Plant Molecular Biology

, Volume 24, Issue 1, pp 217–222

Functional loss of all ndh genes in an otherwise relatively unaltered plastid genome of the holoparasitic flowering plant Cuscuta reflexa

  • Gerd Haberhausen
  • Klaus Zetsche
Short Communication

Abstract

We have cloned and sequenced an area of about 9.0 kb of the plastid DNA (ptDNA) from the holoparasitic flowering plant Cuscuta reflexa to investigate the evolutionary response of plastid genes to a reduced selective pressure. The region contains genes for the 16S rRNA, a subunit of a plastid NAD(P)H dehydrogenase (ndhB), three transfer RNAs (trnA, trnI, trnV) as well as the gene coding for the ribosomal protein S7 (rps7). While the other genes are strongly conserved in C. reflexa, the ndhB gene is a pseudogene due to many frameshift mutations. In addition we used heterologous gene probes to identify the other ndh genes encoded by the plastid genome in higher plants. No hybridization signals could be obtained, suggesting that these genes are either lost or strongly altered in the ptDNA of C. reflexa. Together with evidence of deleted genes in the ptDNA of C. reflexa, the plastid genome can be grouped into four classes reflecting a different evolutionary rate in each case. The phylogenetic position of Cuscuta and the significance of ndh genes in the plastid genome of higher plants are discussed.

