Skip to main content

Advertisement

SpringerLink
Log in

Identification and organization of chloroplastic and cytosolic l-myo-inositol 1-phosphate synthase coding gene(s) in Oryza sativa: comparison with the wild halophytic rice, Porteresia coarctata

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

The gene coding for rice chloroplastic l-myo-inositol-1-phosphate synthase (MIPS; EC 5.5.1.4) has been identified by matrix-assisted laser desorption time-of-flight mass spectrometry analysis of the purified and immunologically cross-reactive ~60 kDa chloroplastic protein following two-dimensional polyacrylamide gel electrophoresis, which exhibited sequence identity with the cytosolic MIPS coded by OsINO1-1 gene. A possible chloroplastic transit peptide sequence was identified upstream of the OsINO1-1 gene upon analysis of rice genome. RT-PCR and confocal microscope studies confirmed transcription, effective translation and its functioning as a chloroplast transit peptide. Bioinformatic analysis mapped the chloroplastic MIPS (OsINO1-1) gene on chromosome 3, and a second MIPS gene (OsINO1-2) on chromosome 10 which lacks conventional chloroplast transit peptide sequence as in OsINO1-1. Two new PcINO1 genes, with characteristic promoter activity and upstream cis-elements were identified and cloned, but whether these proteins can be translocated to the chloroplast or not is yet to be ascertained. Electrophoretic mobility shift assay carried out with nuclear extract of Porteresia coarctata leaves grown under both control and stressed condition shows binding of nuclear proteins with the upstream elements. Nucleotide divergence among the different Oryza and Porteresia INO1 genes were calculated and compared.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

Abbreviations

MIPS:

l-myo-Inositol-1-phosphate synthase

MALDI-TOF MS:

Matrix-assisted laser desorption ionization time-of-flight mass spectrometry

CaMV:

Cauliflower mosaic virus

GFP:

Green fluorescent protein

2D PAGE:

Two-dimensional polyacrylamide gel electrophoresis

ORF:

Open reading frame

GUS:

β-Glucuronidase

References

  • Adhikari J, Majumder AL, Bhaduri TJ, DasGupta S, Majumder AL (1987) Chloroplast as a locale of l-myo-inositol 1-phosphate synthase. Plant Physiol 85:611–614

    Article  CAS  PubMed  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    CAS  PubMed  Google Scholar 

  • Armbruster U, Hertle A, Makarenko E, Zühlke J, Pribil M, Dietzmann A, Schliebner I, Aseeva E, Fenino E, Scharfenberg M, Voigt C, Leister D (2009) Chloroplast proteins without cleavable transit peptides: rare exceptions or a major constituent of the chloroplast proteome? Mol Plant 6:1325–1335

    Article  Google Scholar 

  • Bachhawat N, Mande SC (2000) Complex evolution of the inositol-1-phosphate synthase gene among archaea and eubacteria. Trends Genet 16:111–113

    Article  CAS  PubMed  Google Scholar 

  • Bannai H, Tamada Y, Maruyama O, Nakai K, Miyano S (2002) Extensive feature detection of N-terminal protein sorting signals. Bioinformatics 18:298–305

    Article  CAS  PubMed  Google Scholar 

  • Barcisewski J, Barciszewska M, Suter B, Kubli E (1985) Plant tRNA suppressors: in vivo readthrough properties and nucleotide sequence of yellow lupin seeds tRNATyr. Plant Sci 4:193–196

    Article  Google Scholar 

  • Beier H, Barciszewska M, Krupp G, Mitnacht R, Gross HJ (1984) UAG readthrough during TMV RNA translation: isolation and sequence of two tRNAs Tyr with suppressor activity from tobacco plants. EMBO J 3:351–356

    CAS  PubMed  Google Scholar 

  • Birney E, Clamp M, Durbin R (2004) Genewise and genomewise. Genome Res 14:988–995

