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Evolutionary modification of specification for the endomesoderm in the direct developing echinoid Peronella japonica: loss of the endomesoderm-inducing signal originating from micromeres

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Abstract

We investigated the inductive signals originating from the vegetal blastomeres of embryos of the sand dollar Peronella japonica, which is the only direct developing echinoid species that forms micromeres. To investigate the inductive signals, three different kinds of experimental embryos were produced: micromere-less embryos, in which all micromeres were removed at the 16-cell stage; chimeric embryos produced by an animal cap (eight mesomeres) recombined with a micromere quartet isolated from a 16-cell stage embryo; and chimeric embryos produced by an animal cap recombined with a macromere-derived layer, the veg1 or veg2 layer, isolated from a 64-cell stage embryo. Novel findings obtained from this study of the development of these embryos are as follows. Micromeres lack signals for endomesoderm specification, but are the origin of a signal establishing the oral–aboral (O–Ab) axis. Some non-micromere blastomeres, as well as micromeres, have the potential to form larval skeletons. Macromere descendants have endomesoderm-inducing potential. Based on these results, we propose the following scenario for the first step in the evolution of direct development in echinoids: micromeres lost the ability to send a signal endomesoderm induction so that the archenteron was formed autonomously by macromere descendants. The micromeres retained the ability to form larval spicules and to establish the O–Ab axis.

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Acknowledgments

We thank the members of the Misaki Marine Biological Station of the University of Tokyo and the Noto Marine Laboratory of Kanazawa University for supplying the animals. Many thanks are due to Dr. Masaaki Yamaguchi and all of the members of his laboratory for invaluable discussion and their help in animal collection. This study was partially supported by a “Grant-in-Aid for Young Scientists” (18770191) from the Ministry of Education, Culture, Sports, Science, and Technology of Japan, a Narishige Zoological Science Award, and a research grant from the graduate school of life sciences, Tohoku University, to T.M.

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Authors and Affiliations

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

    Minoru Iijima, Yasuhiro Ishizuka & Takuya Minokawa

  2. Department of Earth Evolution Sciences, Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Ibaraki, 305-8572, Japan

    Minoru Iijima

  3. Kaijo Junior & Senior High School, 3-6-1 Okubo, Shinjuku-ku, Tokyo, 169-0072, Japan

    Yasuhiro Ishizuka

  4. Department of Biology, Keio University, Yokohama, Kanagawa, 223-8521, Japan

    Yoko Nakajima

  5. Department of Integrated Biosciences, Graduate School of Frontier Sciences, University of Tokyo, Kashiwa, Chiba, 277-8562, Japan

    Shonan Amemiya

  6. Research Center for Marine Biology, Tohoku University, 9 Sakamoto, Asamushi, Aomori, Aomori, 039-3501, Japan

    Takuya Minokawa

Authors
  1. Minoru Iijima
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  2. Yasuhiro Ishizuka
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  3. Yoko Nakajima
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  4. Shonan Amemiya
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  5. Takuya Minokawa
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Correspondence to Takuya Minokawa.

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Communicated by: H. Nishida

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Iijima, M., Ishizuka, Y., Nakajima, Y. et al. Evolutionary modification of specification for the endomesoderm in the direct developing echinoid Peronella japonica: loss of the endomesoderm-inducing signal originating from micromeres. Dev Genes Evol 219, 235–247 (2009). https://doi.org/10.1007/s00427-009-0286-8

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  • DOI: https://doi.org/10.1007/s00427-009-0286-8

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