Skip to main content
PMC home page
Physiology and Molecular Biology of Plants logoLink to Physiology and Molecular Biology of Plants
. 2010 Aug 13;16(1):59–68. doi: 10.1007/s12298-010-0008-8

Regulation of sugar metabolism in rice (Oryza sativa L.) seedlings under arsenate toxicity and its improvement by phosphate

Bhaskar Choudhury 1, Souvik Mitra 1, Asok K Biswas 1,✉
PMCID: PMC3550626  PMID: 23572955

Abstract

The effect of arsenate with or without phosphate on the growth and sugar metabolism in rice seedlings cv. MTU 1010 was studied. Arsenate was found to be more toxic for root growth than shoot growth and water content of the seedlings gradually decreased with increasing concentrations. Arsenate exposure at 20 μM and 100 μM resulted in an increase in reducing sugar content and decrease in non-reducing sugar content. There was a small increase in starch content, the activity of starch phosphorylase was increased but α-amylase activity was found to be decreased. Arsenate toxicity also affected the activities of different carbohydrate metabolizing enzymes. The activities of sucrose degrading enzymes viz., acid invertase and sucrose synthase were increased whereas, the activity of sucrose synthesizing enzyme, viz. sucrose phosphate synthase declined. The combined application of arsenate with phosphate exhibited significant alterations of all the parameters tested under the purview of arsenate treatment alone which was congenial to better growth and efficient sugar metabolism in rice seedlings. Thus, the use of phosphorus enriched fertilizers may serve to ensure the production of healthy rice plants in arsenic contaminated soils.

Keywords: Amelioration, Arsenic, Phosphate, Rice, Sugar metabolism

Full Text

The Full Text of this article is available as a PDF (287.6 KB).

Abbreviations

As

arsenic

cv.

