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Starch degradation and sucrose metabolism during anaerobic growth of pondweed (Potamogeton distinctus A. Benn.) turions

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Abstract

Stem growth in pondweed (Potamogeton distinctus A. Benn.) turions was stimulated in anaerobic conditions. Decreases in starch contents in turion cells, the number of amyloplasts in a cell and sizes of starch granules in amyloplasts clearly showed enhancement of starch consumption in turions during anaerobic growth of stems of pondweed. Although the total activities of both α-amylase and starch phosphorylase were not stimulated by anaerobic conditions, the activities of one amylase and two isozymes of starch phosphorylase, separated by native polyacrylamide gel electrophoresis, were enhanced in anaerobic conditions. The sucrose content in turion cells decreased rapidly in the early stage of anaerobic growth but then remained constant after the enhanced growth had started, suggesting active sucrose metabolism. The activities of sucrose-phosphate synthase, sucrose synthase and acid invertase, measured in vitro, were enhanced in extracts from turions in anaerobic conditions. The induction of the activity of sucrose synthase was most significant, suggesting that sucrose synthase plays an important role in sucrose metabolism in pondweed turions growing in anaerobic conditions.

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References

  • Barclay A M and Crawford R M M 1982 Plant Growth and survival under strict anaerobiosis. J. Exp. Bot. 33, 541-549.

    Google Scholar 

  • Bradford M M 1976 A rapid and sensitive method for the quantification of microgram qualities of protein utilizing of dye-binding. Anal. Biochem. 72, 248-254.

    Google Scholar 

  • Crawford R M M and Brändle R 1996 Oxygen deprivation stress in a changing environment. J. Exp. Bot. 47, 145-159.

    Google Scholar 

  • Dennis D T and Blakeley S D 2000 Carbohydrate metabolism. In Biochemistry & Molecular Biology of Plants. Ed. B B Buchanan, W Gruissem and R L Jones. pp. 630-675. American Society of Plant Physiologists, Rockvell, USA.

    Google Scholar 

  • Dennis E S, Dolferus R, Ellis E, Rahman M, Wu Y, Hoeren F U, Grover A, Ismond K P. Good A G and Peacock W J 2000 Molecular strategies for improving waterlogging tolerance in plants. J. Exp. Bot. 51, 89-97.

    Google Scholar 

  • Doehlert D C and Duke S H 1983 Specific determination of ?-amylase activity in crude plant extracts containing ?-amylase. Plant Physiol.71, 229-234.

    Google Scholar 

  • Drew M C 1990 Sensing soil oxygen. Plant Cell Environ 13, 681-693.

    Google Scholar 

  • Duwenig E, Steup M, Willmitzer L and Kossmann J 1997 Antisense inhibition of cytosolic phospholylase in potato plants (Solanum tuberosum L.) affects tuber sprouting and flower formation with only little impact on carbohydrate metabolism. Plant J. 12, 323-333.

    Google Scholar 

  • Gibbs J, Morrell S, Valdez A, Setter T L and Greenway H 2000 Regulation of alcoholic fermentation in coleoptiles of two rice cultivars differing in tolerance to anoxia. J. Exp. Bot. 51, 785-796.

    Google Scholar 

  • Givan C V 1999 Evolving concepts in plant glycolysis: two centuries of progress. Biol. Rev. 74, 277-309.

    Google Scholar 

  • Guglielminetti L, Yamaguuchi J, Perata P and Apli A 1995 Amylolytic activities in cereal seeds under aerobic and anaerobic conditions. Plant Physiol. 109, 1069-1076.

    Google Scholar 

  • Hanhijärvi A M and Fagerstedt K V 1995 Comparison of carbohydrate utilization and energy charge in the yellow flag iris (Iris pseudacorus) and garden iris (Iris germanica) under anoxia. Physiol. Plant. 93, 493-497.

    Google Scholar 

  • Hill L M, Reimholz R, Schröder R, Nielsen T H and Stitt M 1996 The onset of sucrose accumulation in cold-stored potato tubers is caused by an increased rate of sucrose synthesis and coincides with low levels of hexose-phosphates, an activation of sucrose phosphate synthase and the appearance of a new form of amylase. Plant Cell Environ. 19, 1223-1237.

    Google Scholar 

  • Ishizawa K, Murakami S, Kawakami Y and Kuramochi H 1999 Growth and energy status of arrowhead, pondweed turions and rice seedlings under anoxic conditions. Plant Cell Environ. 22, 505-514.

    Google Scholar 

  • Kennedy R A, Rumpho M E and Fox T C 1992 Anaerobic metabolism in plants. Plant Physiol. 100, 1-6.

    Google Scholar 

  • Levi C and Preiss J 1978 Amylopectin degradation in pea chloroplasts. Planta 158, 179-184.

    Google Scholar 

  • Lorberth R, Ritte G, Wilmitzer L and Kossmann J 1998 Inhibition of a starch-granule-bound protein leads to modified starch and repression of cold sweetening. Nature Biotech. 16, 473-477.

    Google Scholar 

  • McElfresh K C and Chourey P S 1988 Anaerobiosis induces transcription of sucrose synthase in maize. Plant Physiol. 87, 542-546.

    Google Scholar 

  • Menegus F, Cattaruzza L, Scaglioni L and Ragg E 1992 Effects of oxygen level on metabolism and development of seedlings of Trapa natans and two ecologically related species. Physiol. Plant. 86, 168-172.

