The mechanisms by which higher plants recognize and respond to sugars are largely unknown. Here, we present evidence that the first enzyme in the hexose assimilation pathway, hexokinase (HXK), acts as a sensor for plant sugar responses. Transgenic Arabidopsis plants expressing antisense hexokinase (AtHXK) genes are sugar hyposensitive, whereas plants overexpressing AtHXK are sugar hypersensitive. The transgenic plants exhibited a wide spectrum of altered sugar responses in seedling development and in gene activation and repression. Furthermore, overexpressing the yeast sugar sensor YHXK2 caused a dominant negative effect by elevating HXK catalytic activity but reducing sugar sensitivity in transgenic plants. The result suggests that HXK is a dual-function enzyme with a distinct regulatory function not interchangeable between plants and yeast.
Complex and interconnected signaling networks allow organisms to control cell division, growth, differentiation, or programmed cell death in response to metabolic and environmental cues. In plants, it is known that sugar and nitrogen are critical nutrient signals; however, our understanding of the molecular mechanisms underlying nutrient signal transduction is very limited. To begin unraveling complex sugar signaling networks in plants, DNA microarray analysis was used to determine the effects of glucose and inorganic nitrogen source on gene expression on a global scale in Arabidopsis thaliana. In whole seedling tissue, glucose is a more potent signal in regulating transcription than inorganic nitrogen. In fact, other than genes associated with nitrate assimilation, glucose had a greater effect in regulating nitrogen metabolic genes than nitrogen itself. Glucose also regulated a broader range of genes, including genes associated with carbohydrate metabolism, signal transduction, and metabolite transport. In addition, a large number of stress responsive genes were also induced by glucose, indicating a role of sugar in environmental responses. Cluster analysis revealed significant interaction between glucose and nitrogen in regulating gene expression because glucose can modulate the effects of nitrogen and vise versa. Intriguingly, cycloheximide treatment appeared to disrupt glucose induction more than glucose repression, suggesting that de novo protein synthesis is an intermediary event required before most glucose induction can occur. Cross talk between sugar and ethylene signaling may take place on the transcriptional level because several ethylene biosynthetic and signal transduction genes are repressed by glucose, and the repression is largely unaffected by cycloheximide. Collectively, our global expression data strongly support the idea that glucose and inorganic nitrogen act as both metabolites and signaling molecules.
Glucose is an essential signaling molecule that controls plant development and gene expression through largely unknown mechanisms. To initiate the dissection of the glucose signal transduction pathway in plants by using a genetic approach, we have identified an Arabidopsis mutant, gin1 (glucose-insensitive), in which glucose repression of cotyledon greening and expansion, shoot development, f loral transition, and gene expression is impaired. Genetic analysis indicates that GIN1 acts downstream of the sensor hexokinase in the glucose signaling pathway. Surprisingly, gin1 insensitivity to glucose repression of cotyledon and shoot development is phenocopied by ethylene precursor treatment of wild-type plants or by constitutive ethylene biosynthesis and constitutive ethylene signaling mutants. In contrast, the ethylene insensitive mutant etr1-1 exhibits glucose hypersensitivity. Epistasis analysis places GIN1 downstream of the ethylene receptor, ETR1, and defines a new branch of ethylene signaling pathway that is uncoupled from the triple response induced by ethylene. The isolation and characterization of gin1 reveal an unexpected convergence between the glucose and the ethylene signal transduction pathways. GIN1 may function to balance the control of plant development in response to metabolic and hormonal stimuli that act antagonistically.Glucose has profound effects on gene expression, metabolism, and development in microorganisms, animals, and plants (1-9). Although the glucose signal transduction pathways are well characterized in unicellular microorganisms, relatively little is known about the molecular basis of glucose responses in multicellular eukaryotes. In higher plants, glucose has been implicated to be the primary sugar signal that controls many aspects of plant development, including germination, hypocotyl elongation, cotyledon greening and expansion, primary and lateral root growth, true leaf development, floral transition, and the onset of senescence. At the molecular level, the expression of a broad spectrum of genes is either repressed or induced by glucose (4-9). Recently, hexokinase (HXK), the enzyme that catalyzes the phosphorylation of hexose sugars at the first step of the glycolytic pathway, has been shown to be the glucose sensor in plants (9-12). Studies in transgenic Arabidopsis plants with elevated or reduced Arabidopsis thaliana HXK levels or with a heterologous yeast HXK provide supporting evidence that HXK is a bifunctional enzyme with catalytic and regulatory activities, and glucose signaling may be uncoupled from glucose metabolism in plants (12). However, the downstream components in the glucose-signaling pathway are mostly unknown. Although interactions between sugar and light or hormonal signaling pathways have been suggested (13-23), the mechanisms underlying the crosstalk between glucose and other signaling pathways remain obscure.We report here the phenotypic, molecular, and genetic analyses of a recessive Arabidopsis mutant (glucose-insensitive, gin1) that is defective...