    Article  CAS  PubMed  Google Scholar 

  • Bradford MM (1976) Quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Brown CM, Stockwell PA, Trotman CNA, Tate WP (1990) Sequence analysis suggests that tetra-nucleotides signal the termination of protein synthesis in eukaryotes. Nucleic Acids Res 18:6339–6345

    Article  CAS  PubMed  Google Scholar 

  • Chatterjee A, Majee M, Ghosh S, Majumder AL (2004) sll1722, an unassigned open reading frame of Synechocystis PCC 6803, codes for l-myo-inositol-1-phosphate synthase. Planta 218:989–998

    Article  CAS  PubMed  Google Scholar 

  • Chatterjee A, Dastidar KG, Maitra S, Majumder AL (2006) sll1981, an acetolactate synthase homologue of Synechocystis sp. PCC6803, functions as l-myo-inositol-1-phosphate synthase. Planta 224:367–379

    Article  CAS  PubMed  Google Scholar 

  • Clauser KR, Baker PR, Burlingame AL (1999) Role of accurate mass measurement (±10 ppm) in protein identification strategies employing MS or MS/MS and database searching. Anal Chem 71:2871–2882

    Article  CAS  PubMed  Google Scholar 

  • Dellaporta S, Wood J, Hicks JB (1983) A plant DNA minipreparation: version II. Plant Mol Biol Rep 1:19–21

    Article  CAS  Google Scholar 

  • Dihazi H, Kessler R, Eschrich K (2001) One-step purification of recombinant yeast 6-phosphofructo-2-kinase after the identification of contaminants by MALDI-TOF MS. Protein Exp Purif 21:201–209

    Article  CAS  Google Scholar 

  • Emanuelsson O, Nielsen H, Brunak S, von Heijne G (2000) Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 300:1005–1016

    Article  CAS  PubMed  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  • GhoshDastidar K, Maitra S, Goswami L, Roy D, Das KP, Majumder AL (2006) An insight into the molecular basis of salt tolerance of l-myo-inositol 1-P synthase (PcINO1) from Porteresia coarctata (Roxb.) Tateoka, a halophytic wild rice. Plant Physiol 140:1279–1296

    Article  Google Scholar 

  • Guillot-Salomon T, Farineau N, Oursel A, Tuquet C (1987) Isolation and characterization of developing chloroplasts from light grown barley leaves. Physiol Plant 69:113–122

    Article  CAS  Google Scholar 

  • Hait NC, Ray Chaudhuri A, Das A, Bhattacharyya S, Majumder AL (2002) Processing and activation of chloroplast l-myo-inositol 1-phosphate synthase from Oryza sativa requires signals from both light and salt. Plant Sci 162:559–568

    Article  CAS  Google Scholar 

  • Herr AJ, Atkins JF, Gesteland RF (2000) Coupling of open reading frames by translational bypassing. Annu Rev Biochem 69:343–372

    Article  CAS  PubMed  Google Scholar 

  • Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Res 27:297–300

    Article  CAS  PubMed  Google Scholar 

  • Imhoff V, Bourdu R (1973) Formation, d’inositol par les chloroplasts isoles de pois. Phytochemistry 12:331–336

    Article  CAS  Google Scholar 

  • Jarvis P, Soll J (2001) Toc, tic, and chloroplast protein import. Biochim Biophys Acta 1541:64–79

    Article  CAS  PubMed  Google Scholar 

  • Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism. Academic Press, New York, pp 21–132

    Google Scholar 

  • Lackey KH, Pope PM, Johnson MD (2003) Expression of 1l-myo-inositol-1-phosphate synthase in organelles. Plantphysiology 132:2240–2247

    CAS  Google Scholar 

  • Laemmli VK (1970) Cleavages of structural proteins during assembly of the head of bacteriophage T4. Nature 227:680–685

    Article  CAS  PubMed  Google Scholar 

  • Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouzé P, Rombauts S (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30(1):325–327

