Massively Convergent Evolution for Ribosomal Protein Gene Content in Plastid and Mitochondrial Genomes

Abstract

Plastid and mitochondrial genomes have undergone parallel evolution to encode the same functional set of genes. These encode conserved protein components of the electron transport chain in their respective bioenergetic membranes and genes for the ribosomes that express them. This highly convergent aspect of organelle genome evolution is partly explained by the redox regulation hypothesis, which predicts a separate plastid or mitochondrial location for genes encoding bioenergetic membrane proteins of either photosynthesis or respiration. Here we show that convergence in organelle genome evolution is far stronger than previously recognized, because the same set of genes for ribosomal proteins is independently retained by both plastid and mitochondrial genomes. A hitherto unrecognized selective pressure retains genes for the same ribosomal proteins in both organelles. On the Escherichia coli ribosome assembly map, the retained proteins are implicated in 30S and 50S ribosomal subunit assembly and initial rRNA binding. We suggest that ribosomal assembly imposes functional constraints that govern the retention of ribosomal protein coding genes in organelles. These constraints are subordinate to redox regulation for electron transport chain components, which anchor the ribosome to the organelle genome in the first place. As organelle genomes undergo reduction, the rRNAs also become smaller. Below size thresholds of approximately 1,300 nucleotides (16S rRNA) and 2,100 nucleotides (26S rRNA), all ribosomal protein coding genes are lost from organelles, while electron transport chain components remain organelle encoded as long as the organelles use redox chemistry to generate a proton motive force.

Mitochondrial genomes are retained by selective constraints on protein targeting

“…For example, genes for SdhD, ATP1, ATP3, and ATP9 in the R. americana and other jakobid protists are too short, do not contain hydrophobic TMDs, or the C-terminal tail following the TMD segment is too short to allow arrest by SRP. These mitochondrial genomes also encode several ribosomal proteins, which serve key functions in ribosomal assembly and initial rRNA binding (50). Interestingly, a similar set of ribosomal proteins is also encoded by chloroplast genomes, indicative of convergent evolution in response to similar selective constraints.…”

Why chloroplasts and mitochondria retain their own genomes and genetic systems: Colocation for redox regulation of gene expression

“…Indeed, chloroplast ribosomal protein gene expression was found to be redox-independent in the experiments of Pfannschmidt et al (27,28), in contrast to the marked redox dependency of photosynthetic reaction center gene transcription. From genome sequence comparisons, Maier et al (90) report conservation of genes for the same conserved subset of ribosomal proteins in both mitochondria and chloroplasts (Fig. 4).…”

“…Because chloroplasts and mitochondria had independent origins, this observation indicates convergent evolution, with natural selection operating on gene location. By comparison with Escherichia coli, Maier et al observe that the conserved proteins are implicated in 30S and 50S ribosomal subunit assembly and in initial binding of rRNA (90). Maier et al propose that the presence of these genes in organelle DNA enhances their function in ribosome synthesis whereas the requirement for organelle ribosomes in the first place is sufficiently explained by CoRR.…”

Early Microbial Evolution: The Age of Anaerobes

“…That is particularly true in the plant lineage (Martin et al 2002;Ku et al 2015). Until methods emerge that permit eukaryotes to be classified on the basis of all genes, we will have to be content with classifications based on ribosomes, keeping in mind that eukaryotes have either one set of ribosomes (lineages with hydrogenosomes or mitosomes) (Embley et al 2003), two sets (lineages with respiring mitochondria), three sets ( plants), or four sets (complex algae) (Maier et al 2013) of evolutionarily distinct ribosomes operating simultaneously, because of endosymbiosis (Zimorski et al 2014). Methods to investigate the evolution of all genes in eukaryote genomes are emerging, and the data indicate endosymbiotic origins of eukaryotic genes (Ku et al 2015), hence, of eukaryote cells, whereby the formal classification issue remains unresolved.…”