Redundant and non-redundant roles of the trehalose-6-phosphate phosphatases in leaf growth, root hair specification and energy-responses in Arabidopsis

Plant Signaling and Behavior

Volumn 8, Issue 3, 2013, Pages

  Houtte, Hilde Van ^a,b   López Galvis, Lorena ^a,b,c   Vandesteene, Lies ^a,b   Beeckman, Tom ^a,c   Van Dijck, Patrick ^a,b  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^b UNIVERSITY OF LEUVEN   (Belgium)

^c GHENT UNIVERSITY   (Belgium)

Author keywords

Cell division and atrichoblast; Leaf area; Multigene family; Sugar signaling; TPPA; TPPB; TPPG; Trehalose 6 phosphate phosphatase

Indexed keywords

ARABIDOPSIS PROTEIN; DRUG DERIVATIVE; PHOSPHATASE; SUCROSE; SUGAR PHOSPHATE; TREHALOSE; TREHALOSE 6 PHOSPHATE; TREHALOSE-6-PHOSPHATE; TREHALOSE-PHOSPHATASE; TREHALOSEPHOSPHATASE;

ARABIDOPSIS; ARTICLE; CELL DIVISION AND ATRICHOBLAST; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; LEAF AREA; LIGHT; METABOLISM; MULTIGENE FAMILY; MUTATION; PLANT EPIDERMIS; PLANT GENE; PLANT LEAF; PLANT ROOT; SUGAR SIGNALING; TPPA; TPPB; TPPG; TRANSGENIC PLANT; TREHALOSE-6-PHOSPHATE PHOSPHATASE;

CELL DIVISION AND ATRICHOBLAST; LEAF AREA; MULTIGENE FAMILY; SUGAR SIGNALING; TPPA; TPPB; TPPG; TREHALOSE-6-PHOSPHATE PHOSPHATASE;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; LIGHT; MUTATION; PHOSPHORIC MONOESTER HYDROLASES; PLANT EPIDERMIS; PLANT LEAVES; PLANT ROOTS; PLANTS, GENETICALLY MODIFIED; SUCROSE; SUGAR PHOSPHATES; TREHALOSE;

EID: 84874733292     PISSN: 15592316     EISSN: 15592324     Source Type: Journal    
DOI: 10.4161/psb.23209     Document Type: Article

References (37)

