Advertisement

Planta

, Volume 221, Issue 3, pp 437–445 | Cite as

Identification and cloning of a submergence-induced gene OsGGT (glycogenin glucosyltransferase) from rice (Oryza sativa L.) by suppression subtractive hybridization

  • YanHua Qi
  • Naoyoshi Kawano
  • Yasuo Yamauchi
  • JianQun Ling
  • DeBao Li
  • Kiyoshi TanakaEmail author
Original Article

Abstract

A submergence-induced gene, OsGGT, was cloned from 7-day submerged rice (Oryza sativa L. plants, FR13A (a submergence-tolerant cultivar, Indica), using suppression subtractive hybridization and both 5′- and 3′-rapid amplification of cDNA ends (RACE). The full-length OsGGT cDNA contains 1,273 bp with an open reading frame of 1,140 bp (17–1,156) that encodes 379 amino acids. Its deduced amino acid sequence is homologous with glycogenin glucosyltransferase. We found that the OsGGT gene is located in the 17,970–20,077 bp region of genome fragment AAAA01002475.1 of the Indica cultivar and in the 53,293–51,186 bp region of genome fragment AC037426.12 of chromosome 10 of the Japanica cultivar. A time-course study showed that OsGGT-gene expression increased in FR13A during submergence but decreased in IR42 (submergence-intolerant cultivar, Indica). The expression of the OsGGT gene in FR13A was induced by salicylic acid and benzyladenine. The accumulation of OsGGT mRNA in FR13A also increased in response to ethylene, gibberellin, abscisic acid, drought and salt treatment, but methyl jasmonate treatment and cold stress had no effect on expression. These results suggest that the OsGGT gene could be related to submergence stress and associated with a general defensive response to various environmental stresses.

Keywords

Glycogenin glucosyltransferase Oryza sativa RACE Submergence Suppression subtractive hybridization Stress 

