Search tips
Search criteria 


Logo of molcellbPermissionsJournals.ASM.orgJournalMCB ArticleJournal InfoAuthorsReviewers
Mol Cell Biol. 1993 December; 13(12): 7349–7357.
PMCID: PMC364805

Unidirectional dominance of cytoplasmic inheritance in two genetic crosses of Plasmodium falciparum.


Malarial parasites have two highly conserved cytoplasmic DNA molecules: a 6-kb tandemly arrayed DNA that has characteristics of a mitochondrial genome, and a 35-kb circular DNA that encodes functions commonly found in chloroplasts. We examined the inheritance pattern of these elements in two genetic crosses of Plasmodium falciparum clones. Parent-specific oligonucleotide probes and single-strand conformation polymorphism analysis identified single nucleotide changes that distinguished the parental 6- and 35-kb DNA molecules in the progeny. In all 16 independent recombinant progeny of a cross between a Central American clone, HB3, and a Southeast Asian clone, Dd2, the 6- and 35-kb DNAs were inherited from the Dd2 parent. In all nine independent recombinant progeny of a cross between clone HB3 and a likely African clone, 3D7, the 6-kb DNA was inherited from the 3D7 parent. Inheritance of cytoplasmic genomes of the Dd2 and 3D7 parents was, therefore, dominant over that of the HB3 parent. Cytoplasmic DNA molecules were found almost exclusively in the female gametes of malarial parasites; hence, clone HB3 did not appear to have served as a maternal parent for the progeny of two crosses. Defective differentiation into male gametes by clone Dd2 is likely to be a reason for the cytoplasmic inheritance pattern seen in the HB3 x Dd2 cross. However, incompetence of male or female gametes is unlikely to explain the uniparental dominance in recombinant progeny of the HB3 x 3D7 cross, since both parents readily self-fertilized and completed the malaria life cycle on their own. Instead, the data suggest unidirectional parental incompatibility in cross-fertilization of these malarial parasites, where a usually cosexual parental clone can participate only as a male or as a female. Such an incompatibility may be speculated as indicating an early phase of reproductive isolation of P. falciparum clones from different geographical regions.

Full text

Full text is available as a scanned copy of the original print version. Get a printable copy (PDF file) of the complete article (2.4M), or click on a page image below to browse page by page. Links to PubMed are also available for Selected References.

