Trehalose-6-Phosphate Synthase/Phosphatase Regulates Cell Shape and Plant Architecture in Arabidopsis

Chary, S. Narasimha; Hicks, Glenn R.; Choi, Yoon Gi; Carter, David; Raikhel, Natasha V.

doi:10.1104/pp.107.107441

Cited by 132 publications

(120 citation statements)

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“…In this case, EMS mutagenesis and confocal microscopy were used to identify Arabidopsis plants with aberrant distribution of a GFP fusion to a d-tonoplast intrinsic protein. With the same approach, Chary et al (2008) identified a mutant involved in ascribing cell shape and size, dubbed cell shape phenotype-1. Fine mapping identified the gene as a glycosyl-transferase family 20 member, trehalose-6-P synthase/phosphatase.…”

Section: Optical Imaging As a Mutant Screening Toolmentioning

confidence: 99%

Advances in Fluorescent Protein-Based Imaging for the Analysis of Plant Endomembranes

2008

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An exciting new era for live cell imaging of plant endomembranes was ushered in just over 10 years ago when Jim Haseloff and colleagues reported on the removal of a cryptic intron in the sequence of wildtype GFP for successful expression in plant cells (Haseloff et al., 1997). Haseloff's success was quickly welcomed by labs around the globe; by targeting GFP to secretory organelles, scientists could now bring to light the secret life of plant endomembranes. The plant endomembranes comprise several organelles functionally interlinked for the production and transport of secretory compounds, such as proteins, lipids, and sugars. Most of the secretory compounds are synthesized in the endoplasmic reticulum (ER) and then transported to the Golgi apparatus to be sorted for transport to distal compartments such as the plasma membrane and vacuoles. A forward transport of secretory molecules from the ER is counterbalanced by a retrograde flow from distal compartments that allows membrane homeostasis and communication with the cell's surroundings. Fluorescent protein technology applied to live cell imaging of plant endomembranes has aided immensely in providing subcellular markers for the study of the complex spatial and temporal relationships among secretory organelles. Live cell imaging is now moving forward to novel challenges. With the integration of genomic, transcriptomic, and proteomic techniques, we begin to collect data on the putative functions of plant genes; we need to understand the intricate relationships among thousands of proteins. To complete the puzzle, we must understand how the pieces fit together; we must define the functions of gene products. Important questions include: When are our proteins synthesized? Where are they targeted? With what elements do they interact? Advances in the development of optical imaging at the cellular level now offer the exciting opportunity to answer these questions.In this Update, we discuss several state-of-the-art applications of GFP imaging and how these techniques have been used to answer critical biological questions, with a focus on plant endomembrane trafficking.

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Section: Optical Imaging As a Mutant Screening Toolmentioning

confidence: 99%

Advances in Fluorescent Protein-Based Imaging for the Analysis of Plant Endomembranes

2008

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“…A TPP from corn, RAMOSA3, for example is expressed in a very restricted cell-file and preliminary results suggest that some TPSs from Arabidopsis have very restricted expression patterns (Satoh-Nagasawa et al, 2006). This contrasts with the expression patterns of AtTPS1 and AtTPS6 that are expressed ubiquitously at all stages of development (Chary et al, 2007;van Dijken et al, 2004). Analysis of the expression of all genes associated with trehalose metabolism in Arabidopsis roots using a dataset generated from cell-sorted root protoplasts is shown in Figure 5 ( Birnbaum et al, 2003;Brady et al, 2007).…”

Section: Expression Of the Genes Associated With Arabidopsis Trehalosmentioning

confidence: 77%

“…AtTPS5 interacts with the transcriptional co-activator MBF1c in vitro in S. cerevisiae two-hybrid assays and is thought to be required for basal thermo-tolerance of Arabidopsis (Suzuki et al, 2008). AtTPS6 was reported to complement S. cerevisiae strains deficient in ScTPS1 growing on glucose and S. cerevisiae strains deficient in ScTPS2 growing at 38 o C (Chary et al, 2007) but this result required further confirmation. Phylogenetic trees constructed with Class II TPS from Arabidopsis, poplar and rice support 5 orthologous groups each including AtTPS5, AtTPS6, AtTPS7, AtTPS8-10 and AtTPS11 (Lunn, 2007).…”

