Journal of Experimental Botany, Vol. 54, No. 382, pp. 467-475,
January 1, 2003
© 2003 Oxford University Press
Metabolic signalling and carbon partitioning: role of Snf1-related (SnRK1) protein kinase
Received 8 April 2002; Accepted 4 September 2002
1 Crop Performance and Improvement, Rothamsted Research, Harpenden, Hertfordshire AL5 2JQ, UK
2 Crop Performance and Improvement, Long Ashton Research Station, Long Ashton, Bristol BS41 9AF, UK
3 To whom correspondence should be addressed. Fax: +44 (0)1582 736010. E-mail: nigel.halford{at}bbsrc.ac.uk
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Abstract |
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 Top Abstract IntroductionThe SnRK gene familySnRK1 activityRegulation of SnRK1 activitySnRK1 substratesSnRK1 regulates gene expressionSnRK1 and developmentIdentification of SnRK1...Evidence that SnRK1 is...Concluding remarksReferences |
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A protein kinase that plays a key role in the global control of plant carbon metabolism is SnRK1 (sucrose non-fermenting-1-related protein kinase 1), so-called because of its homology and functional similarity with sucrose non-fermenting 1 (SNF1) of yeast. This article reviews studies on the characterization of SnRK1 gene families, SnRK1 regulation and function, interacting proteins, and the effects of manipulating SnRK1 activity on carbon metabolism and development.
Key words: Carbon partitioning, metabolic signalling, protein kinase, SnRK1.
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Introduction |
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TopAbstractIntroductionThe SnRK gene familySnRK1 activityRegulation of SnRK1 activitySnRK1 substratesSnRK1 regulates gene expressionSnRK1 and developmentIdentification of SnRK1...Evidence that SnRK1 is...Concluding remarksReferences |
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SnRK1 (SNF1-Related Protein Kinase-1) is a plant protein kinase with a catalytic domain similar to that of SNF1 (Sucrose Non-fermenting-1) of yeast and AMPK (AMP-activated protein kinase) of animals. The SNF1 family of protein kinases are a distinct group within the protein kinase superfamily, but are closely related to the calcium-dependent protein kinase (CDPK) group, which includes the animal calmodulin-dependent protein kinases and the plant calmodulin-like domain protein kinases (Hardie, 2000).
SNF1 (Celenza and Carlson, 1986) is activated in response to low cellular glucose levels and is required for the derepression of a battery of genes that are repressed by glucose (Gancedo, 1998; Ronne, 1995; Dickinson, 1999). It also directly modulates the phosphorylation state of a number of metabolic enzymes, including acetyl-CoA carboxylase (Woods et al., 1994) and glycogen synthase (Hardy et al., 1994), and is required for the arrest of growth and the cell cycle under conditions of glucose deprivation (Thompson-Jaeger et al., 1991).
AMPK is activated by AMP (Carling et al., 1987, 1989) and by phosphorylation by an upstream protein kinase (AMP-activated protein kinase kinase (AMPKK)) (Hawley et al., 1996). Activation of AMPK by AMP is antagonized by high (mM) concentrations of ATP and a high AMP:ATP ratio is symptomatic of low cellular energy levels. For this reason, AMPK has been likened to a cellular fuel gauge (Hardie and Carling, 1997). When activated, it acts to conserve ATP by phosphorylating and inactivating regulatory enzymes of ATP-consuming, anabolic pathways such as acetyl-CoA carboxylase (fatty acid synthesis) (Davies et al., 1990, 1992) and HMG-CoA reductase (sterol/isoprenoid synthesis) (Clarke and Hardie, 1990; Gillespie and Hardie, 1992).
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The SnRK gene family |
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TopAbstractIntroductionThe SnRK gene familySnRK1 activityRegulation of SnRK1 activitySnRK1 substratesSnRK1 regulates gene expressionSnRK1 and developmentIdentification of SnRK1...Evidence that SnRK1 is...Concluding remarksReferences |
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The first plant SnRK1 sequence to be reported was a cDNA isolated from a rye endosperm cDNA library (Alderson et al., 1991). It encoded a 57.7 kDa protein of 502 amino acid residues showing 48% amino acid sequence identity with SNF1 and AMPK, rising to 62–64% amino acid sequence identity in the kinase catalytic domain.
