Repression of both isoforms of disproportionating enzyme leads to higher malto-oligosaccharide content and reduced growth in potato

Planta

Volumn 232, Issue 5, 2010, Pages 1127-1139

  Lütken, Henrik ^a,b   Lloyd, James R ^b,c   Glaring, Mikkel A ^a   Baunsgaard, Lone ^a   Laursen, Kristian Holst ^a   Haldrup, Anna ^a   Kossmann, Jens ^b,c   Blennow, Andreas ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^c STELLENBOSCH UNIVERSITY   (South Africa)

Author keywords

Disproportionating enzyme 1; Disproportionating enzyme 2; Malto oligosaccharides; Photosystem; Potato; Starch

Indexed keywords

4 ALPHA GLUCANOTRANSFERASE; 4 ALPHA-GLUCANOTRANSFERASE; CHLOROPHYLL; GLYCOGEN DEBRANCHING ENZYME; ISOENZYME; MALTOOLIGOSACCHARIDES; OLIGOSACCHARIDE; VEGETABLE PROTEIN;

ARABIDOPSIS; ARTICLE; ENZYMOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNOBLOTTING; METABOLISM; POTATO; TOBACCO;

ARABIDOPSIS; CHLOROPHYLL; GLYCOGEN DEBRANCHING ENZYME SYSTEM; IMMUNOBLOTTING; ISOENZYMES; OLIGOSACCHARIDES; PLANT PROTEINS; SOLANUM TUBEROSUM; TOBACCO;

ARABIDOPSIS; ARABIDOPSIS THALIANA; NICOTIANA TABACUM; SOLANUM TUBEROSUM;

EID: 77956713405     PISSN: 00320935     EISSN: 14322048     Source Type: Journal    
DOI: 10.1007/s00425-010-1245-3     Document Type: Article

References (51)