Abbreviations

BA

Benzyladenine

Eth

Ethephon

GA

Gibberellin

Me-JA

Methyl jasmonate

OsCTP

Oryza sativa cation transport protein

OsGGT

Oryza sativa glycogenin glucosyltransferase

OsMGD

Oryza sativa monogalactosyldiacylglycerol synthase

RACE

Rapid amplification of cDNA ends

SSC

Sodium chloride sodium citrate buffer

SSH

Suppression subtractive hybridization

SA

Salicylic acid

References

  1. Alonso MD, Lomako J, Lomako WM, Whelan WJ, Preiss J (1994) Properties of carbohydrate-free recombinant glycogenin expressed in an Escherichia coli mutant lacking UDP-glucose pyrophosphorylase activity. FEBS Lett 352:222–226PubMedGoogle Scholar
  2. Bachem CW, Van der Hoeven RS, De Bruijin SM, Vreugdenhil D, Zabeau M, Visser RG (1996) Visualization of differential gene expression using a novel method of RNA fingerprinting based on AFLP: analysis of gene expression during potato tuber development. Plant J 9:745–753CrossRefPubMedGoogle Scholar
  3. Carrizo ME, Miozzo MC, Goldraij A, Curtino JA (1997) Purification of rabbit skeletal muscle proteoglycogen: studies on the glucosyltransferase activity of polysaccharide-free and -bound glycogenin. Glycobiology 7(4):571–578PubMedGoogle Scholar
  4. Chaturvedi GS, Mishra CH, Singh ON, Pandey CB, Yadav VP, Singh AK, Dwivedi JL, Singh BB, Singh RK (1995) Physiological basis and screening for tolerance for flash flooding. In: Ingram KT (ed) Rainfed lowland rice–agriculture research for high risk environ ments. International Rice Research Institute, Manila, pp 79–96Google Scholar
  5. Chaturvedi GS, Ram PC, Singh AK, Ram P, Ingram KT, Singh BB, Singh RK, Singh VP (1996) Carbohydrate status of rainfed lowland rices in relation to submergence, drought and shade tolerance. In: Singh VP, Singh RK, Singh BB, Zeigler RS (eds) Physiology of stress tolerance in plants. International Rice Research Institute, Los Banos, pp 103–122Google Scholar
  6. Cohen E, Kende H (1987) In vivo 1-aminocyclopropane-1-carboxylate synthase activity in internodes of deepwater rice: enhancement by submergence and low oxygen levels. Plant Physiol 84:282–286Google Scholar
  7. Emes MJ, Wilkins CP, Smith PA, Kupkanchanakul K, Hawker K., Charlton WA, Cutter EG (1988) Starch utilization by deepwater rices during submergence. In: 1987 international deepwater rice workshop. International Rice Research Institute, Manila, pp 319–326Google Scholar
  8. Gibbons BJ, Roach PJ, Hurley TD (2002) Crystal structure of the autocatalytic initiator of glycogen biosynthesis, glycogenin. J Mol Biol 319(2):463–477PubMedGoogle Scholar
  9. Jackson MB, Ram PC (2003) Physiological and molecular basis of susceptibility and tolerance of rice plants to complete submergence. Ann Bot (Lond) 91:227–241Google Scholar
  10. Jackson MB, Waters I, Setter T, Greenway H (1987) Injury to rice plants caused by complete submergence; a contribution by ethylene (ethene). J Exp Bot 38:1826–1838Google Scholar
  11. Kawano N, Evangelina E, Osamu I, Yamauchi Y, Tanaka K (2002a) Metabolic changes in rice seedlings with different submergence tolerance after desubmergence. Environ Exp Bot 47:195–203Google Scholar
  12. Kawano N, Evangelina E, Osamu I, Yamauchi Y, Tanaka K (2002b) Comparison of adaptability to flash flood between rice cultivars differing in flash flood tolerance. Soil Sci Plant Nutr 48:659–665Google Scholar
  13. Letham DS, Palni LMS (1983) The biosynthesis and metabolism of cytokinins. Annu Rev Plant Physiol 134:163–197CrossRefGoogle Scholar
  14. Lin A, Mu J, Yang J, Roach PJ (1999) Self-glucosylation of glycogenin, the initiator of glycogen biosynthesis, involves an inter-subunit reaction. Arch Biochem Biophys 363:163–170Google Scholar
  15. Lomako J, Lomako WM, Whelan WJ (1988) A self-glucosylating protein is the primer for rabbit muscle glycogen biosynthesis. FASEB J 2:3097–3103PubMedGoogle Scholar
  16. Maleck K, Levine A, Eulgem T, Morgan A, Schmid J, Lawton KA, Dangl JL, Dietrich RA (2000) The transcriptome of Arabiposis thaliana during systemic acquired resistance. Nat Genet 26:403–410CrossRefPubMedGoogle Scholar
  17. Mallik S, Kundu C, Banerji C, Nayak DK, Chatterji SD, Nanda PK, Ingram KT, Setter TL (1995) Rice germplasm evaluation and improvement for stagnant flooding. In: Ingram KT (ed) Rainfed lowland rice—agricultural research for high risk environments. International Rice Research Institute, Manila, pp 97–109Google Scholar
  18. Metraux JP, Kende H (1983) The role of ethylene in the growth response of submergence deepwater rice. Plant Physiol 72:441–446Google Scholar
  19. Miyazawa Y, Sakai A, Miyagishima S, Takano H, Kawano S, Kuroiwa T (1999) Auxin and cytokinin have opposite effects on amyloplast development and the expression of starch synthesis genes in cultured bright yellow-2 tobacco cells. Plant Physiol 121(2):461–469PubMedGoogle Scholar
  20. Miyazawa Y, Kato H, Muranaka T, Yoshida S (2002) Amyloplast formation in cultured tobacco BY-2 cells requires a high cytokinin content. Plant Cell Physiol 43(12):1534–1541PubMedGoogle Scholar
  21. Musgrave A, Jackson MB, Ling E (1972) Callitriche stem elongation is controlled by ethylene and gibberellin. Nat New Biol 238:93–96Google Scholar
