Centrosomal RNA correlates with intron-poor nuclear genes in Spisula oocytes.
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.
Alliegro
Mark C
MC
Josephine Bay Paul Center, Marine Biological Laboratory, Woods Hole, MA 02543, USA. malliegro@mbl.edu
Alliegro
Mary Anne
MA
D000818:Animals; D002467:Cell Nucleus / Q000235:genetics*; D018385:Centrosome / Q000378:metabolism*; D004247:DNA / Q000378:metabolism; D005786:Gene Expression Regulation; D016678:Genome; D007438:Introns / Q000235:genetics*; D009865:Oocytes / Q000166:cytology / Q000378:metabolism*; D016133:Polymerase Chain Reaction; D012313:RNA / Q000737:chemistry / Q000378:metabolism*; D034443:RNA Transport; D049890:Spisula / Q000166:cytology* / Q000235:genetics*
D012313:RNA; D004247:DNA