1. Baunsgaard L, Lütken H, Mikkelsen R, Glaring MA, Pharm TT, Blennow A (2005) A novel isoform of glucan, water dikinase phosphorylates pre-phosporylated α-glucans and is involved in starch degradation. Plant J 41: 595-605.
2. Blennow A, Bay-Smidt AM, Wischmann B, Olsen CE, Møller BL (1998) The degree of starch phosphorylation is related to the chain length distribution of the neutral and the phosphorylated chains of amylopectin. Carbohydr Res 307: 45-54.
3. Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
4. 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.
5. Christiansen C, Hachem MA, Janeček Š, Viksø-Nielsen A, Blennow A, Svensson B (2009) The carbohydrate-binding module family 20-diversity, structure, and function. FEBS J 276: 5006-5029.
6. 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.
7. Delatte T, Umhang M, Trevisan M, Eicke S, Thorneycroft D, Smith SM, Zeeman SC (2006) Evidence for distinct mechanisms of starch granule breakdown in plants. J Biol Chem 281: 12050-12059.
8. Fettke J, Poeste S, Eckermann N, Tiessen A, Pauly M, Geigenberger P, Steup M (2005) Analysis of cytosolic heteroglycans from leaves of transgenic potato (Solanum tuberosum L.) plants that under- or overexpress the Pho 2 phosphorylase isozyme. Plant Cell Physiol 46: 1987-2004.
9. Fettke J, Chia T, Eckermann N, Smith A, Steup M (2006) A transglucosidase necessary for starch degradation and maltose metabolism in leaves at night acts on cytosolic heteroglycans (SHG). Plant J 46: 668-684.
10. Fettke J, Hejazi M, Smirnova J, Höchel E, Stage M, Steup M (2009) Eukaryotic starch degradation: integration of plastidial and cytosolic pathways. J Exp Bot 60: 2907-2922.
11. Fulton DC, Stettler M, Mettler T, Vaughan CK, Li J, Francisco P, Gil M, Reinhold H, Eicke S, Messerli G, Dorken G, Halliday K, Smith AM, Smith SM, Zeeman SC (2008) β-AMYLASE4, a noncatalytic protein required for starch breakdown, acts upstream of three active β-amylases in Arabidopsis chloroplasts. Plant Cell 20: 1040-1058.
12. Glaring MA, Zygadlo A, Thorneycroft D, Schulz A, Smith SA, Blennow A, Baunsgaard Lone (2007) An extra-plastidial α-glucan, water dikinase from Arabidopsis phosphorylates amylopectin in vitro and is not necessary for transient starch degradation. J Exp Bot 58: 3949-3960.
13. Haldrup A, Naver H, Scheller HV (1999) The interaction between plastocyanin and photosystem I is inefficient in transgenic Arabidopsis plants lacking the PSI-N subunit of photosystem I. Plant J 17: 689-698.
14. Haldrup A, Simpson DJ, Scheller HV (2000) Down-regulation of the PSI-F subunit of photosystem I (PSI) in Arabidopsis thaliana. The PSI-F subunit is essential for photoautotrophic growth and contributes to antenna function. J Biol Chem 275: 31211-31218.
15. Kaplan F, Guy CL (2005) RNA interference of Arabidopsis beta-amylase8 prevents maltose accumulation upon cold shock and increases sensitivity of PSII photochemical efficiency to freezing stress. Plant J 44: 730-743.
16. Kötting O, Pusch K, Tiessen A, Geigenberger P, Steup M, Ritte G (2005) Identification of a novel enzyme required for starch metabolism in Arabidopsis leaves. The phosphoglucan, water dikinase. Plant Physiol 137: 242-252.
17. Kötting O, Kossmann J, Zeeman SC, Lloyd JR (2010) Regulation of starch metabolism: the age of enlightenment? Curr Opin Plant Biol. doi: 10. 1016/j. pbi. 2010. 01. 003.
18. Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148: 350-382.
19. Lloyd JR, Blennow A, Burhenne K, Kossmann J (2004) Repression of a novel isoform of disproportionating enzyme (stDPE2) in potato leads to inhibition of starch degradation in leaves but not tubers stored at low temperature. Plant Physiol 134: 1347-1354.
20. Lloyd JR, Kossmann J, Ritte G (2005) Leaf starch degradation comes out of the shadows. Trends Plant Sci 10: 130-137.
21. 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: 473-477.
22. Lu Y, Sharkey TD (2004) The role of amylomaltase in maltose metabolism in the cytosol of photosynthetic cells. Planta 218: 466-473.
23. Monte E, Ludevid D, Prat S (1999) Leaf C40. 4: a carotenoid-associated protein involved in the modulation of photosynthetic efficiency? Plant J 19: 399-410.
24. Müller-Röber B, Kossmann J, Hannah LC, Willmitzer L, Sonnewald U (1990) One of two different ADP-glucose pyrophosphorylase genes from potato responds strongly to elevated levels of sucrose. Mol Gen Genet 224: 136-146.
25. Müller-Röber B, Sonnewald U, Willmitzer L (1992) Inhibition of the ADP-glucose pyrophosphorylase in transgenic potatoes leads to sugar-storing tubers and influences tuber formation and expression of tuber storage proteins. EMBO J 11: 1229-1238.
26. Nielsen TH, Skjærbæk HC, Karlsen P (1991) Carbohydrate metabolism during fruit development in sweet pepper (Capsicum annuum) plants. Physiol Plant 82: 311-319.
