Abstract
As a first step toward the exploitation of the disaccharide trehalose as a stress-protective and preservative agent in plants, we engineered trehalose biosynthesis in tobacco (Nicotiana tabacum) and potato (Solanum tuberosum) by introducing the otsA and otsB genes from Escherichia coli, which encode trehalose-6-phosphate synthase and trehalose-6-phosphate phosphatase, respectively. In leaves of transgenic tobacco plants, very low levels of trehalose accumulation were obtained (0.11 mg g-1 fresh weight), whereas in transgenic potato tubers, no trehalose accumulated at all. Plant trehalase activity was shown to affect the accumulation of trehalose in these plants. An increase in trehalose accumulation, up to 0.41 and 4.04 mg g-1 fresh weight in tobacco leaves and potato micro-tubers, respectively, was noted when the potent trehalase inhibitor validamycin A was added to in vitro plants and to hydroponically grown greenhouse plants. Stunted growth and the formation of lancet-shaped leaves by trehalose-accumulating tobacco plants suggest a negative effect of trehalose biosynthesis on N. tabacum development. It is surprising that experiments with wild-type plants cultured in the presence of validamycin A indicate that, despite current belief, the capacity to synthesize trehalose may not be restricted to primitive phyla of vascular plants and certain "resurrection plants," but may exist throughout the angiosperms.
MeSH Terms
Cloning, Molecular
Escherichia coli/genetics
Glucosyltransferases/genetics
Inositol/analogs & derivatives,pharmacology
Phosphoric Monoester Hydrolases/genetics
Plants, Genetically Modified/enzymology,genetics,metabolism
Plants, Toxic
Solanum tuberosum/genetics
Tobacco/genetics
Trehalase/antagonists & inhibitors
Trehalose/metabolism
Chemicals
validamycin A
Inositol
Trehalose
Glucosyltransferases
trehalose-6-phosphate synthase
trehalose-phosphatase
Phosphoric Monoester Hydrolases
Trehalase
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Verwoerd T C
Voogd E
Krutwagen R W
de Graaf P T
van Dun K
Poels J
Ponstein A S
Damm B
Pen J
References (24)
24 references, click to expand
-
Functional analysis of the 3' control region of the potato wound-inducible proteinase inhibitor II gene.
Plant Cell. 1989 Jan;1(1):115-22
PMID: 2535459
-
Stabilization of dry phospholipid bilayers and proteins by sugars.
Biochem J. 1987 Feb 15;242(1):1-10
PMID: 2954537
-
METHOD FOR ASSAY OF INTESTINAL DISACCHARIDASES.
Anal Biochem. 1964 Jan;7:18-25
PMID: 14106916
-
The metabolism of alpha,alpha-trehalose.
Adv Carbohydr Chem Biochem. 1974;30:227-56
PMID: 4377836
-
A mutant neomycin phosphotransferase II gene reduces the resistance of transformants to antibiotic selection pressure.
Proc Natl Acad Sci U S A. 1990 May;87(9):3435-9
PMID: 2159150
-
The structure and transcription start site of a major potato tuber protein gene.
Nucleic Acids Res. 1986 Jun 11;14(11):4625-38
PMID: 3714488
-
Role of the trehalose carrier in dehydration resistance of Saccharomyces cerevisiae.
Biochim Biophys Acta. 1993 Mar 21;1156(3):263-6
PMID: 8461315
-
Stomachic principles in ginger. III. An anti-ulcer principle, 6-gingesulfonic acid, and three monoacyldigalactosylglycerols, gingerglycolipids A, B, and C, from Zingiberis Rhizoma originating in Taiwan.
Chem Pharm Bull (Tokyo). 1994 Jun;42(6):1226-30
PMID: 8069973
-
Analysis of the otsBA operon for osmoregulatory trehalose synthesis in Escherichia coli and homology of the OtsA and OtsB proteins to the yeast trehalose-6-phosphate synthase/phosphatase complex.
Gene. 1994 Jul 22;145(1):9-15
PMID: 8045430
-
Accumulation of fructose polymers in transgenic tobacco.
Biotechnology (N Y). 1994 Mar;12(3):272-5
PMID: 7764488
-
Trehalose Toxicity in Cuscuta reflexa: CORRELATION WITH LOW TREHALASE ACTIVITY.
Plant Physiol. 1981 Dec;68(6):1369-74
PMID: 16662110
-
Extraordinary stability of enzymes dried in trehalose: simplified molecular biology.
Biotechnology (N Y). 1992 Sep;10(9):1007-11
PMID: 1369408
-
Biochemical and genetic characterization of osmoregulatory trehalose synthesis in Escherichia coli.
J Bacteriol. 1988 Jun;170(6):2841-9
PMID: 3131312
-
The physical map of the whole E. coli chromosome: application of a new strategy for rapid analysis and sorting of a large genomic library.
Cell. 1987 Jul 31;50(3):495-508
PMID: 3038334
-
Production of correctly processed human serum albumin in transgenic plants.
Biotechnology (N Y). 1990 Mar;8(3):217-21
PMID: 1366404
-
Trehalose-6-phosphate, a new regulator of yeast glycolysis that inhibits hexokinases.
FEBS Lett. 1993 Aug 23;329(1-2):51-4
PMID: 8354408
-
Trehalose metabolism in Escherichia coli: stress protection and stress regulation of gene expression.
Mol Microbiol. 1993 Apr;8(2):205-10
PMID: 8391102
-
Complete nucleotide sequence of alfalfa mosaic virus RNA 4.
Nucleic Acids Res. 1980 May 24;8(10):2213-23
PMID: 7433090
-
Trehalose-6-phosphate synthase/phosphatase complex from bakers' yeast: purification of a proteolytically activated form.
J Gen Microbiol. 1991 Feb;137(2):323-30
PMID: 1849964
-
A simple and general method for transferring genes into plants.
Science. 1985 Mar 8;227(4691):1229-31
PMID: 17757866
-
Molecular cloning and physical mapping of the otsBA genes, which encode the osmoregulatory trehalose pathway of Escherichia coli: evidence that transcription is activated by katF (AppR)
J Bacteriol. 1992 Feb;174(3):889-98
PMID: 1310094
-
A small-scale procedure for the rapid isolation of plant RNAs.
Nucleic Acids Res. 1989 Mar 25;17(6):2362
PMID: 2468132
-
Validoxylamines as trehalase inhibitors.
J Antibiot (Tokyo). 1987 Apr;40(4):563-5
PMID: 3294776
-
Effect of validamycins on glycohydrolases of Rhizoctonia solani.
J Antibiot (Tokyo). 1987 Apr;40(4):526-32
PMID: 3583921