The Evolutionary History of Saccharomyces Species Inferred from Completed Mitochondrial Genomes and Revision in the 'yeast Mitochondrial Genetic Code'

Overview

Journal DNA Res

Publisher Oxford University Press

Specialties Genetics
Molecular Biology

Date 2017 Oct 10

PMID 28992063

Citations 18

Authors

Pavol Sulo

Dana Szaboova

Peter Bielik

Silvia Polakova

Katarina Soltys

Katarina Jatzova

Tomas Szemes

Affiliations

Soon will be listed here.

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.

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References

Clark-Walker G, Weiller G . The structure of the small mitochondrial DNA of Kluyveromyces thermotolerans is likely to reflect the ancestral gene order in fungi. J Mol Evol. 1994; 38(6):593-601. DOI: 10.1007/BF00175879. View

Foury F, Roganti T, Lecrenier N, Purnelle B . The complete sequence of the mitochondrial genome of Saccharomyces cerevisiae. FEBS Lett. 1999; 440(3):325-31. DOI: 10.1016/s0014-5793(98)01467-7. View

Clark-Walker G . Evolution of mitochondrial genomes in fungi. Int Rev Cytol. 1992; 141:89-127. DOI: 10.1016/s0074-7696(08)62064-1. View

Schafer B . RNA maturation in mitochondria of S. cerevisiae and S. pombe. Gene. 2005; 354:80-5. DOI: 10.1016/j.gene.2005.03.032. View

Hofmann T, Min J, Zassenhaus H . Formation of the 3' end of yeast mitochondrial mRNAs occurs by site-specific cleavage two bases downstream of a conserved dodecamer sequence. Yeast. 1993; 9(12):1319-30. DOI: 10.1002/yea.320091205. View

Turk E, Das V, Seibert R, Andrulis E . The mitochondrial RNA landscape of Saccharomyces cerevisiae. PLoS One. 2013; 8(10):e78105. PMC: 3797045. DOI: 10.1371/journal.pone.0078105. View

Osinga K, de Vries E, van der Horst G, Tabak H . Initiation of transcription in yeast mitochondria: analysis of origins of replication and of genes coding for a messenger RNA and a transfer RNA. Nucleic Acids Res. 1984; 12(4):1889-900. PMC: 318628. DOI: 10.1093/nar/12.4.1889. View

Peris D, Sylvester K, Libkind D, Goncalves P, Sampaio J, Alexander W . Population structure and reticulate evolution of Saccharomyces eubayanus and its lager-brewing hybrids. Mol Ecol. 2014; 23(8):2031-45. DOI: 10.1111/mec.12702. View

Lang B, Jakubkova M, Hegedusova E, Daoud R, Forget L, Brejova B . Massive programmed translational jumping in mitochondria. Proc Natl Acad Sci U S A. 2014; 111(16):5926-31. PMC: 4000857. DOI: 10.1073/pnas.1322190111. View

10.

Wolters J, Chiu K, Fiumera H . Population structure of mitochondrial genomes in Saccharomyces cerevisiae. BMC Genomics. 2015; 16:451. PMC: 4464245. DOI: 10.1186/s12864-015-1664-4. View

11.

Petersen R, Langkjaer R, Hvidtfeldt J, Gartner J, Palmen W, Ussery D . Inheritance and organisation of the mitochondrial genome differ between two Saccharomyces yeasts. J Mol Biol. 2002; 318(3):627-36. DOI: 10.1016/S0022-2836(02)00037-2. View

12.

Fields D, Gutell R . An analysis of large rRNA sequences folded by a thermodynamic method. Fold Des. 1996; 1(6):419-30. DOI: 10.1016/S1359-0278(96)00058-2. View

13.

Langkjaer R, Casaregola S, Ussery D, Gaillardin C, Piskur J . Sequence analysis of three mitochondrial DNA molecules reveals interesting differences among Saccharomyces yeasts. Nucleic Acids Res. 2003; 31(12):3081-91. PMC: 162263. DOI: 10.1093/nar/gkg423. View

14.

Gaillardin C, Neuveglise C, Kerscher S, Nicaud J . Mitochondrial genomes of yeasts of the Yarrowia clade. FEMS Yeast Res. 2011; 12(3):317-31. DOI: 10.1111/j.1567-1364.2011.00782.x. View

15.

Lecrenier N, Foury F . New features of mitochondrial DNA replication system in yeast and man. Gene. 2000; 246(1-2):37-48. DOI: 10.1016/s0378-1119(00)00107-4. View

16.

Lee C, Zeng J, Drew B, Sallam T, Martin-Montalvo A, Wan J . The mitochondrial-derived peptide MOTS-c promotes metabolic homeostasis and reduces obesity and insulin resistance. Cell Metab. 2015; 21(3):443-54. PMC: 4350682. DOI: 10.1016/j.cmet.2015.02.009. View

17.

Moran J, Zimmerly S, Eskes R, Kennell J, Lambowitz A, Butow R . Mobile group II introns of yeast mitochondrial DNA are novel site-specific retroelements. Mol Cell Biol. 1995; 15(5):2828-38. PMC: 230514. DOI: 10.1128/MCB.15.5.2828. View

18.

Konings D, Gutell R . A comparison of thermodynamic foldings with comparatively derived structures of 16S and 16S-like rRNAs. RNA. 1995; 1(6):559-74. PMC: 1369301. View

19.

Dubot A, Godinot C, Dumur V, Sablonniere B, Stojkovic T, Cuisset J . GUG is an efficient initiation codon to translate the human mitochondrial ATP6 gene. Biochem Biophys Res Commun. 2003; 313(3):687-93. DOI: 10.1016/j.bbrc.2003.12.013. View

20.

Sipiczki M . Interspecies hybridization and recombination in Saccharomyces wine yeasts. FEMS Yeast Res. 2008; 8(7):996-1007. DOI: 10.1111/j.1567-1364.2008.00369.x. View