Limits...
Intron evolution in Saccharomycetaceae.

Hooks KB, Delneri D, Griffiths-Jones S - Genome Biol Evol (2014)

Bottom Line: Analysis of these intron sets shows that intron loss is at least two orders of magnitude more frequent than intron gain.Fine mapping of intron positions shows that intron sliding is rare, and that introns are almost always removed without changing the primary sequence of the encoded protein.However, we also find evidence that loss of a small number of introns is mediated by micro-homology, and that the number of intron losses is diminished in yeast species that have lost the microhomology end joining and nonhomologous end joining machinery.

View Article: PubMed Central - PubMed

ABSTRACT
Introns in protein-coding genes are very rare in hemiascomycetous yeast genomes. It has been suggested that these species have experienced extensive intron loss during their evolution from the postulated intron-rich fungal ancestor. However, no intron-devoidy east species have been identified and some of the introns remaining within the genomes of intron-poor species, such as Saccharomyces cerevisiae, appear to be beneficial during growth under stress conditions. In order to reveal the pattern of intron retention within intron-poor yeast species and better understand the mechanisms of intron evolution, we generated a comprehensive set of 250 orthologous introns in the 20 species that comprise the Saccharomycetaceae, by analyzing RNA deep-sequencing data and alignments of intron-containing genes. Analysis of these intron sets shows that intron loss is at least two orders of magnitude more frequent than intron gain. Fine mapping of intron positions shows that intron sliding is rare, and that introns are almost always removed without changing the primary sequence of the encoded protein. The latter finding is consistent with the prevailing view that homologous recombination between reverse-transcribed mature mRNAs and the corresponding genomic locus is the primary mechanism of intron loss. However, we also find evidence that loss of a small number of introns is mediated by micro-homology, and that the number of intron losses is diminished in yeast species that have lost the microhomology end joining and nonhomologous end joining machinery.

Show MeSH

Related in: MedlinePlus

Heatmap showing intron evolution within YGOB species. Each row represents one of the species listed on the right. Each column corresponds to an ancestral intron. For post-WGD species columns are divided in two to represent the presence of the duplicate copies. Blue indicates intron presence, orange indicates loss by replacement of the gene with cDNA, red shows intron loss accompanied by additional codons inserted or deleted, and gray shows unknown state of intron.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC4202332&req=5

evu196-F4: Heatmap showing intron evolution within YGOB species. Each row represents one of the species listed on the right. Each column corresponds to an ancestral intron. For post-WGD species columns are divided in two to represent the presence of the duplicate copies. Blue indicates intron presence, orange indicates loss by replacement of the gene with cDNA, red shows intron loss accompanied by additional codons inserted or deleted, and gray shows unknown state of intron.

Mentions: Across the 20 species and 235 ancestral genes, there were total of 5,553 “intron sites,” defined as sites that could contain an intron based on the presence of an intron at that position in at least one other species. In total, 1,168 of these intron sites are without an intron (0.21 introns missing per site per species) and 4,385 contained an intron (fig. 4, supplementary table S1, Supplementary Material online). The majority of missing introns (825/1,168, 71%) left the gene replaced with its cDNA version (adding or deleting a maximum of two codons, fig. 5A). There were 33 instances in 14 genes when intron removal was accompanied by a deletion or insertion of 3–40 codons. We found one clear case of intron sliding in the RPS22B gene in Eremothecium cymbalariae, E. gossypii, and K. lactis, where the 5′-UTR intron has been moved into the open reading frame (ORF) and is present after the initial A (fig. 5B). Finally, 310 additional introns, mainly in 5′-UTRs, appear to have been lost, but the mechanism of loss is unclear.Fig. 4.—


Intron evolution in Saccharomycetaceae.

Hooks KB, Delneri D, Griffiths-Jones S - Genome Biol Evol (2014)

Heatmap showing intron evolution within YGOB species. Each row represents one of the species listed on the right. Each column corresponds to an ancestral intron. For post-WGD species columns are divided in two to represent the presence of the duplicate copies. Blue indicates intron presence, orange indicates loss by replacement of the gene with cDNA, red shows intron loss accompanied by additional codons inserted or deleted, and gray shows unknown state of intron.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4202332&req=5

evu196-F4: Heatmap showing intron evolution within YGOB species. Each row represents one of the species listed on the right. Each column corresponds to an ancestral intron. For post-WGD species columns are divided in two to represent the presence of the duplicate copies. Blue indicates intron presence, orange indicates loss by replacement of the gene with cDNA, red shows intron loss accompanied by additional codons inserted or deleted, and gray shows unknown state of intron.
Mentions: Across the 20 species and 235 ancestral genes, there were total of 5,553 “intron sites,” defined as sites that could contain an intron based on the presence of an intron at that position in at least one other species. In total, 1,168 of these intron sites are without an intron (0.21 introns missing per site per species) and 4,385 contained an intron (fig. 4, supplementary table S1, Supplementary Material online). The majority of missing introns (825/1,168, 71%) left the gene replaced with its cDNA version (adding or deleting a maximum of two codons, fig. 5A). There were 33 instances in 14 genes when intron removal was accompanied by a deletion or insertion of 3–40 codons. We found one clear case of intron sliding in the RPS22B gene in Eremothecium cymbalariae, E. gossypii, and K. lactis, where the 5′-UTR intron has been moved into the open reading frame (ORF) and is present after the initial A (fig. 5B). Finally, 310 additional introns, mainly in 5′-UTRs, appear to have been lost, but the mechanism of loss is unclear.Fig. 4.—

Bottom Line: Analysis of these intron sets shows that intron loss is at least two orders of magnitude more frequent than intron gain.Fine mapping of intron positions shows that intron sliding is rare, and that introns are almost always removed without changing the primary sequence of the encoded protein.However, we also find evidence that loss of a small number of introns is mediated by micro-homology, and that the number of intron losses is diminished in yeast species that have lost the microhomology end joining and nonhomologous end joining machinery.

View Article: PubMed Central - PubMed

ABSTRACT
Introns in protein-coding genes are very rare in hemiascomycetous yeast genomes. It has been suggested that these species have experienced extensive intron loss during their evolution from the postulated intron-rich fungal ancestor. However, no intron-devoidy east species have been identified and some of the introns remaining within the genomes of intron-poor species, such as Saccharomyces cerevisiae, appear to be beneficial during growth under stress conditions. In order to reveal the pattern of intron retention within intron-poor yeast species and better understand the mechanisms of intron evolution, we generated a comprehensive set of 250 orthologous introns in the 20 species that comprise the Saccharomycetaceae, by analyzing RNA deep-sequencing data and alignments of intron-containing genes. Analysis of these intron sets shows that intron loss is at least two orders of magnitude more frequent than intron gain. Fine mapping of intron positions shows that intron sliding is rare, and that introns are almost always removed without changing the primary sequence of the encoded protein. The latter finding is consistent with the prevailing view that homologous recombination between reverse-transcribed mature mRNAs and the corresponding genomic locus is the primary mechanism of intron loss. However, we also find evidence that loss of a small number of introns is mediated by micro-homology, and that the number of intron losses is diminished in yeast species that have lost the microhomology end joining and nonhomologous end joining machinery.

Show MeSH
Related in: MedlinePlus