title: Group II Intron-Mediated Trans-Splicing in the Gene-Rich Mitochondrial Genome of an Enigmatic Eukaryote, Diphylleia rotans.
abstract: Although mitochondria have evolved from a single endosymbiotic event, present day mitochondria of diverse eukaryotes display a great range of genome structures, content and features. Group I and group II introns are two features that are distributed broadly but patchily in mitochondrial genomes across branches of the tree of eukaryotes. While group I intron-mediated trans-splicing has been reported from some lineages distantly related to each other, findings of group II intron-mediated trans-splicing has been restricted to members of the Chloroplastida. In this study, we found the mitochondrial genome of the unicellular eukaryote Diphylleia rotans possesses currently the second largest gene repertoire. On the basis of a probable phylogenetic position of Diphylleia, which is located within Amorphea, current mosaic gene distribution in Amorphea must invoke parallel gene losses from mitochondrial genomes during evolution. Most notably, although the cytochrome c oxidase subunit (cox) 1 gene was split into four pieces which located at a distance to each other, we confirmed that a single mature mRNA that covered the entire coding region could be generated by group II intron-mediated trans-splicing. This is the first example of group II intron-mediated trans-splicing outside Chloroplastida. Similar trans-splicing mechanisms likely work for bipartitely split cox2 and nad3 genes to generate single mature mRNAs. We finally discuss origin and evolution of this type of trans-splicing in D. rotans as well as in eukaryotes.
authors.affiliation: Graduate School of Human and Environmental Studies, Kyoto University, Japan Graduate School of Global Environmental Studies, Kyoto University, Japan kamikawa.ryoma.7v@kyoto-u.ac.jp.
authors.forename: Ryoma
authors.initials: R
authors.lastname: Kamikawa
authors.affiliation: Graduate School of Life and Environmental Sciences, University of Tsukuba, Ibaraki, Japan.
authors.forename: Takashi
authors.initials: T
authors.lastname: Shiratori
authors.affiliation: Faculty of Life and Environmental Sciences, University of Tsukuba, Ibaraki, Japan.
authors.forename: Ken-Ichiro
authors.initials: K
authors.lastname: Ishida
authors.affiliation: Graduate School of Human and Environmental Studies, Kyoto University, Japan Graduate School of Global Environmental Studies, Kyoto University, Japan.
authors.forename: Hideaki
authors.initials: H
authors.lastname: Miyashita
authors.affiliation: Centre for Comparative Genomics and Evolutionary Bioinformatics, Department of Biochemistry and Molecular Biology, Dalhousie University, Halifax, Nova Scotia, Canada Program in Integrated Microbial Biodiversity, Canadian Institute for Advanced Research, Halifax, Nova Scotia, Canada.
authors.forename: Andrew J
authors.initials: AJ
authors.lastname: Roger
mesh_terms: D003576:Electron Transport Complex IV / Q000235:genetics; D056890:Eukaryota / Q000145:classification / Q000235:genetics*; D019143:Evolution, Molecular; D054629:Genome, Mitochondrial; D007438:Introns; D016366:Open Reading Frames; D010802:Phylogeny; D012326:RNA Splicing
chemical_list: D003576:Electron Transport Complex IV
keywords: Diphyllatia; introns; inverted repeats; mitochondria; trans-splicing
references.citation: Protist. 2009 Aug;160(3):364-75
references.pmid: 19346162
references.citation: Plant Mol Biol. 1994 Jan;24(2):273-81
references.pmid: 7509206
references.citation: Proc Biol Sci. 2013 Oct 22;280(1769):20131755
references.pmid: 23986111
references.citation: Curr Biol. 2014 Feb 17;24(4):465-70
references.pmid: 24508168
references.citation: PLoS One. 2012;7(5):e37307
references.pmid: 22606358
references.citation: PLoS One. 2013;8(2):e56777
references.pmid: 23437234
references.citation: Genome Biol Evol. 2010;2:897-910
references.pmid: 21081313
references.citation: Int J Syst Evol Microbiol. 2003 Nov;53(Pt 6):1741-58
references.pmid: 14657102
references.citation: Cold Spring Harb Perspect Biol. 2012 Sep;4(9):a011403
