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Thursday, 7 July 2016
How Do Sugars Regulate Plant Growth and Development? New Insight into the Role of Trehalose-6-Phosphate
Published Date
March 2013, Vol.6(2):261–274, doi:10.1093/mp/sss120
Open Archive, Elsevier user license
Review Article
Title
How Do Sugars Regulate Plant Growth and Development? New Insight into the Role of Trehalose-6-Phosphate
Author
Liam E. O’Hara a
Matthew J. Paul b
Astrid Wingler a,,
aGenetics, Evolution and Environment, University College London, Gower Street, London, WC1E 6BT, UK
bPlant Science, Rothamsted Research, Harpenden, Hertfordshire, AL5 2JQ, UK
Received 25 June 2012. Accepted 15 October 2012. Available online 9 December 2014. ABSTRACT Plant growth and development are tightly controlled in response to environmental conditions that influence the availability of photosynthetic carbon in the form of sucrose. Trehalose-6-phosphate (T6P), the precursor of trehalose in the biosynthetic pathway, is an important signaling metabolite that is involved in the regulation of plant growth and development in response to carbon availability. In addition to the plant’s own pathway for trehalose synthesis, formation of T6P or trehalose by pathogens can result in the reprogramming of plant metabolism and development. Developmental processes that are regulated by T6P range from embryo development to leaf senescence. Some of these processes are regulated in interaction with phytohormones, such as auxin. A key interacting factor of T6P signaling in response to the environment is the protein kinase sucrose non-fermenting related kinase-1 (SnRK1), whose catalytic activity is inhibited by T6P. SnRK1 is most likely involved in the adjustment of metabolism and growth in response to starvation. The transcription factor bZIP11 has recently been identified as a new player in the T6P/SnRK1 regulatory pathway. By inhibiting SnRK1, T6P promotes biosynthetic reactions. This regulation has important consequences for crop production, for example, in the developing wheat grain and during the growth of potato tubers. Key words
bZIP11
carbon availability
plant development
starvation
sucrose non-fermenting related kinase-1 (SnRK1)
trehalose
trehalose-6-phosphate
INTRODUCTION
Trehalose-6-phosphate (T6P) is the metabolic precursor of the non-reducing disaccharide trehalose. It is the product of the condensation reaction of UDP-glucose and glucose-6-phosphate (G6P) (Cabib and Leloir, 1958) which is catalyzed by the enzyme trehalose-6-phosphate synthase (TPS). T6P is further metabolized to trehalose by trehalose-6-phosphate phosphatase (TPP). Trehalose itself is eventually hydrolyzed by trehalase into two molecules of glucose (Figure 1) (Elbein et al., 2003).
Figure 1. Trehalose Metabolism in Plants. Trehalose-6-phosphate (T6P) is produced from UDP-glucose and glucose-6-phosphate (G6P) by the enzyme trehalose-6-phosphate synthase (TPS). T6P is dephosphorylated by trehalose-6-phosphate phosphatase (TPP) to produce trehalose. Trehalose is hydrolyzed by trehalase into two molecules of glucose.
Trehalose is an osmoprotectant which counters the effects of desiccation from drought, salt, or low-temperature stresses in the basal lineages of life (Crowe et al., 1992). Whilst trehalose was also successfully isolated from desiccation-tolerant vascular plants, such as the spikemoss Selaginella lepidophylla and the angiosperm Myrothamnus flabellifolius, it has proven more difficult to demonstrate that its presence is of plant, rather than of microbial, origin (Anselmino and Gilg, 1913; Gussin, 1972; Müller et al., 1995b). In addition, sucrose content was demonstrated to increase more strongly than trehalose during dehydration in the leaves of M. flabellifolius, indicating that sucrose and trehalose together are responsible for protecting this plant against the effects of desiccation (Drennan et al., 1993). At the time, prior to the discovery of plant enzymes for trehalose biosynthesis, Müller et al. (1995b) concluded that trehalose was restricted to the basal phyla of vascular plants and certain rare examples of desiccation-tolerant angiosperms.
Subsequently, the Arabidopsis genes necessary for the trehalose metabolic pathway were identified through yeast-complementation studies. This resulted in the identification of Arabidopsis TPS1 as a gene encoding a functional TPS enzyme (Blázquez et al., 1998) and of TPPA and TPPB as genes encoding functional TPP enzymes (Vogel et al., 1998). In total, Arabidopsis has 11 genes with homology to TPS and 10 with homology to TPP. The TPS genes can further be subdivided into class I (TPS1–TPS4) and class II (TPS5–TPS11). The latter have a synthase and a phosphatase domain, but their function remains elusive. While Chary et al. (2008) and Singh et al. (2011) showed complementation of the yeast tps1 and tps2 mutants by expression of Arabidopsis TPS6 and TPS11, respectively, Ramon et al. (2009)question that class II TPSs have catalytic activity.
Eventually, trehalose was detected in higher plants conclusively using gas chromatography–mass spectrometry (GC–MS), first from extracts of potato tubers, which had been grown axenically and therefore demonstrating that the trehalose was indeed of plant origin (Roessner et al., 2000), and then in Arabidopsis (Vogel et al., 2001). The difficulty of isolating trehalose from higher plants (Gussin, 1972; Müller et al., 1995b) is not surprising given that trehalose content is usually very low, often below the detection limit.
Recent reviews on the trehalose biosynthetic pathway in plants focus on the role of trehalose in stress responses (Fernandez et al., 2010), the function of T6P in development (Ponnu et al., 2011), and the regulation of growth by T6P (Schluepmann et al., 2012). The aim of this review is to integrate findings on the regulatory function of T6P with interactors such as the sucrose non-fermenting related kinase-1 (SnRK1) and the auxin signaling pathway to explain effects on growth, development, and crop yield.
FUNCTION OF TREHALOSE AND TREHALOSE-6-PHOSPHATE IN PLANTS
As trehalose exists in very low abundance in the majority of higher plants, its role as a primary metabolite or as a stress protectant, except in certain species mentioned above, is uncertain. This raises the question of why plants have functional genes for the synthesis and breakdown of trehalose.
Trehalose: A Toxin?
