Skip to main content
SpringerLink
Log in

Rice mitochondrial genome contains a rearranged chloroplast gene cluster

  • Published:
Molecular and General Genetics MGG Aims and scope Submit manuscript

Summary

We have previously reported the isolation and partial sequence analysis of a rice mitochondrial DNA fragment (6.9 kb) which contains a transferred copy of a chloroplast gene cluster coding for the large subunit of ribulose-1,5-bisphosphate carboxylase (rbcL), β and ε subunits of ATPase (atpB and atpE), methionine tRNA (trnM) and valine tRNA (trnV). We have now completely sequenced this 6.9 kb fragment and found it to also contain a sequence homologous to the chloroplast gene coding for the ribosomal protein L2 (rpl2), beginning at a site 430 bp downstream from the termination codon of rbcL. In the chloroplast genome, two copies of rpl2 are located at distances of 20 kb and 40 kb, respectively, from rbcL. We have sequenced these two copies of rice chloroplast rpl2 and found their sequences to be identical. In addition, a 151 bp sequence located upstream of the chloroplast rpl2 coding region is also found in the 3′ noncoding region of chloroplast rbcL and other as yet undefined locations in the rice chloroplast genome. Hybridization analysis revealed that this 151 bp repeat sequence identified in rice is also present in several copies in 11 other plant species we have examined. Findings from these studies suggest that the translocation of rpl2 to the rbcL gene cluster found in the rice mitochondrial genome might have occurred through homologous recombination between the 151 bp repeat sequence present in both rpl2 and rbcL.

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

Similar content being viewed by others

References

  • Bowman CM, Dyer TA (1986) The location and possible evolutionary significance of small dispersed repeats in wheat ctDNA. Curr Genet 10:931–941

    Google Scholar 

  • Chen K, Wildman SG, Smith HH (1977) Chloroplast DNA distribution in parasexual hybrids as shown by polypeptide composition of fraction I protein. Proc Natl Acad Sci USA 74:5109–5112

    Google Scholar 

  • Day A, Ellis THN (1984) Chloroplast DNA deletions associated with wheat plants regenerated from pollen: possible basis for maternal inheritance of chloroplasts. Cell 39:359–368

    Google Scholar 

  • Dover GA, Brown S, Coen E, Dallas J, Strachan T, Trick M (1982) In: Dover GA, Flavell RB (eds) Genome evolution. Academic Press, London New York, pp 343–372

    Google Scholar 

  • Flick CE, Evans Da (1982) Evolution of cytoplasmic segregation in somatic hybrids of Nicotiana: tentoxin sensitivity. J Hered 73:264–266

    Google Scholar 

  • Fluhr R, Aviv D, Edelman M, Galun E (1983) Cybrids containing mixed and sorted-out chloroplasts following interspecific somatic fusions in Nicotiana. Theor Appl Genet 65:289–294

    Google Scholar 

  • Fluhr R, Aviv D, Galun E, Edelman M (1984) Generation of heteroplastidic Nicotiana cybrids by protoplasts fusion: analysis for plastid recombinant types. Theor Appl Genet 67:491–497

    Google Scholar 

  • Howe CJ (1985) The endpoints of an inversion in wheat chloroplast DNA are associated with short repeated sequences containing homology to att-lambda. Curr Genet 10:139–145

    Google Scholar 

  • Jeffreys A, Wilson V, Thein SW (1985) Hypervariable ‘minisatellite’ regions in human DNA. Nature London 314:67–73

    Google Scholar 

  • Kao TH, Moon E, Wu R (1984) Cytochrome oxidase subunit II gene of rice has an insertion sequence within the intron. Nucleic Acids Res 12:7305–7315

    Google Scholar 

  • Kolodner R, Tewari KK (1979) Inverted repeats in chloroplast DNA from higher plants. Proc Natl Acad Sci USA 76:41–45

    Google Scholar 

  • Lee RW, Lemieux C (1986) Nonreciprocal recombination between alleles of the chloroplast 23S rRNA gene in interspecific Chlamydomonas crosses. Genetics 113:589–600

    Google Scholar 

  • Lemieux C, Lee RW (1987) Nonreciprocal recombination between alleles of the chloroplast 23S rRNA gene in interspecific Chlamydomonas crosses. Proc Natl Acad Sci USA 84:4166–4170

    Google Scholar 

  • Lemieux C, Turmel M, Lee RW (1981) Physical evidence for recombination of chloroplast DNA in hybrid progeny of Chlamydomonas-eugametos and Chlamydomonas-moewusii. Curr Genet 3:97–103

    Google Scholar 

  • Lonsdale DM, Hodge TP, Favron CM-R (1984) The physical map and organization of the mitochondrial genome from the fertile cytoplasm of maize. Nucleic Acids Res 12:9249–9261

    Google Scholar 

  • Maliga P, Lorz H, Lazar G, Nagy F (1982) Cytoplast-protoplast fusion for interspecific chloroplast transfer in Nicotiana. Mol Gen Genet 185:211–215

    Google Scholar 

  • Medgyesy P, Fejes E, Maliga P (1985) Interspecific chloroplast recombination in a Nicotiana somatic hybrid. Proc Natl Acad Sci USA 82:6960–6964

    Google Scholar 

  • Mets LJ, Geist LJ (1983) Linkage of known chloroplast gene mutation to the uniparental genome of Chlamydomonas reinhardii. Genetics 105:559–579

    Google Scholar 

  • Michalowski C, Breunig KD, Bohnert HJ (1987) Points of rearrangements between plastid chromosomes: location of protein coding regions on broad bean chloroplast DNA. Curr Genet 11:265–274

