Advertisement

Journal of Ocean University of China

, Volume 13, Issue 1, pp 125–131 | Cite as

Cytogenetic mechanism for the aneuploidy and mosaicism found in tetraploid Pacific oyster Crassostrea gigas (Thunberg)

  • Zhengrui Zhang
  • Xinglian Wang
  • Quanqi ZhangEmail author
  • Standish AllenJr.
Article

Abstract

Chromosome constitution was investigated in adult tetraploid Pacific oyster produced by blocking the first polar body of triploid eggs which were fertilized with haploid sperms. A high incidence of aneuploid and heteroploid mosaics were found among the offspring. Of 20 individuals identified, only 9 (45%) were eutetraploid which contained 40 chromosomes; 2 (10%) were aneuploid (hypotetraploid), which contained 39 and 38 chromosomes, respectively; and 9 (45%) were heteroploid mosaics. One mosaic was consisted of cells containing 40 and 39 chromosomes, respectiovely (1:1 in cell number), while the other 8 were consisted of cells containing chromosomes varying between tetraploid and triploid. It was also interesting to note that 3 mosaics even contained some diploid cells with 20 chromosomes. A certain number of cells of 2 tetraploids and 8 mosaics spread with 32–37 well-scattered and some clumped chromosomes at metaphase. The percentage of aneuploid cells with chromosomes varying between triploid and tetraploid correlated significantly with that of heteroploid mosaics cells with clumping chromosomes (P<0.05). Our findings suggested that reversion existed in both tetraploid and triploid oyster and chromosome clumping may underline the chromosome elimination in tetraploid oyster. It seems that the reversing cells, at least some of them, continuously eliminate their chromosomes until the most stable diploid state is established.