    Google Scholar 

  • Michal G 1984 D-Glucose 1-phosphate. In Method of Enzymatic Analysis. Vol VI Metabolites 1: Carbohydrates. Ed. H U Bergmeyer. pp 185-191. Verlag Chemie, Weinheim.

    Google Scholar 

  • Morrell S and ap Rees T 1986 Control of the hexose content of potato tubers. Phytochemistry 25, 1073-1076.

    Google Scholar 

  • Nelson N 1944 A photometric adaptation of the Somogyi method for the determination of glucose. J. Biol. Chem. 153, 375-380.

    Google Scholar 

  • Nguyen-Quoc B and Foyer C H 2001 A role of 'futile cycles' involving invertase and sucrose synthase in sucrose metabolism of tomato fruit. J. Exp. Bot. 52, 881-889.

    Google Scholar 

  • Perata P, Pozueta-Romero J, Akazawa T and Yamaguchi J 1992 Effect of anoxia on starch breakdown in rice and wheat seeds. Planta 188, 611-618.

    Google Scholar 

  • Perata P and Alpi A 1993 Plant responses to anaerobiosis. Plant Sci. 93, 1-17.

    Google Scholar 

  • Ricard B, Rivoal J, Spiteri A and Pradet A 1990 Anaerobic stress induces the transcription and translation of sucrose synthase in rice. Plant Physiol. 95, 669-674.

    Google Scholar 

  • Ritte G, Eckermann N, Haebel S, Lorberth R and Steup M 2000 Compartmentation of the starch-related R1 protein in higher plants. Starch/Stärke 52, 145-149.

    Google Scholar 

  • Roe J H 1934 A colorimetric method for the determination of fructose in blood and urine. J. Biol. Chem. 107, 15-22.

    Google Scholar 

  • Sachs M M, Subbaiah C C and Saab I N 1996 Anaerobic gene expression and flooding tolerance in maize. J. Exp. Bot. 47, 1-15.

    Google Scholar 

  • Sato T, Harada T and Ishizawa K 2002 Stimulation of glycolysis in anaerobic elongation of pondweed (Potamogeton distinctus) turions. J. Exp. Bot. 53, 1847-1856.

    Google Scholar 

  • Schlüter U and Crawford R M M 2001 Long-term anoxia tolerance in leaves of Acorus calamus L. and Iris pseudacorus L. J. Exp. Bot. 52, 2213-2225.

    Google Scholar 

  • Sieber M and Brändle R 1991 Energy metabolism in rhizomes of Acorus calamus (L.) and in tubers of Solanum tuberosum (L.) with regard to their anoxia tolerance. Bot. Acta. 104, 279-282.

    Google Scholar 

  • Small J G C, Potgieter G P and Botha F C 1989 Anoxic seed germination of Erythrina caffra: ethanol fermentation and response to metabolic inhibitors. J. Exp. Bot. 40, 375-381.

    Google Scholar 

  • Spurr A R 1969 A low-viscosity epoxy resin embedding medium for electron microscopy.J. Ultrastr. Res. 26, 31-43.

    Google Scholar 

  • Stitt M and Heldt HW 1981 Physiological rates of starch breakdown in isolated intact spinach chloroplasts. Plant Physiol. 68, 755-761.

    Google Scholar 

  • Summers J E and Jackson M B 1994 Anaerobic conditions strongly promote extension by stems of overwintering tubers of Potamogeton pectinatus L. J. Exp. Bot. 45, 1309-1318.

    Google Scholar 

  • Summers J E, Ratcliffe R G and Jackson M B 2000 Anoxia tolerance in the aquatic monocot Potamaogeton pectinatus: absence of oxygen stimulates elongation in association with an unusually large Pasteur effect. J. Exp. Bot. 51, 1413-1422.

    Google Scholar 

  • Sun Z and Henson C A 1991 A Quantitative assessment of the importance of barley seed ?-amylase, ?-amylase, debranching enzyme, and ?-glucosidase in starch degradation. Arch. Biochm. Biophy. 284, 298-305.

    Google Scholar 

  • Tokutake S, Uchida R, Kotani K, Saito K and Yamaji N 1993. Syntheses of modified 2-chloro-4-nitrophenyl ?-D-maltopentaosides as useful substrates for assay of human alpha amylase. Carb. Res. 238, 109-133.

    Google Scholar 

  • Tsuji H 1972 Respiratory activity in rice seedlings germinated under strictly anaerobic conditions. Bot. Mag. Tokyo 85, 207-218.

    Google Scholar 

  • Vartapetian B B and Jackson M B 1997 Plant adaptations to anaerobic stress. Ann. Bot. 79 (Sup. A), 3-20.

    Google Scholar 

  • Zeeman S C, Northrop F, Smith A M and ap Rees T 1998 A starch-accumulating mutant of Arabidopsis thaliana deficient in a chloroplastic starch-hydrolysing enzyme. Plant J. 15, 357-365.

    Google Scholar 

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  1. Department of Developmental Biology and Neuroscience, Graduate School of Life Sciences, Tohoku University, 980-8578, Sendai, Japan

    Taro Harada & Kimiharu Ishizawa

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  1. Taro Harada
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  2. Kimiharu Ishizawa
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Correspondence to Kimiharu Ishizawa.

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Harada, T., Ishizawa, K. Starch degradation and sucrose metabolism during anaerobic growth of pondweed (Potamogeton distinctus A. Benn.) turions. Plant and Soil 253, 125–135 (2003). https://doi.org/10.1023/A:1024585015697

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