    Article  CAS  PubMed  Google Scholar 

  • Loewus FA, Loewus MW (1983) Myo-inositol: its biosynthesis and metabolism. Annu Rev Plant Physiol 34:132–161

    Article  Google Scholar 

  • Majee M, Maitra S, Ghosh Dastidar K, Pattnaik S, Chatterjee A, Hait N, Das KP, Majumder AL (2004) A novel salt-tolerant l-myo-inositol 1-phosphate synthase from Porteresia coarctata Tateoka, a halophytic wild rice: molecular cloning, bacterial overexpression, characterization and functional introgression into tobacco conferring salt-tolerance phenotype. J Biol Chem 279(27):28539–28552

    Article  CAS  PubMed  Google Scholar 

  • Majumder AL, Johnson MD, Henry SA (1997) 1l-myo-inositol-1-phosphate synthase. Biochim Biophys Acta 1348:245–256

    CAS  PubMed  Google Scholar 

  • Majumder AL, Chatterjee A, Ghosh Dastidar K, Majee M (2003) Diversification and evolution of l-myo-inositol 1-phosphate synthase. FEBS Letts 553:3–10

    Article  CAS  Google Scholar 

  • Matsufuji S, Matsufuji T, Miyazaki Y, Murakami Y, Atkins J, Gesteland R, Hayashi S (1995) Autoregulatory frameshifting in decoding mammalian ornithine decarboxylase antizyme. Cell 80:51–60

    Article  CAS  PubMed  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Nakagawa H, Ohmiya K, Hattori T (1996) A rice bZIP protein, designated OSBZ8, is rapidly induced by abscisic acid. Plant J 9:217–227

    Article  CAS  PubMed  Google Scholar 

  • Nakai K, Horton P (1996) PSORT: a program for detecting sorting signals in proteins and predicting their subcellular localization. Trends Biochem Sci 24:34–35

    Article  Google Scholar 

  • Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3:418–426

    CAS  PubMed  Google Scholar 

  • Nielsen H, Engelbrecht J, Brunak S, von Heijne G (1997) Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng 10:1–6

    Article  CAS  PubMed  Google Scholar 

  • Nishiguchi R, Takanami M, Oka A (1987) Characterization and sequence determination of the replicator region in the hairy-root-inducing plasmid pRiA4b. Mol Gen Genet 206:1–8

    Article  CAS  Google Scholar 

  • Ohyanagi H, Tanaka T, Sakai H, Shigemoto Y, Yamaguchi K, Habara T, Fujii Y, Antonio BA, Nagamura Y, Imanishi T, Ikeo K, Itoh T, Gojobori T, Sasaki T (2006) The Rice Annotation Project Database (RAP-DB): hub for Oryza sativa ssp. japonica genome information. Nucleic Acids Res 34:D741–D744

    Article  CAS  PubMed  Google Scholar 

  • Rathnam CKM, Edwards GE (1976) Protoplasts as a tool for isolating functional chloroplast from leaves. Plant Cell Physiol 17:177–186

    CAS  Google Scholar 

  • Ratnam SS, Lakshmanan J, Casanova MF, Parthasarathy RN (2009) Identification of myo-inositol-3-phosphate synthase isoforms: characterization, expression and putative role of a 16 kDa γc isoform. J Biol Chem 284:9443–9457

    Article  Google Scholar 

  • Ray Chaudhuri A, Majumder AL (1996) Salinity induced enhancement of l-myo-inositol 1-phosphate synthase in rice (Oryza sativa L.). Plant Cell Environ 19:1337–1342

    Google Scholar 

  • Ray Chaudhuri A, Hait NC, DasGupta S, Bhaduri TJ, Deb R, Majumder AL (1997) l-myo-inositol 1-phosphate synthase from plant sources: characteristics of the chloroplastic and cytosolic enzymes. Plant Physiol 115:727–736

    CAS  Google Scholar 

  • Ribiero S, Golding GB (1998) The mosaic nature of the eukaryotic nucleus. Mol Biol Evol 15:779–788

