TY - JOUR
T1 - Different strategies for tissue scaling in dwarf tailbud embryos revealed by single-cell analysis
AU - Matsumura, Kaoru D.
AU - Nakamura, Mitsuru J.
AU - Koizumi, Wataru C.
AU - Hotta, Kohji
AU - Oka, Kotaro
N1 - Funding Information:
We would like to thank Prof. Hiroki Nishida (Osaka Univ.) for the kind gift of NileBlue B and important advice for this study. We would also like to thank Emmanuel Faure (CNRS, France) and Takumi Shito for their help with the cell volume analysis. We thank Masahiro Inda for advice on ROC analysis and cell volume analysis. The Ciona samples were provided by Yutaka Satou, Kyoto University and Manabu Yoshida, The University of Tokyo, with support by the National Bio-Resource Project of AMED, Japan. K. H. was supported by Keio Research Grant KLL and JSPS KAKENHI (Grant Numbers JP16H01451 and JP16K07426).
Funding Information:
We would like to thank Prof. Hiroki Nishida (Osaka Univ.) for the kind gift of NileBlue B and important advice for this study. We would also like to thank Emmanuel Faure (CNRS, France) and Takumi Shito for their help with the cell volume analysis. We thank Masahiro Inda for advice on ROC analysis and cell volume analysis. The Ciona samples were provided by Yutaka Satou, Kyoto University and Manabu Yoshida, The University of Tokyo , with support by the National Bio-Resource Project of AMED, Japan . K. H. was supported by Keio Research Grant KLL and JSPS KAKENHI (Grant Numbers JP16H01451 and JP16K07426 ).
Publisher Copyright:
© 2020 Elsevier Inc.
PY - 2020/4/15
Y1 - 2020/4/15
N2 - The tailbud stage is part of the organogenesis period—an evolutionarily conserved developmental period among chordates that is essential for determining the characteristics of the chordate body plan. When the volume of the egg is artificially decreased by cutting, ascidians produce a normal-looking but miniature (dwarf) tailbud embryo. Although cell lineages during ascidian embryogenesis are invariant, the number of cell divisions in the dwarf embryo is altered by a different mechanism in each tissue (Yamada and Nishida, 1999). Here, to elucidate the size-regulation strategies of the Ciona robusta dwarf tailbud embryo, we compared anatomical structure, developmental speed, and cell number/volume in each tissue between dwarf and wild type (WT) embryos. To do this, we constructed a 3D virtual mid-tailbud embryo (Nakamura et al., 2012). We could make a Ciona dwarf tailbud embryo from eggs with a diameter over 108 μm (correspond to > 40% of the wild type egg volume). The timings of cleavage (~St. 12) and subsequent morphogenesis were nearly the same but blastomeres of animal hemisphere slightly delayed the timing of mitosis in the early cleavage period. Intriguingly, the tissue-to-tissue volume ratios of dwarf tailbud embryos were similar to those of wild type embryos suggesting that the ratio of tissue volumes is essential for maintaining the proper shape of the tailbud embryo. The number of cells in the epidermis, nervous system, and mesenchyme was significantly reduced in the dwarf embryos whereas the cell volume distribution of these tissues was similar in the dwarf and wild type. In contrast, the number of cells in the notochord, muscle, heart, and endoderm were maintained in the dwarf embryos; cell volumes were significantly reduced. Neither parameter changed in germline precursors. These results indicate that each tissue uses different scaling strategies to coordinate cell number and cell volume in accordance with the embryo size.
AB - The tailbud stage is part of the organogenesis period—an evolutionarily conserved developmental period among chordates that is essential for determining the characteristics of the chordate body plan. When the volume of the egg is artificially decreased by cutting, ascidians produce a normal-looking but miniature (dwarf) tailbud embryo. Although cell lineages during ascidian embryogenesis are invariant, the number of cell divisions in the dwarf embryo is altered by a different mechanism in each tissue (Yamada and Nishida, 1999). Here, to elucidate the size-regulation strategies of the Ciona robusta dwarf tailbud embryo, we compared anatomical structure, developmental speed, and cell number/volume in each tissue between dwarf and wild type (WT) embryos. To do this, we constructed a 3D virtual mid-tailbud embryo (Nakamura et al., 2012). We could make a Ciona dwarf tailbud embryo from eggs with a diameter over 108 μm (correspond to > 40% of the wild type egg volume). The timings of cleavage (~St. 12) and subsequent morphogenesis were nearly the same but blastomeres of animal hemisphere slightly delayed the timing of mitosis in the early cleavage period. Intriguingly, the tissue-to-tissue volume ratios of dwarf tailbud embryos were similar to those of wild type embryos suggesting that the ratio of tissue volumes is essential for maintaining the proper shape of the tailbud embryo. The number of cells in the epidermis, nervous system, and mesenchyme was significantly reduced in the dwarf embryos whereas the cell volume distribution of these tissues was similar in the dwarf and wild type. In contrast, the number of cells in the notochord, muscle, heart, and endoderm were maintained in the dwarf embryos; cell volumes were significantly reduced. Neither parameter changed in germline precursors. These results indicate that each tissue uses different scaling strategies to coordinate cell number and cell volume in accordance with the embryo size.
KW - 3D anatomy
KW - Cell lineage
KW - Chordate evolution
KW - Dwarf embryo
KW - Nuclear-to-cytoplasmic volume ratio
KW - Organogenesis
KW - Scaling
KW - Tunicate
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U2 - 10.1016/j.ydbio.2020.01.008
DO - 10.1016/j.ydbio.2020.01.008
M3 - Article
C2 - 31981562
AN - SCOPUS:85078794708
SN - 0012-1606
VL - 460
SP - 215
EP - 223
JO - Developmental Biology
JF - Developmental Biology
IS - 2
ER -