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Expansive evolution of the TREHALOSE-6-PHOSPHATE PHOSPHATASE gene family in Arabidopsis

(2012) PLANT PHYSIOLOGY. 160(2). p.884-896
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Abstract
Trehalose is a nonreducing sugar used as a reserve carbohydrate and stress protectant in a variety of organisms. While higher plants typically do not accumulate high levels of trehalose, they encode large families of putative trehalose biosynthesis genes. Trehalose biosynthesis in plants involves a two-step reaction in which trehalose-6-phosphate (T6P) is synthesized from UDPglucose and glucose-6-phosphate (catalyzed by T6P synthase [TPS]), and subsequently dephosphorylated to produce the disaccharide trehalose (catalyzed by T6P phosphatase [TPP]). In Arabidopsis (Arabidopsis thaliana), 11 genes encode proteins with both TPS- and TPP-like domains but only one of these (AtTPS1) appears to be an active (TPS) enzyme. In addition, plants contain a large family of smaller proteins with a conserved TPP domain. Here, we present an in-depth analysis of the 10 TPP genes and gene products in Arabidopsis (TPPA-TPPJ). Collinearity analysis revealed that all of these genes originate from whole-genome duplication events. Heterologous expression in yeast (Saccharomyces cerevisiae) showed that all encode active TPP enzymes with an essential role for some conserved residues in the catalytic domain. These results suggest that the TPP genes function in the regulation of T6P levels, with T6P emerging as a novel key regulator of growth and development in higher plants. Extensive gene expression analyses using a complete set of promoter-beta-glucuronidase/green fluorescent protein reporter lines further uncovered cell- and tissue-specific expression patterns, conferring spatiotemporal control of trehalose metabolism. Consistently, phenotypic characterization of knockdown and overexpression lines of a single TPP, AtTPPG, points to unique properties of individual TPPs in Arabidopsis, and underlines the intimate connection between trehalose metabolism and abscisic acid signaling.
Keywords
CRYSTAL-STRUCTURE, DROUGHT TOLERANCE, VEGETATIVE GROWTH, METABOLIC PATHWAYS, BIOLOGICAL IMPLICATIONS, TREHALOSE 6-PHOSPHATE, SACCHAROMYCES-CEREVISIAE, GENOME DUPLICATIONS, ESCHERICHIA-COLI, ABSCISIC-ACID

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Chicago
Vandesteene, Lies, Lorena Lopez Galvis, Kevin Vanneste, Regina Feil, Steven Maere, Willem Lammens, Filip Rolland, et al. 2012. “Expansive Evolution of the TREHALOSE-6-PHOSPHATE PHOSPHATASE Gene Family in Arabidopsis.” Plant Physiology 160 (2): 884–896.
APA
Vandesteene, L., Lopez Galvis, L., Vanneste, K., Feil, R., Maere, S., Lammens, W., Rolland, F., et al. (2012). Expansive evolution of the TREHALOSE-6-PHOSPHATE PHOSPHATASE gene family in Arabidopsis. PLANT PHYSIOLOGY, 160(2), 884–896.
Vancouver
1.
Vandesteene L, Lopez Galvis L, Vanneste K, Feil R, Maere S, Lammens W, et al. Expansive evolution of the TREHALOSE-6-PHOSPHATE PHOSPHATASE gene family in Arabidopsis. PLANT PHYSIOLOGY. 2012;160(2):884–96.
MLA
Vandesteene, Lies, Lorena Lopez Galvis, Kevin Vanneste, et al. “Expansive Evolution of the TREHALOSE-6-PHOSPHATE PHOSPHATASE Gene Family in Arabidopsis.” PLANT PHYSIOLOGY 160.2 (2012): 884–896. Print.
@article{3059149,
  abstract     = {Trehalose is a nonreducing sugar used as a reserve carbohydrate and stress protectant in a variety of organisms. While higher plants typically do not accumulate high levels of trehalose, they encode large families of putative trehalose biosynthesis genes. Trehalose biosynthesis in plants involves a two-step reaction in which trehalose-6-phosphate (T6P) is synthesized from UDPglucose and glucose-6-phosphate (catalyzed by T6P synthase [TPS]), and subsequently dephosphorylated to produce the disaccharide trehalose (catalyzed by T6P phosphatase [TPP]). In Arabidopsis (Arabidopsis thaliana), 11 genes encode proteins with both TPS- and TPP-like domains but only one of these (AtTPS1) appears to be an active (TPS) enzyme. In addition, plants contain a large family of smaller proteins with a conserved TPP domain. Here, we present an in-depth analysis of the 10 TPP genes and gene products in Arabidopsis (TPPA-TPPJ). Collinearity analysis revealed that all of these genes originate from whole-genome duplication events. Heterologous expression in yeast (Saccharomyces cerevisiae) showed that all encode active TPP enzymes with an essential role for some conserved residues in the catalytic domain. These results suggest that the TPP genes function in the regulation of T6P levels, with T6P emerging as a novel key regulator of growth and development in higher plants. Extensive gene expression analyses using a complete set of promoter-beta-glucuronidase/green fluorescent protein reporter lines further uncovered cell- and tissue-specific expression patterns, conferring spatiotemporal control of trehalose metabolism. Consistently, phenotypic characterization of knockdown and overexpression lines of a single TPP, AtTPPG, points to unique properties of individual TPPs in Arabidopsis, and underlines the intimate connection between trehalose metabolism and abscisic acid signaling.},
  author       = {Vandesteene, Lies and Lopez Galvis, Lorena and Vanneste, Kevin and Feil, Regina and Maere, Steven and Lammens, Willem and Rolland, Filip and Lunn, John E and Avonce, Nelson and Beeckman, Tom and Van Dijck, Patrick},
  issn         = {0032-0889},
  journal      = {PLANT PHYSIOLOGY},
  keyword      = {CRYSTAL-STRUCTURE,DROUGHT TOLERANCE,VEGETATIVE GROWTH,METABOLIC PATHWAYS,BIOLOGICAL IMPLICATIONS,TREHALOSE 6-PHOSPHATE,SACCHAROMYCES-CEREVISIAE,GENOME DUPLICATIONS,ESCHERICHIA-COLI,ABSCISIC-ACID},
  language     = {eng},
  number       = {2},
  pages        = {884--896},
  title        = {Expansive evolution of the TREHALOSE-6-PHOSPHATE PHOSPHATASE gene family in Arabidopsis},
  url          = {http://dx.doi.org/10.1104/pp.112.201400},
  volume       = {160},
  year         = {2012},
}

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