The concept that photosynthetic flux is influenced by the accumulation of photo-assimilate persisted for 100 years before receiving any strong experimental support. Precise analysis of the mechanisms of photosynthetic responses to sink activity required the development of a battery of appropriate molecular techniques and has benefited from contemporary interest in the effects of elevated CO2 on photosynthesis. Photosynthesis is one of the most highly integrated and regulated metabolic processes to maximize the use of available light, to minimize the damaging effects of excess light and to optimize the use of limiting carbon and nitrogen resources. Hypotheses of feedback regulation must take account of this integration. In the short term, departure from homeostasis can lead to redox signals, which cause rapid changes in the transcription of genes encoding photosystems I and II. End-product synthesis can exert short-term metabolic feedback control through Pi recycling. Beyond this, carbohydrate accumulation in leaves when there is an imbalance between source and sink at the whole plant level can lead to decreased expression of photosynthetic genes and accelerated leaf senescence. In a high CO2 world this may become a more prevalent feature of photosynthetic regulation. However, sink regulation of photosynthesis is highly dependent on the physiology of the rest of the plant. This physiological state regulates photosynthesis through signal transduction pathways that co-ordinate the plant carbon : nitrogen balance, which match photosynthetic capacity to growth and storage capacity and underpin and can override the direct short-term controls of photosynthesis by light and CO2. Photosynthate supply and phytohormones, particularly cytokinins, interact with nitrogen supply to control the expression of photosynthesis genes, the development of leaves and the whole plant nitrogen distribution, which provides the dominant basis for sink regulation of photosynthesis.
Trehalose-6-phosphate (T6P) is a proposed signaling molecule in plants, yet how it signals was not clear. Here, we provide evidence that T6P functions as an inhibitor of SNF1-related protein kinase1 (SnRK1; AKIN10/AKIN11) of the SNF1-related group of protein kinases. T6P, but not other sugars and sugar phosphates, inhibited SnRK1 in Arabidopsis (Arabidopsis thaliana) seedling extracts strongly (50%) at low concentrations (1-20 mM). Inhibition was noncompetitive with respect to ATP. In immunoprecipitation studies using antibodies to AKIN10 and AKIN11, SnRK1 catalytic activity and T6P inhibition were physically separable, with T6P inhibition of SnRK1 dependent on an intermediary factor. In subsequent analysis, T6P inhibited SnRK1 in extracts of all tissues analyzed except those of mature leaves, which did not contain the intermediary factor. To assess the impact of T6P inhibition of SnRK1 in vivo, gene expression was determined in seedlings expressing Escherichia coli otsA encoding T6P synthase to elevate T6P or otsB encoding T6P phosphatase to decrease T6P. SnRK1 target genes showed opposite regulation, consistent with the regulation of SnRK1 by T6P in vivo. Analysis of microarray data showed up-regulation by T6P of genes involved in biosynthetic reactions, such as genes for amino acid, protein, and nucleotide synthesis, the tricarboxylic acid cycle, and mitochondrial electron transport, which are normally down-regulated by SnRK1. In contrast, genes involved in photosynthesis and degradation processes, which are normally up-regulated by SnRK1, were down-regulated by T6P. These experiments provide strong evidence that T6P inhibits SnRK1 to activate biosynthetic processes in growing tissues.
Genes for trehalose metabolism are widespread in higher plants. Insight into the physiological role of the trehalose pathway outside of resurrection plant species is lacking. To address this lack of insight, we express Escherichia coli genes for trehalose metabolism in Arabidopsis thaliana, which manipulates trehalose 6-phosphate (T6P) contents in the transgenic plants. Plants
Trehalose metabolism and signaling is an area of emerging significance. In less than a decade our views on the importance of trehalose metabolism and its role in plants have gone through something of a revolution. An obscure curiosity has become an indispensable regulatory system. Mutant and transgenic plants of trehalose synthesis display wide-ranging and unprecedented phenotypes for the perturbation of a metabolic pathway. Molecular physiology and genomics have provided a glimpse of trehalose biology that had not been possible with conventional techniques, largely because the products of the synthetic pathway, trehalose 6-phosphate (T6P) and trehalose, are in trace abundance and difficult to measure in most plants. A consensus is emerging that T6P plays a central role in the coordination of metabolism with development. The discovery of trehalose metabolism has been one of the most exciting developments in plant metabolism and plant science in recent years. The field is fast moving and this review highlights the most recent insights.
