Skip to main content
Log in

Epifluorescent microscopic studies on the mechanism of preferential destruction of chloroplast nucleoids of male origin in young zygotes ofChlamydomonas reinhardtii

  • Published:
Protoplasma Aims and scope Submit manuscript

Summary

The studies on the kinetics of nucleoid destruction reported here showed that destruction of chloroplast nucleoids (ct nucleoids) of male origin began to occur at about 30 minutes after mixing of male (mt) and female (mt+) gametes. The timing of initiation of the destruction differed among zygotes but usually occurred during 50–120 minutes after mixing. About 10 minutes was required for complete digestion of the ct nucleoids. UV irradiation on young zygotes or addition of an RNA-synthesis inhibitor, actinomycin D, to the incubation medium during the first 0–30 minutes after mixing almost completely inhibited the incorporation of3H uridine into the cell nuclei and the preferential destruction without inhibiting cell nuclear fusion. These results suggest that soon after mating,de novo RNA synthesis is concerned for the preferential destruction of ct nucleoids. To determine in which of the two cell nuclei in the zygotes the RNA is synthesized, each gamete (mt, mt+) was irradiated with UV and mated with unirradiated gametes of opposite mating type. This treatment of the male gametes had no effect on the incorporation of3H uridine into cell nuclei and the preferential destruction of ct nucleoids but UV irradiation of female gametes almost completely inhibited the incorporation of3H uridine into cell nuclei and the preferential destruction of ct nucleoids. Similar phenomena occurred in other crosses. The UV effect was photoreactivated in about 50% by white light, suggesting that the UV target is DNA. Thus, RNA synthesized in the cell nucleus of female origin soon after mating may be responsible for the preferential destruction of ct nucleoids of male origin

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Burton, W. G., Grabowy, C. T., Sager, R., 1979: Role of methylation in the modification and restriction of chloroplast DNA inChlamydomonas. Proc. Nat. Acad. Sci. U.S.A.76, 1390–1394.

    Google Scholar 

  • —,Roberts, R. J., Myers, P. A., Sager, R., 1977: A site-specific single strand endonuclease from the eukaryoteChlamydomonas. Proc. Nat. Acad. Sci. U.S.A.74, 2687–2691.

    Google Scholar 

  • Coleman, A. W., Maguire, M. J., 1983: Cytological detection of the basis of uniparental inheritance of plastid DNA inChlamydomonas moewusii. Curr. Genet.7, 211–218.

    Google Scholar 

  • Gillham, N. W., 1974: Genetic analysis of the chloroplast and mitochondrial genomes. Ann. Review Genet.8, 347–391.

    Google Scholar 

  • Kuroiwa, T., Kawano, S., Sato, C., 1983 a: Mechanisms of maternal inheritance. I. Protein synthesis involved in preferential destruction of chloroplast DNA of male origin. Proc. Japan Acad.59, 177–181.

    Google Scholar 

  • — — —, 1983 b: Mechanisms of maternal inheritance. II. RNA synthesis involved in preferential destruction of chloroplast DNA of male origin. Proc. Japan Acad.59, 182–185.

    Google Scholar 

  • —,Nishibayashi, S., Kawano, S., 1981: Visualization of DNA in plant mitochondria, various phages and single DNA molecule by ethidium bromide epifluorescent microscopy. Proc. XIII Inter. Bot. Cong. Sydney13, 250a.

    Google Scholar 

  • —,Kawano, S., Nishibayashi, S., Sato, C., 1982 a: Epifluorescent microscopic evidence for maternal inheritance of chloroplast DNA. Nature298, 481–483.

    Google Scholar 

  • — —,Sato, C., Tanaka, K., 1982 b: Preferential destruction of chloroplast nuclei from mt parent should lead to maternal inheritance. Jap. J. Genet.57, 692.

    Google Scholar 

  • Matsuda, Y., Tamaki, S., Tsubo, Y., 1978: Mating type specific induction of cell wall lytic factor by agglutination of gametes inChlamydomonas reinhardtii. Plant Cell Physiol.19, 1253–1261.

    Google Scholar 

  • Ogawa, K.,Kuroiwa, T., 1984: Polymorphism of Ca++ dependent nuclease inChlamydomonas reinhardtii. Proc. the 24th Ann. Meeting of Jap. Soc. Plant Physiologists, 1984.

  • Sager, R., 1954: Mendelian and non-Mendelian inheritance of streptomycin resistance inChlamydomonas. Proc. Nat. Acad. Sci. U.S.A.40, 356–362.

    Google Scholar 

  • —, 1981: The application of DNA methylation studies to the analysis of chloroplast evolution. Ann. N.Y. Acad. Sci.361, 209–218.

    Google Scholar 

  • —,Granick, S., 1954: Nutritional control of sexuality inChlamydomonas reinhardii. J. gen. Physiol.37, 729.

    Google Scholar 

  • —,Ramanis, Z., 1973: The mechanisms of maternal inheritance inChlamydomonas: Biochemical and genetic studies. Theor. appl. Genet.43, 101–108.

    Google Scholar 

  • — —, 1974: Mutations that alter the transmission of chloroplast genes inChlamydomonas. Proc. Nat. Acad. Sci. U.S.A.71, 4698–4702.

    Google Scholar 

  • —,Tsubo, Y., 1961: Genetic analysis of streptomycin resistance and dependence inChlamydomonas. Z. Vererbungsl.92, 420–438.

    Google Scholar 

  • Sears, B. B., 1980: Disappearance of the heteroplasmic state for chloroplast markers in zygospores ofChlamydomonas reinhardtii. Plasmid3, 18–34.

    Google Scholar 

  • Suzuki, T., Nishibayashi, S., Kuroiwa, T., Kanbe, T., Tanaka, K., 1982: Variance of ploidy inCandida albicans. J. Bacteriol.152, 893–896.

    Google Scholar 

  • Sueoka, N., 1960: Mitotic replication of deoxyribonucleic acid inChlamydomonas reinhardtii. Proc. Nat. Acad. Sci. U.S.A.46, 83–88.

    Google Scholar 

  • Takaiwa, F., Sugiura, M., 1980: Cloning and characterization of 4.5 S and 5 S RNA genes in tobacco chloroplasts. Gene10, 95–103.

    Google Scholar 

  • Tsubo, Y., Matsuda, Y., 1984: Transmission of chloroplast genes in crosses betweenChlamydomonas reinhardtii diploids: Correlation with chloroplast nucleoid behavior in young zygotes. Curr. Genet.8, 223–229.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kuroiwa, T., Nakamura, S., Sato, C. et al. Epifluorescent microscopic studies on the mechanism of preferential destruction of chloroplast nucleoids of male origin in young zygotes ofChlamydomonas reinhardtii . Protoplasma 125, 43–52 (1985). https://doi.org/10.1007/BF01297349

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01297349

Keywords

Navigation