Early experiments on the impact of trehalose on higher plants, via trehalase inhibition, in species with very low trehalase activity and/or with trehalose supplementation, concluded that accumulation of trehalose was toxic, or at least that trehalose acted as an inhibitor of plant growth (Veluthambi et al., 1981), likely through the disruption of cell wall biosynthesis (Veluthambi et al., 1982a). This effect was reported to be associated with a perturbation of carbohydrate metabolism as indicated by a decline in sucrose (Veluthambi et al., 1982b). In species with high trehalase activity, the toxicity and growth inhibition were not seen (Veluthambi et al., 1981). However, recent work suggests that trehalase may not be involved in trehalose tolerance (Delatte et al., 2011; Gravot et al., 2011; see below). In soybean plantlets, treatment with validamycin A, a specific and potent inhibitor of trehalase (Asano et al., 1987), in the presence of trehalose resulted in an accumulation of trehalose to up to 80 mg g–1 dry weight without any effect on growth or plant health (Müller et al., 1995a). Furthermore, the activity of trehalase was not induced by trehalose, but by auxin. Treatment with validamycin A resulted in reduced sucrose and starch contents in the roots of soybean plantlets, and this effect was exacerbated by addition of trehalose in combination with validamycin A (Müller et al., 1995a). Accumulation of trehalose and a reduction in carbohydrate contents in response to validamycin A treatment were also found in Arabidopsis (Müller et al., 2001). However, starch content was increased after supply of trehalose (Wingler et al., 2000). It is therefore possible that validamycin A is less specific than suggested by Asano et al. (1987) and thus has unknown deleterious effects. The observation that feeding of high trehalose concentrations results in the accumulation of T6P (Schluepmann et al., 2004; see below) could also explain the differences between treatment with validamycin A and trehalose.
Support for the hypothesis that effects of trehalose metabolism on growth are caused by changes in carbohydrate metabolism is found in the observation that simultaneous addition of sucrose restores growth in the presence of trehalose and in the accumulation of starch in response to trehalose supply (Wingler et al., 2000). Trehalose feeding resulted in increased expression of the ADP-glucose pyrophosphorylase (AGPase) gene ApL3, as well as increased activity of AGPase, which is a key enzyme in starch biosynthesis (Wingler et al., 2000). In addition, T6P is involved in the redox activation of AGPase (Kolbe et al., 2005; see below). Growth was impaired after constitutive expression of an AGPase gene from Escherichia coliin potato plants, but could be restored by the addition of sucrose (Stark et al., 1992). This suggested that growth inhibition by trehalose may be caused by reduced availability of carbon for export to the growth zones as a consequence of excessive starch accumulation. The starchless adg1-1 mutant, which is mutated in the small subunit of AGPase, showed partial trehalose resistance (Fritzius et al., 2001), but trehalose-inhibited growth in the starchless phosphoglucomutase (pgm-1) mutant of Arabidopsis (Fritzius et al., 2001; Delatte et al., 2011). It is therefore not entirely clear to what extent the inhibition of growth in the presence of trehalose is directly caused by the sequestration of carbon as starch.
Trehalose and Growth Inhibition: Enter Trehalose-6-Phosphate
Schluepmann et al. (2004) attributed the growth inhibition in response to high concentrations of trehalose to the significant and rapid (within 30 min, declining thereafter) accumulation of T6P in seedlings treated with 100 mM trehalose, which is accompanied by a decrease in the G6P pool. This is confirmed by the finding that transgenic seedlings expressing an E. coli trehalase gene were able to grow uninhibited on 100 mM trehalose (Schluepmann et al., 2004). The same effect was seen, although growth was slower, in transgenic seedlings expressing the E. colitrehalose-6-phosphate hydrolase, TPH, which hydrolyses T6P to glucose and G6P (Schluepmann et al., 2004). Seedlings overexpressing TPP were, however, not rescued when grown on 100 mM trehalose, which was explained by the fact that the dephosphorylation of T6P to trehalose is thermodynamically unfavorable at high trehalose concentrations.
Microarray analysis of gene expression in plants with genetically altered T6P or increased T6P through feeding of trehalose revealed that T6P correlates with the expression of genes involved in responses to biotic and abiotic stress (Schluepmann et al., 2004). Although the exact mechanism as to how T6P accumulation, as a result of trehalose feeding, inhibits growth is still not known, it is possible that, in addition to carbon limitation in the growth zones described above, activation of some of these stress genes is also directly responsible for the growth inhibition.
Trehalose-6-Phosphate Is Indispensible for Growth
Whilst it appears that T6P is responsible for growth inhibition of plants on a medium containing high trehalose concentrations, clearly, T6P is also necessary for normal growth, since the Arabidopsis tps1 mutant, lacking TPS1, fails to germinate—terminating at the ‘torpedo’ stage, namely before the deposition of lipid and protein reserves (Eastmond et al., 2002; Schluepmann et al., 2003). tps1 mutants cannot be rescued by supplementation with trehalose (Eastmond et al., 2002), but rescue is achieved by the expression of E. coli TPS (Schluepmann et al., 2003), suggesting a role for T6P in embryo development. In addition to embryo development, T6P affects the vegetative growth of plants. Complementation of a tps1 mutant using a dexamethasone-inducible system to express TPS1 rescued embryo development, but resulted in reduced growth in the absence of further dexamethasone induction (van Dijken et al., 2004). Similarly, complementation using a seed-specific promoter rescued the embryo-lethal phenotype, but growth was still retarded compared to wild-type plants (Gómez et al., 2010). Moreover, vegetative growth was also delayed in TILLING mutants with weak TPS1 alleles.
The importance of T6P for growth is further emphasized in seedlings expressing TPP or TPH, both of which lead to reduced T6P levels, but produce different end products (Schluepmann et al., 2003). Plants with reduced T6P could not make use of supplied sugars and even experienced growth inhibition, whereas plants with elevated T6P exhibited significant growth increases over wild-type in response to sugar supply. The effect of T6P on growth is unconnected to levels of trehalose, as shown by overexpression of trehalase (Schluepmann et al., 2003). This requirement of T6P for carbohydrate utilization during growth is in agreement with its effect on the expression of genes for biosynthetic reactions, such as protein and nucleotide synthesis (Zhang et al., 2009). However, as outlined above, artificially high T6P can also result in growth inhibition. The observation that trehalose-dependent growth inhibition can be overcome by adding sucrose to the medium (Wingler et al., 2000; Schluepmann et al., 2004) indicates that T6P can promote growth when carbon supply is high, but growth is inhibited when T6P is not increased in balance with carbon availability.
