. Several different groups have devised a number of such screens. Examples thereof are the gin (
glucose-
insensitive; Zhou et al., 1998), sig (
sucrose-
insensitive
growth; Pego et al., 1998), sis (
sugar-
in
sensitive; Gibson et al., 1998), and cai (
carbohydrate-
insensitive; Boxall et al., 1996) screens (Table 2). Mutants generated in these screens are putative sugar-insensitive mutants. In order to obtain putative sugar-hypersensitive mutants, a similar strategy was used except that seeds were screened for their inability to germinate or develop in the presence of otherwise non-inhibiting sugar concentrations. The gss (
glucose-
super
sensitive; Pego et al., 1998) and sss (
sucrose-
super
sensitive; Pego et al., 1998) are, as far as is known, the only such screens belonging to this class.
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Another approach used to obtain putative sugar-sensing mutants was to fuse a promoter of a sugar-regulated gene to a reporter gene. The plastocyanin gene promoter has been fused to the firefly luciferase gene and transformed into Arabidopsis (Dijkwel et al., 1997). Plastocyanin gene expression is repressed by 88 mM (3%) sucrose and, when present in the medium, luciferase is not transcribed and light is not emitted by the transgenic seedlings. By screening an ethyl methanesulphonate (EMS)-mutagenized population on 3% sucrose, 18 independent sucrose uncoupled (sun) mutants were isolated. A similar approach has been used (Martin et al., 1997) with a gene specific for sink tissues. These authors transformed Arabidopsis with the ß-glucuronidase gene, expression of which is enhanced by sugars, under the control of a class I patatin promoter. In the transgenic plants GUS staining is seen in the roots when 90 mM sucrose is present in the medium. By screening an EMS-mutagenized population on 90 mM sucrose with a non-destructive screening system for GUS activity, four different rsr ( reduced sucrose response) mutants were isolated.
Three other screens involving the sugar-inducible ß-amylase gene have yielded the low ß-amylase (lba; Mita et al., 1997a), reduced ß-amylase (ram; Donggiun et al., 1998), and high ß-amylase (hba; Mita et al., 1997b) mutants. The first two display reduced sugar-induction of ß-amylase gene expression whereas in the hba mutants this induction is increased. Although these screening strategies employed a gene which does not encode a protein of photosynthesis, it is conceivable that these mutants are also defective in sugar-mediated regulation of genes coding for photosynthetic components, but this remains to be tested.
Knowledge of the molecular mechanisms by which carbon metabolites regulate gene expression is still very limited, but mutants isolated from these screens are already proving to be highly useful in understanding the underlying mechanism(s). The gin1 mutant (Zhou et al., 1998) showed an unexpected link between the sugar signalling pathway and ethylene signalling. Both the ethylene overexpression mutant eto1-1, and the constitutive ethylene triple response mutant ctr1-1, had glucose-insensitive (gin) phenotypes, whereas the ethylene-insensitive mutant etr1-1 displayed a glucose hypersensitive phenotype. Epistasis analysis placed GIN1 downstream of the ethylene receptor ETR1 in the ethylene signalling pathway. GIN1 may function to balance the control of plant development in response to metabolic and hormonal stimuli that act antagonistically. Other interesting insights were obtained by directly measuring photosynthesis and respiration in three sun mutants (Van Oosten et al., 1997). Arabidopsis plants at the rosette stage were watered with 2-deoxyglucose (2-dG), a glucose analogue capable of repressing several genes encoding photosynthesis proteins (Jang and Sheen, 1994). Upon addition of the sugar analogue, respiration remained stable and, as expected, photosynthesis decreased in the wild type and also sun5 and sun7. In sun6, however, photosynthesis proceeded at rates close to those obtained in the absence of 2-dG. In the sun6 mutant the feedback loop, by which sugar can repress photosynthesis, is no longer functional. The recent cloning of the sun6 mutation revealed a surprising link between sugar-mediated gene regulation and abscisic acid signalling (C Huijser and S Smeekens, unpublished results). New insights into this interaction are expected to be obtained soon with this mutant.
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The mig mutant screen |
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TopAbstractIntroductionCarbon metabolite-mediated...Screening strategies for mutants...The mig mutant screenThe mig screen and...ConclusionsReferences |
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A different screen from the ones described above is the mannose-insensitive germination (mig) screen. It was based on the knowledge that mannose, a glucose epimer at the second carbon atom, was capable of repressing promoters of genes for photosynthetic components (Jang and Sheen, 1994) at considerably lower concentrations than glucose itself. It has also been found that even low concentrations of mannose are capable of repressing Arabidopsis germination and that additions of metabolizable sugars were sufficient to overcome this repression (Pego et al., 1999). With the use of several different metabolizable and non-metabolizable glucose analogues, it was shown that the inhibition of germination is mediated by hexokinase (HXK). These results were corroborated by the finding that mannoheptulose, a specific HXK inhibitor, restored germination to seeds grown in the presence of mannose. The conclusion that HXK is involved in the mannose-mediated repression of germination of Arabidopsis seeds is relevant, since HXK is thought to be the primary sensor in sugar-mediated regulation of the expression of many plant genes (Graham et al., 1994; Jang and Sheen, 1994).
