Physiological basis for enhanced sucrose accumulation in an engineered sugarcane cell line

Functional Plant Biology

Volumn 37, Issue 12, 2010, Pages 1161-1174

  Wu, Luguang ^a   Birch, Robert G ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

invertase; isomaltulose; parallel activation; Saccharum; SnRK1; sucrose isomerase; sucrose phosphate synthase; sucrose synthase; suspension culture; trehalose 6 phosphate.

Indexed keywords

INVERTASE; ISOMALTULOSE; PARALLEL ACTIVATION; SACCHARUM; SNRK1; SUCROSE ISOMERASE; SUCROSE SYNTHASE; SUCROSE-PHOSPHATE SYNTHASE; SUSPENSION CULTURES; TREHALOSE-6-PHOSPHATE.;

BIOCHEMISTRY; CATALYSTS; CELL CULTURE; CELL GROWTH; ENZYMES; GLUCOSE; GROWTH KINETICS; ISOMERS; PHYSIOLOGY; PLANTS (BOTANY);

SUGAR (SUCROSE);

ASSAY; BIOACCUMULATION; CELL ORGANELLE; DEVELOPMENTAL BIOLOGY; ENZYME ACTIVITY; FERMENTATION; GENOTYPE; INTERSPECIFIC VARIATION; METABOLITE; PROTEIN; SUCROSE; SUGAR CANE;

SACCHARUM; SACCHARUM OFFICINARUM;

EID: 78649249525     PISSN: 14454408     EISSN: None     Source Type: Journal    
DOI: 10.1071/FP10055     Document Type: Article

References (51)