Altered T6P results in changes to the contents of hexose phosphates: plants with increased T6P had lower G6P and fructose-6-phosphate (F6P) contents, whereas contents of these hexose phosphates were higher in plants with reduced T6P (Schluepmann et al., 2003). This T6P-dependent effect on hexose phosphates is enhanced with sucrose feeding, but there is little change in intermediates such as glucose-1-phosphate (G1P) or uridine di-phosphate glucose (UDPG), excluding fluxes from starch and sucrose synthesis, and instead indicating that the changes arise from glycolytic flux (Schluepmann et al., 2003). Furthermore, glucose and fructose feeding provoked changes to the hexose phosphate pool, but not in a T6P-dependent manner as with sucrose. Yet, glucose and fructose, which are sensed directly by hexokinase (Jang et al., 1997), elicit the same growth acceleration in plants with elevated T6P as seen with sucrose feeding (Schluepmann et al., 2003). T6P has been shown to inhibit the activity of hexokinases I and II at a micromolar range in the yeast Saccharomyces cerevisiae (Blázquez et al., 1993). However, even in excess of physiological concentrations, T6P has no significant inhibitory effects on the hexokinase activities of spinach (Wiese et al., 1999), Arabidopsis (Eastmond et al., 2002), or tomato (Kandel-Kfir et al., 2006).
Trehalose-6-Phosphate Synthesis Is Required for Pathogen Infection
In common with other microbes, microbial plant pathogens can accumulate much larger amounts of trehalose than can normally be found in plants. It is possible that, by releasing trehalose into the plant, pathogens can interfere with the sugar sensing pathways of their host and thereby manipulate plant metabolism to their favor. A strong accumulation of trehalose was found in the roots and hypocotyls of Arabidopsis plants infected with the protist Plasmodiophora brassicae, which causes clubroot disease (Brodmann et al., 2002). Expression of the P. brassicae PbTPS1gene in infected roots and hypocotyls suggests that the trehalose is mainly of pathogen origin (Brodmann et al., 2002). Trehalose content also increased in the stems and leaves where the pathogen does not usually spread and where no PbTPS1expression was found. This indicates that trehalose may be transported throughout the plant from the infected organs.
Together with trehalose accumulation, infection with P. brassicae resulted in enhanced expression of the Arabidopsis trehalase gene and also an increase in trehalase activity in the roots and hypocotyls (Brodmann et al., 2002). This could prevent further trehalose accumulation in the plant tissues. However, recent research has shown that trehalase activity is only induced by infection of the Col-0, but not of the Bur-0 accession of Arabidopsis (Gravot et al., 2011). Bur-0, which shows partial resistance to clubroot, is also more tolerant of externally supplied trehalose than Col-0, despite accumulating this compound. QTL analysis showed that a QTL for clubroot resistance co-localized with a QTL for trehalose tolerance, suggesting a role of trehalose in pathogenesis (Gravot et al., 2011). In addition to swelling of the root and hypocotyls, disease symptoms include the accumulation of starch, but expression of the trehalose-inducible ADP-glucose pyrophosphorylase (AGPase) gene ApL3 was not increased in clubroot-diseased Arabidopsis (Brodmann et al., 2002). In contrast, Gamm et al. (2011) found that AGPase activity was increased after infection of grapevine leaves with the oomycete Plasmopara viticola, together with accumulation of trehalose and the induction of trehalase.
Interestingly, trehalose application to wheat can induce partial protection against the powdery mildew pathogen Blumeria graminis (Reignault et al., 2001; Renard-Merlier et al., 2007), indicating potential utility in protection against biotic stress in addition to abiotic stress. Thus, it may be possible to utilize the trehalose pathway to elicit multiple stress-tolerance traits in crops. It was proposed that increased resistance to powdery mildew was due to activation of plant defense responses (Reignault et al., 2001; Renard-Merlier et al., 2007). Since the supply of trehalose to plants results in the accumulation of T6P (Schluepmann et al., 2004) and given the demonstrated role of T6P in sugar signaling, it is likely that at least some of the responses to trehalose synthesized by pathogens are caused by T6P and not trehalose accumulation. Unfortunately, T6P is notoriously difficult to measure and information about the effect of pathogen infection on T6P in plant cells is lacking.
In addition to influencing plant metabolism and defense responses, the trehalose biosynthetic pathway plays an important role within the pathogen during infection. The TPS1 gene of the rice blast fungus Magnaporthe grisea is required for colonization of the plant tissue (Foster et al., 2003). Despite the involvement of this gene in trehalose synthesis, site-directed mutagenesis of TPS1 has shown that the catalytic function can be uncoupled from pathogenicity (Wilson et al., 2007). Instead of affecting pathogenicity by synthesizing T6P, the TPS1 protein appears to play a role in G6P sensing and activation of NADPH production by the oxidative pentose phosphate pathway. According to this model, NADPH, in turn, inhibits the TPS reaction by displacing the substrates G6P and UDPG (Wilson et al., 2010), which results in a feedback loop. In addition, the NADPH/NADP ratio is involved in regulating the expression of virulence-associated genes which play a role in appressorium formation. This regulation may be important to adjust energy and nitrogen metabolism of the rice blast fungus according to changes in energy supply in the form of G6P during infection. Schluepmann et al. (2012) propose that T6P also affects NADPH-dependent redox signaling in plants, which could be a means by which AGPase is redox activated by T6P (Kolbe et al., 2005).