    Google Scholar 

  • Roy Choudhury S, Roy S, Saha PP, Singh SK, Sengupta DN (2008) Characterization of differential ripening pattern in association with ethylene biosynthesis in the fruits of five naturally occurring banana cultivars and detection of a GCC-box-specific DNA-binding protein. Plant Cell Rep 27:1235–1249

    Article  Google Scholar 

  • Rozas J, Sánchez-DelBarrio JC, Messegyer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497

    Article  CAS  PubMed  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol and Evol 4:406–425

    CAS  Google Scholar 

  • Sherman WR, Stewart M, Zinbo M (1969) Mass spectrometric study on the mechanism of d-glucose 6 phosphate–l-myo-inositol 1-phosphate cyclase. J Biol Chem 244:5703–5708

    CAS  PubMed  Google Scholar 

  • Siemering KR, Golbik R, Sever R, Haseloff J (1996) Mutations that suppress the thermosensitivity of green fluorescent protein. Curr Biol 6:1653–1663

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  CAS  PubMed  Google Scholar 

  • Villarejo A, Buren S, Larsson S, Dejardin A, Monne M, Rudhe C, Karlsson J, Jansson S, Lerouge P, Rolland N, von Heijne G, Grebe M, Bako L, Samuelsson G (2005) Evidence for a protein transported through the secretory pathway en route to the higher plant chloroplast. Nat Cell Biol 7:1224–1231

    Article  PubMed  Google Scholar 

  • Yoshida KT, Wada T, Koyama H, Mizobuchi-Fukuoka R, Naito S (1999) Temporal and spatial patterns of accumulation of the transcript of myo-inositol-1-phosphate synthase and phytin-containing particles during seed development in rice. Plant Physiol 119:65–72

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The work is supported by grants to A.L.M. from the Department of Biotechnology, Government of India. S.R. and A.D.C. thank the Council of Scientific and Industrial Research, Government of India for Research Fellowships. Thanks are due to Dr Anka Hanemanne and Prof Klaus Eschrich, Institute of Biochemistry, Faculty of Medicine, University of Leipzig, Liebigstrasse 16, Leipzig D-04103, Germany, for help in analysis of the MALDI-TOF data.

Author information

Author notes

  1. Sudipta Ray

    Present address: Department of Botany, Centre of Advanced Studies, University of Calcutta, 35, Ballygunge Circular Road, Kolkata, 700019, India

  2. Barunava Patra

    Present address: Kentucky Tobacco Research and Development Centre, University of Kentucky, Lexington, KY, USA

  3. Aparajita Das-Chatterjee

    Present address: Molecular and Cell Biology Department, Goldman School of Dental Medicine, Boston University Medical Center, Boston, MA, 02118, USA

  4. Arnab Ganguli

    Present address: Chembiotek, Block BN, Plot 7, Sector V, Salt lake Electronic Complex, Kolkata, 700091, India

Authors and Affiliations

  1. Plant Molecular and Cellular Genetics, Bose Institute (Centenary Campus), P1/12 CIT Scheme VII M, Kolkata, 700054, India

    Sudipta Ray, Barunava Patra, Aparajita Das-Chatterjee, Arnab Ganguli & Arun Lahiri Majumder

Authors
  1. Sudipta Ray
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Barunava Patra
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Aparajita Das-Chatterjee
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Arnab Ganguli
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Arun Lahiri Majumder
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Arun Lahiri Majumder.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ray, S., Patra, B., Das-Chatterjee, A. et al. Identification and organization of chloroplastic and cytosolic l-myo-inositol 1-phosphate synthase coding gene(s) in Oryza sativa: comparison with the wild halophytic rice, Porteresia coarctata . Planta 231, 1211–1227 (2010). https://doi.org/10.1007/s00425-010-1127-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-010-1127-8

Keywords

Search

Navigation