Mitochondrial Genome Mitochondrial Genome EvolutionEvolution

Level 3 Molecular Evolution and Level 3 Molecular Evolution and BioinformaticsBioinformatics

Jim ProvanJim Provan

ReferencesReferencesGray MW, Burger G, Lang BF (1999) “Mitochondrial Gray MW, Burger G, Lang BF (1999) “Mitochondrial

evolution” evolution” Science Science 283283: 1476-1481: 1476-1481Leblanc C, Richard O, Kloareg B Leblanc C, Richard O, Kloareg B et alet al. (1997) “Origin . (1997) “Origin

and evolution of mitochondria: what have we learnt and evolution of mitochondria: what have we learnt from red algae?” from red algae?” Current Genetics Current Genetics 3131: 193-207: 193-207

Lang BF, Gray MW, Burger G (1999) “Mitochondrial Lang BF, Gray MW, Burger G (1999) “Mitochondrial genome evolution and the origin of eukaryotes” genome evolution and the origin of eukaryotes” Annual Review of Genetics Annual Review of Genetics 3333: 351-397: 351-397

Turmel M, Otis C, Lemieux C (2003) “The Turmel M, Otis C, Lemieux C (2003) “The mitochondrial genome of mitochondrial genome of Chara vulgarisChara vulgaris: insights : insights into the mitochondrial DNA of the last common into the mitochondrial DNA of the last common ancestor of green algae and land plants” ancestor of green algae and land plants” Plant Cell Plant Cell 1515: 1888-1903: 1888-1903

The mitochondrionThe mitochondrion

Primary site of oxidative Primary site of oxidative phosphorylationphosphorylationContains own genomeContains own genomeGene sequences Gene sequences suggest closest suggest closest relationship with relationship with --proteobacteriaproteobacteriaBelieved to be of Believed to be of endosymbiotic originendosymbiotic origin

The animal mitochondrial The animal mitochondrial genomegenome

Daphnia pulexDaphnia pulex(15,333bp)(15,333bp)

14kb - 42kb in size14kb - 42kb in sizeGenerally same 37 Generally same 37 genes:genes:

12S and 16S rRNA12S and 16S rRNA13 proteins13 proteins22 tRNAs22 tRNAs

No recombinationNo recombinationLittle intergenic DNALittle intergenic DNANo intronsNo intronsVariable control regionVariable control regionOwn genetic codeOwn genetic code

The plant mitochondrial genomeThe plant mitochondrial genome

~200kb - 2400kb in size~200kb - 2400kb in sizeExtra genes:Extra genes:

Open Reading FramesOpen Reading FramesRibosomal proteinsRibosomal proteinsChloroplast tRNAsChloroplast tRNAs

Generally multi-circularGenerally multi-circularOver 90% non-coding Over 90% non-coding DNADNAUniversal genetic codeUniversal genetic code

Marchantia polymorphaMarchantia polymorpha(184,000 bp)(184,000 bp)

Diversity of mitochondrial Diversity of mitochondrial genomesgenomes

SizeSizeNon-coding DNANon-coding DNAMutation rateMutation rate HighHigh

Very LowVery Low14kb - 42kb14kb - 42kb

RecombinationRecombinationIntronsIntrons

Universal genetic codeUniversal genetic code

LowLowVariableVariable

17kb - 180kb17kb - 180kb

//

MostlyMostly

Very LowVery LowVery HighVery High

184kb - 2,400kb184kb - 2,400kb

AnimalsAnimals Fungi Fungi Plants Plants

Reclinomonas americana Reclinomonas americana - the - the ancestral mitochondrial ancestral mitochondrial

genome?genome?Total of 97 genes:Total of 97 genes:

All protein-coding genes All protein-coding genes found in all mtDNAsfound in all mtDNAs18 protein genes unique 18 protein genes unique to to ReclinomonasReclinomonas

Four genes (Four genes (rpoA-DrpoA-D) ) encode a eubacteria-encode a eubacteria-like RNA polymerase like RNA polymerase ((22’’))Vestigial prokaryotic Vestigial prokaryotic operon organisationoperon organisationUniversal genetic codeUniversal genetic code

Ancestral and derived Ancestral and derived mitochondrial genomesmitochondrial genomes

AncestralAncestral

Many genesMany genesBacteria-like rRNA Bacteria-like rRNA genesgenesComplete set of tRNAsComplete set of tRNAsMostly coding Mostly coding sequencesequenceGene clustersGene clustersStandard genetic codeStandard genetic code

DerivedDerived

Loss of genesLoss of genesDivergent rDNA / rRNADivergent rDNA / rRNAHigh mutation rateHigh mutation rateNon-coding DNANon-coding DNABiased codon usageBiased codon usageNon-standard genetic Non-standard genetic codecode

Mitochondrial phylogeny - a Mitochondrial phylogeny - a separate origin for plant mtDNA?separate origin for plant mtDNA?

