Spiralian quartet developmental potential is regulated by specific localization elements that mediate asymmetric RNA segregation

Development. 2010 Dec;137(23):4039-49. doi: 10.1242/dev.055269. Epub 2010 Nov 1.

Abstract

Spiralian embryos are found in a large group of invertebrate phyla but are largely uncharacterized at a molecular level. These embryos are thought to be particularly reliant on autonomous cues for patterning, and thus represent potentially useful models for understanding asymmetric cell division. The series of asymmetric divisions that produce the micromere quartets are particularly important for patterning because they subdivide the animal-vegetal axis into tiers of cells with different developmental potentials. In the embryo of the snail Ilyanassa, the IoLR5 RNA is specifically segregated to the first quartet cells during the third cleavage. Here, we show that this RNA, and later the protein, are maintained in the 1q(121) cells and their descendents throughout development. Some IoLR5-expressing cells become internalized and join the developing cerebral ganglia. Knockdown of IoLR5 protein results in loss of the larval eyes, which normally develop in association with these ganglia. Segregation of this RNA to the first quartet cells does not occur if centrosomal localization is bypassed. We show that the specific inheritance of the RNA by the first quartet cells is driven by a discrete RNA sequence in the 3' UTR that is necessary and sufficient for localization and segregation, and that localization of another RNA to the first quartet is mediated by a similar element. These results demonstrate that micromere quartet identity, a hallmark of the ancient spiralian developmental program, is controlled in part by specific RNA localization motifs.

Publication types

  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Base Sequence
  • Centrosome / metabolism
  • Embryo, Nonmammalian / cytology
  • Embryo, Nonmammalian / metabolism*
  • Gene Expression Regulation, Developmental
  • Gene Knockdown Techniques
  • Larva / cytology
  • Larva / metabolism
  • Molecular Sequence Data
  • Nucleic Acid Conformation
  • Phenotype
  • RNA / chemistry
  • RNA / genetics*
  • RNA Transport
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Regulatory Sequences, Ribonucleic Acid / genetics*
  • Snails / cytology
  • Snails / embryology*
  • Snails / genetics*

Substances

  • RNA, Messenger
  • Regulatory Sequences, Ribonucleic Acid
  • RNA