INTERACTION OF TREHALOSE-6-PHOSPHATE WITH THE SUCROSE NON-FERMENTING RELATED KINASE-1
The AMPK/SNF1/SnRK1 Family of Protein Kinases
Given the lack of evidence for a direct connection between T6P and the hexokinase-dependent sugar signaling pathway, Schluepmann et al. (2004) suggested there may be a link between T6P and sucrose non-fermenting related kinase-1 (SnRK1), which is a protein kinase involved in plant energy signaling (Baena-González et al., 2007). SnRK1 shares significant homology with the yeast sucrose non-fermenting-1 kinase (SNF1) and can complement yeast snf1 mutants (Alderson et al., 1991). Yeast snf1mutants are unable to utilize sucrose and other non-fermentable carbohydrates due lack of de-repression of glucose-repressible genes of carbon catabolism, such as the invertase gene (Sarokin and Carlson, 1985) and many other genes (Hardie et al., 1998). Furthermore, SNF1 shares extensive homology with mammalian AMP-activated protein kinase (AMPK) and likewise demonstrates serine/threonine phosphorylation activity (Celenza and Carlson, 1986). AMPK has a well-established role in mammalian energy signaling and is activated when glucose demand is high and availability low, such as during exercise. Parallel research into the plant 3-hydroxymethylglutaryl-CoA reductase kinase-A revealed this protein to be the same as SnRK1 (Ball et al., 1995). There is conservation of substrate recognition motifs between plant SnRK1, mammalian AMPK, and yeast SNF1 (Dale et al., 1995).
Snf1 and AMPK are both involved in chromatin remodeling. AMPK was shown to phosphorylate histone H2B, thereby activating transcription in response to stress (Bungard et al., 2010), while Snf1 can activate gene expression, such as by histone H3 acetylation, probably through recruiting the acetyl transferase Gcn5 (Abate et al., 2012). It is not known whether plant SnRK1 has a similar role in chromatin remodeling.
Plant Sucrose Non-Fermenting-Related Kinase-1
Snf1, AMPK, and SnRK1 are all heterotrimeric complexes, composed of three different subunits: α, β, and γ. In addition to two genes encoding the catalytically active α-subunit (AKIN10 = SnRK1.1 and AKIN11 = SnRK1.2), three genes encoding β-subunits and one encoding a γ-subunit, Arabidopsis also has a gene for a plant-specific βγ-subunit (Polge and Thomas, 2007).
The role of SnRK1 in regulating plant metabolism is well established (Polge and Thomas, 2007; Halford and Hey, 2009). For example, SnRK1 directly phosphorylates and thereby inactivates enzymes involved in plant metabolism, including 3-hydroxymethylglutaryl-CoA reductase, sucrose phosphate synthase, nitrate reductase, and TPS5. However, the regulation of SnRK1 itself in response to the availability of metabolites has been difficult to demonstrate (Halford and Hey, 2009). Activation by phosphorylation of SnRK1 in response to glucose has recently been shown by Jossier et al. (2009). Although, in contrast to AMPK, AMP does not activate SnRK1 directly; instead, AMP inhibits the dephosphorylation of SnRK1, thus preventing its inactivation (Sugden et al., 1999).
The requirement of SnRK1 for the expression of α-amylase during sugar starvation in wheat and rice embryos (Laurie et al., 2003; Lu et al., 2007) suggests that SnRK1 plays a role in starch breakdown during starvation. However, other evidence demonstrates that SnRK1 is also involved in activating starch synthesis in plants. McKibbin et al. (2006) showed that overexpression of SnRK1 was able to increase the expression of sucrose synthase and AGPase genes, resulting in an increased starch content of potato tubers. The SnRK1-mediated accumulation of starch can also be explained by evidence that SnRK1 is required for the sucrose-dependent redox activation of AGPase (Tiessen et al., 2003). Additionally, the transcripts of the rice SnRK1 homolog, OSK1, localize to vascular tissues of developing caryopses, suggesting a role in starch accumulation during grain filling (Kanegae et al., 2005). In contrast, Jossier et al. (2009) found that starch content was reduced in response to glucose supply in the leaves of Arabidopsis lines overexpressing KIN10, which encodes a catalytically active α-subunit of SnRK1. The opposite effect of SnRK1 on starch synthesis in potato tubers and Arabidopsis leaves may be due to differences in the regulation of starch metabolism in sink and source tissues. The paradox created by these two apparently incompatible roles of SnRK1 might also be resolved by differential effects of sucrose compared with glucose and other hexoses (Halford and Hey, 2009). For example, sucrose-dependent redox activation of AGPase requires SnRK1, whereas the effect of glucose is hexokinase-dependent (Tiessen et al., 2003). SnRK1 may therefore have a role as a positive or negative regulator of starch synthesis, depending on the levels of different metabolites and tissue type.
Convincing evidence that SnRK1 is involved in starvation signaling, consistent with the role of SNF1 and AMPK, was provided by Baena-González et al. (2007). Overexpression of the SnRK1 gene KIN10 revealed about 1000 putative KIN10 target genes, with those involved in catabolism being induced and those involved in biosynthetic reactions repressed (Baena-González and Sheen, 2008). A strong positive correlation was found between gene expression during low-sugar conditions and KIN10 gene targets and a strong negative correlation with transcripts active during sugar feeding.
Trehalose-6-Phosphate Inhibits SnRK1
It was shown that T6P inhibits the catalytic activity of SnRK1 in vitro at physiological concentrations (Zhang et al., 2009). Indirect evidence that T6P inhibits SnRK1 activity in vivo was gathered by monitoring the expression of KIN10 marker genes (Zhang et al., 2009). Among the genes up-regulated in Arabidopsis plants expressing bacterial TPS, those involved in biosynthetic processes were overrepresented. These include genes for nucleotide, amino acid, and protein synthesis. Simultaneously, there was down-regulation of genes associated with photosynthesis, starch breakdown, and gluconeogenesis. This regulation is opposite to the effect of KIN10 overexpression and consistent with inactivation of SnRK1 by T6P in response to high sugar availability.
In agreement with T6P inhibition of SnRK1 and the sugar hypersensitivity of seedlings with low T6P (Schluepmann et al., 2003), seedlings overexpressing SnRK1 from Arabidopsis or rice show a glucose-hypersensitive phenotype (Jossier et al., 2009; Cho et al., 2012). Increased growth in response to sugar supply seen in plants with elevated T6P (Schluepmann et al., 2003; Paul et al., 2010) might be explained by the fact that some of the most strongly up-regulated genes by T6P encode UDP-glucose dehydrogenases (Paul et al., 2010) which are involved in cell wall biosynthesis during growth (Klinghammer and Tenhaken, 2007).