  22. Ni W, Fahrendorf T, Ballance GM, Lamb CJ, Dixon RA (1996) Stress responses in alfalfa (Medicago sativa L). Transcriptional activation of phenlpropanoid pathway genes in elicitor-induced cell suspension cultures. Plant Mol Biol 30:427–438Google Scholar
  23. Palada MC, Vergara BS (1972) Environmental effects on the resistance of rice seedlings to complete submergence. Crop Sci 12:209–212Google Scholar
  24. Park YS, Min HJ, Ryang SH, Oh KJ, Cha JS, Kim HY, Cho TJ (2003) Characterization of salicylic acid-induced genes in Chinese cabbage. Plant Cell Rep 21(10):1027–1034PubMedGoogle Scholar
  25. Pitcher J, Smythe C, Cohen P (1988) Glycogenin is the priming glucosyltransferase required for the initiation of glycogen biogenesis in rabbit skeletal muscle. Eur J Biochem 176:391–395PubMedGoogle Scholar
  26. Qi Y, Yamauchi Y, Ling J, Kawano N, Li D, Tanaka K (2004a) Cloning of a putative monogalactosyldiacylglycerol synthase gene from rice (Oryza sativa L.) plants and its expression in response to submergence and other stresses. Planta 219(3):450– 458PubMedGoogle Scholar
  27. Qi Y, Yamauchi Y, Ling J, Kawano N, Li D, Tanaka K (2005). The submergence-induced gene OsCTP in rice (Oryza sativa L) is similar to Escherichia coli cation transport protein ChaC. Plant Sci 168(1):15–22Google Scholar
  28. Rabbani MA, Maruyama K, Abe H, Khan MA, Katsura K, Ito Y, Yoshiwara K, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Monitoring expression profiles of rice genes under cold, drought, and high-salinity stresses and abscisic acid application using cDNA microarray and RNA gel-blot analyses. Plant Physiol 133(4):1755–1767CrossRefPubMedGoogle Scholar
  29. Raskin I, Kende H (1984a) Regulation of growth in stem sections of deep-water rice. Planta 160:66–72Google Scholar
  30. Raskin I, Kende H (1984b) Role of gibberellin in the growth response of submerged deep water rice. Plant Physiol 76:947–950Google Scholar
  31. Roach PJ, Skurat AV (1997) Self-glucosylating initiator proteins and their role in glycogen biosynthesis. Prog Nucl Acid Res Mol Biol 57:289–316Google Scholar
  32. Roach PJ, Skurat AV, Harris RA (2000) Regulation of glycogen metabolism. In: Jefferson LS, Cherrington AD (eds) Oxford University Press, New York, pp 609–647Google Scholar
  33. Toojinda T, Siangliw M, Tragoonrung S, Vanavichit A (2003) Molecular genetics of submergence tolerance in rice: QTL analysis of key traits. Ann Bot (Lond) 91:243–253Google Scholar
  34. Uquillas C, Letelier I, Blanco F, Jordana X, Holuigue L (2004) NPR1- independent activation of immediate early salicylic acid-responsive genes in Arabidopsis. Mol Plant-Microbe Interact 17(1):34–42Google Scholar
  35. Viskupic E, Cao Y, Zhang W, Cheng C, DePaoli-Roach AA, Roach PJ (1992) Rabbit skeletal muscle glycogenin. Molecular cloning and production of fully functional protein in Escherichia coli. J Biol Chem 267:25759–25763PubMedGoogle Scholar
  36. Yamada N (1959) Physiological basis of resistance of rice plant against overhead flooding. Bull Natl Inst Agric Sci Ser D 8:1–112Google Scholar
  37. Yamaryo Y, Kanai D, Awai K, Shimojima M, Masuda T, Shimada H, Takamiya K, Ohta H (2003) Light and cytokinin play a co-operative role in MGDG synthesis in greening cucumber cotyledons. Plant Cell Physiol 44:844–855PubMedGoogle Scholar
  38. Setter TL, Waters I, Wallace I, Bhekasut P, Greenway H (1998) Submergence of rice I: growth and photosynthetic response to CO2 enrichment of floodwater. Aust J Plant Physiol 16:251–263Google Scholar
  39. Whelan WJ (1986) The initiation of glycogen synthesis. Bioessays 5:136–140PubMedGoogle Scholar
  40. Smythe C, Caudwell FC, Ferguson M, Coden P (1988) Isolation and structural analysis of a peptide containing the novel tyrosyl-glucose linkage in glycogenin. EMBO J 7:2681–2686PubMedGoogle Scholar
  41. Singh DG, Lomako J, Lomako WM, Whelan WJ, Meyer HE, Serwe M, Metzger JW (1995) Beta-Glucosylarginine: a new glucose-protein bond in a self-glucosylating protein from sweet corn. FEBS Lett 376(1–2):61–64PubMedGoogle Scholar
  42. Takahashi R, Joshee N, Kitagawa Y (1994) Induction of chilling resistance by water stress, and cDNA sequence analysis and expression of water stress-regulated genes in rice. Plant Mol Biol 26(1):339–352PubMedGoogle Scholar
  43. Sambrook J, Russell DW (2001) In: Sambrook J, Russell DW (eds) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor, New York, pp 7.31–7.34Google Scholar
  44. Diatchenko L, Lau YFC, Campbell AP, Chenchik A, Moqadam F, Huang B, Lukyanov K, Gurskaya N, Sverdlov ED, Siebert PD (1996) Suppression subtractive hybridization: a method of generating differentially regulated or tissue-specific cDNA probes and libraries. Proc Natl Acad Sci 93:6025–6030CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • YanHua Qi
    • 1
  • Naoyoshi Kawano
    • 1
  • Yasuo Yamauchi
    • 1
  • JianQun Ling
    • 2
  • DeBao Li
    • 2
  • Kiyoshi Tanaka
    • 1
    Email author
  1. 1.Laboratory of Plant Biotechnology, Faculty of AgricultureTottori UniversityKoyamaJapan
  2. 2.Institute of BiotechnologyZhejiang UniversityHangzhouPeople’s Republic of China

Personalised recommendations