Molecular mechanism of cytoplasmic inheritance: Active digestion of mt- cpDNA as a driving force for maternal inheritance in Chlamydomonas reinhardtii

Yoshiki Nishimura

doi:10.5685/plmorphol.13.69

Yoshiki Nishimura

Author information

Keywords: Non-Mendelian inheritance, SYBR Green I, chloroplast transformation, aadA(aminoglycoside adenyl transferase), optical tweezers, nativePAGE

JOURNAL FREE ACCESS

2001 Volume 13 Issue 1 Pages 69-76

DOI https://doi.org/10.5685/plmorphol.13.69

Details

Published: 2001 Received: - Available on J-STAGE: June 28, 2010 Accepted: - Advance online publication: - Revised: -
Correction information
Date of correction: June 28, 2010 Reason for correction: - Correction: PDF FILE Details: -

Date of correction: June 28, 2010 Reason for correction: - Correction: KEYWORD Details: Wrong : Key words: Non-Mendelian inheritance, SYBR Green I, chloroplast transformation, aadA(aminoglycoside adenyl transferase), optical tweezers, nativePAGE
Right : Non-Mendelian inheritance, SYBR Green I, chloroplast transformation, aadA(aminoglycoside adenyl transferase), optical tweezers, nativePAGE

Date of correction: June 28, 2010 Reason for correction: - Correction: CITATION Details: Wrong : E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E

