Advertisement

Current Genetics

, Volume 26, Issue 3, pp 263–268 | Cite as

An atpE-specific promoter within the coding region of the atpB gene in tobacco chloroplast DNA

  • Sanjay Kapoor
  • Tatsuya Wakasugi
  • Hiroshi Deno
  • Masahiro Sugiura
Original Articles

Abstract

The atpB and atpE genes encode β and ɛ subunits, respectively, of chloroplast ATP synthase and are co-transcribed in the plant species so far studied. In tobacco, an atpB gene-specific probe hybridizes to 2.7- and 2.3-kb transcripts. In addition to these, a probe from the atpE coding region hybridizes also to a 1.0-kb transcript. The 5′ end of the atpE-specific transcript has been mapped 430/431 nt upstream of the atpE translation initiation site, within the coding region of the atpB gene. In-vitro capping revealed that this transcript results from a primary transcriptional event and is also characterized by -10 and-35 canonical sequences in the 5′ region. It has been found to share a common 3′ end with the bi-cistronic transcripts that has been mapped within the coding region of the divergently transcribed trnM gene, approximately 236 nt downstream from the atpE termination codon. Interestingly, this transcript accumulates only in leaves and not in proplastid-containing cultured (BY-2) cells, indicating that, unless it is preferentially degraded in BY-2 cells, its expression might be transcriptionally controlled.

