Abstract
The ciliate Oxytricha trifallax maintains two genomes: a germline genome that is active only during sexual conjugation and a transcriptionally active, somatic genome that derives from the germline via extensive sequence reduction and rearrangement. Previously, we found that long noncoding (lnc) RNA “templates”—telomere-containing, RNA-cached copies of mature chromosomes—provide the information to program the rearrangement process. Here we used a modified RNA-seq approach to conduct the first genome-wide search for endogenous, telomere-to-telomere RNA transcripts. We find that during development, Oxytricha produces long noncoding RNA copies for over 10,000 of its 16,000 somatic chromosomes, consistent with a model in which Oxytricha transmits an RNA-cached copy of its somatic genome to the sexual progeny. Both the primary sequence and expression profile of a somatic chromosome influence the temporal distribution and abundance of individual template RNAs. This suggests that Oxytricha may undergo multiple rounds of DNA rearrangement during development. These observations implicate a complex set of thousands of long RNA molecules in the wiring and maintenance of a highly elaborate somatic genome architecture.
Highlights
Long noncoding RNAs, defined as transcripts >200 nt with no protein coding function, were once thought to represent primarily nonfunctional “junk” transcription
Our laboratory experimentally demonstrated that epigenetically inherited, maternal Long noncoding RNAs (lncRNAs) are essential for genome remodeling in the ciliate Oxytricha trifallax (Nowacki et al 2008)
The six time points include: zero hours post-mixing (0 h), after compatible Oxytricha strains are combined but before mating begins; 6 h post-mixing, shortly after the first putative template RNAs were detected in Nowacki et al (2008); 12 h post-mixing, which previous studies suggested might be the peak of template RNA production; 18 h post-mixing; and 36 and 60 h post-mixing, when few or no templates were previously observed
Summary
Long noncoding RNAs (lncRNAs), defined as transcripts >200 nt with no protein coding function, were once thought to represent primarily nonfunctional “junk” transcription. Our laboratory experimentally demonstrated that epigenetically inherited, maternal lncRNAs are essential for genome remodeling in the ciliate Oxytricha trifallax (Nowacki et al 2008). We present evidence that Oxytricha produces complete RNA copies of thousands of its somatic chromosomes during nuclear differentiation and development. The larger macronucleus (MAC) contains the somatic genome, which is the source of gene transcription during asexual growth and reproduction. While the micronuclear genome consists of long diploid chromosomes, the MAC genome contains over 16,000 different chromosomes, most of which bear only a single gene and are a median length of 2515 bp (mean 3.2 kb) at a typical copy number of ∼1900n (Prescott 1994)
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