Right : Armbrust, E. V., Ferris, P. J., Goodenough, U. W.(1993)A mating type-linked gene cluster expressed in Chlamydomonas zygotes participates in the uniparental inheritance of the chloroplast genome. Cell 74: 801-811.
Ashkin, A., Dziedzic, J. M.(1987)Optical trapping and manipulation of viruses and bacteria. Science 235: 1517-1520.
Birky, C. W. Jr.(1995)Uniparental inheritance of mitochondrial and chloroplast genes: mechanisms and evolution. Proc. Natl. Acad. Sci. USA 92: 11331-11338.
Bolen, B. L., Grant, D. M., Swinton, D., Boynton, J. E., Gillham, N. W.(1982)Extensive methylation of chloroplast DNA by a nuclear gene mutation does not affect chloroplast gene transmission in Chlamydomonas. Cell 28: 335-343.
Boynton, J. E., Gillham, N. W., Harris, E. H. Advances in Plant Gene Research.(Springer Verlag, New York. 1990)
Burton, W. G., Gravowy, C. T., Sager, R.(1979)Role of methylation in the modification and restriction of chloroplast DNA in chlamydomonas. Proc. Natl. Acad. Sci. USA 76: 1390-1394.
Correns, C.(1909)Vererbungsversuche mit blass(gelb)grunen und buntblattrigen sippen bei Mirabilis jalapa, Urtica pilulifera und Lunaria annua. Z. Verebungs 1: 291-329.
Corriveau, J. S., Coleman, A .W.(1988)Rapid screening method to detect potential biparental inheritance of plastid DNA and results for over 200 angiosperms species. Am. J. Bot. 75: 1443-1458.
Eckenrode, V. K., Levings III, C. S.(1986)Maize mitochondrial genes. In vitro. Cell. Dev. Biol. 22: 169-176.
Feng, T-Y., Chiang, K-S.(1984)The persistence of maternal inheritance in Chlamydomonas despite hypomethylation of chloroplast DNA induced by inhibitors. Proc. Natl. Acad. Sci. USA 81: 3438-3442.
Giles, R. E., Blanc, H., Cann, H. M., Wallace, D. C.(1980)Maternal inheritance of human mitochondria DNA. Proc. Natl. Acad. Sci. USA 77: 6715-6719.
Gillham, N. W.(1994)in Organelle Genes and Genomes(Oxford Univ. Press, New York, Oxford)pp. 149-152.
Gray, M. W.(1992)The endosymbiont hypothesis revisited. Int. Rev. Cytl. 141: 233-357.
Gyllenstein, U., Wharton, D., Wilson, A. C.(1991)Paternal inheritance of mitochondrial DNA in mice. Nature 352: 255-257.
Hutchison, C. A. III, Newbold, J. E., Potter, S. S., Edgell, M. H.(1974)Maternal inheritance of mammalian mitochondrial DNA. Nature 251: 536-538.
Ishihama, A.(1999)Modulation of the nucleoid, the transcription apparatus and the translation machinery in bacteria for stationary phase survival. Genes to Cells. 4: 135-143.
Kaneda, H., Hayashi, J., Takahama, S., Taya, C., Lindahl, K. F., Yonekawa, H. 1995. Elimination of paternal mitochondrial DNA in intraspecific crosses during early mouse embryogenesis. Proc. Natl. Acad. Sci. USA 92: 4542-4546.
Kawano, S., Anderson, R. W., Nanba, T., Kuroiwa, T.(1987)Polymorphism and uniparental inheritance of mitochondrial DNA in Physarum polycephalum. J. Gen. Microbiol. 133: 3175-3182.
Kuroiwa, H., Sugai, M., Kuroiwa, T.(1988)Behavior of chloroplasts and chloroplast nuclei during spermatogenesis in the fern, Pteris vittata L. Protoplasma 146: 89-100.
Kuroiwa, T., Suzuki, T., Ogawa, K., Kawano, S.(1981)The chloroplast nucleus: distribution, number, size, and shape, and a model for the multiplication of the chloroplast genome during chloroplast development. Plant. Cell. Physiol. 22: 381-396.
Kuroiwa, T.(1985)Mechanisms of maternal inheritance of chloroplast DNA: an active digestion hypothesis. Microbiol. Sci. 2: 267-272.
Kuroiwa, T.(1991)The replication, differentiation, and inheritance of plastids with emphasis on the concept of organelle nuclei. Int. Rev. Cytl. 128: 1-60.
Kuroiwa, T., Kawano, S., Nishibayashi, S., Sato, C.(1982)Epifluorescent microscopic evidence for maternal inheritance of chloroplast DNA. Nature 298: 481-483.
Levings, C. S. III(1990)The Texas cytoplasm of maize: cytoplasmic male sterility and disease susceptibility. Science 250: 942-947.
Mitchell, M. B., Mitchell, H. K.(1952)A case of “maternal” inheritance in Neurospora crassa. Proc. Natl. Acad. Sci. USA 38: 442-449.
Miyamura, S., Kuroiwa, T., Nagata, T.(1987)Difference of plastid and mitochondrial nucleoids during the formation of generative cells of higher plants revealed by fluorescence microscopy. Protoplasma 141: 149-159.
Nakamura, S., Sato, C., Kuroiwa, T.(1988)Polypeptides related to preferential digestion of male chloroplast nucleoids in Chlamydomonas. Plant Sci. 56: 129-136.
Nishimura, Y., Higashiyama, T., Suzuki, L., Misumi, O., Kuroiwa, T.(1998)The biparental transmission of the mitochondrial genome in Chlamydomonas reinhardtii visualized in living cells. Eur. J. Cell. Biol. 77: 124-133.
Nishimura, Y., Misumi, O., Matsunaga, S., Higashiyama, T., Yokota, A., and Kuroiwa, T.(1999)The active digestion of uniparental chloroplast DNA in a single zygote of Chlamydomonas reinhardtii is revealed by using the optical tweezers. Proc. Natl. Acad. Sci. 96: 12577-12582.
Ogawa, K., Kuroiwa, T.(1985a)Nuclease C: polymorphism of calcium-dependent nucleases in Chlamydomonas reinhardtii. Plant. Cell. Physiol. 26: 481-491.
Ogawa, K., Kuroiwa, T.(1985b)Destruction of chloroplast nuclei of the male gamete by calcium-dependent nucleases in Chlamydomonas reinhardtii. Plant. Cell. Physiol. 26: 493-503.
Royer, H. D., Sager, R.(1979)Methylation of chloroplast DNAs in the life cycle of Chlamydomonas. Proc. Natl. Acad. Sci. USA 76: 5794-5798.
Sager, R., and Lane, D.(1972)Molecular basis of maternal inheritance. Proc. Natl. Acad. Sci. USA 69; 2410-2413.
Sager, R.(1954)Mendelian and non-Mendelian inheritance of streptomycin resistance in Chlamydomonas reinhardtii. Proc. Natl. Acad. Sci. USA 40:356-363.
Sano, H., Gravowy, C. T., Sager, R.(1981)Differential activity of DNA methyltransferase in the life cycle of Chlamydomonas reinhardtii. Proc. Natl. Acad. Sci. USA 78: 3118-3122.
Whatley, J. M.(1982)Ultrastructure of plastid inheritance: green algae to angiosperms. Biol. Rev. 57: 527-569.

Abstract

Summary: The non-Mendelian inheritance of organelle genes is a phenomenon that is common to almost all sexual eukaryotes. In the isogamous alga Chlamydomonas reinhardtii, chloroplast(cp)genes are transmitted from the mating type plus(mt+)parent. In this study, the preferential disappearance of fluorescent cp nucleoids of the mating type minus(mt-)parent in living young zygotes was observed. To study the change in cpDNA molecules during this process, the cpDNA of mt+ and mt origin was labeled separately with bacterial aadA gene sequences. Then, a single zygote with or without cp nucleoids was obtained using the optical tweezers, and investigated by nested PCR. This demonstrated the active digestion of mt cpDNA during the preferential disappearance of mt cp nucleoids. To identify factors that cause the active digestion, nuclease activities in C. reinhardtii cells were surveyed. Consequently, a Ca2+-dependent nuclease(NUC-C)that is detected only in mt+ gametes was identified. Further analysis of NUC-C activity in chloroplasts of young zygotes detected NUC-C activity in mt chloroplasts60-90min after mating, which precisely corresponds to the timing of preferential digestion. These results indicate that the maternal nuclease NUC-C is the driving force for the maternal inheritance of cpDNA, which is achieved by the preferential digestion of mt cpDNA in young zygotes.

Corresponding author

Correction information

Register with J-STAGE for free!