Delayed embryo development in the ARABIDOPSIS TREHALOSE-6-PHOSPHATE SYNTHASE 1 mutant is associated with altered cell wall structure, decreased cell division and starch accumulation

Plant Journal

Volumn 46, Issue 1, 2006, Pages 69-84

  Gómez, Leonardo D ^a   Baud, Sébastien ^a   Gilday, Alison ^a   Li, Yi ^a   Graham, Ian A ^a  

^a UNIVERSITY OF YORK   (United Kingdom)

Author keywords

Arabidopsis; Embryo development; Microarray; Trehalose; Trehalose 6 phosphate synthase

Indexed keywords

GENES; METABOLISM; MORPHOLOGY; PROTEINS; STARCH;

ARABIDOPSIS; EMBRYO DEVELOPMENT; MICROARRAY; TREHALOSE; TREHALOSE-6-PHOSPHATE SYNTHASE;

PLANT CELL CULTURE;

ANATOMY; CELLS; GENES; MUTATION; PLANTS; PROTEINS; STARCH;

ARABIDOPSIS;

ARABIDOPSIS PROTEIN; CARBON; GLUCOSYLTRANSFERASE; PLANT RNA; STARCH; TREHALOSE 6 PHOSPHATE SYNTHETASE; TREHALOSE-6-PHOSPHATE SYNTHASE;

ARABIDOPSIS; ARTICLE; CARBOHYDRATE METABOLISM; CELL DIFFERENTIATION; CELL DIVISION; CELL WALL; CYTOLOGY; DOWN REGULATION; GENE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; LIPID METABOLISM; METABOLISM; MUTATION; PHYSIOLOGY; PLANT SEED; PRENATAL DEVELOPMENT; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CARBOHYDRATE METABOLISM; CARBON; CELL DIFFERENTIATION; CELL DIVISION; CELL WALL; DOWN-REGULATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GLUCOSYLTRANSFERASES; LIPID METABOLISM; MICROSCOPY, ELECTRON, TRANSMISSION; MUTATION; RNA, PLANT; SEEDS; STARCH;

EID: 33646852603     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2006.02662.x     Document Type: Article

References (38)