SnRK1 genes have since been identified and characterized in many plant species (reviewed by Halford and Hardie, 1998). They are present in small to medium-sized gene families, comprising, for example, three members in arabidopsis and 10–20 in barley. The SnRK1 gene family of cereals can be subdivided further into two groups, SnRK1a and SnRK1b, on the basis of amino acid sequence similarity and expression patterns (Halford and Hardie, 1998). SnRK1a is expressed throughout the plant and is more closely related to SnRK1 from dicotyledonous plants. SnRK1b is expressed at the highest levels in the seed, although low levels of expression can be detected elsewhere, and is only present in monocotyledonous plants. The functional significance of this divergence of the gene family in cereals is not known.
Plants contain two other subfamilies of protein kinases, SnRK2 and SnRK3, containing catalytic domains with sequences that place them clearly within the SNF1 family. They have 42–45% amino acid sequence identity with SnRK1, SNF1 and AMPK in this region; they are, therefore, significantly less similar to SNF1 and AMPK than SnRK1 is. The SnRK2 and SnRK3 gene subfamilies appear to be unique to plants and are relatively large and diverse compared with SnRK1. The SnRK2 subfamily includes PKABA1 from wheat, which is involved in mediating ABA-induced changes in gene expression (Anderberg and Walker-Simmons, 1992; Gómez-Cadenas et al., 1999). The SnRK3 gene family includes SOS2, an arabidopsis protein kinase involved in conferring salt tolerance (Halfter et al., 2000; Liu et al., 2000). The completion of the arabidopsis genome sequencing project means that the full complement of the arabidopsis SnRK family can now be identified. These are shown as a dendrogram in Fig. 1.
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SnRK1 activity |
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TopAbstractIntroductionThe SnRK gene familySnRK1 activityRegulation of SnRK1 activitySnRK1 substratesSnRK1 regulates gene expressionSnRK1 and developmentIdentification of SnRK1...Evidence that SnRK1 is...Concluding remarksReferences |
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The cloning of SnRK1 genes and cDNAs allowed antisera to be raised to heterologously expressed SnRK1 and to synthetic peptides based on the predicted SnRK1 peptide sequence. Use of these antibodies led to the confirmation that a plant protein kinase related to AMPK, that was being studied independently at the biochemical level, was, indeed, SnRK1 (Ball et al., 1995; Barker et al., 1996). This made SnRK1 the first plant protein kinase for which biochemical and molecular biological studies came together. It had already been shown to phosphorylate the SAMS peptide (His Met Arg Ser Ala Met Ser Gly Leu His Leu Val Lys Arg Arg), a synthetic peptide based on the sequence around the primary phosphorylation site for AMPK on rat acetyl-CoA carboxylase (MacKintosh et al., 1992) and had been purified from cauliflower (Ball et al., 1994). Although it was not activated by AMP, it was found to have similar biochemical properties to those of mammalian AMPK in other respects (Ball et al., 1994; MacKintosh et al., 1992). It was shown to phosphorylate and inactivate a bacterially-expressed arabidopsis HMG-CoA reductase (Ball et al., 1994).
A recognition motif for SnRK1 was established using variant peptide substrates (Weekes et al., 1993). It comprises the phosphorylated serine (SnRK1 will phosphorylate threonine, but phosphorylates serine much more efficiently), hydrophobic residues at positions –5 and +4 relative to the serine, and at least one basic residue which could be at –3 or –4 (Fig. 2). The AMARA peptide (Ala Met Ala Arg Ala Ala Ser Ala Ala Ala Leu Ala Arg Arg Arg), in which the minimal recognition motif is retained, but other residues are alanine, apart from the basic C-terminus which is not essential, appears to be a better substrate than the SAMS peptide (Dale et al., 1995b). More recently, basic residues at positions –6 and +5 have been shown to enhance activity and a proline residue at position –4 has been found to favour phosphorylation by SnRK1 relative to CDPKs (Huang and Huber, 2001).
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The identification of peptide substrates for SnRK1 allowed SnRK1 activity to be measured using a convenient assay. Interestingly, although SnRK2 and SnRK3 might be expected to have similar substrate specificity to SnRK1, whenever SAMS or AMARA peptide kinase activity has been purified SnRK1 has accounted for most of it. A minor SAMS peptide kinase activity has been tentatively assigned to SnRK2, but has not been characterized in detail (Ball et al., 1994; Barker et al., 1996; Sugden et al., 1999b). This suggests that SnRK2 and SnRK3 might require slightly different recognition sequences to SnRK1.
