Dynamic evolution of plant mitochondrial genomes: Mobile genes and introns and highly variable mutation rates

Abstract

We summarize our recent studies showing that angiosperm mitochondrial (mt) genomes have experienced remarkably high rates of gene loss and concomitant transfer to the nucleus and of intron acquisition by horizontal transfer. Moreover, we find substantial lineage-specific variation in rates of these structural mutations and also point mutations. These findings mostly arise from a Southern blot survey of gene and intron distribution in 281 diverse angiosperms. These blots reveal numerous losses of mt ribosomal protein genes but, with one exception, only rare loss of respiratory genes. Some lineages of angiosperms have kept all of their mt ribosomal protein genes whereas others have lost most of them. These many losses appear to reflect remarkably high (and variable) rates of functional transfer of mt ribosomal protein genes to the nucleus in angiosperms. The recent transfer of cox2 to the nucleus in legumes provides both an example of interorganellar gene transfer in action and a starting point for discussion of the roles of mechanistic and selective forces in determining the distribution of genetic labor between organellar and nuclear genomes. Plant mt genomes also acquire sequences by horizontal transfer. A striking example of this is a homing group I intron in the mt cox1 gene. This extraordinarily invasive mobile element has probably been acquired over 1,000 times separately during angiosperm evolution via a recent wave of cross-species horizontal transfers. Finally, whereas all previously examined angiosperm mtDNAs have low rates of synonymous substitutions, mtDNAs of two distantly related angiosperms have highly accelerated substitution rates.

Horizontal gene transfer from a flowering plant to the insular pine Pinus canariensis (Chr. Sm. Ex DC in Buch)

“…Sequencing the angiosperm-type nad5-1 in 22 individuals throughout the range of P. canariensis revealed no intraspecific variation. In contrast, genes transferred from mitochondria to nuclei often exhibit accelerated substitution rates (Palmer et al, 2000). These results are consistent with previous observations that most transferred mt genes are integrated into the receptors' mt genomes (Bock, 2010).…”

Covariation of Mitochondrial Genome Size with Gene Lengths: Evidence for Gene Length Reduction During Mitochondrial Evolution

“…Gene length evolution in plants may be the result of an ancestral selection process leading to strongly reduced gene lengths in ancestral plants, followed by a phase of relaxation during which genomes could expand. The genomes expanded in part by recombination events and in part by acquiring external sequences (Palmer et al 2000). Our data seem to indicate that the length of the protein coding regions (coxI-III and cytb) did not expand, while the rRNA genes expanded and became even longer than their bacterial counterparts.…”

Many Parallel Losses of infA from Chloroplast DNA during Angiosperm Evolution with Multiple Independent Transfers to the Nucleus

“…This possibility is strongest for Arabidopsis, given that its entire genome has been sequenced (Arabidopsis Genome Initiative, 2000). In contrast, a number of recently transferred plant genes of mitochondrial origin have recruited preexisting transit peptides from long-established nuclear genes encoding mitochondrial proteins (Kadowaki et al, 1996;Figueroa et al, 1999;Kubo et al, 1999;Adams et al, 2000).…”