Key words

tetraploid oyster aneuploidy mosaicism reversion cytogenetic mechanism 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Allen Jr., S. K., 1983. Flow cytometry: Assaying experimental polyploid fish and shellfish. Aquaculture, 33: 317–328.CrossRefGoogle Scholar
  2. Allen Jr., S. K., 1988. Triploid oysters ensure year-round supply. Oceanus, 31: 58–63.Google Scholar
  3. Allen Jr., S. K., and Bushek, D., 1992. Large scale production of triploid Crassostrea virginica (Gmelin) using ‘stripped’ gametes. Aquaculture, 103: 241–251.CrossRefGoogle Scholar
  4. Allen Jr., S. K., Downing, S. L., and Chew, K. K., 1989. Hatchery Manual for Producing Triploid Oyster. University of Washington Press, Seattle, Washington, 1–27.Google Scholar
  5. Allen Jr., S. K., Guo, X., Burreson, G., and Mann, R., 1996. Heteroploid mosaics and reversion among triploid oysters, Crassostrea gigas: Fact or artifact. Journal of Shellfish Research, 15: 514–522.Google Scholar
  6. Allendorf, F. W., and Thorgaard, G. H., 1984. Tetraploidy and the evolution of salmonid fishes. In: Evolutionary Genetics of Fishes. Turner, B. J., ed., Plenum, New York, 1–53.CrossRefGoogle Scholar
  7. Andreassen, P. R., Martineau, S. N., and Margolis, R. L., 1996. Chemical induction of mitotic checkpoint override in mammalian cells results in aneuploidy following a transient tetraploid state. Mutegenesis Research, 372: 181–194, DOI: 10.1016/S0027-5107(96)00138-8.Google Scholar
  8. Arai, K., 2001. Genetic improvement of aquaculture finfish species by chromosome manipulation techniques in Japan. Aquaculture, 197: 205–228.CrossRefGoogle Scholar
  9. Darlington, C. D., 1953. Polyploidy in animals. Nature, 171: 191–194.CrossRefGoogle Scholar
  10. Davisson, M. T., Wright, J. E., and Atherton, L. M., 1972. Centric fusion and trisomy for the LDH-B locus in brood trout, Salvelinus fontinalis. Science, 178: 992–994.CrossRefGoogle Scholar
  11. de Met, J. M. J., 1971. Reversible tetraploidy as an evolutionary mechanism. Evolution, 25: 545–548.CrossRefGoogle Scholar
  12. de Met, J. M. J., and Harlan, J. R., 1970. Apomixis, polyploidy and speciation in Dichanthium. Evolution, 24: 270–277.CrossRefGoogle Scholar
  13. Ferris, S. D., 1984. Tetraploidy and evolution of the catostomid fishes. In: Evolutionary Genetics of Fishes. Turner, B. J., ed., Plenum, New York, 55–93.CrossRefGoogle Scholar
  14. Giareti, W., 1994. A model of DNA aeuploidization and evolution in colorectal cancer. Laboratory Investigation, 71: 904–910.Google Scholar
  15. Gong, N., Yang, H., Zhang, G., Landau, B. J., and Guo, X., 2004. Chromosome inheritance in triploid Pacific oyster Crassostrea gigas Thunberg. Heredity, 93(5): 408–415.CrossRefGoogle Scholar
  16. Guo, X., and Allen Jr., S. K., 1994. Viable tetraploids in the Pacific oyster (Crassostrea gigas Thunberg) produced by inhibiting polar body I in eggs from triploids. Molecular Marine Biology and Biotechnology, 3: 42–50.Google Scholar
  17. Guo, X., and Allen Jr., S. K., 1997. Sex and meiosis in autotetraploid Pacific oyster, Crassostrea gigas (Thunberg). Genome, 40: 397405.CrossRefGoogle Scholar
  18. Guo, X., Cooper, K., Hershberger, W. K., and Chew, K. K., 1992a. Genetic consequences of blocking polar body I with cytochalasin B in fertilized eggs of the Pacific oyster, Crassostrea gigas: I. Ploidy of resultant embryos. Biological Bulletin, 183: 381–386.CrossRefGoogle Scholar
  19. Guo, X., Cooper, K., Hershberger, W. K., and Chew, K. K., 1992b. Genetic consequences of blocking polar body I with cytochalasin B in fertilized eggs of the Pacific oyster, Crassostrea gigas: II. Segregation of chromosomes. Biological Bulletin, 183: 387–393.CrossRefGoogle Scholar
  20. Guo, X., Debrosse, G. A., and Allen Jr., S. K., 1996. All triploid Pacific oyster (Crassostrea gigas Thunberg) produced by mating tetraploids and diploids. Aquaculture, 142: 149–161.CrossRefGoogle Scholar
  21. Guo, X., Wang, Y., Xu, Z., and Yang, H., 2009. Chromosome set manipulation in shellfish. In: New Technologies in Aquaculture: Improving Production Efficiency, Quality and Environ mental Management. Burnell, G., and Allan, G., eds., Woodhead Publishing, 165–195.CrossRefGoogle Scholar
  22. Johnannes, A., Breeuwer, J., and Werren, J. H., 1990. Microorganisms associated with chromosome destruction and reproductive isolation between two insect species. Nature, 346: 558–560.CrossRefGoogle Scholar
  23. Kimber, G., and Riley, R., 1963. Haploid angiosperms. Botanical Review, 29: 480–531.CrossRefGoogle Scholar
  24. Komaru, A., Matsuda, H., Yamakawa, T., and Wada, K. T., 1990. Chromosome-behavior of meiosis-inhibited eggs with cytochalasin B in Japanese pearl oyster. Nippon Suisan Gakkaishi, 569: 1419–1422.CrossRefGoogle Scholar
  25. Levine, D. S., Sanchez, C. A., Rabinovitch, P. S., and Reid, B. J., 1991. Formation of the tetraploid intermediate is associated with the development of cells with more than four centrioles in the elastase-simian virus 40 tumor antigen transgenic mouse model of pancreatic cancer. Medical Science, 88: 6427–6431.Google Scholar
  26. Lewis, W. H., Oliver, R. L., and Luikart, T. J., 1971. Multiple genotypes in individuals of Claytonia virginica. Science, 172: 564–565.CrossRefGoogle Scholar
  27. Li, Y. J., Yu, Z., Zhang, M. Z., Qian, C., Abe, S., and Arai, K., 2011. The origin of natural tetraploid loach Misgurnus anguillicaudatus (Teleostei: Cobitidae) inferred from meiotic chromosome configurations. Genetica, 139: 805–811, DOI: 10.1007/s10709-011-9585-x.CrossRefGoogle Scholar
