A high frequency of overlapping gene expression in compacted eukaryotic genomes

Abstract

The gene density of eukaryotic nuclear genomes is generally low relative to prokaryotes, but several eukaryotic lineages (many parasites or endosymbionts) have independently evolved highly compacted, gene-dense genomes. The best studied of these are the microsporidia, highly adapted fungal parasites, and the nucleomorphs, relict nuclei of endosymbiotic algae found in cryptomonads and chlorarachniophytes. These systems are now models for the effects of compaction on the form and dynamics of the nuclear genome. Here we report a large-scale investigation of gene expression from compacted eukaryotic genomes. We have conducted EST surveys of the microsporidian Antonospora locustae and nucleomorphs of the cryptomonad Guillardia theta and the chlorarachniophyte Bigelowiella natans. In all three systems we find a high frequency of mRNA molecules that encode sequence from more than one gene. There is no bias for these genes to be on the same strand, so it is unlikely that these mRNAs represent operons. Instead, compaction appears to have reduced the intergenic regions to such an extent that control elements like promoters and terminators have been forced into or beyond adjacent genes, resulting in long untranslated regions that encode other genes. Normally, transcriptional overlap can interfere with expression of a gene, but these genomes cope with high frequencies of overlap and with termination signals within expressed genes. These findings also point to serious practical difficulties in studying expression in compacted genomes, because many techniques, such as arrays or serial analysis of gene expression will be misleading.genome compaction ͉ microsporidia ͉ nucleomorph ͉ overlapping transcription

The endosymbiotic origin, diversification and fate of plastids

“…Other interesting differences have been found in how these genomes have reacted to whatever process led to their severe reduction and compaction. For example, introns in cryptomonad nucleomorphs are not unusual in size or sequence, but they are extremely rare in number: the G. theta genome has only 18 introns (Douglas et al 2001;Williams et al 2005), and the nucleomorph of Hemiselmis andersenii has lost them altogether (Lane et al 2007). In contrast, chlorarachniophyte nucleomorph genes are riddled with introns: the B. natans genome retains over 800 identified introns, and most seem to be ancient introns conserved with green algae and other chlorarachniophytes (Gilson et al 2006).…”

“…Between these repeats, the chromosomes are 'jam-packed' with genes, the sequenced genomes have gene densities of about one gene per kilobase, the highest known density for a nuclear genome. This tight organization has apparently affected gene expression in nucleomorphs in both cryptomonads and chlorarachniophytes, so that there is now a high frequency of overlapping transcription: in Guillardia theta, nearly 100 per cent of characterized transcripts either begin in an upstream gene, terminate within or beyond a downstream gene, or both (Williams et al 2005).…”

Microsporidian genome analysis reveals evolutionary strategies for obligate intracellular growth

“…Most genes are encoded by discrete transcripts with either unusually short UTRs or no UTRs at all (Supplemental Fig. S2; Supplemental Material), in contrast to the large multigenic transcripts previously identified in E. cuniculi (Williams et al 2005;Gill et al 2010). Calculation of RNA-seq read coverage across five feature types (coding, 59 UTR, 39 UTR, antisense, and intergenic) showed that antisense transcription is approximately equivalent to intergenic transcription (Supplemental Fig.…”

An Automated Proteogenomic Method Uses Mass Spectrometry to Reveal Novel Genes in Zea mays

“…Antisense Overlapping Genes-Overlapping natural antisense transcripts (NATs), once believed to predominantly exist in bacterial and viral genomes (28), have recently been observed in eukaryotes (29) including humans (30). Although most overlapping NATs are identified by transcriptional evidence (31) and homology (32), there are few documented cases of overlapping NATs in which both genes are translated.…”