EMS- and T-DNA-mutated Arabidopsis seeds were plated on media containing 7.5 mM mannose and seedlings that germinated were taken from the plates. These plants were allowed to set seed and each line was rescreened for the mannose-insensitive germination (mig) phenotype. Under these conditions, wild-type seed displays a 2–3% germination frequency background. Lines with a 12%, or higher, germination frequency were chosen as putative mig mutants. Approximately 13 000 independent EMS-mutagenized lines of ecotype Columbia glabrous (Lehle Seeds, Round Rock, TX, USA), and 6 500 independent T-DNA tagged lines (Ws ecotype) generated by Kenneth Feldmann, University of Arizona, were screened. From these two mutant seed collections, 31 putative mig mutants were isolated, with germination frequencies on 7.5 mM mannose of up to 86% (Fig. 1). Allelic tests are currently under way to determine the number of independent mutations present in this population.
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The mig screen is different from the ones described above for several reasons. Free mannose exists in plants only in trace amounts and is readily phosphorylated by HXK to mannose-6-phosphate (M-6-P). In many plant species M-6-P is only slowly metabolized (Herold and Lewis, 1977; Walker and Sivak, 1986) and, therefore, the addition of higher concentrations of mannose leads to the depletion of ATP and phosphate. Nevertheless, it was shown that the relatively low concentration of 7.5 mM mannose, used for the mig screen, did not provoke ATP depletion, and addition of phosphate to the mannose-containing medium did not restore germination to Arabidopsis seeds (Pego et al., 1999). Thus 7.5 mM mannose does not provoke ATP or phosphate depletion in Arabidopsis seeds and germination is repressed via an unknown, HXK-dependent mechanism. However, since ATP was only measured in whole seedlings, one may speculate about the possibility of ATP depletion in a specific cellular compartment which might be enough to block germination. Another peculiarity of the mig screen is that while high glucose and sucrose concentrations (over 300 mM) are needed to block seedling development, mannose can block germination at low concentrations (5 mM). This minimizes the probability of isolating undesired osmotic mutants.
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The mig screen and other putative sugar-sensing mutant screens |
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TopAbstractIntroductionCarbon metabolite-mediated...Screening strategies for mutants...The mig mutant screenThe mig screen and...ConclusionsReferences |
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Due to the similarity of several of the screens for mutants in sugar-mediated gene regulation (Table 2), and to the considerable number of mutants isolated to date, there is a possibility of mutant overlap between different screens. An experiment was set up to determine if this was indeed the case and, if so, to obtain a general idea of the extent of overlap. Seed from 30 mig mutants was plated on MS (Murashige and Skoog, 1962) medium, under the screening conditions for the mig (7.5 mM mannose), the sig and sis (350 mM sucrose), and the gin (333 mM glucose) screens. A plate containing 333 mM fructose was used in order to determine whether fructose may be equivalent to glucose in the isolation of the gin mutants. An additional plate containing 333 mM maltose was used for comparison with the gin, sig, and sis screens and 350 mM sorbitol was used as osmotic control. Consistent results were also seen with 3 and 5 mM mannose, 321 and 380 mM sucrose, and 389 mM glucose or fructose, but here data are only presented from the concentrations mentioned above.
The results obtained (Fig. 2) were quite surprising. Sucrose gives rise to glucose which, like mannose, is phosphorylated by HXK, but further metabolism of these two monosaccharides is distinct. One might have expected only a small overlap between the mig screen and other screens, since mannose exists in plants only in trace amounts and is capable of blocking germination at concentrations far lower than those of the other naturally-occurring sugars. The results showed, however, that there is considerable overlap between the mig screen and the gin, sig, and sis screens. In some extreme cases, such as with mig2 and mig3, it would have been possible to detect the mutants with any of the five sugar media tested. This suggests that mannose, glucose, fructose, sucrose, and maltose share a pathway by which Arabidopsis germination can be inhibited in mig2 and mig3. This pathway probably includes HXK since both the mig and the gin phenotypes have been reported to be, at least partly, mediated by a HXK-associated step (Jang et al., 1997; Pego et al., 1999). However, mannose is also capable of repressing germination via unique pathway(s) as can be seen by the results obtained with mig1 and mig7, for example.