Key words

Cuscuta reflexa parasitic plant plastid evolution ndh genes 16S rDNA tRNA 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Bennoun P: Evidence for a respiratory chain in the chloroplast. Proc Natl Acad Sci USA 79: 4352–4356 (1982).Google Scholar
  2. 2.
    Bömmer D, Haberhausen G, Zetsche K: A large deletion in the plastid DNA of the holoparasitic flowering plant Cuscuta reflexa concerning two ribosomal proteins (rpl2, rpl23), one transfer RNA (trnI) and an ORF 2280 homologue. Curr Genet 24: 171–176 (1993).CrossRefPubMedGoogle Scholar
  3. 3.
    dePamphilis CW, Palmer JD: Loss of photosynthetic and chlororespiratory genes from the plastid genome of a parasitic flowering plant. Nature 348: 337–339 (1990).CrossRefPubMedGoogle Scholar
  4. 4.
    Ellersiek U, Steinmüller K: Cloning and transcription analysis of the ndh (A-I-G-E) gene cluster and the ndhD gene of the cyanobacterium Synechocystic sp. PCC6803. Plant Mol Biol 20: 1097–1110 (1992).CrossRefPubMedGoogle Scholar
  5. 5.
    Godde D, Trebst A: NADH as electron donor for the photosynthetic membrane of Chlamydomonas reinhardii. Arch Microbiol 127: 245–252 (1980).Google Scholar
  6. 6.
    Haberhausen G, Valentin K, Zetsche K: Organization and sequence of photosynthetic genes from the plastid genome of the holoparasitic flowering plant Cuscuta reflexa. Mol Gen Genet 232: 154–161 (1992).CrossRefPubMedGoogle Scholar
  7. 7.
    Hiratsuka J, Shimada H, Whittier R, Ishibashi T, Sakamoto M, Mori M, Kondo C, Honji Y, Sun CR, Meng BY, Li YQ, Kanno A, Nishizawa Y, Hirai A, Shinozaki K, Sugiura M: The complete sequence of the rice (Oryza sativa) chloroplast genome: intermolecular recombination between distinct tRNA genes accounts for a major plastic DNA inversion during the evolution of the cereals. Mol Gen Genet 217: 185–194 (1986).Google Scholar
  8. 8.
    Machado MA, Zetsche K: A structural, functional and molecular analysis of plastids of the holoparasites Cuscuta reflexa and Cuscuta europaea. Planta 181: 91–96 (1990).CrossRefGoogle Scholar
  9. 9.
    Matsubayashi T, Wakasugi T, Shinozaki K, Yamagushi-Shinozaki K, Zaita N, Hidaka T, Meng BY, Ohto C, Tanaka M, Kato A, Maruyama T, Sugiura M: Six chloroplast genes (ndhA-F) homologous to human mitochondrial genes encoding components of the respiratory chain NADH dehydrogenase are actively expressed: determination of splice sites in ndhA and ndhB pre-mRNAs. Mol Gen Genet 210: 385–393 (1987).CrossRefPubMedGoogle Scholar
  10. 10.
    Ohyama K, Fukuzawa H, Kohchi T, Shirai H, Sano T, Sano S, Umesono K, Shiki Y, Takeuchi M, Chang Z, Aota S, Inokuchi H, Ozeki H: Chloroplast gene organization deduced from complete sequence of liverwort Marchantia polymorpha chloroplast DNA. Nature 322: 572–574 (1986).Google Scholar
  11. 11.
    Palmer JD: Comparative organization of chloroplast genomes. Annu Rev Genet 19: 325–354 (1985).CrossRefPubMedGoogle Scholar
  12. 12.
    Peltier G, Schmidt GW: Chlororespiration: an adaption to nitrogen deficiency in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 88: 4791–4795 (1991).PubMedGoogle Scholar
  13. 13.
    Schwarz ZS, Koessel H: The primary structure of 16S rDNA from Zea mays chloroplast is homologous to E. coli 16S rRNA. Nature 283: 739–742 (1980).Google Scholar
  14. 14.
    shinozaki K, Ohme M, Tanaka T, Wakasugi T, Hayashida N, Matsubayashi T, Zaita N, Chunwongse J, Obokata J, Yamaguchi-Shinozaki K, Ohto C, Torazawa K, Meng BY, Sugita M, Deno H, Kamogashira T, Yamada K, Kusuda J, Takaiwa F, Kato A, Tohdoh N, Shimada H, Sugiura M: The complete nucleotide sequence of the tobacco chloroplast geneme: its gene organization and expression. EMBO J 5: 2043–2049 (1986).Google Scholar
  15. 15.
    Sugiura M: The chloroplast genome. Plant Mol Biol 19: 149–168 (1992).PubMedGoogle Scholar
  16. 16.
    Whelan J, Young S, Day DA: Cloning of ndhK from soybean chloroplasts using antibodies raised to mitochondrial complex I. Plant Mol Biol 20: 887–895 (1992).PubMedGoogle Scholar
  17. 17.
    Wimpee CF, Morgan R, Wrobel R: An aberrant plastid ribosomal RNA gene cluster in the root parasite Conopholis americana. Plant Mol Biol 18: 275–285 (1992).PubMedGoogle Scholar
  18. 18.
    Wimpee CF, Morgan R, Wrobel RL: Loss of transfer RNA genes from the plastid 16S–23S ribosomal RNA gene spacer in a parasitic plant. Curr Genet 21: 417–422 (1992).PubMedGoogle Scholar
  19. 19.
    Wolfe KH, Katz-Downie DS, Morden CW, Palmer JD: Evolution of the plastid ribosomal RNA operon in a nongreen parasitic plant: accelerated sequence evolution, altered promoter structure, and tRNA pseudogenes. Plant Mol Biol 18: 1037–1048 (1992).PubMedGoogle Scholar
  20. 20.
    Wolfe KH, Morden CW, Palmer JD: Function and evolution of a minimal plastid genome from a nonphotosynthetic parasitic plant. Proc Natl Acad Sci USA 89: 10648–10652 (1992).PubMedGoogle Scholar

Copyright information

© Kluwer Academic Publishers 1994

Authors and Affiliations

  • Gerd Haberhausen
    • 1
  • Klaus Zetsche
    • 1
  1. 1.Institut für PflanzenphysiologieJustus Liebig UniversitätGiessenGermany
  2. 2.Institut für HumangenetikJustus Liebig UniversitätGiessenGermany

Personalised recommendations