Diurnal changes in the transcriptome encoding enzymes of starch metabolism provide evidence for both transcriptional and posttranscriptional regulation of starch metabolism in arabidopsis leaves

Plant Physiology

Volumn 136, Issue 1, 2004, Pages 2687-2699

  Smith, Steven M ^a   Fulton, Daniel C ^a   Chia, Tansy ^b   Thorneycroft, David ^a   Chapple, Andrew ^b   Dunstan, Hannah ^a   Hylton, Christopher ^b   Zeeman, Samuel C ^c   Smith, Alison M ^b  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b JOHN INNES CENTRE   (United Kingdom)

^c UNIVERSITY OF BERN   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

BIOSYNTHESIS; DEGRADATION; METABOLISM; PLANTS (BOTANY); RNA; STARCH;

DIURNAL CYCLE; ENZYME ACTIVITY; POSTTRANSCRIPTIONAL REGULATION; STARCH METABOLISM;

ENZYMES;

BIOSYNTHESIS; DEGRADATION; ENZYMES; LEAVES; METABOLISM; NUCLEIC ACIDS; PLANTS; STARCH;

ARABIDOPSIS;

MESSENGER RNA; PLANT RNA; STARCH; STARCH SYNTHASE; STARCH SYNTHASE II; VEGETABLE PROTEIN;

ARABIDOPSIS; ARTICLE; CIRCADIAN RHYTHM; DNA MICROARRAY; ENZYMOLOGY; GENE; GENE EXPRESSION PROFILING; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; PLANT LEAF; RNA PROCESSING; VALIDATION STUDY;

ARABIDOPSIS; CIRCADIAN RHYTHM; GENE EXPRESSION PROFILING; GENES, PLANT; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PLANT LEAVES; PLANT PROTEINS; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, MESSENGER; RNA, PLANT; STARCH; STARCH SYNTHASE; TRANSCRIPTION, GENETIC;

EID: 14744275289     PISSN: 00320889     EISSN: None     Source Type: Journal    
DOI: 10.1104/pp.104.044347     Document Type: Article

References (53)