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Although sucrose and maltose are both disaccharides, it was observed that there is not complete overlap between seedling development on 350 mM sucrose (sig and sis screens) and on similar maltose concentrations. The same holds true for the gin screen and development on maltose. One can only speculate on the real significance of this observation and on the need for a maltose-insensitive screen to obtain saturation in the sugar-mediated gene regulation pathway.
The finding that mig12 and mig13 are hypersensitive for all the sugars tested was initially surprising. However, the observation that they are also hypersensitive for sorbitol indicates that they probably represent mutants hypersensitive to osmotic potential and are, therefore, incapable of germinating on the elevated concentrations of all the sugars tested. On the other hand mig4 and mig9 appear to be less sensitive to sorbitol, or insensitive to osmotic potential. Osmosis-related mutants were particularly unexpected, since the mig screen is based on the seed's ability to germinate on 7.5 mM mannose which had no osmotic effect on germination.
It was concluded that there is partial overlap between all of the different screening strategies tested. It is tempting to speculate that a similar situation exists in relation to the other sugar-sensing screens (Table 2). Supporting this notion is the observation that sun6 is also a gin and mig mutant (Van Oosten et al., 1997; Pego et al., 1999) and that several cai mutants are also mig mutants (Martin et al., 1998). However, the results also show that there is a certain degree of specificity for each one of the screens. mig1 and mig7, for example, would not have been detected in any of the other screens whereas mig22 would have been detected in a gin, but not a sig or sis screen.
The results suggest that sugar-mediated regulation of gene expression occurs via a complex and branched pathway (Koch, 1996; Jang and Sheen, 1997; Smeekens and Rook, 1997; Halford et al., 1999). Part of this sugar-sensing mechanism seems to be at least partly conserved throughout eukaryotes and HXK has been reported to be a glucose sensor in sugar-mediated gene regulation in yeast, plant, and animal cells (Entian and Fröhlich, 1984; Matschinsky et al., 1993; Heimberg et al., 1996; Jang et al., 1997). There are, however, also reports of sucrose-dependent–glucose-independent (Wenzler et al., 1989; Chiou and Bush, 1998; Rook et al., 1998) and glucose-dependent–HXK-independent (Roitsch et al., 1995; Martin et al., 1997) pathways or branches thereof in plants. Additional interactions with existent light and hormone pathways (Szekeres et al., 1996; Dijkwel et al., 1997; Mustilli and Bowler, 1997; Perata et al., 1997; Zhou et al., 1998) further add to the complexity of the system.
Integrated analysis of mutants from all of the existing screens will maximise the potential for unravelling the sugar-mediated mechanisms controlling gene regulation and, ultimately, plant development. Additional screens and screening approaches may, however, be necessary to obtain saturation of all of the pathways involved. By analogy with yeast, mutants in one such pathway may be totally absent from the existing collections. Galactose and galactokinase are implicated in the regulation of gene transcription in yeast (Zenke et al., 1996), and possibly plant and animal cells (Fischer et al., 1988; Kakidani and Ptashne, 1988; Ma et al., 1988). S. cerevisiae galactokinase and its homologue GAL3, are the sensors of a sugar-signalling cascade which, in the presence of galactose, activates the genes necessary for further galactose metabolization (Zenke et al., 1996; Platt and Reece, 1998). The cascade itself is relatively simple and additionally requires the transcriptional activator GAL4 (Hashimoto et al., 1983) and GAL80, its negative regulator (Nogi and Fukasawa, 1984). In yeast, this mechanism is coupled to the HXK-dependent sugar-signalling pathway, whose activation by glucose leads to the repression of the GAL1 (galactokinase) and GAL4 genes (Nehlin et al., 1991; Dong and Dickson, 1997; Frolova et al., 1999) and, therefore, to the inactivation the galactokinase-dependent pathway.
The presence of such a mechanism in plants is not certain although galactokinase activity has been demonstrated in purified extracts from several plant species (Neufeld et al., 1960; Chan and Hassid, 1975; Foglietti, 1976; Dey, 1983). Recently, the isolation of an Arabidopsis thaliana galactokinase cDNA was accomplished by functional expression in yeast (Kaplan et al., 1997). This may allow the cloning of possible plant GAL4 and GAL80 homologues using the yeast two-hybrid system (Fields and Song, 1989). Since galactose is capable of inhibiting Arabidopsis germination and seedling development (J Pego and S Smeekens, unpublished data) it is proposed that a galactose-insensitive screen could be a valuable addition to the ones already available. Such mutants would easily be detected by growth on galactose-containing medium.
The current screening strategies have been useful tools in the isolation of mutants involved in sugar-mediated regulation of gene expression. However, the recent identification of gin1 and sun6, mutated in interacting hormone pathway components, demonstrates the need for more specific screening strategies capable of discriminating between the primary sugar-signalling cascades and secondary pathways subject to their control.