references.pmid: 22952398
references.citation: J Biol Chem. 2008 Sep 12;283(37):25200-8
references.pmid: 18644794
references.citation: J Eukaryot Microbiol. 2012 Sep;59(5):429-93
references.pmid: 23020233
references.citation: Mitochondrion. 2008 Jan;8(1):26-34
references.pmid: 18006386
references.citation: Mol Biol Evol. 1998 Jun;15(6):690-701
references.pmid: 9615450
references.citation: EMBO J. 1987 Aug;6(8):2185-95
references.pmid: 16453785
references.citation: Curr Biol. 2011 Feb 22;21(4):311-5
references.pmid: 21315596
references.citation: Genome Biol Evol. 2013;5(9):1628-43
references.pmid: 23925788
references.citation: Nucleic Acids Res. 1997 Mar 1;25(5):955-64
references.pmid: 9023104
references.citation: Mob Genet Elements. 2014 May 27;4:e29384
references.pmid: 25054084
references.citation: Trends Genet. 2005 Apr;21(4):240-7
references.pmid: 15797620
references.citation: Biol Lett. 2010 Jun 23;6(3):342-5
references.pmid: 20031978
references.citation: Genome Biol Evol. 2013;5(2):418-38
references.pmid: 23335123
references.citation: J Mol Evol. 2004 Jul;59(1):80-9
references.pmid: 15383910
references.citation: Bioessays. 2009 Sep;31(9):921-34
references.pmid: 19644921
references.citation: Mol Phylogenet Evol. 2003 Dec;29(3):380-95
references.pmid: 14615181
references.citation: Nature. 2010 Jan 28;463(7280):457-63
references.pmid: 20110989
references.citation: Nucleic Acids Res. 1998 Nov 15;26(22):5190-8
references.pmid: 9801318
references.citation: Protist. 2002 Mar;153(1):59-70
references.pmid: 12022276
references.citation: Nucleic Acids Res. 2009 Aug;37(15):5093-104
references.pmid: 19553190
references.citation: J Mol Biol. 1990 Oct 5;215(3):403-10
references.pmid: 2231712
references.citation: BMC Evol Biol. 2006;6:94
references.pmid: 17101053
references.citation: Int J Parasitol. 2000 Apr 10;30(4):371-90
references.pmid: 10731561
references.citation: Annu Rev Genet. 2004;38:477-524
references.pmid: 15568984
references.citation: Mob DNA. 2015 Apr 01;6:7
references.pmid: 25960782
references.citation: PLoS One. 2010;5(1):e8954
references.pmid: 20126458
references.citation: Mol Biol Evol. 2015 May;32(5):1115-31
references.pmid: 25660376
references.citation: PLoS One. 2013;8(12):e84325
references.pmid: 24386369
references.citation: Proc Natl Acad Sci U S A. 2001 Aug 14;98(17):9724-9
references.pmid: 11493677
references.citation: Curr Opin Genet Dev. 1999 Dec;9(6):678-87
references.pmid: 10607615
references.citation: J Eukaryot Microbiol. 2013 Mar-Apr;60(2):179-91
references.pmid: 23360210
references.citation: Genome Biol Evol. 2014 Feb;6(2):306-15
references.pmid: 24448982
references.citation: Cold Spring Harb Perspect Biol. 2014 Aug;6(8). pii: a016139. doi: 10.1101/cshperspect.a016139
references.pmid: 25085908
references.citation: Curr Genet. 1991 Jul;20(1-2):99-114
references.pmid: 1657415
references.citation: Proc Natl Acad Sci U S A. 2015 Feb 17;112(7):E693-9
references.pmid: 25646484
references.citation: New Phytol. 2012 May;194(3):836-45
references.pmid: 22320438
references.citation: Nucleic Acids Res. 2014 Dec 16;42(22):13764-77
references.pmid: 25429974
references.citation: Nucleic Acids Res. 2011 Feb;39(3):979-88
references.pmid: 20935050
references.citation: Trends Genet. 2009 Sep;25(9):381-6
references.pmid: 19716620
references.citation: PLoS One. 2009;4(12):e8407
references.pmid: 20027311
references.citation: Proc Natl Acad Sci U S A. 1999 Nov 23;96(24):13880-5
references.pmid: 10570167
references.citation: BMC Genomics. 2009;10:132
references.pmid: 19323823
references.citation: Mol Biol Evol. 2000 Nov;17(11):1760-8
references.pmid: 11070063
references.citation: Mol Biol Evol. 2012 Jun;29(6):1557-68
references.pmid: 22319147
references.citation: Nucleic Acids Res. 2003 Jul 1;31(13):3406-15
references.pmid: 12824337
references.citation: Nature. 2008 Sep 25;455(7212):491-6
references.pmid: 18784652
references.citation: Mol Biol Evol. 2012 Sep;29(9):2199-210
references.pmid: 22411852
references.citation: Protist. 2007 Apr;158(2):239-45
references.pmid: 17291829