1. Albertson PL, Peters KF, Grof CPL (2001) An improved method for the measurement of cell wall invertase activity in sugarcane tissue. Australian Journal of Plant Physiology 28, 323-328.
2. Atanassova R, Leterrier M, Gaillard C, Agasse A, Sagot E, Coutos-Thevenot P, Delrot S (2003) Sugar-regulated expression of a putative hexose transport gene in grape. Plant Physiology 131, 326-334. doi:10.1104/pp.009522 (Pubitemid 36141229)
3. Baena-González E, Rolland F, Thevelein JM, Sheen J (2007) A central integrator of transcription networks in plant stress and energy signalling. Nature 448, 938-942. doi:10.1038/nature06069 (Pubitemid 47312777)
4. Baroja-Fernandez E, Munoz FJ, Montero M, Etxeberria E, Sesma MT, et al. (2009) Enhancing sucrose synthase activity in transgenic potato (Solanum tuberosum L.) tubers results in increased levels of starch, ADPglucose and UDPglucose and total yield. Plant&Cell Physiology 50, 1651-1662. doi:10.1093/pcp/pcp108
5. Birch RG (2007) Metabolic engineering in sugarcane: assisting the transition to a bio-based economy. In Applications of plant metabolic engineering. (Eds RA Verpoorte,WAlfermann, TS Johnson) pp. 249-281. (Springer: Berlin)
6. Birch RG, Wu L (2004) Method for increasing product yield. International Patent Specification WO 2004/099403 A1.
7. Börnke F, Hajirezaei M, Heineke D, Melzer M, Herbers K, Sonnewald U (2002) High-level production of the non-cariogenic sucrose isomer palatinose in transgenic tobacco plants strongly impairs development. Planta 214, 356-364. doi:10.1007/s004250100629 (Pubitemid 36065005)
8. Botha FC, Sawyer BJB, Birch RG (2001) Sucrose metabolism in the culm of transgenic sugarcane with reduced soluble acid invertase activity. In Proceedings of the International Society of Sugarcane Technologists XXIV congress. (Ed. DM Hogarth) pp. 588-591. (Australian Society of Sugar Cane Technologists: Mackay)
9. Carter JL, Garrard LA, West SH (1973) Effect of gibberellic acid on starch degrading enzymes in leaves of Digitaria decumbens. Phytochemistry 12, 251-254. doi:10.1016/0031-9422(73)80002-0
10. Chong BF, Bonnett GD, Glassop D, OShea MG, Brumbley SM (2007) Growth and metabolism in sugarcane are altered by the creation of a new hexose-phosphate sink. Plant Biotechnology Journal 5, 240-253. doi:10.1111/j.1467-7652.2006. 00235.x
11. Christensen AH, Quail PH (1996) Ubiquitin promoter-based vectors for high-level expression of selectable and/or screenable marker genes in monocotyledonous plants. Transgenic Research 5, 213-218.doi:10.1007/BF01969712
12. Delatte TL, Selman MHJ, Schluepmann H, Somson GW, Smeekens SCM, de Jong GJ (2009) Determination of trehalose-6-phosphate in Arabidopsis seedlings by successive extractions followed by anion exchange chromatography-mass spectrometry. Analytical Biochemistry 389, 12-17. doi:10.1016/j.ab.2009.03.003
13. Dickson RE (1979) Analytical procedures for the sequential extraction of C-14-labeled constituents from leaves, bark and wood of cottonwood plants. Physiologia Plantarum 45, 480-488. doi:10.1111/j.1399- 3054.1979.tb02618.x
14. Doehlert DC, Huber SC (1983) Regulation of spinich leaf sucrose phosphate synthase by glucose-6-phosphate, inorganic phosphate, and pH. Plant Physiology 73, 989-994. doi:10.1104/pp.73.4.989
15. Ebrahim MKH, Zingsheim O, Veith R, Abo-Kassem EEM, Komor E (1999) Sugar uptake and storage by sugarcane suspension cells at different temperatures and high sugar concentrations. Journal of Plant Physiology 154, 610-616.
16. Fernie AR, Roessner U, Geigenberger P (2001) The sucrose analog palatinose leads to a stimulation of sucrose degradation and starch synthesis when supplied to discs of growing potato tubers. Plant Physiology 125, 1967-1977. doi:10.1104/pp.125.4.1967 (Pubitemid 32375779)
17. Ferreira SJ, Kossmann J, Lloyd JR, Groenewald JH (2008) The reduction of starch accumulation in transgenic sugarcane cell suspension culture lines. Biotechnology Journal 3, 1398-1406. doi:10.1002/biot. 200800106
18. Gnanasambandam A, BirchRG(2004) Efficient developmental mis-targeting by the sporamin NTPP vacuolar signal to plastids in young leaves of sugarcane and Arabidopsis. Plant Cell Reports 23, 435-447. doi:10.1007/ s00299-004-0860-5
19. Groenewald JH, Botha FC (2008) Down-regulation of pyrophosphate: fructose 6-phosphate 1-phosphotransferase (PFP) activity in sugarcane enhances sucrose accumulation in immature internodes. Transgenic Research 17, 85-92. doi:10.1007/s11248-007-9079-x
20. Halford NG, Hey SJ (2009) Snf1-related protein kinases (SnRKs) act within an intricate network that links metabolic and stress signalling in plants. The Biochemical Journal 419, 247-259. doi:10.1042/BJ20082408
21. Hansom SP, Bower RS, Zhang L, Potier BA, Elliott AR, et al. (1999) Regulation of transgene expression in sugarcane. In Proceedings of the International Society of Sugarcane Technologists XXIII Congress. (Ed. V Singh) pp. 278-290. (The Sugar Technologists Association of India: New Delhi)
22. Jacobsen KR, Fisher DG, Maretzki A, Moore PH (1992) Developmental changes in the anatomy of the sugarcane stem in relation to phloem unloading and sucrose storage. Botanica Acta 105, 70-80.
23. Koch K (2004) Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development. Current Opinion in Plant Biology 7, 235-246. doi:10.1016/j.pbi.2004.03.014 (Pubitemid 38611043)
24. Komor E (2000) The physiology of sucrose storage in sugarcane. In Carbohydrate reserves in plants: synthesis and regulation. (Eds AK Gupta, N Kaur) pp. 35-53. (Elsevier: Amsterdam)
25. Kotake T, Yamaguchi D, Ohzono H, Hojo S, Kaneko S, Ishida HK, Tsumuraya Y (2004) UDP-sugar pyrophosphorylase with broad substrate specificity toward various monosaccharide 1-phosphates from pea sprouts. The Journal of Biological Chemistry 279, 45 728-45 736. doi:10.1074/jbc.M408716200 (Pubitemid 39491563)
