High Variability of Mitochondrial Gene Order Among Fungi

Overview

Journal Genome Biol Evol

Publisher Oxford University Press

Specialties Biology
Genetics
Molecular Biology

Date 2014 Feb 8

PMID 24504088

Citations 112

Authors

Gabriela Aguileta

Damien M de Vienne

Oliver N Ross

Michael E Hood

Tatiana Giraud

Elsa Petit

Toni Gabaldon

Affiliations

Soon will be listed here.

Abstract

From their origin as an early alpha proteobacterial endosymbiont to their current state as cellular organelles, large-scale genomic reorganization has taken place in the mitochondria of all main eukaryotic lineages. So far, most studies have focused on plant and animal mitochondrial (mt) genomes (mtDNA), but fungi provide new opportunities to study highly differentiated mtDNAs. Here, we analyzed 38 complete fungal mt genomes to investigate the evolution of mtDNA gene order among fungi. In particular, we looked for evidence of nonhomologous intrachromosomal recombination and investigated the dynamics of gene rearrangements. We investigated the effect that introns, intronic open reading frames (ORFs), and repeats may have on gene order. Additionally, we asked whether the distribution of transfer RNAs (tRNAs) evolves independently to that of mt protein-coding genes. We found that fungal mt genomes display remarkable variation between and within the major fungal phyla in terms of gene order, genome size, composition of intergenic regions, and presence of repeats, introns, and associated ORFs. Our results support previous evidence for the presence of mt recombination in all fungal phyla, a process conspicuously lacking in most Metazoa. Overall, the patterns of rearrangements may be explained by the combined influences of recombination (i.e., most likely nonhomologous and intrachromosomal), accumulated repeats, especially at intergenic regions, and to a lesser extent, mobile element dynamics.

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References

Xavier B, Miao V, Jonsson Z, Andresson O . Mitochondrial genomes from the lichenized fungi Peltigera membranacea and Peltigera malacea: features and phylogeny. Fungal Biol. 2012; 116(7):802-14. DOI: 10.1016/j.funbio.2012.04.013. View

Tuller T, Girshovich Y, Sella Y, Kreimer A, Freilich S, Kupiec M . Association between translation efficiency and horizontal gene transfer within microbial communities. Nucleic Acids Res. 2011; 39(11):4743-55. PMC: 3113575. DOI: 10.1093/nar/gkr054. View

Rawlings T, Collins T, Bieler R . A major mitochondrial gene rearrangement among closely related species. Mol Biol Evol. 2001; 18(8):1604-9. DOI: 10.1093/oxfordjournals.molbev.a003949. View

Eldarov M, Mardanov A, Beletsky A, Ravin N, Skryabin K . Complete sequence and analysis of the mitochondrial genome of the methylotrophic yeast Hansenula polymorpha DL-1. FEMS Yeast Res. 2011; 11(6):464-72. DOI: 10.1111/j.1567-1364.2011.00736.x. View

Posada D, Crandall K . Evaluation of methods for detecting recombination from DNA sequences: computer simulations. Proc Natl Acad Sci U S A. 2001; 98(24):13757-62. PMC: 61114. DOI: 10.1073/pnas.241370698. View

Forget L, Ustinova J, Wang Z, Huss V, Lang B . Hyaloraphidium curvatum: a linear mitochondrial genome, tRNA editing, and an evolutionary link to lower fungi. Mol Biol Evol. 2002; 19(3):310-9. DOI: 10.1093/oxfordjournals.molbev.a004084. View

Vlcek C, Marande W, Teijeiro S, Lukes J, Burger G . Systematically fragmented genes in a multipartite mitochondrial genome. Nucleic Acids Res. 2010; 39(3):979-88. PMC: 3035467. DOI: 10.1093/nar/gkq883. View

Ferandon C, Moukha S, Callac P, Benedetto J, Castroviejo M, Barroso G . The Agaricus bisporus cox1 gene: the longest mitochondrial gene and the largest reservoir of mitochondrial group i introns. PLoS One. 2010; 5(11):e14048. PMC: 2987802. DOI: 10.1371/journal.pone.0014048. View

Nabholz B, Glemin S, Galtier N . The erratic mitochondrial clock: variations of mutation rate, not population size, affect mtDNA diversity across birds and mammals. BMC Evol Biol. 2009; 9:54. PMC: 2660308. DOI: 10.1186/1471-2148-9-54. View

10.

Rocha E . DNA repeats lead to the accelerated loss of gene order in bacteria. Trends Genet. 2003; 19(11):600-3. DOI: 10.1016/j.tig.2003.09.011. View

11.

Lazowska J, Jacq C, SLONIMSKI P . Sequence of introns and flanking exons in wild-type and box3 mutants of cytochrome b reveals an interlaced splicing protein coded by an intron. Cell. 1980; 22(2 Pt 2):333-48. DOI: 10.1016/0092-8674(80)90344-x. View

12.

Hane J, Lowe R, Solomon P, Tan K, Schoch C, Spatafora J . Dothideomycete plant interactions illuminated by genome sequencing and EST analysis of the wheat pathogen Stagonospora nodorum. Plant Cell. 2007; 19(11):3347-68. PMC: 2174895. DOI: 10.1105/tpc.107.052829. View

13.

Gabaldon T, Huynen M . Reconstruction of the proto-mitochondrial metabolism. Science. 2003; 301(5633):609. DOI: 10.1126/science.1085463. View

14.

Taylor J, Berbee M . Dating divergences in the Fungal Tree of Life: review and new analyses. Mycologia. 2007; 98(6):838-49. DOI: 10.3852/mycologia.98.6.838. View

15.

Sanderson M . r8s: inferring absolute rates of molecular evolution and divergence times in the absence of a molecular clock. Bioinformatics. 2003; 19(2):301-2. DOI: 10.1093/bioinformatics/19.2.301. View

16.

Pantou M, Kouvelis V, Typas M . The complete mitochondrial genome of Fusarium oxysporum: insights into fungal mitochondrial evolution. Gene. 2008; 419(1-2):7-15. DOI: 10.1016/j.gene.2008.04.009. View

17.

Bullerwell C, Gray M . Evolution of the mitochondrial genome: protist connections to animals, fungi and plants. Curr Opin Microbiol. 2004; 7(5):528-34. DOI: 10.1016/j.mib.2004.08.008. View

18.

Lavrov D . Rapid proliferation of repetitive palindromic elements in mtDNA of the endemic Baikalian sponge Lubomirskia baicalensis. Mol Biol Evol. 2009; 27(4):757-60. DOI: 10.1093/molbev/msp317. View

19.

Davila J, Arrieta-Montiel M, Wamboldt Y, Cao J, Hagmann J, Shedge V . Double-strand break repair processes drive evolution of the mitochondrial genome in Arabidopsis. BMC Biol. 2011; 9:64. PMC: 3193812. DOI: 10.1186/1741-7007-9-64. View

20.

Bullerwell C, Lang B . Fungal evolution: the case of the vanishing mitochondrion. Curr Opin Microbiol. 2005; 8(4):362-9. DOI: 10.1016/j.mib.2005.06.009. View