Another link between SnRK1 and T6P was established for the redox regulation of AGPase. Feeding of trehalose to potato tubers activates AGPase, but this response was abolished in lines with antisense repression of SnRK1 (Kolbe et al., 2005). By manipulating T6P content Kolbe et al. (2005) found that the effect of trehalose feeding may be caused by T6P accumulation, although the exact mechanism of the interaction of T6P and SnRK1 in the redox regulation of AGPase has not been established.
Importance of an Unknown Factor for Inhibition of SnRK1 by T6P
While it has been demonstrated that T6P inhibits the catalytic activity of SnRK1 from Arabidopsis seedlings, this inhibition was not reproduced for SnRK1 from mature leaves (Zhang et al., 2009). A variation in the extent to which SnRK1 is inhibited by T6P was also found during wheat grain development (Martínez-Barajas et al., 2011). Experimental evidence suggests that a protein factor that is only present in young, growing tissues (such as seedlings, young Arabidopsis and spinach leaves, and cauliflower florets) underlies these developmental changes in the inhibition of SnRK1 by T6P (Zhang et al., 2009). When the catalytic α-subunits of SnRK1, KIN10, and KIN11 were partially purified by immunoprecipitation or anion-exchange chromatography, T6P no longer inhibited SnRK1 activity. However, addition of supernatant of a seedling extract, from which KIN10 and KIN11 had been removed by immunoprecipitation, restored T6P inhibition of partially purified KIN10/KIN11, showing that an intermediary factor required for the inhibition can be separated from the catalytic SnRK1 subunits. Addition of supernatant from seedlings to the immunoprecipitated KIN10/KIN11 from mature leaves also led to inhibition by T6P, but not vice versa. Boiling of the supernatant showed that the intermediary factor is heat labile, which could indicate that it is a protein. Interaction between the factor and KIN10/KIN11 may only occur in the presence of T6P, which would make its identification by co-purification difficult.
Several proteins have been shown to interact with SnRK1 and could therefore play a role in mediating the inhibitory effect of T6P. Examples include the myoinisitol polyphosphate 5-phosphatase 5PTase13 (Ananieva et al., 2008), the SnRK1 kinases GRIK1 (= AtSNAK2) and GRIK2 (= AtSNAK1) (Shen et al., 2009; Crozet et al., 2010), or the N-myristoyltransferases NMT1 and NMT1 (Pierre et al., 2007). However, none of the genes for these proteins shows expression patterns that would suggest that they are present in young, but not in mature, leaves. Interactions of additional proteins with KIN10 and KIN11 are predicted by the recently developed tool ANAP (Wang et al., 2012), providing candidates that can be tested by determining inhibition of SnRK1 by T6P in extracts from mutants. It is also possible that T6P binds to the β- or γ-subunits of the SnRK1 complex, but these subunits may interact tightly with KIN10 and KIN11 and thus co-immunoprecipitate (Bitrián et al., 2011). A role for these subunits in mediating the T6P inhibition of SnRK1 is therefore unlikely, given the separation of the intermediary factor from the catalytic subunit described by Zhang et al. (2009).
TREHALOSE-6-PHOSPHATE AS A SIGNAL FOR HIGH CARBON AVAILABILITY
A significant increase in T6P content is seen after sucrose feeding and after re-illumination at the end of the night (Schluepmann et al., 2004; Lunn et al., 2006). In addition, T6P content was correlated with sucrose during grain development in wheat (Martínez-Barajas et al., 2011). These findings indicate that T6P serves as a signal for high carbon availability in the form of sucrose.
The Role of Trehalose-6-Phosphate Interaction with SnRK1 during Starvation and Stress
T6P inhibits SnRK1 during times of plenty (Zhang et al., 2009) and T6P levels decline when carbon is scarce, thus allowing greater SnRK1 activity to down-regulate carbon-consuming processes and promote catabolic and photosynthetic processes, thereby increasing carbon availability (Baena-González et al., 2007; Baena-González and Sheen, 2008). SnRK1 may be important in signaling energy deficiency during stress conditions, including hypoxia, flooding, and darkness (Baena-González et al., 2007; Cho et al., 2012). Starvation can also be induced by shading or extended nights: an extension of the night by 2–4 h results in the total depletion of starch reserves, followed by a rapid decline in soluble sugars (Gibon et al., 2004; Thimm et al., 2004; Stitt et al., 2007). Re-illumination does not restore growth immediately, but results in the accumulation of sugars and, with them, a rise in T6P (Lunn et al., 2006) that stimulates the redox activation of AGPase (Kolbe et al., 2005). T6P therefore appears to occupy a central role as a signaling molecule that ensures the internal responses of plants are appropriate to stress conditions that result in starvation.
However, stress conditions do not necessarily lead to carbon depletion and can even increase internal carbon availability. For example, photosynthesis is very resilient to soil water deficits, whereas growth is extremely sensitive and is inhibited rapidly by drought conditions (Muller et al., 2011). This can result in an increase in carbohydrate contents during moderate drought stress (Hummel et al., 2010; Muller et al., 2011). Other forms of abiotic stress, such as cold stress, also result in sugar accumulation. In grapevine, T6P content increased in response to chilling and was correlated with sucrose content (Fernandez et al., 2012). Consistent with SnRK1 inhibition by T6P, T6P and SnRK1 may therefore have an antagonistic function during stress: T6P is likely to inhibit SnRK1 under stress conditions that lead to increased carbon availability, whereas high SnRK1 activity is required for the response of plants to conditions that result in starvation.
bZIP11 Mediates SnRK1 Metabolic Regulation in Response to Low Sucrose Availability
The transcription factor bZIP11/ATB2 is involved in regulating gene expression in response to sugar starvation (Hanson et al., 2008). While transcription of the bZIP11gene is increased by sucrose treatment, sucrose inhibits its translation (Rook et al., 1998; Wiese et al., 2004). It was shown that a sucrose control upstream open reading frame (SC-uORF), which is conserved in the upstream regions of S-group bZIP genes of many plant species, is indispensable for this sucrose-induced repression of translation (Wiese et al., 2004). The role of the S-group bZIPs in abiotic stress, which is often associated with significant changes in sucrose concentrations, puts the presence of the SC-uORF into physiological context (Wiese et al., 2004). A connection between SnRK1 and bZIP transcription factors, including bZIP11, was proposed by Baena-González and Sheen (2008) based on synergism between SnRK1 and these transcription factors in regulating gene expression (Baena-González et al., 2007).