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Aldritt SM, Joseph JT, Wirth DF. Sequence identification of cytochrome b in Plasmodium gallinaceum. Mol Cell Biol. 1989 Sep;9(9):3614–3620. [PMC free article] [PubMed]
  • Boer PH, Gray MW. Scrambled ribosomal RNA gene pieces in Chlamydomonas reinhardtii mitochondrial DNA. Cell. 1988 Nov 4;55(3):399–411. [PubMed]
  • Borst P, Nussenzweig V. Molecular parasitology at Woods Hole. Cell. 1992 Dec 11;71(6):895–899. [PubMed]
  • Boynton JE, Harris EH, Burkhart BD, Lamerson PM, Gillham NW. Transmission of mitochondrial and chloroplast genomes in crosses of Chlamydomonas. Proc Natl Acad Sci U S A. 1987 Apr;84(8):2391–2395. [PubMed]
  • Carter R, Gwadz RW, McAuliffe FM. Plasmodium gallinaceum: transmission-blocking immunity in chickens. I. Comparative immunogenicity of gametocyte- and gamete-containing preparations. Exp Parasitol. 1979 Apr;47(2):185–193. [PubMed]
  • Creasey AM, Ranford-Cartwright LC, Moore DJ, Williamson DH, Wilson RJ, Walliker D, Carter R. Uniparental inheritance of the mitochondrial gene cytochrome b in Plasmodium falciparum. Curr Genet. 1993;23(4):360–364. [PubMed]
  • dePamphilis CW, Palmer JD. Loss of photosynthetic and chlororespiratory genes from the plastid genome of a parasitic flowering plant. Nature. 1990 Nov 22;348(6299):337–339. [PubMed]
  • Dore E, Frontali C, Forte T, Fratarcangeli S. Further studies and electron microscopic characterization of Plasmodium berghei DNA. Mol Biochem Parasitol. 1983 Aug;8(4):339–352. [PubMed]
  • Duffy PE, Pimenta P, Kaslow DC. Pgs28 belongs to a family of epidermal growth factor-like antigens that are targets of malaria transmission-blocking antibodies. J Exp Med. 1993 Feb 1;177(2):505–510. [PMC free article] [PubMed]
  • Feagin JE, Werner E, Gardner MJ, Williamson DH, Wilson RJ. Homologies between the contiguous and fragmented rRNAs of the two Plasmodium falciparum extrachromosomal DNAs are limited to core sequences. Nucleic Acids Res. 1992 Feb 25;20(4):879–887. [PMC free article] [PubMed]
  • Gajadhar AA, Marquardt WC, Hall R, Gunderson J, Ariztia-Carmona EV, Sogin ML. Ribosomal RNA sequences of Sarcocystis muris, Theileria annulata and Crypthecodinium cohnii reveal evolutionary relationships among apicomplexans, dinoflagellates, and ciliates. Mol Biochem Parasitol. 1991 Mar;45(1):147–154. [PubMed]
  • Gardner MJ, Bates PA, Ling IT, Moore DJ, McCready S, Gunasekera MB, Wilson RJ, Williamson DH. Mitochondrial DNA of the human malarial parasite Plasmodium falciparum. Mol Biochem Parasitol. 1988 Oct;31(1):11–17. [PubMed]
  • Gardner MJ, Feagin JE, Moore DJ, Spencer DF, Gray MW, Williamson DH, Wilson RJ. Organisation and expression of small subunit ribosomal RNA genes encoded by a 35-kilobase circular DNA in Plasmodium falciparum. Mol Biochem Parasitol. 1991 Sep;48(1):77–88. [PubMed]
  • Gardner MJ, Williamson DH, Wilson RJ. A circular DNA in malaria parasites encodes an RNA polymerase like that of prokaryotes and chloroplasts. Mol Biochem Parasitol. 1991 Jan;44(1):115–123. [PubMed]
  • Joseph JT, Aldritt SM, Unnasch T, Puijalon O, Wirth DF. Characterization of a conserved extrachromosomal element isolated from the avian malarial parasite Plasmodium gallinaceum. Mol Cell Biol. 1989 Sep;9(9):3621–3629. [PMC free article] [PubMed]
  • Kilejian A. Circular mitochondrial DNA from the avian malarial parasite Plasmodium lophurae. Biochim Biophys Acta. 1975 May 16;390(3):276–284. [PubMed]
  • Nijhout MM. Plasmodium gallinaceum: exflagellation stimulated by a mosquito factor. Exp Parasitol. 1979 Aug;48(1):75–80. [PubMed]
  • Orita M, Iwahana H, Kanazawa H, Hayashi K, Sekiya T. Detection of polymorphisms of human DNA by gel electrophoresis as single-strand conformation polymorphisms. Proc Natl Acad Sci U S A. 1989 Apr;86(8):2766–2770. [PubMed]
  • Ossorio PN, Sibley LD, Boothroyd JC. Mitochondrial-like DNA sequences flanked by direct and inverted repeats in the nuclear genome of Toxoplasma gondii. J Mol Biol. 1991 Dec 5;222(3):525–536. [PubMed]
  • Peterson DS, Walliker D, Wellems TE. Evidence that a point mutation in dihydrofolate reductase-thymidylate synthase confers resistance to pyrimethamine in falciparum malaria. Proc Natl Acad Sci U S A. 1988 Dec;85(23):9114–9118. [PubMed]
  • Sanger F, Nicklen S, Coulson AR. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. [PubMed]