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Conclusions |
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TopAbstractIntroductionCarbon metabolite-mediated...Screening strategies for mutants...The mig mutant screenThe mig screen and...ConclusionsReferences |
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Pathways of photosynthesis are well established, but the mechanisms by which they are regulated are less well understood. Progress in their elucidation has, however, been rapid since the discovery that CO2, light, water, and other environmental signals are in some instances integrated, translated, and perceived by the plant as sugar signals. These are then processed, resulting in activation and/or repression of expression of a wide but specific set of genes. This carbohydrate-mediated mode of gene regulation is expected to be complex, as it not only controls genes encoding photosynthetic components, but simultaneously affects processes ranging from pathogen attack and environmental stress to storage protein accumulation and starch, lipid and nitrogen metabolism (reviewed in Koch, 1996; Jang and Sheen, 1997).
The employment of molecular genetic techniques for the isolation of mutants in this sugar-signalling pathway is, therefore, an important development in this field. Although different screening strategies have been employed to isolate such mutants, a certain degree of overlap was found by submitting 30 mig mutants to the conditions used for several of the other mutant screens. Results from the same experiment showed that the overlap between the different mutant screens is only partial, and mutants specific for each individual screen seem to have been isolated.
Although new insights into the mode of regulation of photosynthesis are already being obtained from the analysis of the existing sugar-signalling mutants, their study is still in its early stages and further research is needed to seize their potential fully. The integration of data obtained from all of the existing mutant screens is expected to provide meaningful insights into the mechanism(s) by which carbon metabolites regulate gene expression as a whole and photosynthesis in particular.
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Acknowledgements |
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The authors would like to thank Dr Susan Gibson, Dr Ian Graham, and Dr Jen Sheen for sharing unpublished data presented in Table 2. T-DNA mutagenized seeds were obtained from the Nottingham Arabidopsis Stock Centre (NASC), UK. Due to the restricted amount of space permitted we apologize to those whose work was not cited, or was cited through the writings of others. This work was financially supported by the Fundação para a Ciência e Tecnologia, Lisbon, Portugal (grant PRAXIS XXI/BD/3103/94 awarded to JVP).
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Footnotes |
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1 To whom correspondence should be addressed. Fax: +31 30 251 3655. E-mail:J.Pego{at}bio.uu.nl
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References |
|---|
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TopAbstractIntroductionCarbon metabolite-mediated...Screening strategies for mutants...The mig mutant screenThe mig screen and...ConclusionsReferences |
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Aarts MG, Corzaan P, Stiekema WJ, Pereira A. 1995. A two-element enhancer-inhibitor transposon system in Arabidopsis thaliana. Molecular and General Genetics 247, 555–564.
Arp WJ. 1991. Effects of source–sink relations on photosynthetic acclimation to elevated CO2. Plant, Cell and Environment 14, 869–875.
Bancroft I, Bhatt AM, Sjodin C, Scofield S, Jones JD, Dean C. 1992. Development of an efficient two-element transposon tagging system in Arabidopsis thaliana. Molecular and General Genetics 233, 449–461.
Boxall SF, Martin T, Graham IA. 1996. A new class of Arabidopsis thaliana mutant that is carbohydrate-insensitive. Poster abstracts of the 7th international conference on Arabidopsis research, S96.
Chan PH, Hassid WZ. 1975. One step purification of D-galactose and L-arabinose kinases from Phaseolus aureus seedlings by ATP-sepharose affinity chromatography. Analytical Biochemistry 64, 372–379.[ISI][Medline]
Cheng C-L, Acedo GN, Cristinsin M, Conkling MA. 1992. Sucrose mimics the light induction of Arabidopsis nitrate reductase gene transcription. Proceedings of the National Academy of Sciences, USA 89, 1861–1864.
Chevalier C, Bourgeois E, Just D, Raymond P. 1996. Metabolic regulation of asparagine synthetase gene expression in maize (Zea mays L.) root tips. The Plant Journal 9, 1–11.[ISI][Medline]
Chiou T-J, Bush, DR. 1998. Sucrose is a signal molecule in assimilate partitioning. Proceedings of the National Academy of Sciences, USA 95, 4784–4788.
Criqui MC, Durr A, Parmentier Y, Marbach J, Fleck J, Jamet E. 1992. How are photosynthetic genes repressed in freshly-isolated mesophyll protoplasts of Nicotiana sylvestris? Plant Physiology and Biochemistry 30, 597–601.
Curtis PS, Vogel CS, Pregitzer KS, Zak DR, Teeri JA. 1995. Interacting effects of soil fertility and atmospheric CO2 on leaf area growth and carbon gain physiology in Populusxeuramericana (Dode) Guinier. New Phytologist 129, 253–263.
