Mitochondrial Genome Evolution

Level 3 Molecular Evolution and Bioinformatics Jim Provan

References
Gray MW, Burger G, Lang BF (1999) Mitochondrial evolution Science 283: 1476-1481 Leblanc C, Richard O, Kloareg B et al. (1997) Origin and evolution of mitochondria: what have we learnt from red algae? Current Genetics 31: 193-207 Lang BF, Gray MW, Burger G (1999) Mitochondrial genome evolution and the origin of eukaryotes Annual Review of Genetics 33: 351-397 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: 1888-1903

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

The animal mitochondrial genome

14kb - 42kb in size Generally same 37 genes:
12S and 16S rRNA 13 proteins 22 tRNAs
Daphnia pulex
(15,333bp)

No recombination Little intergenic DNA No introns Variable control region Own genetic code

The plant mitochondrial genome

~200kb - 2400kb in size Extra genes:
Open Reading Frames Ribosomal proteins Chloroplast tRNAs

Marchantia polymorpha
(184,000 bp)

Generally multi-circular Over 90% non-coding DNA Universal genetic code

Diversity of mitochondrial genomes

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

ancestral mitochondrial genome?

Total of 97 genes:
All protein-coding genes found in all mtDNAs 18 protein genes unique to

Reclinomonas americana - the

Reclinomonas

Four genes (rpoA-D) encode a eubacteria-like RNA polymerase (2) Vestigial prokaryotic operon organisation Universal genetic code

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

Mitochondrial phylogeny - a separate origin for plant mtDNA?

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

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 genederived phylogenies acquired before radiation of eukaryotes

Mitochondrial phylogeny - a separate origin for plant mtDNA?

rpl2

rps19

rpl22

rps3

rpl16

rpl29

rps17

rpl2

rps19

rps3

rpl16

Nucleus

Mitochondrion

Escherichia coli Rickettsia prowazekii

Marchantia polymorpha Nephroselmis olivacea Acanthamoeba castellanii Dictyostelium discoideum Naegleria gruberi Reclinomonas americana Jakoba libera

Diversity of streptophyte mitochondrial genomes

Introns
Taxon Size (bp) % coding 45,223 42,424 56,574 67,737 78.5 86.6 76.3 90.7 Genes 63 65 67 68 Gp I Gp II 4 4 9 14 0 3 2 13

Nephroselmis Mesostigma Chaetosphaeridium Chara

Marchantia Arabidopsis Beta Oryza

186,609 366,924 368,799 490,520

65.0 36.8 33.0 ?

69 49 48 53

7 0 0 0

25 23 20 23

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 (55.2-57.6) than to other green algae (65.6-67.8) Group I introns

Acquisition of mitochondria
Anemonia sulcata Small subunit Artemia salina rRNA tree Saccharomyces cerevisiae Mucor racemosus Volvox carterii Oxytricha nova Prorocentrum nicans Ochromonas danica Achlya bisexualis Dictyostelium discoideum Entamoeba histolytica Naegleria gruberi B Physarium polycephalum Euglena gracilis Crithidia fasciculata Trypanosoma brucei Hexamita inflata A Giardia lamblia Trichomonas foetus Vairimorpha nectarix Halobacterium volcanii Thermoplasma acidophilum Sulfolobus solfataricus Escherichia coli Rickettsia rickettsii Mycoplasma gallisepticum

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

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 minimallydiverged -proteobacterial relatives of mitochondria Implications for phylogeny of eukaryotes Evolution of plant mitochondrial genomes radically different