Key words

atpE Chloroplast transcript Internal promoter Nicotiana tabacum 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K (1989) Current protocols in molecular biology. Greene Publishing Associates and Wiley Interscience, New YorkGoogle Scholar
  2. Bird CR, Koller B, Auffret B, Huttly AK, Howe CJ, Dyer TA, Gray JC (1985) The wheat chloroplast gene for CF0 subunit I of ATP synthase contains a large intron. EMBO J 4:1381–1388Google Scholar
  3. Chen L-J, Rogers SA, Benett DC, Hu M-C, Orozco EM Jr (1990) An in-vitro transcription termination system to analyze chloroplast promoters: identification of multiple promoters for the spinach atpB gene. Curr Genet 17:55–64Google Scholar
  4. Cozens AL, Walker JE, Phillips AL, Huttly AK, Gray JC (1986) A sixth subunit of ATP synthase, an F0 component, is encoded in the pea chloroplast genome. EMBO J 5:217–222Google Scholar
  5. Deno H, Kato A, Shinozaki K, Sugiura M (1982) Nucleotide sequence of tobacco chloroplast genes for elongator tRNAMet and tRNAVal (UAC): the tRNAVal (UAC) gene contains a long intron. Nucleic Acids Res 10:7511–7520Google Scholar
  6. Gamble PE, Sexton TB, Mullet JE (1988) Light-dependent changes in psbD and psbC transcripts of barley chloroplasts: accumulation of two transcripts maintain psbD and psbC translation capability in mature chloroplasts. EMBO J 7:1289–1297Google Scholar
  7. Gatenby AA, Rothstein SJ, Nomura M (1989) Translational coupling of the maize chloroplast atpB and atpE genes. Proc Natl Acad Sci USA 86:4066–4070Google Scholar
  8. Haley J, Bogorad L (1990) Alternative promoters are used for genes within the maize chloroplast polycistronic transcription unit. Plant Cell 2:323–333Google Scholar
  9. Hudson GS, Mason JG, Holton TA, Koller B, Cox GB, Whitfeld PR, Bottomley W (1987) A gene cluster in the spinach and pea chloroplast genomes encoding one CF1 and three CF0 subunits of the H+-ATP synthase complex and ribosomal protein S2. J Mol Biol 196:283–298Google Scholar
  10. Kanno A, Hirai A (1993) A transcription map of the chloroplast genome from rice (Oryza sativa). Curr Genet 23:166–174Google Scholar
  11. Kapoor S, Maheshwari SC, Tyagi AK (1993) Organ-specific expression of plastid-encoded genes in rice involves both quantitative and qualitative changes in mRNAs. Plant Cell Physiol 34:943–947Google Scholar
  12. Kennell JC, Pring DR (1989) Initiation and processing of atp6, T-urf13 and the ORF221 transcript from mitochondria of T-cytoplasm maize. Mol Gen Genet 216:16–24Google Scholar
  13. Logemann J, Schell J, Willmitzer L (1987) Improved method for the isolation of RNA from plant tissues. Anal Biochem 163:16–20Google Scholar
  14. Meng B-Y, Wakasugi T, Sugiura M (1991) Two promoters within the psbK-psbI-trnG gene cluster in tobacco chloroplast DNA. Curr Genet 20:259–264Google Scholar
  15. Mullet JE (1993) Dynamic regulation of chloroplast transcription. Plant Physiol 103:309–313Google Scholar
  16. Mullet JE, Orozco Jr. EM, Chua N-H (1985) Multiple transcripts for higher-plant rbcL and atpB genes and localization of the transcription initiation site of the rbcL gene. Plant Mol Biol 4:39–54Google Scholar
  17. Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assay with tobacco tissue cultures. Physiol Plant 15:473–497Google Scholar
  18. Nagata T, Nemoto Y, Hasezawa S (1992) Tobacco BY-2 cell line as the “HeLa” cell in the cell biology of higher plants. Int Rev Cytol 132:1–30Google Scholar
  19. Orozco EM Jr, Chen L-J, Eilers RJ (1990) The divergently-transcribed rbcL and atpB genes of tobacco plastid DNA are separated by nineteen base pairs. Curr Genet 17:65–71Google Scholar
  20. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, New YorkGoogle Scholar
  21. Sexton TB, Christopher DA, Mullet JE (1990) Light-induced switch in barley psbD-psbC promoter utilization: a novel mechanism regulating chloroplast gene expression. EMBO J 9:4485–4494Google Scholar
  22. Shinozaki K, Sugiura M (1982) Sequence of the intercistronic region between the ribulose-1,5-bisphosphate carboxylase/oxygenase large subunit and the coupling factor β subunit gene. Nucleic Acids Res 10:4923–4934Google Scholar
  23. Shinozki K, Deno H, Kato A, Sugiura M (1983) Overlap and cotranscription of the genes for the beta and epsilon subunits of tobacco chloroplast ATPase. Gene 24:147–155Google Scholar
  24. Shinozaki K, Ohme M, Tanaka T, Wakasugi T, Hayashida N, Matsubayashi T, Zaita N, Chunwongse J, Obokata J, Shinozaki KY, Ohto C, Torazawa K, Meng B-Y, Sugita M, Deno H, Kamogashira T, Yamada K, Kusuda J, Takaiwa F, Kato A, Tohdoh N, Shimada H, Sugiura M (1986) The complete nucleotide sequence of the tobacco chloroplast genome: its gene organization and expression. EMBO J 5:2043–2049Google Scholar
  25. Sugiura M, Shinozaki K, Zaita N, Kusuda M, Kumano M (1986) Clone bank of the tobacco (Nicotiana tabacum) chloroplast genome as a set of overlapping restriction endonuclease fragments:mapping of eleven ribosomal protein genes. Plant Sci 44: 211–216Google Scholar
  26. Sugiura M (1992) The chloroplast genome. Plant Mol Biol 19:149–168Google Scholar
  27. Vera A, Sugiura M (1992) Combination of in-vitro capping and ribonuclease protection improves the detection of transcription start sites in chloroplasts. Plant Mol Biol 19:309–311Google Scholar
  28. Vera A, Matsubayashi T, Sugiura M (1992) Active transcription from a promoter positioned within the coding region of a divergently-oriented gene: the tobacco chloroplast rpl32 gene. Mol Gen Genet 233:151–156Google Scholar
  29. Westhoff P, Alt J, Nelson N, Herrmann RG (1985) Genes and transcripts for the ATP synthase CF0 subunit I and II from spinach thylakoid membranes. Mol Gen Genet 199:290–299Google Scholar
  30. Yao WB, Meng B-Y, Tanaka M, Sugiura M (1989) An additional promoter within the protein-coding region of the psbD-psbC gene cluster in tobacco chloroplast DNA. Nucleic Acids Res 17:9583–9591Google Scholar
  31. Zurawski G, Bottomley W, Whitfeld PR (1982) Structure of the genes for the β and ε subunits of spinach chloroplast ATPase indicate a dicistronic mRNA and an overlapping translation stop/start signal. Proc Natl Acad Sci USA 79:6260–6264Google Scholar

Copyright information

© Springer-Verlag 1994

Authors and Affiliations

  • Sanjay Kapoor
    • 1
  • Tatsuya Wakasugi
    • 1
  • Hiroshi Deno
    • 1
  • Masahiro Sugiura
    • 1
  1. 1.Center for Gene ResearchNagoya UniversityNagoyaJapan

Personalised recommendations