Dey PM. 1983. Galactokinase of Vicia faba seeds. European Journal of Biochemistry 136, 155–159.[ISI][Medline]
Dijkwel PP, Kock PA, Bezemer R, Weisbeek PJ, Smeekens SC. 1996. Sucrose represses the developmentally controlled transient activation of the plastocyanin gene in Arabidopsis thaliana. Plant Physiology 110, 455–463.[Abstract]
Dijkwel PP, Huijser C, Weisbeek PJ, Chua N-H, Smeekens SCM. 1997. Sucrose control of phytochrome A signalling in Arabidopsis. The Plant Cell 9, 583–595.[Abstract]
Dong J, Dickson RC. 1997. Glucose represses the lactose-galactose regulon in Kluyveromyces lactis through a SNF1 and MIG1- dependent pathway that modulates galactokinase (GAL1) gene expression. Nucleic Acids Research 25, 3657–3664.
Donggiun K, Laby R, Gibson S. 1998. Regulation of sugar responses and characterisation of Arabidopsis thaliana mutants with reduced beta-amylase activity. Poster abstracts of the 9th international conference on Arabidopsis research, 90.
Drake BG, Gonzàlez-Meler MA, Long SP. 1997. More efficient plants: a consequence of rising atmospheric CO2? Annual Review of Plant Physiology and Plant Molecular Biology 48, 609–639.
Entian K-D, Fröhlich K-U. 1984. Saccharomyces cerevisiae mutants provide evidence of hexokinase PII as a bifunctional enzyme with catalytic and regulatory domains for triggering carbon catabolite repression. Journal of Bacteriology 158, 29–35.
Feldmann KA. 1991. T-DNA insertion mutagenesis in Arabidopsis: mutational spectrum. The Plant Journal 1, 71–82.
Fields S, Song O-K. 1989. A novel genetic system to detect protein–protein interactions. Nature 340, 245–246.[Medline]
Fischer JA, Giniger E, Maniatis T, Ptashne M. 1988. GAL4 activates transcription in Drosophila. Nature 332, 853–856.[Medline]
Foglietti MJ. 1976. Purification d’une galactokinase végétal. Avantages de la chromatographie d’affinité. Journal of Chromatography 128, 309–312.[ISI][Medline]
Frolova E, Johnston M, Majors J. 1999. Binding of the glucose-dependent Mig1p repressor to the GAL1 and GAL4 promoters in vivo: regulation by glucose and chromatin structure. Nucleic Acids Research 27, 1350–1358.
Gancedo JM. 1998. Yeast carbon catabolite repression. Microbiology and Molecular Biology Reviews 62, 334–361.
Gibson S, Laby R, Chengdong Z, Donggiun K. 1998. Regulation of sugar responses and carbon flux in Arabidopsis. Poster abstracts of the 9th international conference on Arabidopsis research, 80.
Graham IA, Denby KJ, Leaver CJ. 1994. Carbon catabolite repression regulates glyoxylate cycle gene expression in cucumber. The Plant Cell 6, 761–772.
Griffin KL, Seemann JR. 1996. Plants, CO2 and photosynthesis in the 21st century. Chemistry and Biology 3, 245–254.[ISI][Medline]
Halford NG, Purcell PC, Hardie DG. 1999. Is hexokinase really a sugar sensor in plants? Trends in Plant Science 4, 117–120.[ISI][Medline]
Harter K, Talke-Messerer C, Barz W, Schäfer E. 1993. Light- and sucrose-dependent gene expression in photomixotrophic cell suspension cultures and protoplasts of rape (Brassica napus L.). The Plant Journal 4, 507–516.
Hashimoto H, Kikuchi Y, Nogi Y, Fukasawa T. 1983. Regulation of expression of the galactose gene cluster in Saccharomyces cerevisiae. Isolation and characterization of the regulatory gene GAL4. Molecular and General Genetics 191, 31–38.
Hattori T, Nakagawa S, Nakamura K. 1990. High-level expression of tuberous root storage protein genes of sweet potato in stems of plantlets grown in vitro on sucrose medium. Plant Molecular Biology 14, 595–604.[ISI][Medline]
Heimberg H, De Vos A, Moens K, Quartier E, Bouwens L, Pipeleers D, Van Schaftingen E, Madsen O, Schuit F. 1996. The glucose sensor protein glucokinase is expressed in glucagon-producing 
-cells. Proceedings of the National Academy of Sciences, USA 93, 7036–7041.
