title: Evolution along the mutation gradient in the dynamic mitochondrial genome of salamanders.
abstract: Mitochondria are intracellular organelles where oxidative phosphorylation is carried out to complete ATP synthesis. Mitochondria have their own genome; in metazoans, this is a small, circular molecule encoding 13 electron transport proteins, 22 tRNAs, and 2 rRNAs. In invertebrates, mitochondrial gene rearrangement is common, and it is correlated with increased substitution rates. In vertebrates, mitochondrial gene rearrangement is rare, and its relationship to substitution rate remains unexplored. Mitochondrial genes can also show spatial variation in substitution rates around the genome due to the mechanism of mtDNA replication, which produces a mutation gradient. To date, however, the strength of the mutation gradient and whether movement along the gradient in rearranged (or otherwise modified) genomes impacts genic substitution rates remain unexplored in the majority of vertebrates. Salamanders include both normal mitochondrial genomes and independently derived rearrangements and expansions, providing a rare opportunity to test the effects of large-scale changes to genome architecture on vertebrate mitochondrial gene sequence evolution. We show that: 1) rearranged/expanded genomes have higher substitution rates; 2) most genes in rearranged/expanded genomes maintain their position along the mutation gradient, substitution rates of the genes that do move are unaffected by their new position, and the gradient in salamanders is weak; and 3) genomic rearrangements/expansions occur independent of levels of selective constraint on genes. Together, our results demonstrate that large-scale changes to genome architecture impact mitochondrial gene evolution in predictable ways; however, despite these impacts, the same functional constraints act on mitochondrial protein-coding genes in both modified and normal genomes.
authors.affiliation: Department of Biology, Colorado State University.
authors.forename: Rebecca A
authors.initials: RA
authors.lastname: Chong
authors.forename: Rachel Lockridge
authors.initials: RL
authors.lastname: Mueller
mesh_terms: D000818:Animals; D004272:DNA, Mitochondrial / Q000235:genetics*; D019143:Evolution, Molecular; D015321:Gene Rearrangement; D054629:Genome, Mitochondrial / Q000235:genetics*; D008928:Mitochondria / Q000235:genetics; D009154:Mutation; D010802:Phylogeny; D012335:RNA, Ribosomal / Q000235:genetics; D012343:RNA, Transfer / Q000235:genetics; D014562:Caudata / Q000235:genetics*
chemical_list: D004272:DNA, Mitochondrial; D012335:RNA, Ribosomal; D012343:RNA, Transfer
keywords: gene rearrangement; genome expansion; selective constraint; substitution rates
references.citation: Evolution. 2011 Sep;65(9):2706-11
references.pmid: 21884067
references.citation: Mol Biol Evol. 2006 Aug;23(8):1516-24
references.pmid: 16705079
references.citation: J Mol Evol. 2001 Dec;53(6):634-41
references.pmid: 11677623
references.citation: BMC Genomics. 2011 Jan 27;12:73
references.pmid: 21269523
references.citation: Gene. 1999 Sep 30;238(1):195-209
references.pmid: 10570997
references.citation: Mol Biol Evol. 2007 Aug;24(8):1586-91
references.pmid: 17483113
references.citation: Genetics. 2003 Oct;165(2):735-45
references.pmid: 14573484
references.citation: DNA Cell Biol. 2004 Oct;23(10):707-14
references.pmid: 15585129
references.citation: J Mol Evol. 1993 Sep;37(3):281-95
references.pmid: 8230252
references.citation: BMC Genomics. 2010 Aug 19;11:479
references.pmid: 20723209
references.citation: Mol Biol Evol. 2005 Oct;22(10):2104-12
references.pmid: 15987876
references.citation: Mol Biol Evol. 1996 Feb;13(2):418-21
references.pmid: 8587506
references.citation: Mol Biol Evol. 1998 Aug;15(8):957-66
references.pmid: 9718723
references.citation: Mol Biol Evol. 2006 Jan;23(1):227-34
references.pmid: 16177229
references.citation: Trends Ecol Evol. 2001 Jun 1;16(6):269-271
references.pmid: 11369092
references.citation: Proc Natl Acad Sci U S A. 1987 Oct;84(20):7183-7
references.pmid: 3478691
references.citation: Genetics. 1992 Jun;131(2):397-412
references.pmid: 1386586
references.citation: Exp Physiol. 2003 Jan;88(1):41-56
references.pmid: 12525854
references.citation: Mol Biol Evol. 2011 Jan;28(1):39-44
references.pmid: 20924083
references.citation: Trends Ecol Evol. 2004 Dec;19(12):645-53
references.pmid: 16701327
references.citation: Mol Biol Evol. 2012 Aug;29(8):2001-18
references.pmid: 22337863
references.citation: Genome Res. 2009 Oct;19(10):1760-5
references.pmid: 19617397
references.citation: Nucleic Acids Res. 1999 Apr 15;27(8):1767-80
references.pmid: 10101183
references.citation: Mol Phylogenet Evol. 2003 Dec;29(3):380-95
references.pmid: 14615181
references.citation: Trends Microbiol. 1998 Jul;6(7):263-8
references.pmid: 9717214
references.citation: Genomics. 1994 Jul 15;22(2):327-35
references.pmid: 7806218
references.citation: Heredity (Edinb). 1987 Apr;58 ( Pt 2):229-38
references.pmid: 3032871
references.citation: Nat Rev Mol Cell Biol. 2007 Nov;8(11):870-9
references.pmid: 17928812
references.citation: Evolution. 2013 Mar;67(3):894-9
references.pmid: 23461338
references.citation: Mol Biol Evol. 1997 Nov;14(11):1167-76
references.pmid: 9364774
references.citation: Heredity (Edinb). 2008 Oct;101(4):301-20
references.pmid: 18612321
references.citation: Mol Cell. 2006 Dec 28;24(6):813-25
references.pmid: 17189185
references.citation: Science. 2006 Mar 24;311(5768):1727-30
references.pmid: 16556832
references.citation: Curr Opin Genet Dev. 1998 Dec;8(6):668-74
references.pmid: 9914213
references.citation: Genetics. 1994 May;137(1):233-41
references.pmid: 8056313
references.citation: Biol Lett. 2009 Jun 23;5(3):413-6
references.pmid: 19324654
references.citation: Mol Biol Evol. 2003 Oct;20(10):1612-9
references.pmid: 12832626
references.citation: Bioinformatics. 2006 Nov 1;22(21):2688-90
references.pmid: 16928733
references.citation: Proc Natl Acad Sci U S A. 1993 May 1;90(9):4087-91
references.pmid: 8483925
references.citation: Genome Biol. 2001;2(6):REVIEWS1018
references.pmid: 11423013
references.citation: Mol Biol Evol. 1994 Jan;11(1):9-21
references.pmid: 8121290
references.citation: Nucleic Acids Res. 2004 Mar 19;32(5):1792-7
references.pmid: 15034147
references.citation: Trends Ecol Evol. 1994 Apr;9(4):125-31
references.pmid: 21236795
references.citation: Curr Opin Genet Dev. 2001 Dec;11(6):667-72
references.pmid: 11682311
references.citation: J Mol Evol. 2006 Sep;63(3):375-92
references.pmid: 16838214
references.citation: Genetics. 1996 May;143(1):427-46
references.pmid: 8722794