title: Expansive evolution of the trehalose-6-phosphate phosphatase gene family in Arabidopsis.
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 UDP-glucose 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-β-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.
authors.affiliation: Department of Molecular Microbiology, VIB, Leuven, Belgium.
authors.forename: Lies
authors.initials: L
authors.lastname: Vandesteene
authors.forename: Lorena
authors.initials: L
authors.lastname: López-Galvis
authors.forename: Kevin
authors.initials: K
authors.lastname: Vanneste
authors.forename: Regina
authors.initials: R
authors.lastname: Feil
authors.forename: Steven
authors.initials: S
authors.lastname: Maere
authors.forename: Willem
authors.initials: W
authors.lastname: Lammens
authors.forename: Filip
authors.initials: F
authors.lastname: Rolland
authors.forename: John E
authors.initials: JE
authors.lastname: Lunn
authors.forename: Nelson
authors.initials: N
authors.lastname: Avonce
authors.forename: Tom
authors.initials: T
authors.lastname: Beeckman
authors.forename: Patrick
authors.initials: P
authors.lastname: Van Dijck
mesh_terms: D000040:Abscisic Acid / Q000494:pharmacology; D017360:Arabidopsis / Q000187:drug effects / Q000201:enzymology / Q000235:genetics*; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism; D050260:Carbohydrate Metabolism; D020134:Catalytic Domain; D004789:Enzyme Activation; D019143:Evolution, Molecular; D020440:Gene Duplication; D015971:Gene Expression Regulation, Enzymologic; D018506:Gene Expression Regulation, Plant; D017343:Genes, Plant; D017930:Genes, Reporter; D005816:Genetic Complementation Test; D018525:Germination; D049452:Green Fluorescent Proteins / Q000378:metabolism; D005810:Multigene Family; D009154:Mutation; D010641:Phenotype; D010744:Phosphoric Monoester Hydrolases / Q000235:genetics / Q000378:metabolism*; D010802:Phylogeny; D011058:Pollen / Q000201:enzymology / Q000235:genetics; D011401:Promoter Regions, Genetic; D012441:Saccharomyces cerevisiae / Q000235:genetics / Q000378:metabolism; D012639:Seeds / Q000187:drug effects / Q000201:enzymology; D013403:Sugar Phosphates / Q000378:metabolism; D059467:Transcriptome; D014199:Trehalose / Q000031:analogs & derivatives / Q000378:metabolism
chemical_list: D029681:Arabidopsis Proteins; D013403:Sugar Phosphates; D049452:Green Fluorescent Proteins; C082722:trehalose-6-phosphate; D000040:Abscisic Acid; D014199:Trehalose; C023178:trehalose-phosphatase; D010744:Phosphoric Monoester Hydrolases