An interaction was also found between bZIP11 and SnRK1 in the response of seedlings to trehalose feeding. Delatte et al. (2011) isolated Arabidopsis plants resistant to growth inhibition by 100 mM trehalose from a collection of transgenic lines constitutively overexpressing Arabidopsis cDNAs. These trehalose-resistant lines were identified to be overexpressors of bZIP11. By crossing them with a trehalase null-mutant, it was shown that trehalase is not required for trehalose resistance. It was established previously that growth on 100 mM trehalose results in an accumulation of T6P (Schluepmann et al., 2004). The finding that the trehalose-resistant bZIP11overexpressing Arabidopsis accumulated unprecedented T6P levels in response to trehalose feeding suggests that bZIP11 is overriding the growth inhibitory effect of high T6P (Delatte et al., 2011). Overexpression of the KIN10 was also able to bring about trehalase-independent resistance to trehalose. By comparing the gene expression profiles resulting from the overexpression of KIN10 and bZIP11, it was found that a subset of genes induced by bZIP11 were also up-regulated by KIN10(Delatte et al., 2011). Furthermore, a significant proportion of genes regulated by bZIP11 and KIN10 respond to trehalose feeding as if both factors were less active, indicating that bZIP11 is a likely target of SnRK1.
Similar to constitutive bZIP11 overexpression reported in Delatte et al. (2011), trehalose-induced growth inhibition was relieved by dexamethasone-induced nuclear-trafficking of bZIP11 (Ma et al., 2011). However, in this case, T6P content was reduced instead of increased, as with the constitutive overexpressors (Delatte et al., 2011), and expression of the trehalase gene TRE1 was increased. A function of trehalase in trehalose resistance is, however, unlikely given that bZIP11 also confers trehalose resistance in the absence of trehalase (Delatte et al., 2011).
For the control of growth by T6P, Delatte et al. (2011) propose a subtle mechanism including a regulatory loop that regulates growth in response to sucrose through an increase in T6P, inhibition of SnRK1, and therefore of bZIP11-dependent gene expression. The apparent contradiction that increased T6P during trehalose feeding as well as decreased T6P in the tps1 mutant inhibit growth can also be explained using this model. Too much T6P in the absence of a sufficient sucrose supply can result in a carbon deficit because of over-activation of biosynthetic pathways and reduced carbon salvage through catabolic pathways, whereas too little T6P inhibits growth because of the down-regulation of biosynthetic pathways required for growth.
Interaction between trehalose-6-phosphate and SnRK1 in the regulation of plant development
The Role of Trehalose-6-Phosphate in Plant Development
Effects of T6P on leaf development were first discovered in transgenic tobacco plants expressing the TPS genes from yeast (Romero et al., 1997) or E. coli (Goddijn et al., 1997). In both cases, leaves were lancet-shaped due to incomplete expansion in the lateral direction. In addition, plant growth was stunted, with a loss of apical dominance. Changes in leaf development were further analyzed by Pellny et al. (2004). Compared to wild-type plants, leaf area was increased in tobacco plants with lower T6P due to expression of bacterial TPP, but decreased in plants with higher T6P due to expression of TPS. While, on an area basis, expression of low T6P decreased photosynthetic activity and high T6P increased it, the overall larger leaf area in TPP-expressing plants resulted in increased plant growth. An Arabidopsis mutant with altered cell shape, retarded development, and changes in plant architecture was identified to harbor a mutation in the Arabidopsis TPS6 gene (Chary et al., 2008). Combined, these observations support a role for the trehalose pathway in regulating cell and leaf development, although how this is achieved mechanistically is not clear.
In Arabidopsis, high T6P led to increased anthocyanin accumulation during later stages of leaf development, whereas anthocyanins were reduced in plants with low T6P (Wingler et al., 2012). Since anthocyanins often accumulate when carbon supply is high, it is likely that T6P signals high sugar availability, thus stimulating the anthocyanin biosynthetic pathway. In addition, low T6P resulted in delayed senescence, both during growth in compost and when senescence was induced by glucose treatment. In agreement with the inhibition of SnRK1 by T6P, plants with altered SnRK1 expression also had senescence phenotypes. Arabidopsis plants in which both genes for the catalytic α-subunit of SnRK1 (KIN10 and KIN11) were silenced showed increased anthocyanin accumulation and early senescence under constant illumination, whereas senescence was delayed in plants overexpressing KIN10 or the rice SnRK1 (Baena-González et al., 2007; Cho et al., 2012). These findings suggest that the interaction between T6P and SnRK1 is important for signaling sugar availability to regulate leaf senescence. However, the SnRK1 from senescent leaves is not inhibited by T6P, probably because of the absence of the intermediary factor (see above). In addition, transfer between media with and without glucose indicates that T6P affects senescence by signaling sugar availability during early development (Wingler et al., 2012). This suggests that T6P inhibition of SnRK1 in young plants has consequences for later developmental stages, including leaf senescence.