Presence of unique 5S Presence of unique 5S RNA gene in plant RNA gene in plant mtDNA and structural mtDNA and structural difference led to theory difference led to theory of separate origin of of separate origin of mitochondria for plantsmitochondria for plantsAnalysis of mitochondrial Analysis of mitochondrial proteins gave topology proteins gave topology similar to nuclear gene-similar to nuclear gene-derived phylogenies derived phylogenies acquired before acquired before radiation of eukaryotesradiation of eukaryotes

Neurospora crassaNeurospora crassaPodospora anserinaPodospora anserina

Aspergillus nidulansAspergillus nidulansSaccharomyces cerevisiaeSaccharomyces cerevisiae

Homo sapiensHomo sapiensMus musculusMus musculusXenopus laevisXenopus laevisStrongylocentrosus purpuratusStrongylocentrosus purpuratus

Drosophila yakubaDrosophila yakubaOryza sativaOryza sativa

Triticum aestivumTriticum aestivumOenothera berterianaOenothera berteriana

Marchantia polymorphaMarchantia polymorphaProthoteca wickerhamiiProthoteca wickerhamiiChondrus crispusChondrus crispus

Cyanidium caldariumCyanidium caldariumAcanthamoeba castellaniiAcanthamoeba castellanii

cox1cox1//cox2cox2//cobcob amino acid sequence amino acid sequence

Mitochondrial phylogeny - a Mitochondrial phylogeny - a separate origin for plant mtDNA?separate origin for plant mtDNA?

rpl2 rps19 rpl22 rps3 rpl16 rpl29 rps17

NucleusNucleus

Escherichia coliEscherichia coliRickettsia Rickettsia prowazekiiprowazekii

rpl2 rps19 rps3 rpl16

MitochondrionMitochondrion

Marchantia Marchantia polymorphapolymorpha

Nephroselmis Nephroselmis olivaceaolivacea

Acanthamoeba Acanthamoeba castellaniicastellanii

Dictyostelium Dictyostelium discoideumdiscoideum

Naegleria gruberiNaegleria gruberiReclinomonas Reclinomonas

americanaamericanaJakoba liberaJakoba libera

Diversity of streptophyte Diversity of streptophyte mitochondrial genomesmitochondrial genomes

TaxonTaxon

NephroselmisNephroselmisMesostigmaMesostigma

ChaetosphaeridiumChaetosphaeridiumCharaChara

MarchantiaMarchantiaArabidopsisArabidopsisBetaBetaOryzaOryza

Size (bp)Size (bp)

45,22345,22342,42442,424

56,57456,57467,73767,737

186,609186,609366,924366,924368,799368,799490,520490,520

% coding% coding

78.578.586.686.6

76.376.390.790.7

65.065.036.836.833.033.0

??

GenesGenes

63636565

67676868

6969494948485353

Gp IGp I

4444

991414

77000000

Gp IIGp II

0033

221313

2525232320202323

IntronsIntrons

Diversity of streptophyte Diversity of streptophyte mitochondrial genomesmitochondrial genomes

Radical changes in size, % coding DNA, gene Radical changes in size, % coding DNA, gene content and intron content between content and intron content between CharaChara//MarchantiaMarchantia and angiosperms and angiospermsDespite differences in size, Despite differences in size, Chara Chara mtDNA is mtDNA is very similar to very similar to Marchantia Marchantia mtDNA:mtDNA:

All except 9 of 68 conserved genes lie within blocks All except 9 of 68 conserved genes lie within blocks of colinear sequencesof colinear sequences% AT-content (59.1) closer to land plants (55.2-57.6) % AT-content (59.1) closer to land plants (55.2-57.6) than to other green algae (65.6-67.8)than to other green algae (65.6-67.8)Group I intronsGroup I introns

Acquisition of mitochondriaAcquisition of mitochondriaSpecies in Species in yellowyellow lack lack mitochondriamitochondriaEntamoeba histolyticaEntamoeba histolytica has has obviously lost mitochondriaobviously lost mitochondriaSuggests mitochondria Suggests mitochondria were gained at position Bwere gained at position BOther evidence suggests Other evidence suggests position A:position A:

Hydrogenosomes of Hydrogenosomes of TrichomonasTrichomonas similar to similar to mitochondriamitochondriaPresence of chaperoninsPresence of chaperonins

Anemonia sulcataAnemonia sulcataArtemia salinaArtemia salina

Saccharomyces cerevisiaeSaccharomyces cerevisiaeMucor racemosusMucor racemosus

Volvox carteriiVolvox carteriiOxytricha novaOxytricha nova

Prorocentrum nicansProrocentrum nicansOchromonas danicaOchromonas danicaAchlya bisexualisAchlya bisexualisDictyostelium discoideumDictyostelium discoideum

Entamoeba histolyticaEntamoeba histolyticaNaegleria gruberiNaegleria gruberi

Physarium polycephalumPhysarium polycephalumEuglena gracilisEuglena gracilis

Crithidia fasciculataCrithidia fasciculataTrypanosoma bruceiTrypanosoma brucei

Hexamita inflataHexamita inflataGiardia lambliaGiardia lamblia

Trichomonas foetusTrichomonas foetusVairimorpha nectarixVairimorpha nectarix

Halobacterium volcaniiHalobacterium volcaniiThermoplasma acidophilumThermoplasma acidophilum

Sulfolobus solfataricusSulfolobus solfataricusEscherichia coliEscherichia coliRickettsia rickettsiiRickettsia rickettsii

Mycoplasma gallisepticumMycoplasma gallisepticum

Small subunitSmall subunitrRNA treerRNA tree

B B

A A

Final remarksFinal remarksMitochondria seem to be monophyletic in origin, Mitochondria seem to be monophyletic in origin, derived from a common protomitochondrial derived from a common protomitochondrial ancestorancestorContinuing quest for mtDNAs older than Continuing quest for mtDNAs older than Reclinomonas americana Reclinomonas americana containing more genescontaining more genesStudies of early-diverging protists to find Studies of early-diverging protists to find minimally-diverged minimally-diverged -proteobacterial relatives of -proteobacterial relatives of mitochondriamitochondriaImplications for phylogeny of eukaryotesImplications for phylogeny of eukaryotesEvolution of plant mitochondrial genomes radically Evolution of plant mitochondrial genomes radically differentdifferent