Sugar repression of photosynthetic genes is likely a central control mechanism mediating energy homeostasis in a wide range of algae and higher plants. It overrides light activation and is coupled to developmental and environmental regulations. How sugar signals are sensed and transduced to the nucleus remains unclear. To elucidate sugar-sensing mechanisms, we monitored the effects of a variety of sugars, glucose analogs, and metabolic intermediates on photosynthetic fusion genes in a sensitive and versatile maize protoplast transient expression system. The results show that sugars that are the substrates of hexokinase (HK) cause repression at a low concentration (1 to 10 mM), indicating a low degree of specificity and the irrelevance of osmotic change. Studies with various glucose analogs suggest that glucose transport across the plasma membrane is necessary but not sufficient to trigger repression, whereas subsequent phosphorylation by HK may be required. The effectiveness of 2-deoxyglucose, a nonmetabolizable glucose analog, and the ineffectiveness of various metabolic intermediates in eliciting repression eliminate the involvement of glycolysis and other metabolic pathways. Replenishing intracellular phosphate and ATP diminished by hexoses does not overcome repression. Because mannoheptulose, a specific HK inhibitor, blocks the severe repression triggered by 2-deoxyglucose and yet the phosphorylated products per se do not act as repression signals, we propose that HK may have dual functions and may act as a key sensor and signal transmitter of sugar repression in higher plants.
Processing bodies (PBs) are specialized cytoplasmic foci where mRNA turnover and translational repression can take place. Stress granules are related cytoplasmic foci. The CCCH tandem zinc finger proteins (TZFs) play pivotal roles in gene expression, cell fate specification, and various developmental processes. Human TZF binds AU-rich elements at the 3# untranslated region and recruits decapping, deadenylation, and exonucleolytic enzymes to PBs for RNA turnover. Recent genetic studies indicate that plant TZFs are involved in gene regulation and hormone-mediated environmental responses. It is unknown if plant TZFs can bind RNA and be localized to PBs or stress granules. The Arabidopsis (Arabidopsis thaliana) AtTZF1/AtCTH/AtC3H23 was identified as a sugar-sensitive gene in a previous microarray study. It is characterized by a TZF motif that is distinct from the human TZF. Higher plants such as Arabidopsis and rice (Oryza sativa) each have a gene family containing this unique TZF motif. Here, we show that AtTZF1 can traffic between the nucleus and cytoplasmic foci. AtTZF1 colocalizes with markers of PBs, and the morphology of these cytoplasmic foci resembles that of mammalian PBs and stress granules. AtTZF1-associated cytoplasmic foci are dynamic and tissue specific. They can be induced by dark and wound stresses and are preferentially present in actively growing tissues and stomatal precursor cells. Since AtTZF1 can bind both DNA and RNA in vitro, it raises the possibility that AtTZF1 might be involved in DNA and/or RNA regulation.
The mechanisms by which higher plants recognize and respond to sugars are largely unknown. Here, we present evidente that the first enzyme in the hexose assimilation pathway, hexokinase (
Glucose (Glc) signaling, along with abscisic acid (ABA) signaling, has been implicated in regulating early plant development in Arabidopsis. It is generally believed that high levels of exogenous Glc cause ABA accumulation, which results in a delay of germination and an inhibition of seedling development-a typical stress response. To test this hypothesis and decipher the complex interactions that occur in the signaling pathways, we determined the effects of sugar and ABA on one developmental event, germination. We show that levels of exogenous Glc lower than previously cited could delay the rate of seed germination in wild-ecotype seeds. Remarkably, this effect could not be mimicked by an osmotic effect, and ABA was still involved. With higher concentrations of Glc, previously known Glc-insensitive mutants gin2 and abi4 exhibited germination kinetics similar to wild type, indicating that Glc-insensitive phenotypes are not the same for all developmental stages of growth and that the signaling properties of Glc vary with concentration. Higher concentrations of Glc were more potent in delaying seed germination. However, Glc-delayed seed germination was not caused by increased cellular ABA concentration, rather Glc appeared to slow down the decline of endogenous ABA. Except for the ABA-insensitive mutants, all tested genotypes appeared to have similar ABA perception during germination, where germination was correlated with the timing of ABA drop to a threshold level. In addition, Glc was found to modulate the transcription of genes involved in ABA biosynthesis and perception only after germination, suggesting a critical role of the developmental program in sugar sensing. On the basis of an extensive phenotypic, biochemical, and molecular analysis, we suggest that exogenous Glc application creates specific signals that vary with concentration and the developmental stage of the plant and that Glc-induced fluctuations in endogenous ABA level generate a different set of signals than those generated by external ABA application.Because metabolic and structural functions require the proper amount of carbon source, different organisms have developed the ability to sense internal levels of sugar and accordingly adjust their cellular and metabolic activities. These regulatory mechanisms are particularly important for plants, because sugar production, consumption, and storage occur in the same organism. On one hand, plants have developed sophisticated programs in managing sugar production in source tissue and sugar storage in sink tissue; on the other hand, a complex regulatory circuit controlling gene expression has evolved to accommodate constant changes of sugar-dependent cellular activities (Smeekens, 2000;Coruzzi and Bush, 2001;Coruzzi and Zhou, 2001).Because sugars affect the expression of a diverse array of genes involved in different cellular processes, it is proposed that distinct signaling pathways are employed for the control of these genes. At least three types of Glc signal transduction mechanisms have been found ...
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