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Interspecific Medaka Hybrids as Experimental Models for Investigating Cell Division and Germ Cell Development

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Medaka

Abstract

Interspecific hybrids in the genus Oryzias (medaka) usually have ­abnormalities in reproduction and development. Analysis of the causes of the abnormalities at cellular and molecular levels will contribute to the understanding of basic mechanisms of cell division and gametogenesis. We describe the molecular and cellular mechanisms of embryonic lethality in a hybrid between Oryzias latipes and Oryzias hubbsi and of sex-specific abnormal gametogenesis in a hybrid between O. latipes and Oryzias curvinotus. Chromosomes derived from O. hubbsi are selectively eliminated in both O. latipes (♀)–hubbsi (♂) and O. hubbsi (♀)–latipes (♂) embryos. We propose a possible cellular mechanism of the abnormal mitosis. We also suggest that the hybrid M-phase-promoting factor (MPF; complex of Cdc2 and cyclin B, each of which is derived from different species) is a general molecule causing defective cell divisions in hybrids. In a hybrid between O. latipes and O. curvinotus, spermiogenesis proceeds and sperm-like cells each having 4C DNA are produced without cytokinesis. In hybrid females, the majority of oocytes stop meiosis at the zygotene stage, although a small number of oocytes give rise to diploid eggs. An incomplete synaptonemal complex devoid of SCP1 is likely to cause the aberrant gametogenesis in both sexes in common.

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Notes

  1. 1.

    Oryzias hubbsi was formerly included in Oryzias javanicus, but it has been reported as a new species (Roberts 1998). However, the nomenclature needs to be reconsidered, in accordance with the habitats of O. hubbsi and O. javanicus. O. hubbsi is an endemic species of Java and West Kalimantan (Iwamatsu et al. 1982), while O. javanicus inhabits Malaysia and Thailand. It is therefore appropriate that O. hubbsi be named O. javanicus (Iwamatsu, personal communication).

Abbreviations

CE:

Central element

CGH:

Comparative genomic hybridization

CPC:

Chromosomal passenger complex

DAPI:

4¢,6-Diamidino-2-phenylindole

FISH:

Fluorescence in situ hybridization

INCENP:

Inner centromere protein

LEs:

Lateral elements

MBT:

Midblastula transition

MPF:

M-phase-promoting factor

SC:

Synaptonemal complex

TFs:

Transverse filaments

WCP:

Whole chromosome painting

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Acknowledgments

We are deeply grateful to the colleagues in our laboratory as well as in our collaborator’s laboratories for their contributions, especially Yohei Shimizu, Yoichi Matsuda, Asato Kuroiwa, Takashi Iwamatsu, Mitsuru Sakaizumi, Naoki Shibata, Koichi Mita, Fumio Kasai, and Hiroshi Mitani. This work was supported by funding to M.Y. from the Program for Promotion of Basic Research Activities for Innovative Biosciences (PROBRAIN), under the auspices of the Bio-Oriented Technology Research Advancement Institution (BRAIN).

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Author notes

  1. Toshiharu Iwai

    Present address: Research Group for Reproductive Physiology, South Ehime Fisheries Research Center, Ehime University, Ainan, Ehime, 798-4292, Japan

  2. Chiharu Sakai

    Present address: Model Fish Genomics Resource Laboratory, Genetic Strains Research Center, National Institute of Genetics, Mishima, Shizuoka, 411-8540, Japan

Authors and Affiliations

  1. Laboratory of Reproductive and Developmental Biology, Faculty of Science, Hokkaido University, Sapporo, 060-0810, Japan

    Toshiharu Iwai

  2. Laboratory of Reproductive and Developmental Biology, Faculty of Science, Hokkaido University, Sapporo, 060-0810, Japan

    Chiharu Sakai

  3. Laboratory of Reproductive and Developmental Biology, Faculty of Science, Hokkaido University, Sapporo, 060-0810, Japan

    Fumiko Konno

  4. Laboratory of Reproductive and Developmental Biology, Faculty of Science, Hokkaido University, Sapporo, 060-0810, Japan

    Masakane Yamashita

Authors
  1. Toshiharu Iwai
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Corresponding author

Correspondence to Masakane Yamashita .

Editor information

Editors and Affiliations

  1. Laboratory of Bioresources, National Institute for Basic Biology, 38 Nishigonaka, Myodaiji, Okazaki, Aichi, 444-8585, Japan

    Kiyoshi Naruse Ph.D. (Associate Professor) (Associate Professor)

  2. Laboratory of Molecular Genetics for Reproduction, National Institute for Basic Biology, 5-1 Higashiyama, Myodaiji, Okazaki, Aichi, 444-8787, Japan

    Minoru Tanaka Ph.D. (Associate Professor) (Associate Professor)

  3. Department of Biological Sciences Graduate School of Science, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo, 113-0033, Japan

    Hiroyuki Takeda Ph.D. (Professor) (Professor)

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Iwai, T., Sakai, C., Konno, F., Yamashita, M. (2011). Interspecific Medaka Hybrids as Experimental Models for Investigating Cell Division and Germ Cell Development. In: Naruse, K., Tanaka, M., Takeda, H. (eds) Medaka. Springer, Tokyo. https://doi.org/10.1007/978-4-431-92691-7_19

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