Heineke D, Wildenberger K, Sonnewald U, Willmitzer L, Heldt HW. 1994. Accumulation of hexoses in leaf vacuoles: studies with transgenic tobacco plants expressing yeast-derived invertase in the cytosol, vacuole or apoplasm. Planta 194, 29–33.[ISI]
Herbers K, Meuwly P, Métraux J-P, Sonnewald U. 1996. Salicylic acid-independent induction of pathogenisis-related protein transcripts by sugars is dependent on leaf development stage. FEBS Letters 397, 239–244.[ISI][Medline]
Herold A, Lewis DH. 1977. Mannose and green plants: occurrence, physiology and metabolism, and use as a tool to study the role of orthophosphate. New Phytologist 79, 1–40.
Jang J-C, Sheen J. 1994. Sugar sensing in higher plants. The Plant Cell 6, 1665–1679.[Abstract]
Jang J-C, Sheen J. 1997. Sugar sensing in higher plants. Trends in Plant Science 2, 208–214.
Jang J-C, León P, Zhou L, Sheen J. 1997. Hexokinase as a sugar sensor in higher plants. The Plant Cell 9, 5–19.[Abstract]
Kakidani H, Ptashne M. 1988. GAL4 activates gene expression in mammalian cells. Cell 52, 161–167.[ISI][Medline]
Kaplan CP, Tugal HB, Baker A. 1997. Isolation of a cDNA encoding an Arabidopsis galactokinase by functional expression in yeast. Plant Molecular Biology 34, 497–506.[ISI][Medline]
Karrer EE, Rodriguez RL. 1992. Metabolic regulation of rice -amylase and sucrose synthase genes in planta. The Plant Journal 2, 517–523.[ISI][Medline]
Klein D, Stitt M. 1998. Effects of 2-deoxyglucose on the expression of rbcS and the metabolism of Chenopodium rubrum cell-suspension cultures. Planta 205, 223–234.
Klimyuk VI, Nussaume L, Harrison K, Jones JD. 1995. Novel GUS expression patterns following transposition of an enhancer trap Ds element in Arabidopsis. Molecular and General Genetics 249, 357–365.
Knight JS, Gray JC. 1994. Expression of genes encoding the tobacco chloroplast phosphate translocator is not light-regulated and is repressed by sucrose. Molecular and General Genetics 242, 586–594.
Koch KE. 1996. Carbohydrate-modulated gene expression in plants. Annual Review of Plant Physiology and Plant Molecular Biology 47, 509–540.[ISI]
Koch KE, Nolte KD, Duke ER, McCarty DR, Avigne WT. 1992. Sugar levels modulate differential expression of maize sucrose synthase genes. The Plant Cell 4, 59–69.
Krapp A, Hofmann B, Schäfer C, Stitt M. 1993. Regulation of the expression of rbcS and other photosynthetic genes by carbohydrates: a mechanism for the ‘sink regulation’ of photosynthesis? The Plant Journal 3, 817–828.
Kuhlemeier C. 1992. Transcriptional and post-transcriptional regulation of gene expression in plants. Plant Molecular Biology 19, 1–14.[ISI][Medline]
Liu Y-G, Mitsukawa N, Oosumi T, Whittier RF. 1995. Efficient isolation and mapping of Arabidopsis thaliana T-DNA insert junctions by thermal asymetric interlaced PCR. The Plant Journal 8, 457–463.[ISI][Medline]
Long D, Martin M, Sundberg E, Swinburne J, Puangsomlee P, Coupland G. 1993. The maize transposable element system Ac/Ds as a mutagen in Arabidopsis: identification of an albino mutation induced by Ds insertion. Proceedings of the National Academy of Sciences, USA 90, 10370–10374.
Ma J, Przibilla E, Hu J, Bogorad L, Ptashne M. 1988. Yeast activators stimulate plant gene expression. Nature 334, 631–633.[Medline]
Martin T, Hellmann H, Schmidt R, Willmitzer L, Frommer WB. 1997. Identification of mutants in metabolically regulated gene expression. The Plant Journal 11, 53–62.[ISI][Medline]
Martin T, Boxall SF, Regad F, Oswald O, Graham IA. 1998. Biochemical and molecular characterisation of carbohydrate-insensitive (cai) Arabidopsis mutants. Poster abstracts of the 9th international conference on Arabidopsis research, 96.
Matschinsky F, Liang Y, Kesavan P, Wang L, Froguel P, Velho G, Cohen D, Permutt MA, Tanizawa Y, Jetton TL, Niswender K, Magnuson M. 1993. Glucokinase as pancreatic ß cell glucose sensor and diabetes gene. Journal of Clinical Investigation 92, 2092–2098.
McElroy MB. 1994. Climate of the earth: an overview. Environmental Pollution 83, 3–21.[Medline]
McLaughlin JC, Smith SM. 1994. Metabolic regulation of glyoxylate-cycle enzyme synthesis in detached cucumber cotyledons and protoplasts. Planta 195, 22–28.
