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Mitochondrial Genome Evolution Level 3 Molecular Evolution and Bioinformatics Jim Provan.

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1 Mitochondrial Genome Evolution Level 3 Molecular Evolution and Bioinformatics Jim Provan

2 References Gray MW, Burger G, Lang BF (1999) “Mitochondrial evolution” Science 283: Leblanc C, Richard O, Kloareg B et al. (1997) “Origin and evolution of mitochondria: what have we learnt from red algae?” Current Genetics 31: Lang BF, Gray MW, Burger G (1999) “Mitochondrial genome evolution and the origin of eukaryotes” Annual Review of Genetics 33: Turmel M, Otis C, Lemieux C (2003) “The mitochondrial genome of Chara vulgaris: insights into the mitochondrial DNA of the last common ancestor of green algae and land plants” Plant Cell 15:

3 The mitochondrion Primary site of oxidative phosphorylation Contains own genome Gene sequences suggest closest relationship with  -proteobacteria Believed to be of endosymbiotic origin

4 The animal mitochondrial genome Daphnia pulex (15,333bp) 14kb - 42kb in size Generally same 37 genes: 12S and 16S rRNA 13 proteins 22 tRNAs No recombination Little intergenic DNA No introns Variable control region Own genetic code

5 The plant mitochondrial genome ~200kb kb in size Extra genes: Open Reading Frames Ribosomal proteins Chloroplast tRNAs Generally multi-circular Over 90% non-coding DNA Universal genetic code Marchantia polymorpha (184,000 bp)

6 Diversity of mitochondrial genomes Size Non-coding DNA Mutation rate High Very Low 14kb - 42kb Recombination Introns Universal genetic code    Low Variable 17kb - 180kb /  /   Mostly Very Low Very High 184kb - 2,400kb Animals Fungi Plants Animals Fungi Plants

7 Reclinomonas americana - the ancestral mitochondrial genome? Total of 97 genes: All protein-coding genes found in all mtDNAs 18 protein genes unique to Reclinomonas Four genes (rpoA-D) encode a eubacteria-like RNA polymerase (  2  ’  ) Vestigial prokaryotic operon organisation Universal genetic code

8 Ancestral and derived mitochondrial genomes Ancestral Many genes Bacteria-like rRNA genes Complete set of tRNAs Mostly coding sequence Gene clusters Standard genetic code Derived Loss of genes Divergent rDNA / rRNA High mutation rate Non-coding DNA Biased codon usage Non-standard genetic code

9 Mitochondrial phylogeny - a separate origin for plant mtDNA? Presence of unique 5S RNA gene in plant mtDNA and structural difference led to theory of separate origin of mitochondria for plants Analysis of mitochondrial proteins gave topology similar to nuclear gene- derived phylogenies  acquired before radiation of eukaryotes Neurospora crassa Podospora anserina Aspergillus nidulans Saccharomyces cerevisiae Homo sapiens Mus musculus Xenopus laevis Strongylocentrosus purpuratus Drosophila yakuba Oryza sativa Triticum aestivum Oenothera berteriana Marchantia polymorpha Prothoteca wickerhamii Chondrus crispus Cyanidium caldarium Acanthamoeba castellanii cox1/cox2/cob amino acid sequence

10 Mitochondrial phylogeny - a separate origin for plant mtDNA? rpl2rps19rpl22rps3rpl16rpl29rps17Nucleus Escherichia coli Rickettsia prowazekii rpl2rps19 rps3rpl16Mitochondrion Marchantia polymorpha Nephroselmis olivacea Acanthamoeba castellanii Dictyostelium discoideum Naegleria gruberi Reclinomonas americana Jakoba libera

11 Diversity of streptophyte mitochondrial genomes TaxonNephroselmisMesostigmaChaetosphaeridiumCharaMarchantiaArabidopsisBetaOryza Size (bp) 45,22342,42456,57467,737186,609366,924368,799490,520 % coding ?Genes Gp I Gp II Introns

12 Diversity of streptophyte mitochondrial genomes Radical changes in size, % coding DNA, gene content and intron content between Chara/Marchantia and angiosperms Despite differences in size, Chara mtDNA is very similar to Marchantia mtDNA: All except 9 of 68 conserved genes lie within blocks of colinear sequences % AT-content (59.1) closer to land plants ( ) than to other green algae ( ) Group I introns

13 Acquisition of mitochondria Species in yellow lack mitochondria Entamoeba histolytica has obviously lost mitochondria Suggests mitochondria were gained at position B Other evidence suggests position A: Hydrogenosomes of Trichomonas similar to mitochondria Presence of chaperonins Anemonia sulcata Artemia salina Saccharomyces cerevisiae Mucor racemosus Volvox carterii Oxytricha nova Prorocentrum nicans Ochromonas danica Achlya bisexualis Dictyostelium discoideum Entamoeba histolytica Naegleria gruberi Physarium polycephalum Euglena gracilis Crithidia fasciculata Trypanosoma brucei Hexamita inflata Giardia lamblia Trichomonas foetus Vairimorpha nectarix Halobacterium volcanii Thermoplasma acidophilum Sulfolobus solfataricus Escherichia coli Rickettsia rickettsii Mycoplasma gallisepticum Small subunit rRNA tree B  A 

14 Final remarks Mitochondria seem to be monophyletic in origin, derived from a common protomitochondrial ancestor Continuing quest for mtDNAs older than Reclinomonas americana containing more genes Studies of early-diverging protists to find minimally- diverged  -proteobacterial relatives of mitochondria Implications for phylogeny of eukaryotes Evolution of plant mitochondrial genomes radically different


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