Section: Protein Structures and Possible Functions Of Different Genesmentioning

confidence: 95%

“…H. Schluepmann thanks Dr. John Lunn for critical appraisal of (Chary et al, 2007), she further acknowledges financial support from NWO-MEERVOUD. Rothamsted Research receives grant-aided support from the Biotechnological and Biological Sciences Research Council (BBSRC) of the United Kingdom.…”

Section: Acknowledgementsmentioning

confidence: 99%

“…Trehalose is cleaved into two moieties of glucose by specific trehalases (TreH pathway). Plants have been shown to encode enzymes capable of trehalose synthesis via the TPS/TPP pathway (Blazquez et al, 1998;Chary et al, 2007;Pramanik and Imai, 2005;Satoh-Nagasawa et al, 2006;Shima et al, 2007;Vogel et al, 1998). Plants also contain genes that encode trehalase (Aeschbacher et al, 1999;Muller et al, 2001), but lack genes with homology to enzymes from the other pathways.…”

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Trehalose Metabolites in Arabidopsis—elusive, active and central

Schluepmann

Paul

2009

The Arabidopsis Book

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Trehalose is an alpha,alpha-1,1-linked glucose disaccharide. In plants, trehalose is synthesized in two steps. Firstly, trehalose-6-phosphate synthase (TPS) converts UDP-glucose and glucose-6-phosphate to trehalose-6-phosphate (T6P); secondly, T6P-phosphatase (TPP) converts T6P into trehalose and Pi. Trehalose is further cleaved into glucose by trehalase. In extracts of most plants, including Arabidopsis, levels of both trehalose and T6P are low, nearing detection limits, and this has delayed research into their function. Trehalose is transported widely in plants, but transport of T6P is not thought to occur except possibly at the subcellular level. Feeding trehalose to Arabidopsis seedlings alters carbon allocation with massive starch accumulation in cotyledons and leaves and absence of starch and growth in shoot and root apices.The Arabidopsis genome has experienced extensive radiation of genes likely encoding enzymes of T6P metabolism: 4 and 10 genes are found with homology to TPS and TPP respectively and 7 genes are found with homology to both TPS and TPP. Complementation of Saccharomyces cerevisiae mutants has shown that AtTPS1, AtTPPA and AtTPPB are functional enzymes. In contrast just a single gene encoding a protein with trehalase activity has been found. Whilst most TPS proteins appear cytosolic, strikingly, some TPPs appear targeted to chloroplasts; trehalase on the other hand is extracellular. Transporters of trehalose and T6P have yet to be described. Arabidopsis tps1 mutants are embryo lethal and results suggest that T6P is essential for several other steps in development including root growth and floral transition. Accordingly, altering T6P content has a profound effect on plant habitus and impacts metabolite profiles, sugar utilization and photosynthesis. These large effects have hindered dissection of cause and effect. In contrast, plants with large alterations in sucrose-6-phosphate concentrations are indistinguishable from wild type, suggesting very different functions for these compounds. Recently, T6P at low micromolar concentrations has been shown in vitro and in vivo to inhibit SnRK1 of the SNF1/AMPK group of protein kinases. This supports a function for T6P as a sugar signaling molecule integrating metabolism and development in plants in relation to carbon supply.Genetic engineering of Arabidopsis as well as tobacco, potato and rice with TPS or TPS/TPP protein fusions reveals that trehalose metabolism also mediates multiple abiotic stress tolerances. Trehalose applications also mediate biotic stress resistances. Both Escherichia coli and Saccharomyces cerevisiae TPS/TPP protein fusions can be used to engineer stress tolerance suggesting that metabolites rather than proteins of the trehalose pathway are key stress tolerance elicitors. Results underscore the central role of trehalose metabolites in integrating carbon metabolism and stress responses with plant development.

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Wild Relative and Transgenic Innovation for Enhancing Crop Adaptation to Warmer and Drier Climate

Gong

McIntyre

2011

Crop Adaptation to Climate Change

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Trehalose-6-Phosphate Synthase/Phosphatase Regulates Cell Shape and Plant Architecture in Arabidopsis

Cited by 132 publications

References 54 publications

Advances in Fluorescent Protein-Based Imaging for the Analysis of Plant Endomembranes

Advances in Fluorescent Protein-Based Imaging for the Analysis of Plant Endomembranes

Trehalose Metabolites in Arabidopsis—elusive, active and central

Wild Relative and Transgenic Innovation for Enhancing Crop Adaptation to Warmer and Drier Climate

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