Mita S, Murano N, Akaike M, Nakamura K.1997a. Mutants of Arabidopsis thaliana with pleiotropic effects on the expression of the gene for ß-amylase and on the accumulation of anthocyanin that are inducible by sugars. The Plant Journal 11, 841–851.[ISI][Medline]
Mita S, Hirano H, Nakamura K.1997b. Negative regulation in the expression of a sugar-inducible gene in Arabidopsis thaliana. A recessive mutation causing enhanced expression of a gene for ß-amylase. Plant Physiology 114, 575–582.[Abstract]
Monroy AF, Schwartzbach SD.1983. Photocontrol of the polypeptide composition of Euglena. Planta 158, 249–258.
Murashige T, Skoog F. 1962. A revised medium for rapid growth and bio assays with tobacco tissue cultures. Plant Physiology 15, 473–497.
Mustilli AC, Bowler C. 1997. Tuning in to the signals controlling photoregulated gene expression in plants. The EMBO Journal 16, 5801–5806.[ISI][Medline]
Nakamura K, Ohto M-A, Yoshida N, Nakamura K. 1991. Sucrose-induced accumulation of ß-amylase occurs concomitant with the accumulation of starch and sporamin in leaf-petiole cuttings of sweet potato. Plant Physiology 96, 902–909.
Nehlin JO, Carlberg M, Ronne H. 1991. Control of yeast GAL genes by MIG1 repressor: a transcriptional cascade in the glucose response. The EMBO Journal 10, 3373–3377.[ISI][Medline]
Nelson T, Langdale JA. 1989. Patterns of leaf development in C4 plants. The Plant Cell 1, 3–13.
Neufeld EF, Feingold DS, Hassid WZ. 1960. Phosphorylation of D-galactose and L-arabinose by extracts from Phaseolus aureus seedlings. Journal of Biological Chemistry 235, 906–909.
Nogi Y, Fukasawa T. 1984. Nucleotide sequence of the yeast regulatory gene GAL80. Nucleic Acids Research 12, 9287–9298.
Ochman H, Gerber AS, Hartl DL.1988. Genetic applications of an inverse polymerase chain reaction. Genetics 120, 621–623.
Pego J, Kortstee A, Huijser C, Smeekens S. 1998. Searching for genes involved in sugar sensing and signalling. Poster abstracts of the 3rd Gatersleben research conference on plant metabolism and development, 12.
Pego J, Weisbeek P, Smeekens S. 1999. Mannose inhibits Arabidopsis thaliana germination via a hexokinase-mediated step. Plant Physiology 119, 1017–1023.
Perata P, Matsukura C, Vernieri P, Yamaguchi J. 1997. Sugar repression of gibberellin-dependent signalling pathways in barley embryos. The Plant Cell 9, 2197–2208.[Abstract]
Platt A, Reece RJ. 1998. The yeast galactose genetic switch is mediated by the formation of a Gal4p–Gal80p–Gal3p complex. The EMBO Journal 17, 4086–4091.[ISI][Medline]
Prata RTN, Williamson JD, Conkling MA, Pharr DM. 1997. Sugar repression of mannitol dehydrogenase activity in celery cells. Plant Physiology 114, 307–314.[Abstract]
Quick PW, Schaffer AA. 1996. Sucrose metabolism in sinks and sources. In: E Zamski, A Schaffer, eds. Photoassimilate distribution in plants and crops. New York: Marcel Dekker, 115–156.
Raines CA, Horsnell PR, Holder C, Lloyd JC. 1992. Arabidopsis thaliana carbonic anhydrase: cDNA sequence and effect of CO2 on mRNA levels. Plant Molecular Biology 20, 1143–1148.[ISI][Medline]
Reinbothe S, Reinbothe C, Parthier B. 1991. Glucose repression of chloroplast development in Euglena gracilis. Plant Physiology and Biochemistry 29, 297–307.
Roitsch T, Bittner M, Godt DE. 1995. Induction of apoplastic invertase of Chenopodium rubrum by D-glucose and a glucose analog and tissue-specific expression suggests a role in sink-source regulation. Plant Physiology 108, 285–294.[Abstract]
Ronne H. 1995. Glucose repression in fungi. Trends in Genetics 11, 12–17.[ISI][Medline]
Rook F, Gerrits N, Kortstee A, Van Kampen M, Borrias M, Weisbeek P, Smeekens S. 1998. Sucrose-specific signalling represses the translation of the Arabidopsis ATB2 bZIP transcription factor gene. The Plant Journal 15, 253–263.[ISI][Medline]
Sheen J. 1990. Metabolic repression of transcription in higher plants. The Plant Cell 2, 1027–1038.
Sheu J-J, Jan S-H, Lee H-T, Yu S-M. 1994. Control of transcription and mRNA turnover as mechanisms of metabolic repression of -amylase gene expression. The Plant Journal 5, 655–664.