27. Nielsen TH, Deiting U, Stitt M (1997) A β-amylase in potato tubers is induced by storage at low temperature. Plant Physiol 113: 503-510.
28. Niittylä T, Messerli G, Trevisan M, Chen J, Smith AM, Zeeman S (2004) A previously unknown maltose transporter essential for starch degradation in leaves. Science 303: 87-89.
29. Nour-Eldin HH, Hansen BG, Nørholm MHH, Jensen JK, Halkier BA (2006) Advancing uracil-excision based cloning towards an ideal technique for cloning PCR fragments. Nucleic Acids Res 34: e122.
30. Quick WP, Stitt M (1989) An examination of factors contributing to non-photochemical quenching of chlorophyll in barley leaves. Biochim Biophys Acta 977: 287-296.
31. Scheidig A, Fröhlich A, Schulze S, Lloyd JR, Kossmann J (2002) Downregulation of a chloroplast-targeted β-amylase leads to a starch excess phenotype in leaves. Plant J 30: 581-591.
32. Schneider A, Hausler RE, Kolukisaoglu U, Kunze R, van der Graaf E, Schwacke R, Catoni E, Desimone M, Flügge U-I (2002) An Arabidopsisthaliana knock-out mutant of the triose phosphate/phosphate translocator is severely compromised only when starch synthesis, but not starch mobilisation is abolished. Plant J 32: 685-699.
33. Smith AM, Zeeman SC, Smith SM (2005) Starch degradation. Annu Rev Plant Biol 56: 73-98.
34. Soitamo AJ, Zhou G, Clarke AK, Oquist G, Aro EM, Gustafsson P (1994) Over-production of the D1 protein of photosystem II reaction centre in the cyanobacterium Synechococcus sp. PCC 7942. Plant Mol Biol 26: 709-721.
35. Steichen JM, Petty RV, Sharkey TD (2008) Domain characterization of a 4-α-glucanotransferase essential for maltose metabolism in photosynthetic leaves. J Biol Chem 283: 20797-20804.
36. Stensballe A, Hald S, Bauw G, Blennow A, Welinder KG (2008) The amyloplast proteome of potato tuber. FEBS J 275: 1723-1741.
37. Stettler M, Eicke S, Mettler T, Messerli G, Hörtensteiner S, Zeeman SC (2009) Blocking the metabolism of starch breakdown products in Arabidopsis leaves triggers chloroplast degradation. Mol Plant 2: 1233-1246.
38. Steup M (1990) Starch degrading enzymes. In: Lea PJ (ed) Methods in plant biochemistry, vol 3. Academic Press, London, pp 103-128.
39. Takaha T, Yanase M, Okada S, Smith SM (1993) Disproportionating enzyme (4-α-glucanotransferase, EC 2. 4. 1. 25) of potato. Purification, molecular cloning, and potential role in starch metabolism. J Biol Chem 268: 1391-1396.
40. Takaha T, Critchley J, Okada S, Smith SM (1998) Normal starch content and composition in tubers of antisense potato plants lacking D-enzyme (4-α-glucanotransferase). Planta 205: 445-451.
41. Voinnet O, Rivas S, Mestre P, Baulcombe D (2003) An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J 33: 949-956.
42. von Schaewen A, Stitt M, Schmidt R, Sonnewald U, Willmitzer L (1990) Expression of a yeast-derived invertase in the cell wall of tobacco and Arabidopsis plants leads to accumulation of carbohydrate and inhibition of photosynthesis and strongly influences growth and phenotype of transgenic tobacco plants. EMBO J 9: 3033-3044.
43. Weise SE, Schrader SM, Kleinbeck KR, Sharkey TD (2006) Carbon balance and circadian regulation of hydrolytic and phosphorolytic breakdown of transitory starch. Plant Physiol 14: 879-886.
44. Wesley AV, Helliwell CA, Smith NA, Wang M, Rouse DT, Liu Q, Gooding PS, Singh SP, Abbott D, Stoutjesdijk PA, Robinson SP, Gleave AP, Green AG, Waterhouse PM (2001) Construct design for efficient, effective and high-throughput gene silencing in plants. Plant J 27: 581-590.
45. Wolf S (1993) Effect of leaf age on photosynthesis, carbon transport and carbon allocation in potato plants. Potato Res 36: 253-262.
46. Yu T-S, Kofler H, Häusler RE, Flügge U-I, Zeeman SC, Smith AM, Kossmann J, Lloyd JR, Ritte G, Steup M, Lue W-L, Chen J, Weber A (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.
47. Yu T-S, Zeeman SC, Thorneycroft D, Fulton DC, Dunstan H, Lue W-L, Hegemann B, Tung S-Y, Umemoto T, Chapple A, Tsai D-L, Wang SM, Smith AM, Chen J, Smith SM (2005) α-amylase is not required for breakdown of transitory starch in Arabidopsis leaves. J Biol Chem 280: 9773-9779.
48. Zeeman SC, Northrop F, Smith AM, ap Rees T (1998) A starch-accumulating mutant of Arabidopsis thaliana deficient in chloroplastic starch-hydrolysing enzyme. Plant J 15: 357-365.
49. Zeeman SC, Thorneycroft D, Schupp N, Chapple A, Weck M, Dunstan H, Haldimann P, Bechtold N, Smith AM, Smith SM (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.
50. Zeeman SC, Smith SM, Smith AM (2007) The diurnal metabolism of leaf starch. Biochem J 401: 13-28.
51. Zeeman SC, Kossmann J, Smith AM (2010) Starch: its metabolism, evolution and biotechnological modification in plants. Annu Rev Plant Biol 61: 209-234.