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Published online on May 5, 2008
Proc. Natl. Acad. Sci. USA, 10.1073/pnas.0802293105


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EVOLUTION
Centrosomal RNA correlates with intron-poor nuclear genes in Spisula oocytes

Mark C. Alliegro* and Mary Anne Alliegro

Josephine Bay Paul Center, Marine Biological Laboratory, Woods Hole, MA 02543

Communicated by Lynn Margulis, University of Massachusetts, Amherst, MA, March 12, 2008 (received for review November 1, 2007)

Abstract

The evolutionary origin of centriole/kinetosomes, centrosomes, and other microtubule organizing centers (MTOCs), whether by direct filiation or symbiogenesis, has been controversial for >50 years. Centrioles, like mitochondria and chloroplasts, duplicate independently of the nucleus and constitute a heritable system independent of chromosomal DNA. Nucleic acids endogenous to the MTOC would support evolutionary origin by symbiogenesis. To date, most reports of centrosome-associated nucleic acids have used generalized reagents such as RNases and nucleic acid dyes. Here, from a library of RNAs extracted from isolated surf clam (Spisula solidissima) centrosomes, we describe a group of centrosome-associated transcripts representing a structurally unique intron-poor collection of nuclear genes skewed toward nucleic acid metabolism. Thus, we resolve the debate over the existence of centrosome-associated RNA (cnRNA). A subset of cnRNAs contain functional domains that are highly conserved across distant taxa, such as nucleotide polymerase motifs. In situ localization of cnRNA65, a molecule with an RNA polymerase domain, showed it is present in the intact oocyte nucleus (germinal vesicle). Its expression, therefore, precedes the appearance of {gamma}-tubulin-containing centrosomes. At this stage, the in situ signal resembles the nucleolinus, a poorly understood organelle proposed to play a role in spindle formation. After oocyte activation and germinal vesicle breakdown, cnRNA65 persists as a cytoplasmic patch within which {gamma}-tubulin-stained centrosomes can be seen. These observations provoke the question of whether cnRNAs and the nucleolinus serve as cytological progenitors of the centrosome and may support a symbiogenetic model for its evolution.

centrosome | evolution | nucleolinus


Footnotes

Author contributions: M.C.A. and M.A.A. designed research; M.C.A. and M.A.A. performed research; M.C.A. and M.A.A. contributed new reagents/analytic tools; M.C.A. and M.A.A. analyzed data; and M.C.A. wrote the paper.

The authors declare no conflict of interest.

*To whom correspondence should be addressed. E-mail: malliegro{at}mbl.edu

© 2008 by The National Academy of Sciences of the USA


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