1. Elbein AD, Pan YT, Pastuszak I, Carroll D. New insights on trehalose: a multifunctional molecule. Glycobiology 2003; 13:17R-27R. PMID:12626396; http://dx.doi.org/10.1093/glycob/cwg047.
2. Cabib E, Leloir LF. The biosynthesis of trehalose phosphate. J Biol Chem 1958; 231:259-75. PMID:13538966.
3. Goddijn OJM, Verwoerd TC, Voogd E, Krutwagen RWHH, de Graaf PTHM, van Dun K, et al. Inhibition of trehalase activity enhances trehalose accumulation in transgenic plants. Plant Physiol 1997; 113:181-90. PMID:9008394; http://dx.doi.org/10.1104/pp.113.1.181.
4. Leyman B, Van Dijck P, Thevelein JM. An unexpected plethora of trehalose biosynthesis genes in Arabidopsis thaliana. Trends Plant Sci 2001; 6:510-3. PMID:11701378; http://dx.doi.org/10.1016/S1360-1385(01)02125-2.
5. Lunn JE, Feil R, Hendriks JHM, Gibon Y, Morcuende R, Osuna D, et al. Sugar-induced increases in trehalose 6-phosphate are correlated with redox activation of ADPglucose pyrophosphorylase and higher rates of starch synthesis in Arabidopsis thaliana. Biochem J 2006; 397:139-48. PMID:16551270; http://dx.doi.org/10.1042/BJ20060083.
6. Lunn JE. Gene families and evolution of trehalose metabolism in plants. Funct Plant Biol 2007; 34:550-63; http://dx.doi.org/10.1071/FP06315.
7. Blázquez MA, Santos E, Flores CL, Martínez-Zapater JM, Salinas J, Gancedo C. Isolation and molecular characterization of the Arabidopsis TPS1 gene, encoding trehalose-6-phosphate synthase. Plant J 1998; 13:685-9. PMID:9681010; http://dx.doi.org/10.1046/j.1365-313X.1998.00063.x.
8. Vandesteene L, Ramon M, Le Roy K, Van Dijck P, Rolland F. A single active trehalose-6-P synthase (TPS) and a family of putative regulatory TPS-like proteins in Arabidopsis. Mol Plant 2010; 3:406-19. PMID:20100798; http://dx.doi.org/10.1093/mp/ssp114.
9. Vogel G, Fiehn O, Jean-Richard-dit-Bressel L, Boller T, Wiemken A, Aeschbacher RA, et al. Trehalose metabolism in Arabidopsis: occurrence of trehalose and molecular cloning and characterization of trehalose-6-phosphate synthase homologues. J Exp Bot 2001; 52:1817-26. PMID:11520870; http://dx.doi.org/10.1093/jexbot/52.362.1817.
10. Harthill JE, Meek SE, Morrice N, Peggie MW, Borch J, Wong BH, et al. Phosphorylation and 14-3-3 binding of Arabidopsis trehalose-phosphate synthase 5 in response to 2-deoxyglucose. Plant J 2006; 47:211-23. PMID:16771775; http://dx.doi.org/10.1111/j.1365-313X.2006.02780.x.
11. Ramon M, De Smet I, Vandesteene L, Naudts M, Leyman B, Van Dijck P, et al. Extensive expression regulation and lack of heterologous enzymatic activity of the Class II trehalose metabolism proteins from Arabidopsis thaliana. Plant Cell Environ 2009; 32:1015-32. PMID:19344332; http://dx.doi.org/10.1111/j.1365-3040.2009.01985.x.
12. Thaller MC, Schippa S, Rossolini GM. Conserved sequence motifs among bacterial, eukaryotic, and archaeal phosphatases that define a new phosphohydrolase superfamily. Protein Sci 1998; 7:1647-52. PMID:9684901; http://dx.doi.org/10.1002/pro.5560070722.
13. Avonce N, Wuyts J, Verschooten K, Vandesteene L, Van Dijck P. The Cytophaga hutchinsonii ChTPSP: First characterized bifunctional TPS-TPP protein as putative ancestor of all eukaryotic trehalose biosynthesis proteins. Mol Biol Evol 2010; 27:359-69. PMID:19812028; http://dx.doi.org/10.1093/molbev/msp241.
14. Vandesteene L, López-Galvis L, Vanneste K, Feil R, Maere S, Lammens W, et al. Expansive evolution of the TREHALOSE-6-PHOSPHATE PHOSPHATASE gene family in Arabidopsis thaliana. [epub ahead of print]. Plant Physiol 2012; 160:884-96. PMID:22855938; http://dx.doi.org/10.1104/pp.112.201400.
15. Holmström KO, Mäntylä E, Welin B, Mandal A, Palva ET, Tunnela OE, et al. Drought tolerance in tobacco. Nature 1996; 379:683-4; http://dx.doi.org/10.1038/379683a0.
16. Eastmond PJ, van Dijken AJH, Spielman M, Kerr A, Tissier AF, Dickinson HG, et al. Trehalose-6-phosphate synthase 1, which catalyses the first step in trehalose synthesis, is essential for Arabidopsis embryo maturation. Plant J 2002; 29:225-35. PMID:11851922; http://dx.doi.org/10.1046/j.1365-313x.2002.01220.x.
17. Avonce N, Leyman B, Mascorro-Gallardo JO, Van Dijck P, Thevelein JM, Iturriaga G. The Arabidopsis trehalose-6-P synthase AtTPS1 gene is a regulator of glucose, abscisic acid, and stress signaling. Plant Physiol 2004; 136:3649-59. PMID:15516499; http://dx.doi.org/10.1104/pp.104.052084.
