RNA interference of Arabidopsis beta-amylase8 prevents maltose accumulation upon cold shock and increases sensitivity of PSII photochemical efficiency to freezing stress

Plant Journal

Volumn 44, Issue 5, 2005, Pages 730-743

  Kaplan, Fatma ^a   Guy, Charles L ^a  

^a UNIVERSITY OF FLORIDA   (United States)

Author keywords

Biochemistry; Environmental stress; Metabolism; Starch; Temperature stress

Indexed keywords

BIOCHEMISTRY; CHLOROPHYLL; FREEZING; MALTOSE; METABOLISM; PROTEINS; RNA;

COLD SHOCK; ENVIRONMENTAL STRESS; FREEZING STRESS; TEMPERATURE STRESS;

ENZYME KINETICS;

BIOCHEMISTRY; CHLOROPHYLLS; ENZYMES; MALTOSE; METABOLISM; NUCLEIC ACIDS; PROTEINS;

ARABIDOPSIS;

BETA AMYLASE; BETA AMYLASE8, ARABIDOPSIS; BETA-AMYLASE8, ARABIDOPSIS; MALTOSE;

ARABIDOPSIS; ARTICLE; CHEMISTRY; COLD; ENZYMOLOGY; FREEZING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHENOTYPE; PHOTOSYNTHESIS; PHOTOSYSTEM II; RNA INTERFERENCE;

ARABIDOPSIS; BETA-AMYLASE; COLD; FREEZING; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, PLANT; MALTOSE; MUTAGENESIS, INSERTIONAL; PHENOTYPE; PHOTOSYNTHESIS; PHOTOSYSTEM II PROTEIN COMPLEX; RNA INTERFERENCE;

EID: 33644838804     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2005.02565.x     Document Type: Article

References (41)

