Localized PEM mRNA and Protein Are Involved in Cleavage-Plane Orientation and Unequal Cell Divisions in Ascidians

Takefumi Negishi, Tatsuki Takada, Narudo Kawai, Hiroki Nishida

Research output: Contribution to journalArticle

53 Citations (Scopus)

Abstract

Background: Orientation and positioning of the cell division plane are essential for generation of invariant cleavage patterns and for unequal cell divisions during development. Precise control of the division plane is important for appropriate partitioning of localized factors, spatial arrangement of cells for proper intercellular interactions, and size control of daughter cells. Ascidian embryos show complex but invariant cleavage patterns mainly due to three rounds of unequal cleavage at the posterior pole. Results: The ascidian embryo is an emerging model for studies of developmental and cellular processes. The maternal Posterior End Mark (PEM) mRNA is localized within the egg and embryo to the posterior region. PEM is a novel protein that has no known domain. Immunostaining showed that the protein is also present in the posterior cortex and the in centrosome-attracting body (CAB) and that the localization is extraction-resistant. Here we show that PEM of Halocynthia roretzi is required for correct orientation of early-cleavage planes and subsequent unequal cell divisions because it repeatedly pulls a centrosome toward the posterior cortex and the CAB, respectively, where PEM mRNA and protein are localized. When PEM activity is suppressed, formation of the microtubule bundle linking the centrosome and the posterior cortex did not occur. PEM possibly plays a role in anchoring microtubule ends to the cortex. In our model of orientation of the early-cleavage planes, we also amend the allocation of the conventional animal-vegetal axis in ascidian embryos, and discuss how the newly proposed A-V axis provides the rationale for various developmental events and the fate map of this animal. Conclusions: The complex cleavage pattern in ascidian embryos can be explained by a simple rule of centrosome attraction mediated by localized PEM activity. PEM is the first gene identified in ascidians that is required for multiple spindle-positioning events.

Original languageEnglish
Pages (from-to)1014-1025
Number of pages12
JournalCurrent Biology
Volume17
Issue number12
DOIs
Publication statusPublished - 2007 Jun 19
Externally publishedYes

Fingerprint

Urochordata
centrosomes
Centrosome
Ascidiacea
Cell Division
cell division
embryo (animal)
Embryonic Structures
Cells
cortex
Messenger RNA
Animals
Proteins
proteins
Microtubules
microtubules
Halocynthia roretzi
Poles
Genes
Ovum

Keywords

  • CELLBIO
  • DEVBIO

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)

Cite this

Localized PEM mRNA and Protein Are Involved in Cleavage-Plane Orientation and Unequal Cell Divisions in Ascidians. / Negishi, Takefumi; Takada, Tatsuki; Kawai, Narudo; Nishida, Hiroki.

In: Current Biology, Vol. 17, No. 12, 19.06.2007, p. 1014-1025.

Research output: Contribution to journalArticle

Negishi, Takefumi ; Takada, Tatsuki ; Kawai, Narudo ; Nishida, Hiroki. / Localized PEM mRNA and Protein Are Involved in Cleavage-Plane Orientation and Unequal Cell Divisions in Ascidians. In: Current Biology. 2007 ; Vol. 17, No. 12. pp. 1014-1025.
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