Flowering time and inflorescence architecture are also affected by T6P and SnRK1. TPS1 expression is required for floral transition (van Dijken et al., 2004; Gómez et al., 2010), but flowering is also delayed in plants overexpressing TPS1 (Avonce et al., 2004). The T6P effect on flowering may be mediated by SnRK1 activity, since overexpression of KIN10 results in delayed flowering in combination with altered inflorescence architecture (Baena-González et al., 2007). Increased shoot branching in plants expressing microbial TPS genes (Goddijn et al., 1997; Romero et al., 1997) suggests that T6P regulates meristem activity and identity. More detailed information on the effect of trehalose metabolism on meristem function was obtained using the ramosa3 mutant of maize, which harbors a mutation in a functional TPP gene, RA3(Satoh-Nagasawa et al., 2006; see below). This mutant shows increased branching of the male as well as the female inflorescences, such as branched cobs. However, it is not known whether the effect of RA3 is linked to its catalytic activity in the trehalose biosynthetic pathway. Increased inflorescence branching in the Arabidopsis mutant in TPS6 (Chary et al., 2008), which does not appear to encode a protein with catalytic function in trehalose synthesis (Ramon et al., 2009), indicates that TPS and TPP proteins may have evolved to fulfill a signaling instead of a catalytic function during plant development, viz. by sensing the cellular T6P concentration in response to carbon availability to the meristems. The interaction of these proteins with functional TPS1, as shown for rice (Zang et al., 2011), could regulate T6P synthesis in a feedback loop. In addition, it is possible that TPS and TPP proteins are involved in transcriptional regulation, as proposed for RA3 (Satoh-Nagasawa et al., 2006; Eveland et al., 2010). The regulation of inflorescence development by genes for T6P metabolism has important consequences for crop production (see below).
The Trehalose-6-Phosphate/SnRK1 Regulatory System Is Linked to Auxin-Mediated Growth
There is evidence that the T6P/SnRK1 regulatory system may have connections to the hormonal regulation of plant growth and development. For example, microarray analysis demonstrated a down-regulation of auxin/indole-3-acetic acid (Aux/IAA) genes in seedlings with elevated levels of T6P (Paul et al., 2010). Aux/IAA proteins mediate auxin-regulated gene expression by interacting with corresponding auxin response factors (Hagen and Guilfoyle, 2002).
Levels of auxin are sensed by the auxin receptor transport inhibitor response 1 (TIR1) when a constituent of the Skp, Cullin, F-box containing (SCF) complex, to which auxin binds directly (Dharmasiri et al., 2005). The crucial role of TIR1 in auxin perception is demonstrated by the auxin insensitivity of tir1 mutants (Ruegger et al., 1998). TIR1expression was also down-regulated in plants with elevated levels of T6P (Paul et al., 2010) and SnRK1 has been shown to interact with the Skp1 domain of the SCF complex and the 26S proteasome, possibly acting to phosphorylate SCF-TIR1 substrates (Farras et al., 2001) such as Aux/IAA (Gray et al., 2001; Dos Santos Maraschin et al., 2009). The association of SnRK1 with the proteasomes is strengthened by observations that the repression of SnRK1 results in the down-regulation of the genes encoding 20S and 26S proteasomal subunits and subtilisin protease (Radchuk et al., 2006). Together with Aux/IAA down-regulation, this provides strong evidence for a connection between the T6P-SnRK1 regulatory system and auxin signaling.
The expression of Phytochrome Interacting Factor 4 (PIF4), which is involved in light signaling, was found to be down-regulated in plants with elevated T6P (Paul et al., 2010). PIF4 regulates plant development and growth, such as in shade-avoidance syndrome (Franklin, 2008), and high-temperature responses (Koini et al., 2009). Hypocotyl elongation, a characteristic seedling response to shading and high temperature, is mediated by auxin, the levels of which rise in response to high temperature (Gray et al., 1998). More recently, it was demonstrated that PIF4 mediates this observed high-temperature-induced increase in auxin levels by up-regulating auxin biosynthesis (Franklin et al., 2011). Seedlings with elevated T6P exhibit increased seedling growth in the presence of sucrose and a phenotype consistent with enhanced light signaling (Paul et al., 2010). Sucrose has been shown to increase seedling hypocotyl elongation—a process that requires PIFs (Stewart et al., 2011). In agreement with the proposed function of T6P in sucrose signaling, sucrose treatment resulted in a slight down-regulation of the expression of PIF4 and PIF5, the former of which is down-regulated in seedlings with elevated T6P (Paul et al., 2010). However, sucrose induced an increase in PIF5 protein abundance independently of light or phyB (Stewart et al., 2011).
The evidence that T6P levels influence auxin and PIF signaling provides a tantalizing possibility of carbon status signaling outputs via the T6P/SnRK1 regulatory system to hormonal control over plant development.
ROLE OF TREHALOSE-6-PHOSPHATE IN SINKS AND UTILITY IN CROP IMPROVEMENT
There is much interest in applying knowledge gained from model systems in crop enhancement. In particular, stress tolerance is a trait where progress towards improved crops has occurred. There is promise, too, that modification of the trehalose pathway may benefit intrinsic crop productivity. In contrast with model species, knowledge of fundamental trehalose biology in crops is less advanced. Moreover, the trehalose pathway may have distinct characteristics in crops, given that the most cultivated crops have large sink organs which have been exposed to selective pressures very different to Arabidopsis to maximize crop yield. Variation in the trehalose pathway may already have been selected for to produce traits important in crops. Cereals, for example, possess a distinct clade of TPP genes (Lunn, 2007; Martínez-Barajas et al., 2011), although little is known about the significance of this branch of TPPs. Enhanced stress tolerance in crops has been produced largely through effects on the vegetative part of the plant. In most crops, however, it is the sink tissue in the form of seeds, fruit, tubers, and roots that are harvested as crop yield.
There is evidence that the trehalose pathway has a decisive role in the growth and development of crop sink organs (Figure 2). In maize, there is a strong impact of the trehalose pathway on inflorescence development. Grass and cereal inflorescence morphology is highly variable, a large part of which can be attributed to the control of axillary meristem determinacy. RAMOSA genes RA1, 2, and 3 control axillary meristem growth by imposing determinacy. Loss-of-function ra mutants have a more indeterminate and branched inflorescence (see above). The RA3 gene of maize encodes a functional TPP enzyme (Satoh-Nagasawa et al., 2006). It is expressed at the base of the axillary meristems. Rice has a homolog of RA3 with a similar expression pattern (Satoh-Nagasawa et al., 2006), indicating a widespread nature of this mechanism which may also extend to Arabidopsis (Eveland and Jackson, 2012). Analysis of the transcriptome of RA3 mutants has shown strong effects on transcripts involved in carbohydrate biosynthesis and degradation and energy production. Developmentally regulated transcription factors and genes involved in auxin, ethylene, and brassinosteroid signal transduction were also affected (Eveland et al., 2010). These gene targets bear resemblance to the changes in transcription resulting from the interaction of T6P with SnRK1 (Zhang et al., 2009; Paul et al., 2010). However, in the case of RA3, the interaction of T6P and SnRK1 as a basis for the phenotypic effects has not yet been proven.