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Regulation of SnRK1 activity |
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TopAbstractIntroductionThe SnRK gene familySnRK1 activityRegulation of SnRK1 activitySnRK1 substratesSnRK1 regulates gene expressionSnRK1 and developmentIdentification of SnRK1...Evidence that SnRK1 is...Concluding remarksReferences |
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There is evidence of differential transcriptional regulation of SnRK1 gene expression. In potato, for example, the highest levels of expression occur in stolons as they begin to develop into tubers (Man et al., 1997). Expression gradually declines in maturing tubers, but is lowest in leaves. Experiments in potato also provided evidence for post-transcriptional regulation of SnRK1 activity. SAMS peptide kinase activity in mini-tubers was found to be over 40 times higher than in mature tubers while the levels of transcript were approximately the same (Man et al., 1997). This post-transcription regulation probably occurs through phosphorylation by an upstream kinase kinase. Spinach SnRK1 is regulated in vitro by phosphorylation on a threonine residue within the so-called T-loop that is conserved in many protein kinases (Sugden et al., 1999a).
The exact nature of the signal that brings about changes in SnRK1 gene expression or activation state is not known. Dephosphorylation and inactivation of spinach SnRK1 has been found to be inhibited by low concentrations of 5'-AMP (Sugden et al., 1999a). There is also evidence that SnRK1 may be inhibited by glucose-6-phosphate (Toroser et al., 2000), although others have attributed the apparent inhibition of SnRK1 by glucose-6-phosphate to the presence of a contaminant (Sugden et al., 1999b). However, these remain the only tentative links between induction or repression of SnRK1 activity and metabolic status. Further evidence that SnRK1 is involved in the control of carbon metabolism comes through the identification of its substrates and of the genes that it regulates. This has led to the hypothesis that SnRK1 is activated is response to high intracellular sucrose and/or low intracellular glucose levels (Halford and Dickinson, 2001).
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SnRK1 substrates |
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TopAbstractIntroductionThe SnRK gene familySnRK1 activityRegulation of SnRK1 activitySnRK1 substratesSnRK1 regulates gene expressionSnRK1 and developmentIdentification of SnRK1...Evidence that SnRK1 is...Concluding remarksReferences |
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The first plant protein to be identified as a substrate for SnRK1 was arabidopsis HMG-CoA reductase (Dale et al., 1995a). This enzyme catalyses the NADH-dependent reduction of 3-hydroxy-3-methylglutaryl-coenzyme A (HMG-CoA) to mevalonic acid. The phosphorylation site is Ser-577 and the phosphorylation results in inactivation of the enzyme.
Subsequently, two other important enzymes, sucrose phosphate synthase (SPS) and nitrate reductase (NR) were shown to be substrates for SnRK1. SPS is phosphorylated at Ser-158 and NR at Ser-543 (Bachmann et al., 1996b; Douglas et al., 1995; Su et al., 1996). In both cases phosphorylation results in inactivation of the enzyme, although the inactivation of NR also requires the binding of a 14-3-3 protein to the phosphorylation site (Bachmann et al., 1996a; Moorhead et al., 1996). The sequences around both sites conform to the SnRK1 consensus recognition motif and immunological evidence confirmed that SnRK1 was one of the protein kinases responsible for these phosphorylations (Crawford et al., 2001; Douglas et al., 1997; Sugden et al., 1999b).
Clearly, if SnRK1 plays a role in controlling the activity of HMG-CoA reductase, NR and SPS, then uncoupling them from SnRK1 regulation by removing the phosphorylation site could be important in the metabolic engineering of plants with these enzymes. This might explain why the over-expression of HMG-CoA reductase in arabidopsis led to a 40-fold increase in transcript levels compared with wild-type plants, but only a 3-fold increase in HMG-CoA reductase activity (Re et al., 1995) and no increase in isoprenoids, although over-expression of HMG-CoA reductase in tobacco did increase enzyme activity 3–8-fold (Schaller et al., 1995; Chappell et al., 1995). Tobacco plants expressing a mutant HMG-CoA reductase gene lacking a SnRK1 target site have been produced and are being analysed (S Hey, M Beale, NG Halford, unpublished data).