  28. Liu, S., 2010. Distant hybridization leads to different ploidy fishes. Science in China Life Science, 53(4): 416–25, DOI: 10.1007/s11427-010-0057-9.CrossRefGoogle Scholar
  29. Longo, F. J., 1972. The effects of cytochalasin B on the events of fertilization in the surf clam, Spisula solidissima I polar body formation. Journal of Experimental Zoology, 182: 321–344.CrossRefGoogle Scholar
  30. Longo, F. J., Mathews, L., and Hedgecock, D., 1993. Morphogenesis of maternal and paternal genomes in fertilized oyster eggs (Crassostrea gigas): Effects of cytochalasin B at different periods during meiotic maturation. Biological Bulletin, 185: 197–214.CrossRefGoogle Scholar
  31. Mayer, V. W., and Aguilera, A., 1990. High levels of chromosome instability in polyploids of Saccharomyces cerevisiae. Mutigenesis Research, 231: 177–186.Google Scholar
  32. Ornitz, D. M., Hammer, R. E., Messing, A., Palmiter, R. D., and Brinster, R. L., 1987. Pancreatic neoplasia induced by SV 40 T-antigen expression in acinar cells of transgenic mice. Science, 238: 188–191.CrossRefGoogle Scholar
  33. Que, H., Guo, X., Zhang, F., and Allen Jr., S. K., 1997. Chromosome segregation in fertilized eggs from triploid Pacific oysters, Crassostrea gigas (Thunberg), following inhibition of polar body 1. Biological Bulletin, 193: 14–19.CrossRefGoogle Scholar
  34. Rabinovitch, P. S., Reid, B. J., Haggitt, R. C., Norwood, T. H., and Rubin, C. E., 1989. Progression to cancer in Barrett’s exophagus is associated with genomic instability. Laboratory Investigation, 60: 65–71.Google Scholar
  35. Randolph, L. F., and Fisher, H. E., 1939. The occurrence of parthenogenetic diploids in tetraploid maize. Proceedings of National Academy of Science of USA, 25: 161–164.CrossRefGoogle Scholar
  36. Ryan, S. J., and Saul, G. B., 1968. Post-fertilization effect of incompatibility factors in Mormoniella. Molecular Genetics and Genomics, 103: 29–36.Google Scholar
  37. Sandberg, A. A., 1977. Chromosome markers and progression in bladder cancer. Cancer Research, 37: 2950–2956.Google Scholar
  38. Shackney, S. E., Smith, C. S., Miller, B. W., Burholt, D. R., Murtha, K., Giles, H. R., Ketterer, D. M., and Pollice, A. A., 1989. Model for the genetic evolution of human solid tumors. Cancer Research, 49: 3344–3354.Google Scholar
  39. Snoad, B., 1955. Somatic instability of chromosome number in Himenocallis calathinum. Heredity, 9: 129–134.CrossRefGoogle Scholar
  40. Tan, G. Y., and Dunn, G. M., 1977. Mitotic instabilities in tetraploid, hexaploid, and octoploid Bromus inermis. Canadian Journal of Genetics and Cytology, 19: 531–536.Google Scholar
  41. Thiriot-Quievreux, C., Pogson, G. H., and Zouros, E., 1992. Genetics of growth rate variation in bivalves: Aneuploidy and heterozygosity effects in a Crassostrea gigas family. Genome, 35: 39–45.CrossRefGoogle Scholar
  42. Wang, Z., Guo, X., Allen Jr., S. K., and Wang, R., 1999. Aneuploid Pacific oyster (Crassostrea gigas Thunberg) as incidentals from triploid production. Aquaculture: 173: 347–357.CrossRefGoogle Scholar
  43. Xiao, J., Zou, T., Chen, Y., Chen, L., Liu, S., Tao, M., Zhang, C., Zhao, R., Zhou, Y., Long, Y., You, C., Yan, J., and Liu, Y., 2011. Coexistence of diploid, triploid and tetraploid crucian carp (Carassius auratus) in natural waters. BMC Genetics, 12: e20, DOI: 10.1186/1471-2156-12-20.CrossRefGoogle Scholar
  44. Yi, Q. L., Yu, H. Y., Wang, X. L., Wang, Z. G., Wang, X. B., Qi, J., and Zhang, Q. Q., 2012. Production of viable tetraploid olive flounder (Paralichthys olivaceus) by hydrostatic pressure shock. Oceanologia et Limnologia Sinica, 43(2): 382–388 (in Chinese with English abstract).Google Scholar
  45. Zhang, Q., and Arai, K., 1999. Aberrant meioses and viable aneuploid progeny of induced triploid loach (Misgurnus anguillicaudatus) when crossed to natural tetraploids. Aquaculture, 243: 68–79.Google Scholar
  46. Zhang, Q., and Arai, K., 2003. Extensive karyotype variation in somatic and meiotic cells of the loach Misgurnus anguillicaudatus (Pisces: Cobitidae). Folia Zoologica, 52: 423–429.Google Scholar
  47. Zhang, Q., Yu, H., Howe, A., Chandler, W., and Allen Jr., S. K., 2010a. Cytogenetic mechanism for reversion of triploids to heteroploid mosaics in Crassostrea gigas (Thunberg) and Crassostrea ariakensis. Aquaculture Research, 41: 1658–1667, DOI: 10.1111/j.1365-2109.2010.02541.x.CrossRefGoogle Scholar
  48. Zhang, Q., Zhuang, Y., and Allen Jr., S. K., 2010b. Meiotic chromosome configurations in triploid and heteroploid mosaic males of Crassostrea gigas and Crassostrea ariakensis. Aquaculture Research, 41: 1699–1706, DOI: 10.1111/j.1365-2109.2010.02559.x.CrossRefGoogle Scholar
  49. Zhang, X., and van der Meer, J. P., 1988. Polyploid gametophytes of Gracilaria tikvahiae (Gigartinales, Rhodophyta). Phycologia, 27: 312–318.CrossRefGoogle Scholar
  50. Zouros, E., Thiriot-Quievreux, C., and Kotoulas, G., 1996. The negative correlation between somatic aneuploidy and growth in the oyster Crassostrea gigas and implications for the effects of induced polyploidization. Genetical Research, 68: 109–116.CrossRefGoogle Scholar

Copyright information

© Science Press, Ocean University of China and Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Zhengrui Zhang
    • 1
  • Xinglian Wang
    • 1
  • Quanqi Zhang
    • 1
    Email author
  • Standish AllenJr.
    • 2
  1. 1.College of Marine Life Sciences, Key Laboratory of Marine Genetics and Breeding of Ministry of EducationOcean University of ChinaQingdaoP. R. China
  2. 2.Aquaculture Genetics and Breeding Technology Center, Virginia Institute of Marine ScienceCollege of William and MaryGloucester PointUSA

Personalised recommendations