cultivar

DNSA

3,5-dinitrosalicylic acid

DTT

dithiothreitol

EDTA

ethylenediamine tetraacetic acid

fw

fresh weight

HEPES

N-2-Hydroxyethylpiperazine-N′-2-ethanesulfonic acid

KI

potassium iodide

PFD

photon flux density

PMSF

phenyl methyl sulphonyl fluoride

SE

standard error

SPS

sucrose phosphate synthase

SS

sucrose synthase

TCA

trichloroacetic acid

UDP

uridine-di-phosphate

References

  1. Abedin M.J., Feldmann J., Meharg A.A. Uptake kinetics of arsenic species in rice plants. Plant Physiol. 2002;128:1120–1128. doi: 10.1104/pp.010733. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Blum J.J. Phosphate uptake by phosphate-starved Euglena. J. Gen. Physiol. 1966;49:125–137. doi: 10.1085/jgp.0491125. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Borkowska B., Szczerba J. Influence of different carbon sources on invertase activity and growth of sourcherry (Prunus cerasus L.) shoot cultures. J. Exp. Bot. 1991;42:911–915. doi: 10.1093/jxb/42.7.911. [DOI] [Google Scholar]
  4. Bush D.S., Biswas A.K., Jones R.L. Gibberellic acid stimulate Ca2+ accumulation in barley aleurone endoplasmic reticulum. Calcium transport and steady state levels. Planta. 1989;178:411–420. doi: 10.1007/BF00391870. [DOI] [PubMed] [Google Scholar]
  5. Clark G.T., Dunlop J., Phung H.T. Phosphate absorption by Arabidopsis thaliana: interactions between phosphorus status and inhibition by arsenate. Aust. J. Plant Physiol. 2003;27:959–965. [Google Scholar]
  6. Dhankher O.P., Rosen B.P., McKinney E.C., Meagher R.B. Hyperaccumulation of arsenic in the shoots of Arabidopsis silenced for arsenate reductase. Proceedings of the National Academy of Sciences. 2006;103(14):5413–5418. doi: 10.1073/pnas.0509770102. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Duan G.L., Zhu Y.G., Tong Y.P., Cai C., Kneer R. Characterization of arsenate reductase in the extract of roots and fronds of Chinese brake fern, an arsenic hyperaccumulator. Plant Physiol. 2005;138:461–469. doi: 10.1104/pp.104.057422. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Dubey R.S., Singh A.K. Salinity induces accumulation of soluble sugars and alter the activity of sugar metabolizing enzymes in rice plants. Biol. Plant. 1999;42:233–239. doi: 10.1023/A:1002160618700. [DOI] [Google Scholar]
  9. Dubey R.S. Photosynthesis in plants under stressful conditions. In: Pessa Rakli M., editor. Handbook of photosynthesis. New York: Marcel Dekker; 1997. pp. 859–875. [Google Scholar]
  10. Dubois M., Gilles K.A., Hamilton J.K., Rebers P.A., Smith F. Colororimetric method for determination of sugars and related substances. Anal. Chem. 1956;28:350–356. doi: 10.1021/ac60111a017. [DOI] [Google Scholar]
  11. Ellis DR, Gumaelius L, Indriolo E, Pickerin IJ, Banks JA and Salt DE (2006) A novel arsenate reductase from the arsenic hyperaccumulating fern Pteris vittata. Plant Physiol. DOI:10.1104/pp.106.084079. [DOI] [PMC free article] [PubMed]
  12. Fiske C.H., Subbarow Y. The colorimetric determination of phosphorus. J. Biol. Chem. 1925;66:375. [Google Scholar]
  13. Foyer C.H., Valadier M.H., Migge A., Becker T.W. Drought induced effects on nitrate reductase activity and mRNA and on the coordination of nitrogen and carbon metabolism in maize leaves. Plant Physiol. 1998;117:283–292. doi: 10.1104/pp.117.1.283. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Geigenberger P., Stitt M. Sucrose synthase catalyses a readily revesible reaction in vivo in developing potato tubers and other plant tissues. Planta. 1993;189:329–339. doi: 10.1007/BF00194429. [DOI] [PubMed] [Google Scholar]
  15. Geng C.N., Zhu Y.G., Tong Y.P., Smith S.E., Smith F.A. Arsenate (As) uptake by and distribution in two cultivars of winter wheat (Triticum aestivum L.) Chemosphere. 2006;62:608–615. doi: 10.1016/j.chemosphere.2005.05.045. [DOI] [PubMed] [Google Scholar]
  16. Gunes A., Inal A., Bagci E.G., Pilbeam D.J. Silicon mediated changes of some physiological and enzymatic parameters symptomatic for oxidative stress in spinach and tomato grown in sodic-B toxic soil. Plant Soil. 2008;290:103–114. doi: 10.1007/s11104-006-9137-9. [DOI] [PubMed] [Google Scholar]
  17. Hartley-Whitaker J., Ainsworth G., Meharg A.A. Copper and arsenate-induced oxidative stress in Holcus lanatus L. clones with differential sensitivity. Plant Cell Environ. 2001;24:713–722. doi: 10.1046/j.0016-8025.2001.00721.x. [DOI] [Google Scholar]
  18. Hayashi H., Alia M.L., Deshnium P., Ida M., Murata N. Transformation of Arabidopsis thaliana with the cod A gene for choline oxidase; accumulation of glycine betaine and enhanced tolerance to salt and cold stress. Plant J. 1997;12:133–142. doi: 10.1046/j.1365-313X.1997.12010133.x. [DOI] [PubMed] [Google Scholar]
  19. Hubbard N.L., Huber S.C., Pharr D.M. Sucrose phosphate synthase and acid invertase as determinant of sucrose concentration in developing muskmelon (Cucumis melo L.) fruits. Plant Physiol. 1989;91:1527–1534. doi: 10.1104/pp.91.4.1527. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Hurry V.M., Strand A., Tobiaeson M., Gardestrom P., Oquist G. Cold hardening of spring and winter wheat and rape results in differential effects on growth, carbon metabolism and carbohydrate content. Plant Physiol. 1995;109:697–706. doi: 10.1104/pp.109.2.697. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Krause K.P., Hill L., Reimholz R., Nielsen T.H., Sonnewald U., Stitt M. Sucrose metabolism in cold stored potato tubers with decreased expression of sucrose phosphate synthase. Plant Cell Environ. 1998;21:285–299. doi: 10.1046/j.1365-3040.1998.00271.x. [DOI] [Google Scholar]
