Proliferating cells in suborbital tissue drive eye migration in flatfish

Baolong Bao, Zhonghe Ke, Jubin Xing, Eric Peatman, Zhanjiang Liu, Caixia Xie, Bing Xu, Junwei Gai, Xiaoling Gong, Guimei Yang, Yan Jiang, Wenqiao Tang, Daming Ren

Research output: Contribution to journalArticlepeer-review

29 Scopus citations

Abstract

The left/right asymmetry of adult flatfishes (Pleuronectiformes) is remarkable given the external body symmetry of the larval fish. The best-known change is the migration of their eyes: one eye migrates from one side to the other. Two extinct primitive pleuronectiformes with incomplete orbital migration have again attracted public attention to the mechanism of eye migration, a subject of speculation and research for over a century. Cranial asymmetry is currently believed to be responsible for eye migration. Contrary to that hypothesis, we show here that the initial migration of the eye is caused by cell proliferation in the suborbital tissue of the blind side and that the twist of frontal bone is dependent on eye migration. The inhibition of cell proliferation in the suborbital area of the blind side by microinjected colchicine was able to prevent eye migration and, thereafter, cranial asymmetry in juvenile Solea senegalensis (right sideness, Soleidae), Cynoglossus semilaevis (left sideness, Cynoglossidae), and Paralichthys olivaceus (left sideness, Paralichthyidae) with a bottom-dwelling lifestyle. Our results correct the current misunderstanding that eye migration is driven by the cranial asymmetry and simplify the explanation for broken left/right eye-symmetry. Our findings should help to focus the search on eye migration-related genes associated with cell proliferation. Finally, a novel model is proposed in this research which provides a reasonable explanation for differences in the migrating eye between, and sometimes within, different species of flatfish and which should aid in our overall understanding of eye migration in the ontogenesis and evolution of Pleuronectiformes.

Original languageEnglish (US)
Pages (from-to)200-207
Number of pages8
JournalDevelopmental Biology
Volume351
Issue number1
DOIs
StatePublished - Mar 1 2011

Keywords

  • Cell proliferation
  • Cranial asymmetry
  • Eye migration
  • Flatfish
  • Left/right asymmetry
  • Suborbital tissue

ASJC Scopus subject areas

  • Molecular Biology
  • Developmental Biology
  • Cell Biology

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