  • Scholtyseck E, Mehlhorn H, Hammond DM. Electron microscope studies of microgametogenesis in Coccidia and related groups. Z Parasitenkd. 1972;38(2):95–131. [PubMed]
  • Siemeister G, Buchholz C, Hachtel W. Genes for ribosomal proteins are retained on the 73 kb DNA from Astasia longa that resembles Euglena chloroplast DNA. Curr Genet. 1990 Dec;18(5):457–464. [PubMed]
  • Siemeister G, Hachtel W. Organization and nucleotide sequence of ribosomal RNA genes on a circular 73 kbp DNA from the colourless flagellate Astasia longa. Curr Genet. 1990 May;17(5):433–438. [PubMed]
  • Sinden RE, Canning EU, Bray RS, Smalley ME. Gametocyte and gamete development in Plasmodium falciparum. Proc R Soc Lond B Biol Sci. 1978 Jun 5;201(1145):375–399. [PubMed]
  • Sinden RE, Canning EU, Spain B. Gametogenesis and fertilization in Plasmodium yoelii nigeriensis: a transmission electron microscope study. Proc R Soc Lond B Biol Sci. 1976 Mar 30;193(1110):55–76. [PubMed]
  • Suplick K, Akella R, Saul A, Vaidya AB. Molecular cloning and partial sequence of a 5.8 kilobase pair repetitive DNA from Plasmodium falciparum. Mol Biochem Parasitol. 1988 Sep;30(3):289–290. [PubMed]
  • Suplick K, Morrisey J, Vaidya AB. Complex transcription from the extrachromosomal DNA encoding mitochondrial functions of Plasmodium yoelii. Mol Cell Biol. 1990 Dec;10(12):6381–6388. [PMC free article] [PubMed]
  • Suzuki Y, Orita M, Shiraishi M, Hayashi K, Sekiya T. Detection of ras gene mutations in human lung cancers by single-strand conformation polymorphism analysis of polymerase chain reaction products. Oncogene. 1990 Jul;5(7):1037–1043. [PubMed]
  • Vaidya AB, Akella R, Suplick K. Sequences similar to genes for two mitochondrial proteins and portions of ribosomal RNA in tandemly arrayed 6-kilobase-pair DNA of a malarial parasite. Mol Biochem Parasitol. 1989 Jun 15;35(2):97–107. [PubMed]
  • Vaidya AB, Arasu P. Tandemly arranged gene clusters of malarial parasites that are highly conserved and transcribed. Mol Biochem Parasitol. 1987 Jan 15;22(2-3):249–257. [PubMed]
  • Vaidya AB, Lashgari MS, Pologe LG, Morrisey J. Structural features of Plasmodium cytochrome b that may underlie susceptibility to 8-aminoquinolines and hydroxynaphthoquinones. Mol Biochem Parasitol. 1993 Mar;58(1):33–42. [PubMed]
  • Vermeulen AN, Ponnudurai T, Beckers PJ, Verhave JP, Smits MA, Meuwissen JH. Sequential expression of antigens on sexual stages of Plasmodium falciparum accessible to transmission-blocking antibodies in the mosquito. J Exp Med. 1985 Nov 1;162(5):1460–1476. [PMC free article] [PubMed]
  • Walker-Jonah A, Dolan SA, Gwadz RW, Panton LJ, Wellems TE. An RFLP map of the Plasmodium falciparum genome, recombination rates and favored linkage groups in a genetic cross. Mol Biochem Parasitol. 1992 Apr;51(2):313–320. [PubMed]
  • Walliker D, Quakyi IA, Wellems TE, McCutchan TF, Szarfman A, London WT, Corcoran LM, Burkot TR, Carter R. Genetic analysis of the human malaria parasite Plasmodium falciparum. Science. 1987 Jun 26;236(4809):1661–1666. [PubMed]
  • Waters AP, Higgins DG, McCutchan TF. Plasmodium falciparum appears to have arisen as a result of lateral transfer between avian and human hosts. Proc Natl Acad Sci U S A. 1991 Apr 15;88(8):3140–3144. [PubMed]
  • Wellems TE, Panton LJ, Gluzman IY, do Rosario VE, Gwadz RW, Walker-Jonah A, Krogstad DJ. Chloroquine resistance not linked to mdr-like genes in a Plasmodium falciparum cross. Nature. 1990 May 17;345(6272):253–255. [PubMed]
  • Wellems TE, Walker-Jonah A, Panton LJ. Genetic mapping of the chloroquine-resistance locus on Plasmodium falciparum chromosome 7. Proc Natl Acad Sci U S A. 1991 Apr 15;88(8):3382–3386. [PubMed]
  • Williamson DH, Wilson RJ, Bates PA, McCready S, Perler F, Qiang BU. Nuclear and mitochondrial DNA of the primate malarial parasite Plasmodium knowlesi. Mol Biochem Parasitol. 1985 Feb;14(2):199–209. [PubMed]
  • Wilson RJ, Fry M, Gardner MJ, Feagin JE, Williamson DH. Subcellular fractionation of the two organelle DNAs of malaria parasites. Curr Genet. 1992 Apr;21(4-5):405–408. [PubMed]
  • Wilson RJ, Gardner MJ, Feagin JE, Williamson DH. Have malaria parasites three genomes? Parasitol Today. 1991 Jun;7(6):134–136. [PubMed]

Articles from Molecular and Cellular Biology are provided here courtesy of American Society for Microbiology (ASM)