  22. Livingston D.P., Henson C.A. Apoplastic sugars, fructans, fructans exohydrolase and invertase in winter oat: responses to second phase cold hardening. Plant Physiol. 1998;116:403–408. doi: 10.1104/pp.116.1.403. [DOI] [Google Scholar]
  23. Lohaus G., Winter H., Riens B., Heldt H.W. Further studies of phloem loading process in leaves of and spinach. The comparison of metabolite concentration in the apoplastic compartment with those in the cytosolic compartment and in sieve tubes. Bot. Acta. 1995;108:270–275. [Google Scholar]
  24. McCready R.M., Guggolz J., Silviera V., Owens H.S. Determination of starch and amylase in vegetables. Anal. Chem. 1950;22:1156–1158. doi: 10.1021/ac60045a016. [DOI] [Google Scholar]
  25. Miller G.L. Use of dinitrosalicylic acid reagent for determination of reducing sugars. Anal Chem. 1972;31:426–428. doi: 10.1021/ac60147a030. [DOI] [Google Scholar]
  26. Miron D., Schaffer A.A. Sucrose phosphate synthase, sucrose synthase and invertase activities in developing fruit of Lycopersicon esculentum mill. and the sucrose accumulating Lycopersicon hirsutum humb. and bompl. Plant Physiol. 1991;95:623–627. doi: 10.1104/pp.95.2.623. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Nelson N. A photometric adaptation of the Somogyi method for the determination of glucose. J. Biol. Chem. 1944;153:375–380. [Google Scholar]
  28. Pfeiffer I., Kutschera U. Sucrose metabolism and lipid mobilization during light induced expansion of sunflower leaves. J. Plant Physiol. 1996;147:553–558. [Google Scholar]
  29. Quick P., Siegl G., Neuhaus H.E., Feil R., Stitt M. Short term water stress lead to stimulation of sucrose synthesis by activating sucrose phosphate synthase. Planta. 1989;177:535–546. doi: 10.1007/BF00392622. [DOI] [PubMed] [Google Scholar]
  30. Ranwala A.P., Miller W.B. Sucrose cleaving enzymes and carbohydrate pools in Lilium longiflorum floral organ. Physiol. Plant. 1998;103:541–550. doi: 10.1034/j.1399-3054.1998.1030413.x. [DOI] [Google Scholar]
  31. Rochette E., Tamrat E., Fraud G., Pik R., Courtillot V., Ketefo E., Coulon C., Hoffmann C., Vandamme D., Yirgu G. Magnetostratigraphy and timing of the early Oligocene Ethiopian traps. Earth Planet. Sci. Lett. 1998;164:497–510. doi: 10.1016/S0012-821X(98)00241-6. [DOI] [Google Scholar]
  32. Rosen B.P. Biochemistry of arsenic detoxification. FEBS Lett. 2002;529:86–92. doi: 10.1016/S0014-5793(02)03186-1. [DOI] [PubMed] [Google Scholar]
  33. Rothstein A., Donovan K. Interactions of arsenate with the phosphate-transporting system of yeast. J. Gen. Physiol. 1963;46:1075–1085. doi: 10.1085/jgp.46.5.1075. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Salisbury F.B., Ross C.W. Plant Physiology Fourth Edition-CBS. New Delhi: Publishers and Distributors; 1991. [Google Scholar]
  35. Sinniah U.R., Ellis R.H., John P. Irrigation and seed quality development in rapid recycling Brassica, soluble carbohydrates and heat stable protein. Ann. Bot. 1998;82:647–655. doi: 10.1006/anbo.1998.0738. [DOI] [Google Scholar]
  36. Sneller E.F.C., Van-Heerwaarden L.M., Kraaijeveld-Smit F.J.L., Ten-Bookum W.M., Koevoets P.L.M., Schat H., Verkleij J.A.C. Toxicity of arsenate in Silene vulgaris, accumulation and degradation of arsenate-induced phytochelatins. New Phytol. 1999;144:223–232. doi: 10.1046/j.1469-8137.1999.00512.x. [DOI] [Google Scholar]
  37. Somogyi M. A new reagent for the determination of sugar. J. Biol. Chem. 1945;160:61–68. [Google Scholar]
  38. Stitt M., Huber S., Kerr P. Control of photosynthetic sucrose formation. In: Stumpf P.K., Conn E.E., editors. The Biochemistry of Plants A Comprehensive Treatise. New York: Academic Press; 1987. pp. 327–409. [Google Scholar]
  39. Ullrich-Eberius C.I., Sanz A., Novacky A.J. Evaluation of arsenate- and vanadate-associated changes of electrical membrane potential and phosphate transport in Lemna gibba G1. J. Exp. Bot. 1989;40:119–128. doi: 10.1093/jxb/40.1.119. [DOI] [Google Scholar]
  40. Van den E.W., Michiels A., Le-Roy K., Van-Laere A. Cloning of a vacular invertase from Belgian endive leaves (Cichorium intybus) Physiol. Plant. 2002;115:504–512. doi: 10.1034/j.1399-3054.2002.1150404.x. [DOI] [PubMed] [Google Scholar]
  41. Vassey T.L., Quick W.P., Sharkley T.D., Stitt M. Water stress, CO2 and light effects on sucrose phosphate synthase activity in Phaseolus vulgaris. Physiol. Plant. 1991;81:37–44. doi: 10.1111/j.1399-3054.1991.tb01709.x. [DOI] [Google Scholar]
  42. Witt H.J. Activities of enzymes involved in sucrose and starch metabolism in Riella helicophylla (Bory et mont.) during differentiation. J. Plant Physiol. 1989;135:99–104. [Google Scholar]
  43. Yang J., Zhang J., Wang Z., Zhu Q. Activities of starch hydrolytic enzymes and sucrose phosphate synthase in the stem of rice subjected to water stress during grain filling. J. Exp. Bot. 2001;52:2169–2179. doi: 10.1093/jexbot/52.364.2169. [DOI] [PubMed] [Google Scholar]
  44. Zhou R., Silcher R.C., Quebedeaux B. Apple leaf sucrose phosphate synthase is inhibited by sorbitol-6-phosphate. Funct. Plant Biol. 2002;29:569–574. doi: 10.1071/PP01123. [DOI] [PubMed] [Google Scholar]

Articles from Physiology and molecular biology of plants : an international journal of functional plant biology are provided here courtesy of Springer

RESOURCES