Intron Evolution and Information processing in the DNA polymerase α gene in spirotrichous ciliates: A hypothesis for interconversion between DNA and RNA deletion

Wei-Jen Chang,Victoria M Addis,Laura F Landweber,Anya J Li,David H Ardell,Elin Axelsson

doi:10.1186/1745-6150-2-6

Wei-Jen Chang, Victoria M Addis + Show 4 more

Open Access

https://doi.org/10.1186/1745-6150-2-6

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Abstract

BackgroundThe somatic DNA molecules of spirotrichous ciliates are present as linear chromosomes containing mostly single-gene coding sequences with short 5' and 3' flanking regions. Only a few conserved motifs have been found in the flanking DNA. Motifs that may play roles in promoting and/or regulating transcription have not been consistently detected. Moreover, comparing subtelomeric regions of 1,356 end-sequenced somatic chromosomes failed to identify more putatively conserved motifs.ResultsWe sequenced and compared DNA and RNA versions of the DNA polymerase α (pol α) gene from nine diverged spirotrichous ciliates. We identified a G-C rich motif aaTACCGC(G/C/T) upstream from transcription start sites in all nine pol α orthologs. Furthermore, we consistently found likely polyadenylation signals, similar to the eukaryotic consensus AAUAAA, within 35 nt upstream of the polyadenylation sites. Numbers of introns differed among orthologs, suggesting independent gain or loss of some introns during the evolution of this gene. Finally, we discuss the occurrence of short direct repeats flanking some introns in the DNA pol α genes. These introns flanked by direct repeats resemble a class of DNA sequences called internal eliminated sequences (IES) that are deleted from ciliate chromosomes during development.ConclusionOur results suggest that conserved motifs are present at both 5' and 3' untranscribed regions of the DNA pol α genes in nine spirotrichous ciliates. We also show that several independent gains and losses of introns in the DNA pol α genes have occurred in the spirotrichous ciliate lineage. Finally, our statistical results suggest that proven introns might also function in an IES removal pathway. This could strengthen a recent hypothesis that introns evolve into IESs, explaining the scarcity of introns in spirotrichs. Alternatively, the analysis suggests that ciliates might occasionally use intron splicing to correct, at the RNA level, failures in IES excision during developmental DNA elimination.ReviewersThis article was reviewed by Dr. Alexei Fedorov (referred by Dr. Manyuan Long), Dr. Martin A. Huynen and Dr. John M. Logsdon.

Highlights

The somatic DNA molecules of spirotrichous ciliates are present as linear chromosomes containing mostly single-gene coding sequences with short 5' and 3' flanking regions
Our results suggest that conserved motifs, perhaps participating in gene regulation, are present in both 5' and 3' untranscribed regions of the DNA pol α genes
Our data suggest that several independent gains and losses of introns in DNA pol α genes have occurred in the spirotrichous ciliate lineage

Summary

Introduction

The somatic DNA molecules of spirotrichous ciliates are present as linear chromosomes containing mostly single-gene coding sequences with short 5' and 3' flanking regions. Tens of thousands of IESs must be removed during macronuclear development, while the MDSs are "sewn together" leaving one copy of the pair of direct repeats at the "stitch" (Fig. 1, see Table 1). After this event, the processed germline chromosomes undergo first heavy fragmentation, end-capping with telomeres, and differential replication, to give rise to the macronuclear chromosomes or "nanochromosomes" (Fig. 1). A typical macronuclear chromosome contains the coding region of a gene plus short noncoding regions at the 5' and 3' ends

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