Evolution of Yeast Noncoding RNAs Reveals an Alternative Mechanism for Widespread Intron Loss

Department of Microbiology and Immunology, University of California, San Francisco, San Francisco, CA 94143-2200, USA.
Science (Impact Factor: 33.61). 11/2010; 330(6005):838-41. DOI: 10.1126/science.1194554
Source: PubMed


The evolutionary forces responsible for intron loss are unresolved. Whereas research has focused on protein-coding genes,
here we analyze noncoding small nucleolar RNA (snoRNA) genes in which introns, rather than exons, are typically the functional
elements. Within the yeast lineage exemplified by the human pathogen Candida albicans, we find—through deep RNA sequencing and genome-wide annotation of splice junctions—extreme compaction and loss of associated
exons, but retention of snoRNAs within introns. In the Saccharomyces yeast lineage, however, we find it is the introns that have been lost through widespread degeneration of splicing signals.
This intron loss, perhaps facilitated by innovations in snoRNA processing, is distinct from that observed in protein-coding
genes with respect to both mechanism and evolutionary timing.

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    • "Interestingly , this study revealed 602 novel transcriptionally active regions (TARs) in the Candida genome and numerous novel introns as well [35]. In another study, Mitrovich et al. have analyzed noncoding small nucleolar RNA (snoRNA) genes and revealed an alternative mechanism for widespread intron loss [36]. Application of this method in several other conditions with respect to adherence, disease propagation, biofilm formation, yeast-hyphae transition, and drug resistance will certainly provide an insight into the functioning of this organism in great detail. "

    Full-text · Dataset · Apr 2015
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    • "To determine whether CaEss1 functions in snoRNA termination, we obtained RNA-seq data from ts-mutant and control strains and examined the abundance of sequence reads at non polycistronc, independently-transcribed snoRNA genes of the box H/ACA-class [67]–[70]. In total, we examined expression of 26 H/ACA-class genes using Integrated Genome Viewer (IGV), and found that about one in five show evidence of readthrough as revealed by RNA-seq data. "
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    ABSTRACT: Candida albicans is a fungal pathogen that causes potentially fatal infections among immune-compromised individuals. The emergence of drug resistant C. albicans strains makes it important to identify new antifungal drug targets. Among potential targets are enzymes known as peptidyl-prolyl cis/trans isomerases (PPIases) that catalyze isomerization of peptide bonds preceding proline. We are investigating a PPIase called Ess1, which is conserved in all major human pathogenic fungi. Previously, we reported that C. albicans Ess1 is essential for growth and morphogenetic switching. In the present study, we re-evaluated these findings using more rigorous genetic analyses, including the use of additional CaESS1 mutant alleles, distinct marker genes, and the engineering of suitably-matched isogenic control strains. The results confirm that CaEss1 is essential for growth in C. albicans, but show that reduction of CaESS1 gene dosage by half (δ/+) does not interfere with morphogenetic switching. However, further reduction of CaEss1 levels using a conditional allele does reduce morphogenetic switching. We also examine the role of the linker α-helix that distinguishes C. albicans Ess1 from the human Pin1 enzyme, and present results of a genome-wide transcriptome analysis. The latter analysis indicates that CaEss1 has a conserved role in regulation of RNA polymerase II function, and is required for efficient termination of small nucleolar RNAs and repression of cryptic transcription in C. albicans.
    Full-text · Article · Mar 2013 · PLoS ONE
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    • "Reverse-transcriptase-mediated 3’-biased intron loss model [10] and genomic deletion model [10] were proposed as mechanisms underlying some permanent intron loss from genome. The model of degeneration of splicing signals [15] has been used to explain de-intronization of intronic sequences. On the other hand, intron transposition [10], [25], [26], self-splicing type II intron [10], [27], [28], and genomic duplication [10] have been postulated to explain different intron-gain events, in which newly gained introns are inserted into somewhere else in the genome with the original sequences remaining in the donor sites. "
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    ABSTRACT: The role of spliceosomal intronic structures played in evolution has only begun to be elucidated. Comparative genomic analyses of fungal snoRNA sequences, which are often contained within introns and/or exons, revealed that about one-third of snoRNA-associated introns in three major snoRNA gene clusters manifested polymorphisms, likely resulting from intron loss and gain events during fungi evolution. Genomic deletions can clearly be observed as one mechanism underlying intron and exon loss, as well as generation of complex introns where several introns lie in juxtaposition without intercalating exons. Strikingly, by tracking conserved snoRNAs in introns, we found that some introns had moved from one position to another by excision from donor sites and insertion into target sties elsewhere in the genome without needing transposon structures. This study revealed the origin of many newly gained introns. Moreover, our analyses suggested that intron-containing sequences were more prone to sustainable structural changes than DNA sequences without introns due to intron's ability to jump within the genome via unknown mechanisms. We propose that splicing-related structural features of introns serve as an additional motor to propel evolution.
    Preview · Article · Mar 2013 · PLoS ONE
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