1. Ball SG, Morell MK (2003) From bacterial glycogen to starch: understanding the biogenesis of the plant starch granule. Annu Rev Plant Biol 54: 207-233
2. Boyes DC, Zayed AM, Ascenzi R, McCaskill AJ, Hoffman NE, Davis KR, Gorlach J (2001) Growth stage-based phenotypic analysis of Arabidopsis: a model for high throughput functional genomics in plants. Plant Cell 13: 1499-1510
3. Brenner S, Johnson M, Bridgham J, Golda G, Lloyd DH, Johnson D, Luo S, McCurdy S, Foy M, Ewan M, et al (2000) Gene expression analysis by massively parallel signature sequencing (MPSS) on microbead arrays. Nat Biotechnol 18: 630-634
4. Caspar T, Lin T-P, Monroe J, Bernhard W, Spilatro S, Preiss J, Somerville C (1989) Altered regulation of β-amylase activity in mutants of Arabidopsis with lesions in starch metabolism. Proc Natl Acad Sci USA 86: 5830-5833
5. Chandler JW, Apel K, Melzer S (2001) A novel putative β-amylase gene and ATB-Amy from Arabidopsis thaliana are circadian regulated. Plant Sci 161: 1019-1024
6. Chia T, Thorneycroft D, Chapple A, Messerli G, Chen J, Zeeman SC, Smith SM, Smith AM (2004) A cytosolic glucosyltransferase is required for conversion of starch to sucrose in Arabidopsis leaves at night. Plant J 37: 853-863
7. Crevillén P, Ballicora MA, Mérida A, Preiss J, Romero JM (2003) The different large subunit isoforms of Arabidopsis thaliana ADP-glucose pyrophosphorylase confer distinct kinetic and regulatory properties to the heterotetrameric enzyme. J Biol Chem 278: 28508-28515
8. Critchley JH, Zeeman SC, Takaha T, Smith AM, Smith SM (2001) A critical role for disproportionating enzyme in starch breakdown is revealed by a knock-out mutation in Arabidopsis. Plant J 26: 89-100
9. Denyer K, Sidebottom C, Hylton CM, Smith AM (1993) Soluble isoforms of starch synthase and starch-branching enzyme also occur within starch granules in developing pea embryos. Plant J 4: 191-198
10. Denyer K, Waite D, Motawia S, Lindberg Moller B, Smith AM (1999) Granule-bound starch synthase I in isolated starch granules elongates malto-oligosaccharides processively. Biochem J 340: 183-191
11. Edwards A, Borthakur A, Bornemann S, Venail J, Denyer K, Waite D, Fulton D, Smith AM, Martin C (1999) Specificity of starch synthase isoforms from potato. Eur J Biochem 266: 724-726
12. Fulton DC, Edwards A, Pilling E, Robinson HL, Fahy B, Seale R, Kato L, Donald AM, Geigenberger P, Martin C, et al (2002) Role of granule-bound starch synthase in determination of amylopectin structure and starch granule morphology in potato. J Biol Chem 277: 10834-10841
13. Guerineau F, Benjdia M, Zhou DX (2003) A jasmonate-responsive element within the A. thaliana vsp1 promoter. J Exp Bot 54: 1153-1162
14. Harmer SL, Hogenesch JB, Straume M, Chang H-S, Han B, Zhu T, Wang X, Kreps JA, Kay SA (2000) Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science 290: 2110-2113
15. Hayama R, Coupland G (2003) Shedding light on the circadian clock and the photoperiodic control of flowering. Curr Opin Plant Biol 6: 13-19
16. Hendriks JH, Kolbe A, Gibon Y, Stitt M, Geigenberger P (2003) ADP-glucose pyrophosphorylase is activated by posttranslational redox-modification in response to light and to sugars in leaves of Arabidopsis and other plant species. Plant Physiol 133: 838-849
17. Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database. Nucleic Acids Res 27: 297-300
18. Hussain H, Mant A, Seale R, Zeeman S, Hinchliffe E, Edwards A, Hylton C, Bornemann S, Smith AM, Martin C, et al (2003) Three isoforms of isoamylase contribute different catalytic properties for the debranching of potato glucans. Plant Cell 15: 133-149
19. Jobling S (2004) Improving starch for food and industrial applications. Curr Opin Plant Biol 7: 210-218
20. Jobling SA, Westcott RJ, Tayal A, Jeffcoat R, Schwall GP (2002) Production of a freeze-thaw-stable potato starch by antisense inhibition of three starch synthase genes. Nat Biotechnol 20: 295-299
21. Laby RJ, Kim D, Gibson SI (2001) The ram1 mutant of Arabidopsis exhibits severely decreased β-amylase activity. Plant Physiol 127: 1798-1807
22. Lin T-P, Caspar T, Somerville C, Preiss J (1988a) Isolation and characterisation of a starchless mutant of Arabidopsis thaliana (L.) Heynth lacking ADPglucose pyrophosphorylase activity. Plant Physiol 86: 1131-1135
23. Lin T-P, Caspar T, Somerville C, Preiss J (1988b) A starch deficient mutant of Arabidopsis thaliana with low ADPglucose pyrophosphorylase activity lacks one of the two subunits of the enzyme. Plant Physiol 88: 1175-1181
24. Liu XL, Covington MF, Fankhauser C, Chory J, Wagner DR (2001) ELF3 encodes a circadian clock-regulated nuclear protein that functions in an Arabidopsis PHYB signal transduction pathway. Plant Cell 13: 1293-1304
25. Lorberth R, Ritte G, Willmitzer L, Kossmann J (1998) Inhibition of a starch-granule-bound protein leads to modified starch and repression of cold sweetening. Nat Biotechnol 16: 473-177
26. Lu Y, Sharkey TD (2004) The role of amylomaltase in maltose metabolism in the cytosol of photosynthetic cells. Planta 218: 466-473
