Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2017 Dec 1;24(6):571-583.
doi: 10.1093/dnares/dsx026.

The evolutionary history of Saccharomyces species inferred from completed mitochondrial genomes and revision in the 'yeast mitochondrial genetic code'

Pavol Sulo  1 , Dana Szabóová  1 , Peter Bielik  1 , Silvia Poláková  1 , Katarína Šoltys  2 , Katarína Jatzová  1 , Tomáš Szemes  3   4   5
Affiliations

The evolutionary history of Saccharomyces species inferred from completed mitochondrial genomes and revision in the 'yeast mitochondrial genetic code'

Pavol Sulo et al. DNA Res. .

Abstract

The yeast Saccharomyces are widely used to test ecological and evolutionary hypotheses. A large number of nuclear genomic DNA sequences are available, but mitochondrial genomic data are insufficient. We completed mitochondrial DNA (mtDNA) sequencing from Illumina MiSeq reads for all Saccharomyces species. All are circularly mapped molecules decreasing in size with phylogenetic distance from Saccharomyces cerevisiae but with similar gene content including regulatory and selfish elements like origins of replication, introns, free-standing open reading frames or GC clusters. Their most profound feature is species-specific alteration in gene order. The genetic code slightly differs from well-established yeast mitochondrial code as GUG is used rarely as the translation start and CGA and CGC code for arginine. The multilocus phylogeny, inferred from mtDNA, does not correlate with the trees derived from nuclear genes. mtDNA data demonstrate that Saccharomyces cariocanus should be assigned as a separate species and Saccharomyces bayanus CBS 380T should not be considered as a distinct species due to mtDNA nearly identical to Saccharomyces uvarum mtDNA. Apparently, comparison of mtDNAs should not be neglected in genomic studies as it is an important tool to understand the origin and evolutionary history of some yeast species.

Keywords: genetic code; introns; mitochondrial DNA; phylogeny; yeasts.

PubMed Disclaimer

Figures

Figure 1
Figure 1
The genetic organization of Saccharomyces mtDNA. For simpler comparison, the circular genomes, exported from Vector NTI, were aligned at the beginning of the large rRNA subunit (rnl). Protein-coding genes, ribosomal RNA, rnpB are marked as arrows and bar, tRNA genes as black lines, introns with white rectangles, intronic and free-standing ORFs by gray arrows and replication origins with black circles. Gene nomenclature follows the rules described in GOBASE (atp for ATP synthetase subunits, cox for cytochrome oxidase subunits, cob for cytochrome b, rns for small rRNA ribosomal subunit, rnl for large rRNA ribosomal subunit, T2, C, H, etc. for particular tRNA coding genes, rps3 for ribosomal protein and rnpB for the RNA subunit of RNase P). Sizes are given on the bottom line in kbp.
Figure 2
Figure 2
GTG as the initiation codon and revised yeast mitochondrial code. (A) Initiation codons in cox3 gene. (B) Initiation codons in ORF1 gene. Sequences overlapping with cox2 3′end are underlined. (C) Revised yeast mitochondrial code. Exceptional codons are grey-shadowed.
Figure 3
Figure 3
Occurrence of introns and free-standing ORFs. Introns and free-standing ORFs with at least one motif characteristic for the homing endonucleases (LAGLIDADG, GIY-YIG, etc.) are in black; without reading frame are white; with truncated ORF interrupted by stop codon are spotted. Numbers indicate the base preceding the intron insertion site in the CDS. Positions of introns, known as mobile, in S. cerevisiae are marked in bold; I—group I introns, II—group II introns. ORF1, ORF2 and ORF4 correspond to the nomenclature used in reference (their ORF5 is an ORF coded by the rnl ω intron). Only ORFs containing at least one endonuclease/maturase motif were considered.
Figure 4
Figure 4
Alternative splicing of cox1I5β (A) and cobI1α (B). Arrows mark exons–introns boundaries. Consensus of alternative splice site as described in reference and hypothetical alternative splice site in cobI1α are underlined.
Figure 5
Figure 5
Comparison of mitochondrial gene order in Saccharomyces. Individual gene clusters are highlighted by different shades of grey. Pentagon symbols indicate the transcription direction.
Figure 6
Figure 6
Saccharomyces phylogeny. Both trees were constructed from unambiguously aligned concatenated DNA sequences using the Maximum likelihood phylogeny PhyML program. (A) mtDNA-derived phylogeny from DNA sequences coding for proteins in the order cox1, atp8, atp6, cob, atp9, cox2, cox3. (B) Nuclear DNA-derived phylogenetic tree from CCA1, CYT1, MLS1, RPS5, LAS1, MET4, NUP116, ZDS2, PDR10 and DSN1 protein-coding genes used in population studies. The branch length is proportional to the nucleotide differences indicated by the bar. The numbers given at the nodes are the frequencies of a given branch appearing in 1,000 bootstrap replications. All are above 50%, indicating good statistical support. Naumovia castellii NRRL Y-12630 was used as an outgroup.
See this image and copyright information in PMC

Similar articles

See all similar articles

Cited by

See all "Cited by" articles

References

    1. Vaughan-Martini A., Martini A.. 2011, Saccharomyces meyen ex reess (1870) In: Kurtzman C.P., ed. The Yeasts, A Taxonomic Study, Elsevier: Amsterdam, NL: pp. 733–46.
    1. Replansky T., Koufopanou V., Greig D., Bell G.. 2008, Saccharomyces sensu stricto as a model system for evolution and ecology, Trends Ecol. Evol., 23, 494–501. - PubMed
    1. Sipiczki M. 2008, Interspecies hybridization and recombination in Saccharomyces wine yeasts, FEMS Yeast Res., 8, 996–1007. - PubMed
    1. Borneman A.R., Pretorius I.S.. 2015, Genomic insights into the Saccharomyces sensu stricto complex, Genetics, 199, 281–91. - PMC - PubMed
    1. Baker E., Wang B., Bellora N., et al.2015, The genome sequence of Saccharomyces eubayanus and the domestication of lager-brewing yeasts, Mol. Biol. Evol., 32, 2818–31. - PMC - PubMed
-