1. Avonce N. Leyman B. Mascorro-Gallardo J.O. Van Dijck P. Thevelein J.M. Iturriaga G. 2004 The Arabidopsis trehalose-6-P synthase AtTPS1 gene is a regulator of glucose, abscisic acid, and stress signaling. Plant Physiol. 136, 3649 3659.
2. Baud S. Boutin J.P. Miquel M. Lepiniec L. Rochat C. 2002 An integrated overview of seed development in Arabidopsis thaliana ecotype WS. Plant Physiol. Biochem. 40, 151 160.
3. Bhalerao R.P. Salchert K. Bako L. Okresz L. Szabados L. Muranaka T. Machida Y. Schell J. Koncz C. 1999 Regulatory interaction of PRL1 WD protein with Arabidopsis SNF1-like protein kinases. Proc. Natl Acad. Sci. USA 96, 5322 5327.
4. Chia T.Y. Pike M.J. Rawsthorne S. 2005 Storage oil breakdown during embryo development of Brassica napus (L.). J Exp. Bot. 56, 1285 1296.
5. Clausen M.H. Willats W.G.T. Knox J.P. 2003 Synthetic methyl hexagalacturonate hapten inhibitors of anti-homogalacturonan monoclonal antibodies LM7, JIM5 and JIM7. Carbohydrate Res. 338, 1797 1800.
6. Devic M. Albert S. Delseny M. 1996 Induction and expression of seed-specific promoters in Arabidopsis embryo-defective mutants. Plant J. 9, 205 215.
7. van Dijken A.J. Schluepmann H. Smeekens S.C. 2004 Arabidopsis trehalose-6-phosphate synthase 1 is essential for normal vegetative growth and transition to flowering. Plant Physiol. 135, 969 977.
8. Eastmond P.J. Graham I.A. 2001 Re-examining the role of the glyoxylate cycle in oilseeds. Trends Plant Sci. 6, 72 78.
9. Eastmond P.J. van Dijken A.J. Spielman M. Kerr A. Tissier A.F. Dickinson H.G. Jones J.D. Smeekens S.C. Graham I.A. 2002 Trehalose-6-phosphate synthase 1, which catalyses the first step in trehalose synthesis, is essential for Arabidopsis embryo maturation. Plant J. 29, 225 235.
10. Ferrando A. Koncz-Kalman Z. Farras R. Tiburcio A. Schell J. Koncz C. 2001 Detection of in vivo protein interactions between Snf1-related kinase subunits with intron-tagged epitope-labelling in plants cells. Nucleic Acids Res. 29, 3685 3693.
11. Goddijn O.J. van Dun K. 1999 Trehalose metabolism in plants. Trends Plant Sci. 4, 315 319.
12. Goddijn O. Smeekens S. 1998 Sensing trehalose biosynthesis in plants. Plant J. 14, 143 146.
13. Goddijn O.J. Verwoerd T.C. Voogd E. Krutwagen R.W. de Graaf P.T. van Dun K. Poels J. Ponstein A.S. Damm B. Pen J. 1997 Inhibition of trehalase activity enhances trehalose accumulation in transgenic plants. Plant Physiol. 113, 181 190.
14. Gomez L.D. Baud S. Graham I.A. 2005 The role of trehalose-6-phosphate synthase in Arabidopsis embryo development. Biochem. Soc. Trans. 33, 280 282.
15. Halford N.G. Paul M.J. 2003 Carbon metabolite sensing and signalling. Plant Biotech. J. 1, 381 398.
16. Hall L.N. Tucker G.A. Smith C.J.S. et al. 1993 Antisense inhibition of pectin esterase gene-expression in transgenic tomatoes. Plant J. 3, 121 129.
17. Harada J. 1997 Seed maturation and control of dormancy. In Cellular and Molecular Biology of Plant Seed Development Larkins B.A. Vasil I.K., eds Dordrecht: Kluwer Academic Publishers, pp. 545 592.
18. His I. Driouich A. Nicol F. Jauneau A. Hofte H. 2001 Altered pectin composition in primary cell walls of korrigan, a dwarf mutant of Arabidopsis deficient in a membrane-bound endo-1,4-beta-glucanase. Planta, 212, 348 358.
19. Inze D. 2005 Green light for the cell cycle. Embo J. 24, 657 662.
20. Kolbe A. Tiessen A. Schluepmann H. Paul M. Ulrich S. Geigenberger P. 2005 Trehalose 6-phosphate regulates starch synthesis via posttranslational redox activation of ADP-glucose pyrophosphorylase. Proc. Natl Acad. Sci. USA 102, 11118 11123.
21. Larson T.R. Graham I.A. 2001 Technical advance: a novel technique for the sensitive quantification of acyl CoA esters from plant tissues. Plant J. 25, 115 125.
22. Manfield I.W. Orfila C. McCartney L. Harholt J. Bernal A.J. Scheller H.V. Gilmartin P.M. Mikkelsen J.D. Knox P.J. Willats W.G. 2004 Novel cell wall architecture of isoxaben-habituated Arabidopsis suspension-cultured cells: global transcript profiling and cellular analysis. Plant J. 40, 260 275.
23. Mansfield S.G. Briarty L.G. 1993 Embryogenesis. In Arabidopsis, an Atlas of Morphology and Development Bowman J., ed. Berlin: Springer-Verlag, pp. 376 384.
24. Raz V. Bergervoet J.H. Koornneef M. 2001 Sequential steps for developmental arrest in Arabidopsis seeds. Development, 128, 243 252.
25. Riou-Khamlichi C. Menges M. Healy J.M.S. Murray J.A.H. 2000 Sugar control of the plant cell cycle: differential regulation of Arabidopsis D-type cyclin gene expression. Mol. Cell. Biol. 20, 4513 4521.
26. Romero C. Belles J.M. Vaya J.L. Serrano R. CulianezMacia F.A. 1997 Expression of the yeast trehalose-6-phosphate synthase gene in transgenic tobacco plants: pleiotropic phenotypes include drought tolerance. Planta, 201, 293 297.
27. Ruuska S.A. Girke T. Benning C. Ohlrogge J.B. 2002 Contrapuntal networks of gene expression during Arabidopsis seed filling. Plant Cell, 14, 1191 1206.
28. Scheible W.R. Pauly M. 2004 Glycosyltransferases and cell wall biosynthesis: novel players and insights. Curr. Opin. Plant Biol. 7, 285 295.
29. Schluepmann H. Pellny T. van Dijken A. Smeekens S. Paul M. 2003 Trehalose 6-phosphate is indispensable for carbohydrate utilization and growth in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA 100, 6849 6854.
30. Schluepmann H. van Dijken A. Aghdasi M. Wobbes B. Paul M. Smeekens S. 2004 Trehalose mediated growth inhibition of Arabidopsis seedlings is due to trehalose-6-phosphate accumulation. Plant Physiol. 135, 879 890.
31. Seifert G.J. 2004 Nucleotide sugar interconversions and cell wall biosynthesis: how to bring the inside to the outside. Curr. Opin. Plant Biol. 7, 277 284.
32. Smallwood M. Yates E.A. Willats W.G.T. Martin H. Knox J.P. 1996 Immunochemical comparison of membrane-associated and secreted arabinogalactan-proteins in rice and carrot. Planta, 198, 452 459.
33. Thevelein J.M. Hohmann S. 1995 Trehalose synthase - guard to the gate of glycolysis in yeast. Trends Biochem. Sci. 20, 3 10.
34. Thimm O. Blasing O. Gibon Y. Nagel A. Meyer S. Kruger P. Selbig J. Muller L.A. Rhee S.Y. Stitt M. 2004 MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J. 37, 914 939.
35. Tusher V.G. Tibshirani R. Chu G. 2001 Significance analysis of microarrays applied to the ionizing radiation response. Proc. Natl Acad. Sci. USA 98, 5116 5121.
36. Wiese A. Groner F. Sonnewald U. Deppner H. Lerchl J. Hebbeker U. Flugge U.I. Weber A. 1999 Spinach hexokinase I is located in the outer envelope membrane of plastids. FEBS Lett. 461, 13 18.
37. Wobus U. Weber H. 1999 Seed maturation: genetic programs and control signals. Curr. Opin. Plant Biol. 2, 33 38.
38. Yadegari R. Paiva G. Laux T. Koltunow A.M. Apuya N. Zimmerman J.L. Fischer R.L. Harada J.J. Goldberg R.B. 1994 Cell differentiation and morphogenesis are uncoupled in arabidopsis raspberry embryos. Plant Cell, 6, 1713 1729.