1. Alonso J.M. Stepanova A.N. Leisse T.J. et al. (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science, 301, 653 657.
2. Beck E. Ziegler P. (1989) Biosynthesis and degradation of starch in higher plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 40, 95 117.
3. Chia T. Thorneycroft D. Chapple A. Messerli G. Chen J. Zeeman S.C. Smith S.M. Smith A.M. (2004) A cytosolic glucosyltransferase is required for conversion of starch to sucrose in Arabidopsis leaves at night. Plant J. 37, 853 863.
4. Clough S.J. Bent A.F. (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735 743.
5. Datta R. Selvi M.T. Seetharama N. Sharma R. (1999) Stress-mediated enhancement of beta-amylase activity in pearl millet and maize leaves is dependent on light. J. Plant Physiol. 154, 657 664.
6. Dreier W. Schnarrenberger C. Borner T. (1995) Light- and stress-dependent enhancement of amylolytic activities in white and green barley leaves: beta-amylases are stress-induced proteins. J. Plant Physiol. 145, 342 348.
7. Farrâe E.M. Tiessen A. Roessner U. Geigenberger P. Trethewey R.N. Willmitzer L. (2001) Analysis of the compartmentation of glycolytic intermediates, nucleotides, sugars, organic acids, amino acids, and sugar alcohols in potato tubers using a nonaqueous fractionation method. Plant Physiol. 127, 685 700.
8. Fiehn O. Kopka J. Dèormann P. Altmann T. Trethewey R.N. Willmitzer L. (2000) Metabolite profiling for plant functional genomics. Nat. Biotechnol. 18, 1157 1161.
9. Fowler S. Thomashow M.F. (2002) Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway. Plant Cell, 14, 1675 1690.
10. Gerhardt R. Heldt H.W. (1984) Measurement of subcellular metabolite levels in leaves by fractionation of freeze-stopped material in nonaqueous media. Plant Physiol. 75, 542 547.
11. Harmer S.L. Hogenesch J.B. Straume M. Chang H.S. Han B. Zhu T. Wang X. Kreps J.A. Kay S.A. (2000) Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science, 290, 2110 2113.
12. Jung S.H. Lee J.Y. Lee D.H. (2003) Use of SAGE technology to reveal changes in gene expression in Arabidopsis leaves undergoing cold stress. Plant Mol. Biol. 52, 553 567.
13. Kaplan F. Guy C.L. (2004) β-Amylase induction and the protective role of maltose during temperature shock. Plant Physiol. 135, 1674 1684.
14. Kaplan F. Kopka J. Haskell D.W. Zhao W. Schiller K.C. Gatzke N. Sung D.Y. Guy C.L. (2004) Exploring the temperature-stress metabolome of Arabidopsis. Plant Physiol. 136, 4159 4168.
15. Kreps J.A. Wu Y. Chang H.S. Zhu T. Wang X. Harper J.F. (2002) Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiol. 130, 2129 2141.
16. Laby R.J. Kim D. Gibson S.I. (2001) The ram1 mutant of Arabidopsis exhibits severely decreased beta-amylase activity. Plant Physiol. 127, 1798 1807.
17. Levitt J. (1972) Responses of Plants to Environmental Stresses. New York: Academic Press.
18. Li P.H. Weiser C.J. Van Huystee R. (1965) Changes in metabolites of red-osier dogwood during cold acclimation. J. Amer. Soc. Hort. Sci. 86, 723 730.
19. Lu Y. Sharkey T.D. (2004) The role of amylomaltase in maltose metabolism in the cytosol of photosynthetic cells. Planta, 218, 466 473.
20. 3 or CAM (crassulacean acid metabolism)-induced Mesembryanthemum crystallinum L. Biochem. J. 318, 945 953.
21. Nielsen T.M. Deiting U. Stitt M. (1997) A beta-amylase in potato tubers is induced by storage at low temperature. Plant Physiol. 113, 503 510.
22. Niittylèa T. Messerli G. Trevisan M. Chen J. Smith A.M. Zeeman S.C. (2004) A previously unknown maltose transporter essential for starch degradation in leaves. Science, 303, 87 89.
23. Ritte G. Lloyd J.R. Eckermann N. Rottmann A. Kossmann J. Steup M. (2002) The starch-related R1 protein is an alpha-glucan, water dikinase. Proc. Natl Acad. Sci. USA, 99, 7166 7171.
24. Roessner U. Wagner C. Kopka J. Trethewey R.N. Willmitzer L. (2000) Technical advance: simultaneous analysis of metabolites in potato tuber by gas chromatography-mass spectrometry. Plant J. 23, 131 142.
25. Scheidig A. Frèohlich A. Schulze S. Lloyd J.R. Kossmann J. (2002) Downregulation of a chloroplast-targeted beta-amylase leads to a starch-excess phenotype in leaves. Plant J. 30, 581 591.
26. Seki M. Narusaka M. Abe H. Kasuga M. Yamaguchi-Shinozaki K. Carninci P. Hayashizaki Y. Shinozaki K. (2001) Monitoring the expression pattern of 1300 Arabidopsis genes under drought and cold stresses by using a full-length cDNA microarray. Plant Cell, 13, 61 72.
27. Seki M. Narusaka M. Ishida J. et al. (2002) Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J. 31, 279 292.
28. Servaites J.C. Geiger D.R. (2002) Kinetic characteristics of chloroplast glucose transport. J. Exp. Bot. 53, 1581 1591.
29. 2: a relationship between starch degradation and sugar sensing. Plant Biol. (Stuttg.) 6, 280 288.
30. Smith A.M. Zeeman S.C. Smith S.M. (2004a) Starch degradation. Annu. Rev. Plant Biol. 56, 73 98
31. Smith A.M. (2004b) 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 Physiol. 136, 2687 2699.
32. Sung D.Y. (2001) Characterization of Arabidopsis heat shock protein 70 (Hsp70) gene family and microarray analysis of gene expression in response to temperature extremes. PhD Thesis. University of Florida, FL, USA.
33. Sung D.Y. Guy C.L. (2003) Physiological and molecular assessment of altered expression of Hsc70-1 in Arabidopsis. Evidence for pleiotropic consequences. Plant Physiol. 132, 979 987.
34. Wagner C. Sefkow M. Kopka J. (2003) Construction and application of a mass spectral and retention time index database generated from plant GC/EI-TOF-MS metabolite profiles. Phytochemistry, 62, 887 900.
35. Weise S.E. Weber A.P. Sharkey T.D. (2004) Maltose is the major form of carbon exported from the chloroplast at night. Planta, 218, 474 482.
36. Weise S.E. Kim K.S. Stewart R.P. Sharkey T.D. (2005) β-Maltose is the metabolically active anomer of maltose during transitory starch degradation. Plant Physiol. 137, 756 761.
37. Wesley S.V. Helliwell C.A. Smith N.A. et al. (2001) Construct design for efficient, effective and high-throughput gene silencing in plants. Plant J. 27, 581 590.
38. Yano R. Nakamura M. Yoneyama T. Nishida I. (2005) Starch-related α-glucan/water dikinase is involved in the cold-induced development of freezing tolerance in Arabidopsis. Plant Physiol. 138, 837 846.
39. Yu T.S. Zeeman S.C. Thorneycroft D. et al. (2005) α-Amylase is not required for breakdown of transitory starch in Arabidopsis leaves. J. Biol. Chem. 280, 9773 9779.
40. Zeeman S.C. Tiessen A. Pilling E. Kato K.L. Donald A.M. Smith A.M. (2002) Starch synthesis in Arabidopsis. Granule synthesis, composition, and structure. Plant Physiol. 129, 516 529.
41. Zeeman S.C. Thorneycroft D. Schupp N. Chapple A. Weck M. Dunstan H. Haldimann P. Bechtold N. Smith A.M. Smith S.M. (2004) Plastidial α-glucan phosphorylase is not required for starch degradation in Arabidopsis leaves but has a role in the tolerance of abiotic stress. Plant Physiol. 135, 849 858.