HMG-CoA reductase, NR and SPS are unlikely to represent the final list of metabolic enzyme substrates for SnRK1. It is difficult to perform comprehensive database searches for the presence of the motif because different hydrophobic and basic residues are tolerated at the signature positions relative to the phosphorylated serine. However, a cursory search revealed the presence of a putative site, Phe Arg Gln Phe Ile Ser Ile Gln Cys Val, in an arabidopsis cyclopocyclopropane fatty acid synthase (accession No. AAL66922) and two sites, Met Gly Arg Leu Glu Ser Val Leu Asn Leu and Ile Phe Lys Gly Ile Ser Leu Lys Leu Ile, in arabidopsis trehalose 6-phosphate synthase (accession No. AAL60031). The significance of these sites would have to be tested experimentally, but there is a strong possibility that these enzymes are substrates for SnRK1.
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SnRK1 regulates gene expression |
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TopAbstractIntroductionThe SnRK gene familySnRK1 activityRegulation of SnRK1 activitySnRK1 substratesSnRK1 regulates gene expressionSnRK1 and developmentIdentification of SnRK1...Evidence that SnRK1 is...Concluding remarksReferences |
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One of the functions of SNF1 in yeast is the transcriptional regulation of genes encoding enzymes of carbohydrate metabolism. SnRK1 will perform this role in yeast snf1 mutants to the extent that the yeast can utilize sucrose and non-fermentable carbon sources such as ethanol and glycerol (Alderson et al., 1991; Muranaka et al., 1994). The possibility that SnRK1 might perform a similar role in regulating gene expression in plants has been investigated by expressing an antisense potato SnRK1 sequence in the tubers and leaves of transgenic potato (Purcell et al., 1998). This resulted in a reduction of up to 79% in SAMS peptide kinase activity in the tubers, confirming that SnRK1 is responsible for most if not all of the SAMS peptide kinase activity in this tissue. It also resulted in the reduction of sucrose synthase activity. Sucrose synthase gene expression was shown to have decreased dramatically in transgenic tubers and to be uninducible by sucrose in excised leaves expressing the antisense sequence. In wild-type plants, the sucrose synthase gene, Sus4, is expressed in tubers and is induced in excised leaves by incubation with sucrose (Fu and Park, 1995).
The role of SnRK1 in regulating the expression of other genes encoding enzymes of carbohydrate metabolism is still under investigation. For example, changes in invertase gene expression have been observed in transgenic arabidopsis plants overexpressing SnRK1 (P Lessard, M Thomas, unpublished data) and a transient expression system has been used to show that antisense SnRK1 represses 
-amylase promoter activity in wheat embryos (S Laurie, RS McKibbin, NG Halford, unpublished data).
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SnRK1 and development |
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TopAbstractIntroductionThe SnRK gene familySnRK1 activityRegulation of SnRK1 activitySnRK1 substratesSnRK1 regulates gene expressionSnRK1 and developmentIdentification of SnRK1...Evidence that SnRK1 is...Concluding remarksReferences |
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Expression of antisense SnRK1 sequences in different plant species has had profound effects on development. For example, sprouting was found to be affected in potato tubers expressing antisense SnRK1 (RS McKibbin, NG Halford, unpublished data) and pollen development was arrested in barley plants expressing antisense SnRK1 (Zhang et al., 2001). The pollen grains were small, pear-shaped, contained little or no starch and were non-viable. Intriguingly, the transgene was not passed on to the T1 generation at all, suggesting that ovule development was also affected. Pollen infertility is often associated with a lack of starch accumulation and has been suggested to be caused, in some cases, by an inability to metabolize incoming sucrose (Dorion et al., 1996; Sheoran and Saini, 1996; Saini, 1997). This type of male sterility in wheat and rice is associated predominantly with a decrease in acid invertase rather than sucrose synthase activity (Dorion et al., 1996; Sheoran and Saini, 1996) and SnRK1 has not previously been associated with the regulation of invertase activity in plants. However, antisense repression of extracellular invertase gene expression in tobacco anthers resulted in a similar pollen phenotype to that observed in the antisense SnRK1 transgenic barley lines (Goetz et al., 2001).
