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

Lies Vandesteene, Lorena Lopez Galvis UGent, Kevin Vanneste UGent, Regina Feil, Steven Maere UGent, Willem Lammens, Filip Rolland, John E Lunn, Nelson Avonce and Tom Beeckman UGent, et al. (2012) PLANT PHYSIOLOGY. 160(2). p.884-896
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.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
CRYSTAL-STRUCTURE, DROUGHT TOLERANCE, VEGETATIVE GROWTH, METABOLIC PATHWAYS, BIOLOGICAL IMPLICATIONS, TREHALOSE 6-PHOSPHATE, SACCHAROMYCES-CEREVISIAE, GENOME DUPLICATIONS, ESCHERICHIA-COLI, ABSCISIC-ACID
journal title
PLANT PHYSIOLOGY
Plant Physiol.
volume
160
issue
2
pages
884 - 896
Web of Science type
Article
Web of Science id
000309523800024
JCR category
PLANT SCIENCES
JCR impact factor
6.555 (2012)
JCR rank
8/193 (2012)
JCR quartile
1 (2012)
ISSN
0032-0889
DOI
10.1104/pp.112.201400
language
English
UGent publication?
yes
classification
A1
copyright statement
I have transferred the copyright for this publication to the publisher
id
3059149
handle
http://hdl.handle.net/1854/LU-3059149
date created
2012-11-23 14:02:00
date last changed
2012-12-17 13:29:47
@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},
}

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.