27. Menges M, Hennig L, Gruissem W, Murray JA (2003) Genome-wide gene expression in an Arabidopsis cell suspension. Plant Mol Biol 53: 423-442
28. Merida A, Rodriguez-Galan JM, Vincent C, Romero JM (1999) Expression of the granule-bound starch synthase I (Waxy) gene from snapdragon is developmentally and circadian clock regulated. Plant Physiol 120: 401-410
29. Millar AJ, Kay SA (1991) Circadian control of cab gene transcription and mRNA accumulation in Arabidopsis. Plant Cell 3: 541-550
30. Myers AM, Morell MK, James MG, Ball SG (2000) Recent progress toward understanding biosynthesis of the amylopectin crystal. Plant Physiol 122: 989-997
31. Neuhaus HE, Stitt M (1990) Control analysis of photosynthate partitioning - impact of reduced activity of ADP-glucose pyrophosphorylase or plastid phosphoglucomutase on the fluxes to starch and sucrose in Arabidopsis thaliana (L.) Heynh. Planta 182: 445-454
32. Niittylä T, Messerli G, Trevisan M, Chen J, Smith AM, Zeeman SC (2004) A previously unknown maltose transporter essential for starch degradation in leaves. Science 303: 87-89
33. Ritte G, Lloyd JR, Eckermann N, Rottmann A, Kossmann J, Steup M (2002) The starch-related R1 protein is an a-glucan, water dikinase. Proc Natl Acad Sci USA 99: 7166-7171
34. Rombauts S, Florquin K, Lescot M, Marchal K, Rouze P, van de Peer Y (2003) Computational approaches to identify promoters and cisregulatory elements in plant genomes. Plant Physiol 132: 1162-1176
35. Schaffer R, Landgraf J, Accerbi M, Simon V, Larson M, Wisman E (2001) Microarray analysis of diurnal and circadian-regulated genes in Arabidopsis. Plant Cell 13: 113-123
36. Schwall GP, Safford R, Westcott RJ, Jeffcoat R, Tayal A, Shi YC, Gidley MJ, Jobling SA (2000) Production of very-high-amylose potato starch by inhibition of SBE A and B. Nat Biotechnol 18: 551-554
37. Sehnke FC, Chung HJ, Wu K, Ferl RJ (2001) Regulation of starch accumulation by granule-associated plant 14-3-3 proteins. Proc Natl Acad Sci USA 98: 765-770
38. Smith AM, Zeeman SC, Thorneycroft D, Smith SM (2003) Starch mobilization in leaves. J Exp Bot 54: 577-583
39. Strayer C, Oyama T, Schultz TF, Raman R, Somers DE, Mas P, Panda S, Kreps JA, Kay SA (2000) Cloning of the Arabidopsis clock gene TOC1, an autoregulatory response regulator homolog. Science 289: 768-771
40. Tatge H, Marshall J, Martin C, Edwards EA, Smith AM (1999) Evidence that amylose synthesis occurs within the matrix of starch granules. Plant Cell Environ 22: 543-550
41. Terzaghi WB, Cashmore AR (1995) Light-regulated transcription. Annu Rev Plant Physiol Plant Mol Biol 46: 445-474
42. Tetlow IJ, Wait R, Lu Z, Akkasaeng R, Bowsher CG, Esposito S, Kosar-Hashemi B, Morell MK, Emes MJ (2004) Protein phosphorylation in amyloplasts regulates starch branching enzyme activity and protein-protein interactions. Plant Cell 16: 694-708
43. Wang Q, Monroe J, Sjolund RD (1995) Identification and characterisation of a phloem-specific β-amylase. Plant Physiol 109: 743-750
44. Wang SJ, Yeh KW, Tsai CY (1999) Molecular characterisation and expression of starch granule-bound starch synthase in the sink and source tissues of sweet potato. Physiol Plant 106: 253-261
45. Wang SM, Chu B, Lue WL, Yu TS, Eimert K, Chen J (1997) adg2-1 represents a missense mutation in the ADPG pyrophosphorylase large subunit gene of Arabidopsis thaliana. Plant J 11: 1121-1126
46. Wang SM, Lue WL, Yu TS, Long JH, Wang CN, Eimert K, Chen J (1998) Characterization of ADG1, an Arabidopsis locus encoding for ADPG pyrophosphorylase small subunit, demonstrates that the presence of the small subunit is required for large subunit stability. Plant J 13: 63-70
47. Wang ZY, Tobin EM (1998) Constitutive expression of the CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) gene disrupts circadian rhythms and suppresses its own expression. Cell 93: 1207-1217
48. Weise SE, Weber AP, Sharkey TD (2004) Maltose is the major form of carbon exported from the chloroplast at night. Planta 218: 474-182
49. Yu TS, Kofler H, Hausler RE, Hille D, Flugge UI, Zeeman SC, Smith AM, Kossmann J, Lloyd J, Ritte G, et al (2001) The Arabidopsis sex1 mutant is defective in the R1 protein, a general regulator of starch degradation in plants, and not in the chloroplast hexose transporter. Plant Cell 13: 1907-1918
50. Zeeman SC, Umemoto T, Lue WL, Au-Yeung P, Martin C, Smith AM, Chen J (1998) A mutant of Arabidopsis lacking a chloroplastic isoamylase accumulates both starch and phytoglycogen. Plant Cell 10: 1699-1712
51. Zeeman SC, Tiessen A, Pilling E, Kato KL, Donald AM, Smith AM (2002) Starch synthesis in Arabidopsis. Granule synthesis, composition, and structure. Plant Physiol 129: 516-529
52. Zeeman SC, Thorneycroft D, Schupp N, Chapple A, Weck M, Dunstan H, Haldimann P, Bechtold N, Smith AM, Smith SM (2004a) Chloroplastic starch phosphorylase is not required for transitory starch degradation in Arabidopsis leaves but has a role in the tolerance of abiotic stress. Plant Physiol 135: 849-858
53. Zeeman SC, Smith SM, Smith AM (2004b) The breakdown of starch in leaves. New Phytol 163: 247-261