Cellular analysis of cleavage-stage chick embryos reveals hidden conservation in vertebrate early development.
Birds and mammals, phylogenetically close amniotes with similar post-gastrula development, exhibit little conservation in their post-fertilization cleavage patterns. Data from the mouse suggest that cellular morphogenesis and molecular signaling at the cleavage stage play important roles in lineage specification at later (blastula and gastrula) stages. Very little is known, however, about cleavage-stage chick embryos, owing to their poor accessibility. This period of chick development takes place before egg-laying and encompasses several fundamental processes of avian embryology, including zygotic gene activation (ZGA) and blastoderm cell-layer increase. We have carried out morphological and cellular analyses of cleavage-stage chick embryos covering the first half of pre-ovipositional development, from Eyal-Giladi and Kochav stage (EGK-) I to EGK-V. Scanning electron microscopy revealed remarkable subcellular details of blastomere cellularization and subgerminal cavity formation. Phosphorylated RNA polymerase II immunostaining showed that ZGA in the chick starts at early EGK-III during the 7th to 8th nuclear division cycle, comparable with the time reported for other yolk-rich vertebrates (e.g. zebrafish and Xenopus). The increase in the number of cell layers after EGK-III is not a direct consequence of oriented cell division. Finally, we present evidence that, as in the zebrafish embryo, a yolk syncytial layer is formed in the avian embryo after EGK-V. Our data suggest that several fundamental features of cleavage-stage development in birds resemble those in yolk-rich anamniote species, revealing conservation in vertebrate early development. Whether this conservation lends morphogenetic support to the anamniote-to-amniote transition in evolution or reflects developmental plasticity in convergent evolution awaits further investigation.
Laboratory for Early Embryogenesis, RIKEN Center for Developmental Biology, Kobe, Hyogo 650-0047, Japan.
Hiroki
H
Nagai
Laboratory for Early Embryogenesis, RIKEN Center for Developmental Biology, Kobe, Hyogo 650-0047, Japan.
Maiko
M
Sezaki
Electron Microscopy Laboratory, RIKEN Center for Developmental Biology, Kobe, Hyogo 650-0047, Japan.
Kisa
K
Kakiguchi
Laboratory for Early Embryogenesis, RIKEN Center for Developmental Biology, Kobe, Hyogo 650-0047, Japan.
Yukiko
Y
Nakaya
Department of Agricultural Biotechnology, Seoul National University, Seoul 151-921, Korea.
Hyung Chul
HC
Lee
Laboratory for Sensory Development, RIKEN Center for Developmental Biology, Kobe, Hyogo 650-0047, Japan.
Raj
R
Ladher
Department of Applied Biological Chemistry, Faculty of Agriculture, Shizuoka University, 836 Ohya, Shizuoka 422-8529, Japan.
Tomohiro
T
Sasanami
Department of Agricultural Biotechnology, Seoul National University, Seoul 151-921, Korea.
Jae Yong
JY
Han
Electron Microscopy Laboratory, RIKEN Center for Developmental Biology, Kobe, Hyogo 650-0047, Japan.
Shigenobu
S
Yonemura
Laboratory for Early Embryogenesis, RIKEN Center for Developmental Biology, Kobe, Hyogo 650-0047, Japan sheng@cdb.riken.jp.
Guojun
G
Sheng
D000818:Animals; D002467:Cell Nucleus / Q000378:metabolism; D002642:Chick Embryo; D002970:Cleavage Stage, Ovum / Q000166:cytology* / Q000648:ultrastructure; D004530:Egg Yolk / Q000166:cytology; D004625:Embryo, Nonmammalian / Q000166:cytology / Q000648:ultrastructure; D047108:Embryonic Development; D018507:Gene Expression Regulation, Developmental; D015726:Giant Cells / Q000166:cytology; D008938:Mitosis; D010766:Phosphorylation; D010768:Phosphoserine / Q000378:metabolism; D012319:RNA Polymerase II / Q000378:metabolism; D014714:Vertebrates / Q000196:embryology*; D015053:Zygote / Q000378:metabolism
D010768:Phosphoserine; D012319:RNA Polymerase II
Amniote; Cellularization; Chick; Cleavage; Yolk syncytium; Zygotic gene activation