18. Satoh-Nagasawa N, Nagasawa N, Malcomber S, Sakai H, Jackson D. A trehalose metabolic enzyme controls inflorescence architecture in maize. Nature 2006; 441:227-30. PMID:16688177; http://dx.doi.org/10.1038/nature04725.
19. Paul MJ. Trehalose 6-phosphate: a signal of sucrose status. Biochem J 2008; 412:e1-2. PMID:18426388; http://dx.doi.org/10.1042/BJ20080598.
20. Schluepmann H, Berke L, Sanchez-Perez GF. Metabolism control over growth: a case for trehalose-6-phosphate in plants. J Exp Bot 2012; 63:3379-90. PMID:22058405; http://dx.doi.org/10.1093/jxb/err311.
21. Schluepmann H, van Dijken A, Aghdasi M, Wobbes B, Paul M, Smeekens S. Trehalose mediated growth inhibition of Arabidopsis seedlings is due to trehalose-6-phosphate accumulation. Plant Physiol 2004; 135:879-90. PMID:15181209; http://dx.doi.org/10.1104/pp.104.039503.
22. Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, Shinn P, et al. Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 2003; 301:653-7. PMID:12893945; http://dx.doi.org/10.1126/science.1086391.
23. Sessions A, Burke E, Presting G, Aux G, McElver J, Patton D, et al. A high-throughput Arabidopsis reverse genetics system. Plant Cell 2002; 14:2985-94. PMID:12468722; http://dx.doi.org/10.1105/tpc.004630.
24. Eloy NB, de Freitas Lima M, Van Damme D, Vanhaeren H, Gonzalez N, De Milde L, et al. The APC/C subunit 10 plays an essential role in cell proliferation during leaf development. Plant J 2011; 68:351-63. PMID:21711400; http://dx.doi.org/10.1111/j.1365-313X.2011.04691.x.
25. Donnelly PM, Bonetta D, Tsukaya H, Dengler RE, Dengler NG. Cell cycling and cell enlargement in developing leaves of Arabidopsis. Dev Biol 1999; 215:407-19. PMID:10545247; http://dx.doi.org/10.1006/dbio.1999.9443.
26. De Veylder L, Beeckman T, Beemster GT, de Almeida Engler J, Ormenese S, Maes S, et al. Control of proliferation, endoreduplication and differentiation by the Arabidopsis E2Fa-DPa transcription factor. EMBO J 2002; 21:1360-8. PMID:11889041; http://dx.doi.org/10.1093/emboj/21.6.1360.
27. Bergmann DC, Sack FD. Stomatal development. Annu Rev Plant Biol 2007; 58:163-81. PMID:17201685; http://dx.doi.org/10.1146/annurev.arplant.58.032806.104023.
28. Beemster GT, De Veylder L, Vercruysse S, West G, Rombaut D, Van Hummelen P, et al. Genome-wide analysis of gene expression profiles associated with cell cycle transitions in growing organs of Arabidopsis. Plant Physiol 2005; 138:734-43. PMID:15863702; http://dx.doi.org/10.1104/pp.104.053884.
29. Geelen D, Royackers K, Vanstraelen M, Inze D, Van Dijck P, Thevelein JM, et al. Trehalose-6-P synthase: AtTPS1 high molecular weight complexes in yeast and Arabidopsis. Plant Sci 2007; 173:426-37; http://dx.doi.org/10.1016/j.plantsci.2007.07.002.
30. Heazlewood JL, Tonti-Filippini J, Verboom RE, Millar AH. Combining experimental and predicted datasets for determination of the subcellular location of proteins in Arabidopsis. Plant Physiol 2005; 139:598-609. PMID:16219920; http://dx.doi.org/10.1104/pp.105.065532.
31. Heazlewood JL, Verboom RE, Tonti-Filippini J, Small I, Millar AH. SUBA: the Arabidopsis subcellular database. Nucleic Acids Res 2007; 35(Database issue):D213-8. PMID:17071959; http://dx.doi.org/10.1093/nar/gkl863.
32. Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W. GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol 2004; 136:2621-32. PMID:15375207; http://dx.doi.org/10.1104/pp.104.046367.
33. Gómez LD, Baud S, Gilday A, Li Y, Graham IA. 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 J 2006; 46:69-84. PMID:16553896; http://dx.doi.org/10.1111/j.1365-313X.2006.02662.x.
34. Riou-Khamlichi C, Menges M, Healy JM, Murray JA. Sugar control of the plant cell cycle: differential regulation of Arabidopsis D-type cyclin gene expression. Mol Cell Biol 2000; 20:4513-21. PMID:10848578; http://dx.doi.org/10.1128/MCB.20.13.4513-4521.2000.
35. Masucci JD, Rerie WG, Foreman DR, Zhang M, Galway ME, Marks MD, et al. The homeobox gene GLABRA2 is required for position-dependent cell differentiation in the root epidermis of Arabidopsis thaliana. Development 1996; 122:1253-60. PMID:8620852.
36. Rosso MG, Li Y, Strizhov N, Reiss B, Dekker K, Weisshaar B. An Arabidopsis thaliana T-DNA mutagenized population (GABI-Kat) for flanking sequence tag-based reverse genetics. Plant Mol Biol 2003; 53:247-59. PMID:14756321; http://dx.doi.org/10.1023/B:PLAN.0000009297.37235.4a.
37. Ryan E, Steer M, Dolan L. Cell biology and genetics of root hair formation in Arabidopsis thaliana. Protoplasma 2001; 215:140-9. PMID:11732053; http://dx.doi.org/10.1007/BF01280310.