According to the hypothesis that SnRK1 is activated in response to high sucrose/low glucose and causes the induction of gene expression, the pollen grains in the antisense SnRK1 plants would be unable to respond to their carbon status by expressing invertase and utilizing imported sucrose. They would starve in a similar fashion to yeast snf1 mutants starving on sucrose medium.
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Identification of SnRK1-interacting proteins |
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TopAbstractIntroductionThe SnRK gene familySnRK1 activityRegulation of SnRK1 activitySnRK1 substratesSnRK1 regulates gene expressionSnRK1 and developmentIdentification of SnRK1...Evidence that SnRK1 is...Concluding remarksReferences |
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Both SNF1 and AMPK form complexes with other proteins. The SNF1 complex includes a 36 kDa protein, termed SNF4, which is a regulatory subunit required for full activity of the protein kinase (Celenza et al., 1989). The interaction between SNF1 and SNF4 appears to be regulated by glucose and it has been proposed that SNF4 activates SNF1 by counteracting autoinhibition by the SNF1 regulatory domain (Jiang and Carlson, 1996). The SNF1 complex also includes a second interacting protein from a class of proteins that comprises SIP1 (110 kDa), SIP2 (54 kDa) and GAL83 (64 kDa). These three related proteins are interchangeable in the SNF1 kinase complex and may target the complex to different substrates (Yang et al., 1994). They contain two conserved domains, the ASC domain (Association with SNF1 Complex) (Yang et al., 1994; Jiang and Carlson, 1997). and the KIS domain (Kinase Interacting Sequence) (Jiang and Carlson, 1997). Three further interacting factors have been identified (SIP3, SIP4 and MSN3) that may couple SNF1 complexes to transcriptional regulation (Hubbard et al., 1994; Lesage et al., 1994, 1996). The AMPK complex includes a ß-subunit (38–40 kDa), which corresponds to the yeast SIP proteins, and a
-subunit (36–38 kDa) that is closely related to SNF4 (Woods et al., 1996). Homologues of SNF4 and the SIP1/SIP2/GAL83 family have now been identified in plants. The presence of a SNF4-like protein had been suggested by the demonstration that SnRK1 interacted with yeast SNF4 in two-hybrid experiments (Jiang and Carlson, 1997; Bouly et al., 1999). Moreover, SNF4 was shown to be needed for complementation of snf1 mutants by SnRK1 (Muranaka et al., 1994). The gene, called AtSNF4, was finally cloned from arabidopsis by partial complementation of an snf4 mutant (Kleinow et al., 2000).
Two other families of plant proteins show similarity with SNF4. These are the PV42 family, which includes PV42 from bean (Phaseolus vulgaris) and AKIN from arabidopsis (Abe et al., 1995; Bouly et al., 1999), and the SnIP1 family (Slocombe et al., 2002). These show 20–25% amino acid sequence identity with SNF4 and interact with SnRK1 in two-hybrid assays and in vitro. The PV42 and SnIP1 classes of SNF4-like proteins appear to be unique to plants. Although both will align with SNF4 and AMPK, they show little sequence similarity with each other. They do, however, share a short, hydrophobic motif, called the SnIP motif (Halford et al., 2000; Slocombe et al., 2002). Part of this motif (Hyd-Xxx-Bas-Xxx-Xxx-Xxx-Xxx-Xxx-Xxx-Hyd) bears some resemblance to the SnRK1 recognition sequence without the target serine residue, and could represent a pseudosubstrate site similar to those observed in the regulatory subunits of the cAMP-dependent kinase, PKA, of mammals (Taylor et al., 1990).
Genes related to the SIP1/SIP2/GAL83/AMPKß family have been cloned from arabidopsis (AKINß1 and AKINß2) and potato (StubGAL83) (Bouly et al., 1999; Lakatos et al., 1999). AKINß1 and AKINß2 interact with SnRK1 and AKIN in the two-hybrid system but also with the yeast SNF1 and SNF4 proteins (Bouly et al., 1999). Potato StubGAL83 was isolated by screening of a yeast two-hybrid cDNA library with a potato SnRK1 cDNA (Lakatos et al., 1999).
Plants also contain a protein, AKINß, that contains an N-terminal KIS domain fused with a C-terminal domain similar to that of SNF4 and AMPK -subunit (Lumbreras et al., 2001). This protein complements the snf4 mutation and interacts with SnRK1 in two-hybrid assays. It appears to be unique to plants.