Figure 2. Model for the Function of T6P in Crop Plants.
A hypothetical crop plant is shown. T6P content increases in response to sucrose availability. Most of the processes that are affected by T6P (in italics) are probably mediated by SnRK1, mainly through inhibition of SnRK1 catalytic activity by T6P. Further details are explained in the text.
In wheat grain (Martínez-Barajas et al., 2011), potato tubers (Debast et al., 2011) and sugar cane sink cells (Wu and Birch, 2010) T6P has been shown to inhibit SnRK1. In both wheat grain and potato tubers, there is strong evidence that the same SnRK1 markers as in Arabidopsis are regulated by the T6P/SnRK1 interaction. For example, there were large changes in T6P during the course of the development of wheat grains (Martínez-Barajas et al., 2011). Amounts of T6P were very high in all grain tissues during pre-grain-filling early development—about 100-fold higher than previously reported in Arabidopsis. This was closely correlated to sucrose levels overall. However, beyond 10 d after anthesis (DAA), during grain filling, T6P became restricted to the endosperm with only trace amounts of T6P present in the outer and inner pericarp and in the embryo in spite of the presence of sucrose in these tissues. The data confirm the relationship between sucrose and T6P but also show a strong developmental component involved in regulating T6P content which can override the relationship between T6P and sucrose. The equivalent of TPS1 in wheat is expressed throughout grain development at a relatively stable level. However, class II TPS and TPP genes show larger changes in expression which may be causally related to the developmental regulation of T6P content in combination with TPS1. Interestingly, TPS protein complexes between TPS1 and class II TPSs have been found in rice which supports the view that class II TPSs may regulate TPS1 and T6P synthesis (Zang et al., 2011).
The changes in T6P distribution beyond 10 DAA were correlated with a shift in the expression of SnRK1 markers in wheat grain. This indicates that T6P regulation of SnRK1 in wheat grain is an important component of grain development with a change in regulation imparted by T6P during the transition from pre-grain-filling to grain-filling stages around 10 DAA. Inactivation of SnRK1 during early grain development may be necessary so that carbon can be incorporated into biosynthetic processes in relation to the amount of sucrose available. Subsequent development of the pericarp and embryo during grain filling is characterized by cessation of the inhibition of SnRK1 by T6P. Presumably, SnRK1-dependent processes are then able to proceed in the later stages of the development of these tissues. This developmental regulation of T6P levels ensures active SnRK1 even in the presence of high sucrose. However, grain filling in the endosperm is associated with high T6P. T6P has been shown to activate starch synthesis through redox regulation of AGPase (Kolbe et al., 2005) and through regulation of transcription of genes encoding enzymes involved in starch biosynthesis and degradation mediated by SnRK1 (Zhang et al., 2009). The data are consistent with the view that the inhibition of SnRK1 by T6P is strongly associated with anabolism and end product synthesis, namely biosynthetic processes. Under conditions of low assimilate supply to young grains, low T6P would enable SnRK1 to be active and may initiate metabolic reprogramming necessary for survival of at least some of the grains in the ear. In wheat and rice, active SnRK1 enables seeds and seedlings to respond to anoxic and starvation conditions (Laurie et al., 2003; Lee et al., 2009). Interestingly, embryo development has been found to be critically dependent on TPS1 and presumably T6P (Eastmond et al., 2002), yet T6P content of wheat embryos (Martínez-Barajas et al., 2011) and pea embryos (Radchuk et al., 2010) is very low and too low to inhibit SnRK1. However, T6P levels may be higher during very early embryo development. The critical dependence on TPS1/T6P in embryos requires further investigation.
The role of T6P during potato tuber development has been studied in transgenics through expression of E. coli TPS and TPP which increased and decreased T6P, respectively (Debast et al., 2011). Large effects were produced from sprouting through to final harvest which could be attributed to regulation of SnRK1 by T6P. These effects included impacts on respiration, starch, sugar, and ABA content. Both increase and decrease in the amount of T6P resulted in lower final yield than in wild-type plants.
CONCLUSIONS AND FUTURE PERSPECTIVE
In seedlings, T6P synthesis in response to sucrose availability supports growth probably through the stimulation of cell wall synthesis and interactions with auxin and light signaling (as described above and by Paul et al., 2010). While the effects on auxin signaling may not require T6P inhibition of SnRK1, inhibition of SnRK1 catalytic activity is likely to be responsible for the induction of genes involved in amino acid, protein, and nucleotide synthesis which are required for growth (Zhang et al., 2009). Similar growth mechanisms may also be active in young leaves (Figure 2). The involvement of T6P in the regulation of leaf senescence in response to sugar availability (Wingler et al., 2012) may play an important role in the remobilization of nitrogen to the sinks of crops. While SnRK1 is likely to be involved in senescence regulation, the lack of inhibition of SnRK1 from mature or senescing leaves by T6P suggests that this may not be a direct effect of the T6P accumulation found during senescence. Furthermore, T6P interaction with SnRK1 plays an important role in sink tissues of crop plants. SnRK1 is required for the T6P-dependent redox activation of the starch biosynthetic enzyme AGPase in potato tubers (Kolbe et al., 2005). However, transgenic potato lines with increased tuber T6P due to expression of bacterial TPS had a lower instead of higher starch content, while the tuber starch content of lines expressing bacterial TPP was not affected (Debast et al., 2011). The developmental effects of T6P on tuber and grain development that could be used to improve crop yield are outlined above.
To realize the benefits of T6P on yield formation, it will be necessary to target T6P effectively. As seen in wheat grain from the strong tissue-specific and development-specific patterns of T6P content, a highly targeted approach to its modification, such as using promoters that limit T6P formation to certain cells, is vital. Active SnRK1 is required for plant starvation responses that are necessary for survival. However, for productive growth to occur, plants need a mechanism through which SnRK1 can be inactivated when growing conditions are good and carbon availability is high. It is possible that the enhancement of biosynthetic processes by modifying T6P dependent on the growth conditions, at the right time during development and in the right cells, could result in higher yields.
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