Sims DA, Luo Y, Seemann JR. 1998. Importance of leaf versus whole plant CO2 environment for photosynthetic acclimation. Plant, Cell and Environment 21, 1189–1196.
Smeekens S, Rook F. 1997. Sugar sensing and sugar-mediated signal transduction in plants. Plant Physiology 115, 7–13.[ISI][Medline]
Sonnewald U, Brauer M, Von Schaewen A, Stitt M, Willmitzer L. 1991. Transgenic tobacco plants expressing yeast-derived invertase in either the cytosol, vacuole or apoplast: a powerful tool for studying sucrose metabolism and sink/source interactions. The Plant Journal 1, 95–106.[ISI][Medline]
Souer E, Quattrocchio F, De Vetten N, Mol J, Koes R. 1995. A general method to isolate genes tagged by a high copy number transposable element. The Plant Journal 7, 677–685.[ISI][Medline]
Staub JM, Deng X-W. 1996. Light signal transduction in plants. Photochemistry and Photobiology 64, 897–905.[ISI][Medline]
Stitt M. 1991. Rising CO2 levels and their potential significance for carbon flow in photosynthetic cells. Plant, Cell and Environment 14, 741–762.
Szekeres M, Németh K, Koncz-Kálmán Z, Mathur J, Kauschmann A, Altmann T, Rédei GP, Nagy F, Schell J, Koncz C. 1996. Brassinosteroids rescue the deficiency of CYP90, a cytochrome P450, controlling cell elongation and de-etiolation in Arabidopsis. Cell 85, 171–182.[ISI][Medline]
Thevelein JM. 1994. Signal transduction in yeast. Yeast 10, 1753–1790.[ISI][Medline]
Van Oosten JJ, Besford RT. 1994. Sugar feeding mimics effect of acclimation to high CO2: rapid downregulation of RuBisCO small subunit transcripts, but not of the large subunit transcripts. Journal of Plant Physiology 143, 306–312.[ISI]
Van Oosten JJ, Besford RT. 1995. Some relationships between the gas exchange, biochemistry and molecular biology of photosynthesis during leaf development of tomato plants after transfer to different carbon dioxide concentrations. Plant, Cell and Environment 18, 1253–1266.
Van Oosten JJ, Gerbaud A, Huijser C, Dijkwel PP, Chua N-H, Smeekens SCM. 1997. An Arabidopsis mutant showing reduced feedback inhibition of photosynthesis. The Plant Journal 12, 1011–1020.[ISI][Medline]
Von Schaewen A, Stitt M, Schmidt R, Sonnewald U, Willmitzer L. 1990. Expression of a yeast-derived invertase in the cell wall of tobacco and Arabidopsis plants leads to accumulation of carbohydrate, inhibition of photosynthesis and strongly influences growth and phenotype of transgenic tobacco plants. The EMBO Journal 9, 3033–3044.[ISI][Medline]
Walker DA, Sivak MN. 1986. Photosynthesis and phosphate: a cellular affair? Trends in Biochemical Sciences 11, 176–179.
Webber AN, Nie G-Y, Long SP. 1994. Acclimation of photosynthetic proteins to rising atmospheric CO2. Photosynthesis Research 39, 413–425.
Wei N, Deng X-W. 1996. The role of the COP/DET/FUS genes in light control of Arabidopsis seedling development. Plant Physiology 112, 871–878.[ISI][Medline]
Wenzler HC, Mignery GA, Fisher LM, Park WD. 1989. Analysis of a chimeric class-I patatin-GUS gene in transgenic potato plants: high-level expression in tubers and sucrose-inducible expression in cultured leaf and stem explants. Plant Molecular Biology 12, 41–50.
Wisman E, Cardon GH, Fransz P, Saedler H. 1998. The behavior of the autonomous maize transposable element En/Spm in Arabidopsis thaliana allows efficient mutagenesis. Plant Molecular Biology 37, 989–999.[ISI][Medline]
Wullschleger SD, Norby RJ, Hendrix DL. 1992. Carbon exchange rates, chlorophyll content, and carbohydrate status of two forest tree species exposed to carbon dioxide enrichment. Tree Physiology 10, 21–31.[ISI][Medline]
Zenke FT, Engels R, Vollenbroich V, Meyer J, Hollenberg CP, Breunig KD. 1996. Activation of gal4p by galactose-dependent interaction of galactokinase and gal80p. Science 272, 1662–1665.[Abstract]
Zhou L, Jang J-C, Jones TL, Sheen J. 1998. Glucose and ethylene signal transduction crosstalk revealed by an Arabidopsis glucose-insensitive mutant. Proceedings of the National Academy of Sciences, USA 95, 10294–10299.
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