Trehalose is the most widespread disaccharide in nature, occurring in bacteria, fungi, insects, and plants. Its precursor, trehalose 6-phosphate (T6P), is also indispensable for the regulation of sugar utilization and growth, but the sites of action are largely unresolved. Here we use genetic and biochemical approaches to investigate whether T6P acts to regulate starch synthesis in plastids of higher plants. Feeding of trehalose to Arabidopsis leaves led to stimulation of starch synthesis within 30 min, accompanied by activation of ADP-glucose pyrophosphorylase (AGPase) via posttranslational redox modification. The response resembled sucrose but not glucose feeding and depended on the expression of SNF1-related kinase. We also analyzed transgenic Arabidopsis plants with T6P levels increased by expression of T6P synthase or decreased by expression of T6P phosphatase (TPP) in the cytosol. Compared with wild type, leaves of T6P synthase-expressing plants had increased redox activation of AGPase and increased starch, whereas TPP-expressing plants showed the opposite. Moreover, TPP expression prevented the increase in AGPase activation in response to sucrose or trehalose feeding. Incubation of intact isolated chloroplasts with 100 M T6P significantly and specifically increased reductive activation of AGPase within 15 min. Results provide evidence that T6P is synthesized in the cytosol and acts on plastidial metabolism by promoting thioredoxin-mediated redox transfer to AGPase in response to cytosolic sugar levels, thereby allowing starch synthesis to be regulated independently of light. The discovery informs about the evolution of plant metabolism and how chloroplasts of prokaryotic origin use an intermediate of the ancient trehalose pathway to report the metabolic status of the cytosol.SNF1 kinase ͉ sugar signaling ͉ thioredoxin S tarch is the major carbon store in plants consisting of an insoluble polymer of ␣-1,4-and ␣-1,6-linked glucose units (1). In the chloroplast of leaves, starch is synthesized during the day as a transient store, which is degraded during the night to support nonphotosynthetic leaf metabolism and sucrose export. In heterotrophic storage organs such as potato tubers, most of the incoming sucrose is converted to starch as a long-term carbon store for reproductive growth. In addition to its central role in carbon metabolism of plants, starch is also of great economical importance and is used for food and feed purposes and many industrial applications (2).ADP-glucose pyrophosphorylase (AGPase) catalyzes the first committed step of starch synthesis in the plastid, converting glucose 1-phosphate and ATP to ADP-glucose and PP i . ADP-glucose is subsequently used by starch synthases and branching enzymes to elongate the glucan chains of the starch granule. AGPase is a heterotetramer that contains two large (AGPS, 51 kDa) and two slightly smaller subunits (AGPB, 50 kDa) (3, 4). Work with Arabidopsis mutants (5) and potato tubers (6) showed that the enzyme catalyzes a near rate-limiting step in the pat...
Maize, the highest-yielding cereal crop worldwide, is particularly susceptible to drought during its 2- to 3-week flowering period. Many genetic engineering strategies for drought tolerance impinge on plant development, reduce maximum yield potential or do not translate from laboratory conditions to the field. We overexpressed a gene encoding a rice trehalose-6-phosphate phosphatase (TPP) in developing maize ears using a floral promoter. This reduced the concentration of trehalose-6-phosphate (T6P), a sugar signal that regulates growth and development, and increased the concentration of sucrose in ear spikelets. Overexpression of TPP increased both kernel set and harvest index. Field data at several sites and over multiple seasons showed that the engineered trait improved yields from 9% to 49% under non-drought or mild drought conditions, and from 31% to 123% under more severe drought conditions, relative to yields from nontransgenic controls.
Trehalose-6-phosphate (T6P) is required for carbon utilization during Arabidopsis development, and its absence is embryo lethal. Here we show that T6P accumulation inhibits seedling growth. Wild-type seedlings grown on 100 mM trehalose rapidly accumulate T6P and stop growing, but seedlings expressing Escherichia coli trehalose phosphate hydrolase develop normally on such medium. T6P accumulation likely results from much-reduced T6P dephosphorylation when trehalose levels are high. Metabolizable sugars added to trehalose medium rescue T6P inhibition of growth. In addition, Suc feeding leads to a progressive increase in T6P concentrations, suggesting that T6P control over carbon utilization is related to available carbon for growth. Expression analysis of genes from the Arabidopsis trehalose metabolism further supports this: Suc rapidly induces expression of trehalose phosphate synthase homolog AtTPS5 to high levels. In contrast, T6P accumulation after feeding trehalose in the absence of available carbon induces repression of genes encoding T6P synthases and expression of T6P phosphatases. To identify processes controlled by T6P, we clustered expression profile data from seedlings with altered T6P content. T6P levels correlate with expression of a specific set of genes, including the S6 ribosomal kinase ATPK19, independently of carbon status. Interestingly, Suc addition represses 15 of these genes, one of which is AtKIN11, encoding a Sucrose Non Fermenting 1 (SNF1)-related kinase known to play a role in Suc utilization.
Photosynthesis is regulated as a two-way process. Light regulates the expression of genes for photosynthesis and the activity of the gene products (feedforward control). Rate of end-product use down-stream of the Calvin cycle, determined largely by nutrition and temperature, also affects photosynthetic activity and photosynthetic gene expression (feedback control). Whereas feedforward control ensures efficient light use, feedback mechanisms ensure that carbon flow is balanced through the pathways that produce and consume carbon, so that inorganic phosphate is recycled and nitrogen is distributed optimally to different processes to ensure growth and survival. Actual mechanisms are sketchy and complex, but carbon to nitrogen balance rather than carbon status per se is central to understanding carbon metabolite feedback control of photosynthesis. In addition to determining the activity of the metabolic machinery, carbon metabolite feedback mechanisms also regulate photosynthesis at the leaf level through the regulation of leaf development. This review summarizes the current sketchy, but growing, knowledge of the mechanisms through which carbon metabolite feedback mechanisms regulate leaf photosynthesis.
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