26. Loreti E, Alpi A, Perata P (2000) Glucose and disaccharide-sensing mechanisms modulate the expression of alpha-amylase in barley embryos. Plant Physiology 123, 939-948. doi:10.1104/pp.123.3.939
27. Lunn JE, Hatch MD (1997) The role of sucrose-phosphate synthase in the control of photosynthate partitioning in Zea mays leaves. Australian Journal of Plant Physiology 24, 1-8. doi:10.1071/PP96088
28. Lunn JE, MacRae E (2003) New complexities in the synthesis of sucrose. Current Opinion in Plant Biology 6, 208-214. doi:10.1016/S1369-5266 (03)00033-5
29. Ma H, Albert H, Paull R, Moore P (2000) Metabolic engineering of invertase activities in different subcellular compartments affects sucrose accumulation in sugarcane cells. Australian Journal of Plant Physiology 21, 1021-1030.
30. Matsuoka K, Nakamura K (1991) Propeptide of a precursor to a plant vacuolar protein required for vacuolar targeting. Proceedings of the National Academy of Sciences of the United States of America 88, 834-838. doi:10.1073/pnas.88.3.834
31. Moore PH (1995) Temporal and spatial regulation of sucrose accumulation in the sugarcane stem. Australian Journal of Plant Physiology 22, 661-679. doi:10.1071/PP9950661
32. Morandini P (2009) Rethinking metabolic control. Plant Science 176, 441-451. doi:10.1016/j.plantsci.2009.01.005
33. Paul MJ, Primavesi LF, Jhurreea D, Zhang YH (2008) Trehalose metabolism and signaling. Annual Review of Plant Biology 59, 417-441. doi:10.1146/ annurev.arplant.59.032607.092945
34. Rolland F, Baena-Gonzalez E, Sheen J (2006) Sugar sensing and signaling in plants: conserved and novel mechanisms. Annual Review of Plant Biology 57, 675-709. doi:10.1146/annurev.arplant.57.032905.105441 (Pubitemid 44061041)
35. Rossouw D, Bosch S, Kossmann J, Botha FC, Groenewald JH (2007) Downregulation of neutral invertase activity in sugarcane cell suspension cultures leads to a reduction in respiration and growth and an increase in sucrose accumulation. Functional Plant Biology 34, 490-498. doi:10.1071/FP06214 (Pubitemid 46869642)
36. Schafer WE, Rohwer JM, Botha FC (2005) Partial purification and characterisation of sucrose synthase in sugarcane. Journal of Plant Physiology 162, 11-20. doi:10.1016/j.jplph.2004.04.010
37. Schluepmann H, Dijken AV, Aghdasi M, Wobbes B, Paul M, Smeekens S (2004) Trehalose mediated growth inhibition of Arabidopsis seedlings is due to trehalose-6-phosphate accumulation. Plant Physiology 135, 879-890. doi:10.1104/pp.104.039503 (Pubitemid 38819032)
38. Sinha AK, Hofmann MG, Romer U, Kockenberger W, Elling L, Roitsch T (2002) Metabolizable and non-metabolizable sugars activate different signal transduction pathways in tomato. Plant Physiology 128, 1480-1489. doi:10.1104/pp.010771 (Pubitemid 34305799)
39. Taylor PWJ, Ko H-L, Adkins SW, Rathus C, Birch RG (1992) Establishment of embryogenic callus and high protoplast yielding suspension cultures of sugarcane (Saccharum spp. hybrids). Plant Cell, Tissue and Organ Culture 28, 69-78. doi:10.1007/BF00039917
40. Toroser D, Plaut Z, Huber SC (2000) Regulation of a plant SNF1-related protein kinase by glucose-6-phosphate. Plant Physiology 123, 403-412. doi:10.1104/pp.123.1.403
41. Turner W, Botha FC (2002) Purification and kinetic properties of UDP-glucose dehydrogenase from sugarcane. Archives of Biochemistry and Biophysics 407, 209-216. doi:10.1016/S0003-9861(02)00500-3 (Pubitemid 35341050)
42. Van Handel E (1968) Direct microdetermination of sucrose. Analytical Biochemistry 22, 280-283. doi:10.1016/0003-2697(68)90317-5
43. Vargas WA, Salerno GL (2010) The Cinderella story of sucrose hydrolysis: alkaline/neutral invertases, from cyanobacteria to unforeseen roles in plant cytosol and organelles. Plant Science 178, 1-8. doi:10.1016/j.plantsci.2009.09. 015
44. Vickers JE, Grof CPL, Bonnett GD, Jackson PA, Morgan TE (2005) Effects of tissue culture, biolistic transformation, and introduction of PPO and SPS gene constructs on performance of sugarcane clones in the field. Australian Journal of Agricultural Research 56, 57-68. doi:10.1071/AR04159 (Pubitemid 40374539)
45. Walsh KB, Sky RC, BrownSM(2005) The anatomy of the pathway of sucrose unloading within the sugarcane stalk. Functional Plant Biology 32, 367-374. doi:10.1071/FP04102 (Pubitemid 40728160)
46. Welbaum GE, Meinzer FC, Grayson RL, Thornham KT (1992) Evidence for and consequences of a barrier to solute diffusion between the apoplast and vascular bundles in sugarcane stalk tissue. Australian Journal of Plant Physiology 19, 611-623. doi:10.1071/PP9920611
47. Wendler R, Veith R, Dancer J, Stitt M, Komor E (1991) Sucrose storage in cell-suspension cultures of Saccharum sp. (sugarcane) is regulated by a cycle of synthesis and degradation. Planta 183, 31-39. doi:10.1007/ BF00197564
48. Winter H, Huber SC (2000) Regulation of sucrose metabolism in higher plants: localization and regulation of activity of key enzymes. Critical Reviews in Plant Sciences 19, 31-67. doi:10.1016/S0735-2689(01) 80002-2
49. Wu L, Birch RG (2005) Characterization of the highly efficient sucrose isomerase from Pantoea dispersa UQ68J and cloning of the sucrose isomerase gene. Applied and Environmental Microbiology 71, 1581-1590. doi:10.1128/AEM.71.3. 1581-1590.2005 (Pubitemid 40396699)
50. Wu L, Birch RG (2007) Doubled sugar content in sugarcane plants modified to produce a sucrose isomer. Plant Biotechnology Journal 5, 109-117. doi:10.1111/j.1467-7652.2006.00224.x (Pubitemid 46006532)
51. Zhang YH, Primavesi LF, Jhurreea D, Andralojc PJ, Mitchell RAC, Powers SJ, Schluepmann H, Delatte T, Wingler A, Paul MJ (2009) Inhibition of SNF1-related protein kinase1 activity and regulation of metabolic pathways by trehalose-6-phosphate. Plant Physiology 149, 1860-1871. doi:10.1104/pp.108. 133934