Gene Loss and Organelle Genome Evolution

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Gene Loss and Organelle Genome Evolution

• Level 3 Molecular Evolution and Bioinformatics
• Jim Provan

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References

• Race HL, Herrmann RG, Martin W (1999) Why have
  organelles retained genomes? Trends in Genetics
  15 364-370
• Lang BF, Gray MW, Burger G (1999) Mitochondrial
  genome evolution and the origin of eukaryotes
  Annual Review of Genetics 33 351-397

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Gene loss in early organelle evolution
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Types of genes in organelles and their ancestors
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Genes encoded in plastid genomes
25 16 13
8 7 2
12 12 4
9 8 5
24 2 1
12 4 3
53 48 16
3025 159 2
3168 2569 46
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Evolution of the spc (spectinomycin) operon
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Where did the genes go?

• Obsolete genes eliminated early on
• Nucleotide, lipid and amino acid biosynthesis
  genes not found in mitochondria
• Still found in some chloroplasts ancient
  mitochondrial genomes may exist which contain
  these genes cf. Porphyra vs. angiosperm
  chloroplasts
• Takeover of corresponding function by nuclear
  genes
• Protozoan Paramecium mtDNA contains only three
  tRNA genes
• To translate all codons, tRNAs are imported from
  cytosol

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The mitochondrial RNA polymerase

• Most eukaryote mtDNAs use a nucleus-encoded
  single-subunit polymerase similar to T3/T7 phages
• Jakobid protists J. libera and R. americana mtDNA
  contains genes for multi-subunit RNA polymerase
  like that in bacteria
• Original RNA polymerase has been superseded by
  phage-like enzyme

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Phylogeny of green algae

• Closest relatives to land plants (Embryophyta)
  are Charophyceae
• Complete chloroplast DNA sequence available for
  Trebouxiophyte Chlorella
• Green algae chloroplast structure highly variable
  ? difficult to predict ancestral structure

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Nephroselmis olivacea chloroplast structure

• Quadripartite structure
• 92,126bp LSC
• 16,399bp SSC
• 46,137bp IR
• IRs also found in
• Cyanophora
• Odontella
• Guillardia
• Land plants (mostly)
• but not in
• Chlorella
• Porphyra

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Nephroselmis olivacea gene content

• Total of 127 genes largest among green lineage
• Marchantia - 120 Chlorella - 111 Euglena - 85
• May represent primitive green plastid
• Seven genes not found in other green
  chloroplasts
• rnpB, trnS(cga), ftsW, rne, ycf62 found in
  non-green algae
• ycf81 and ftsI found in bacteria
• ftsW and ftsI involved in formation of
  peptidoglycan
• Cell wall only found in glaucocystophyte
  Cyanophora
• May be more prevalent than first thought
• Ten subunits of NADHubiquinone oxidoreductase
• ndh genes found in four of five land plants
• Pseudogenes in Pinus - transferred to nucleus

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Nephroselmis olivacea gene content

• Atypical codon usage and AT-composition
• Suggests that majority of IR has been gained by
  lateral transfer
• Also noted in green alga Chlamydomonas
• No introns cf. Porphyra, Odontella and
  Guillardia
• Suggests ancestral plastid genome contained very
  few introns
• Intron proliferation seems to be a feature of
  higher plants
• trnL intron in Chlorella seems to have been
  vertically transmitted from cyanobacteria
• Found in Cyanophora
• Found in plants

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Phylogenetic position of Nephroselmis chloroplasts

• Tree based on 37 cpDNA proteins
• Agrees with 18S-rRNA (nuclear) phylogenies
• Nephroselmis represents basal branch of
  Chlorophyta
• Euglena included in Chlorophyta

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Patterns of gene loss in chloroplast genomes
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Gene partitioning

• All but one genes located in single-copy regions
  in Nephroselmis are found in corresponding region
  in Marchantia
• Exception is trnL(UAG)
• Suggests that ancestral green algal plastid
  genome had IR
• Some genes adjacent to IR in Marchantia have been
  subsumed into the IR in Nephroselmis
• In smaller region delineated by rRNA operons (cf.
  SSC), only four of thirteen genes have been
  transferred to large region (cf. LSC) between
  red / green lineages
• Suggests that transfer between LSC and SSC
  regions is rare
• Further evidence for single origin of all plastid
  genomes