Two other proteins that have been found to interact with SnRK1 in two-hybrid experiments are a small heat shock protein that is a substrate, though a relatively poor one, for SnRK1 (SP Slocombe et al., unpublished data) and PRL1 (Bhalerao et al., 1999). In arabidopsis, mutation of PRL1 has pleiotropic effects in sugar-, light- and stress-regulated gene expression, as well as in starch and sugar accumulation and in response to several phytohormones. Binding of PRL1 with SnRK1 was found to be enhanced in the absence of glucose and to inhibit autophosphorylation of the kinase expressed in E. coli. Putative SnRK1 activity was also slightly higher in a PRL1 mutant than in the wild type (Bhalerao et al., 1999), although the activity that was measured was not well characterized and was several orders of magnitude lower than activities measured in plant extracts using the SAMS or AMARA peptides as substrate.
Two-hybrid screening also identified a transcription factor that interacts with SnRK1 (S Laurie, RS McKibbin, NG Halford, unpublished data). This transcription factor is a member of the Apetela2/ethylene-responsive element binding protein family and full-length cDNAs encoding it have been cloned from barley, wheat and potato. Its function and the significance of its interaction with SnRK1 are not yet known, but its identification is a significant development given that SnRK1 has been shown to regulate gene expression.
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Evidence that SnRK1 is a conduit for cross-talk between metabolic and cell cycle signalling |
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TopAbstractIntroductionThe SnRK gene familySnRK1 activityRegulation of SnRK1 activitySnRK1 substratesSnRK1 regulates gene expressionSnRK1 and developmentIdentification of SnRK1...Evidence that SnRK1 is...Concluding remarksReferences |
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Several yeast protein kinases that are involved in cell cycle control are closely related to SNF1. They include NIM1 from fission yeast (Schizosaccharomyces pombe) and its budding yeast homologue NIK1 (nim1-like kinase). NIM1 is a mitotic inducer in fission yeast that phosphorylates and thereby inactivates the cell cycle inhibitory protein kinase, WEE1 (Russell and Nurse, 1987). NIK1 is a negative regulator of SWE1 (Saccharomyces homologue of wee1) that is involved in the calcium-dependent control of mitosis (Tanaka and Nojima, 1996). Furthermore, SNF1 itself has been implicated in cell cycle control, since snf1 mutants fail to arrest the cell cycle when they are in a state of nutrient deprivation, in other words they do not enter a normal stationary phase (Thompson-Jaeger et al., 1991). Other data suggest that SNF1 is also involved in the control of the onset of meiosis (Honigberg and Lee, 1998).
Over-expression of SnRK1 in yeast resulted in a dramatic reduction in yeast cell size, suggesting that the yeast cells were completing their cell cycles too early (Dickinson et al., 1999). One possible interpretation of these results is that SnRK1 was behaving like NIM1 or NIK1 in the yeast cells (over-expression of NIK1 has been shown to have a similar effect (Tanaka and Nojima, 1996)). Another interpretation is that acting as a conduit for cross-talk between metabolic and cell cycle signalling is part of the normal activity of SnRK1 and SNF1, and that this system was perturbed in the yeast cells by over-expression of the SnRK1 protein.
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Concluding remarks |
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TopAbstractIntroductionThe SnRK gene familySnRK1 activityRegulation of SnRK1 activitySnRK1 substratesSnRK1 regulates gene expressionSnRK1 and developmentIdentification of SnRK1...Evidence that SnRK1 is...Concluding remarksReferences |
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The functions of SnRK1 are summarized in Fig. 3. The identification of substrates for and genes that are regulated by SnRK1 is undoubtedly far from complete. Nevertheless, SnRK1 can already be placed at the heart of the control of carbon metabolism and partitioning.
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Acknowledgements |
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IACR receives grant-aided support from the Biotechnology and Biological Sciences Research Council of the United Kingdom. The authors thank Advanced Technologies (Cambridge) Ltd., Biogemma UK and Unilever Research for their support.
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References |
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TopAbstractIntroductionThe SnRK gene familySnRK1 activityRegulation of SnRK1 activitySnRK1 substratesSnRK1 regulates gene expressionSnRK1 and developmentIdentification of SnRK1...Evidence that SnRK1 is...Concluding remarksReferences |
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