    Google Scholar 

  • Moon E, Kao TH, Wu R (1987) Rice chloroplast DNA molecules are heterogeneous as revealed by DNA sequences of a cluster of genes. Nucleic Acids Res 15:611–630

    Google Scholar 

  • Moon E, Wu R (1988) Organization and nucleotide sequence of genes at the two junctions between the two inverted repeats and the large single-copy region in the rice chloroplast genome. Gene (in press)

  • Mubumbila M, Crouse EJ, Weil JH (1984) Transfer RNAs and tRNA genes of Vicia faba chloroplasts. Curr Genet 8:379–385

    Google Scholar 

  • Palmer JD (1983) Chloroplast DNA exists in two orientations. Nature 301:92–93

    Google Scholar 

  • Palmer JD (1985) Evolution of chloroplast and mitochondrial DNA in plants and algae. In: MacIntyre RJ (ed) Molecular evolutionary genetics. Plenum Press, New York, pp 373–402

    Google Scholar 

  • Palmer JD, Thompson WF (1981) Rearrangements in the chloroplast genomes of mung bean and pea. Proc Natl Acad Sci USA 78:5533–5537

    Google Scholar 

  • Palmer JD, Thompson WF (1982) Chloroplast DNA rearrangements are more frequent when a large inverted repeat sequence is lost. Cell 29:537–550

    Google Scholar 

  • Palmer JD, Osorio B, Watson JC, Edwards H, Dodd J, Thompson WF (1984) Evolutionary aspects of chloroplast genome expression and organization. In: Thornber TP, Staehelin A, Hallick RB (eds) Biosynthesis of the photosynthetic apparatus: Molecular biology, development and regulation. Liss (UCLA Symposia on Molecular and Cellular Biology, New Series, vol 14), New York, pp 273–283

    Google Scholar 

  • Palmer JD, Jorgensen RA, Thompson WF (1985) Chloroplast DNA variation and evolution in Pisum: patterns of change and phylogenic analysis. Genetics 109:195–213

    Google Scholar 

  • Palmer JD, Osorio B, Aldrich J, Thompson WF (1987a) Chloroplast DNA evolution among legumes: loss of a large inverted repeat occurred prior to other sequence rearrangements. Curr Genet 11:275–286

    Google Scholar 

  • Palmer JD, Nugent JM, Herbon LA (1987b) Unusual structure of geranium chloroplast DNA: a triple-sized inverted repeat, extensive gene duplications, multiple inversions, and two repeat families. Proc Natl Acad Sci USA 84:769–773

    Google Scholar 

  • Sager R, Ramanis Z (1970) A genetic map of non-mendelian genes in Chlamydomonas. Proc Natl Acad Sci USA 65:593–600

    Google Scholar 

  • Sager R (1977) Genetic analysis of chloroplast DNA in Chlamydomonas. Adv Genet 19:287–340

    Google Scholar 

  • Scherer S, Davis RW (1980) Recombination of dispersed repeated DNA sequences in yeast. Science 209:1380–1384

    Google Scholar 

  • Schiller B, Herrmann RG, Melchers G (1982) Restriction endonuclease analysis of plastid DNA from tomato, potato, and some of their somatic hybrids. Mol Gen Genet 186:453–459

    Google Scholar 

  • Stern DB, Palmer JD (1984) Extensive and widespread homologies between mitochondrial DNA and chloroplast DNA of plants. Proc Natl Acad Sci USA 81:1946–1950

    Google Scholar 

  • Tanaka M, Wakasugi T, Sugita M, Shinozaki K, Sugiura M (1986) Genes for the eight ribosomal proteins are clustered on the chloroplast genome of tobacco (Nicotiana tabacum) similarly to the S10 and spc operons of Escherichia coli. Proc Natl Acad Sci USA 83:6030–6034

    Google Scholar 

  • Whitfeld PR, Bottomley W (1983) Organization and structure of chloroplast genes. Ann Rev Plant Physiol 34:279–310

    Google Scholar 

  • Zurawski G, Bottomley W, Whitfeld PR (1984) Junctions of the large single copy region and the inverted repeats in Spinacea oleracea and Nicotiana debneyi chloroplast DNA: sequence of the genes for the β and ε subunits of ATP synthase from the pea chloroplasts. Nucleic Acids Res 12:6547–6558

    Google Scholar 

  • Zurawski G, Clegg MT (1987) Evolution of higher-plant chloroplast DNA-encoded genes: implications for structure-function and phylogenetic studies. Ann Rev Plant Physiol 38:391–418

    Google Scholar 

Download references

Author information

Author notes

  1. Teh-Hui Kao

    Present address: Department of Molecular and Cell Biology, 403 Althouse Laboratory, The Pennsylvania State University, 16802, University Park, PA, USA

Authors and Affiliations

  1. Section of Biochemistry, Molecular and Cell Biology, Cornell University, 14853, Ithaca, NY, USA

    Eunpyo Moon, Teh-Hui Kao & Ray Wu

Authors
  1. Eunpyo Moon
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Teh-Hui Kao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ray Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Communicated by G.R. Fink

Rights and permissions

Reprints and permissions

About this article

Cite this article

Moon, E., Kao, TH. & Wu, R. Rice mitochondrial genome contains a rearranged chloroplast gene cluster. Mol Gen Genet 213, 247–253 (1988). https://doi.org/10.1007/BF00339588

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00339588

Key words

Search

Navigation