The mitochondrial and plastid genomes of Volvox carteri: bloated molecules rich in repetitive DNA

Background: The magnitude of noncoding DNA in organelle genomes can vary significantly; it is argued that much of this variation is attributable to the dissemination of selfish DNA. The results of a previous study indicate that the mitochondrial DNA (mtDNA) of the green alga Volvox carteri abounds with palindromic repeats, which appear to be selfish elements. We became interested in the evolution and distribution of these repeats when, during a cursory exploration of the V. carteri nuclear DNA (nucDNA) and plastid DNA (ptDNA) sequences, we found palindromic repeats with similar structural features to those of the mtDNA. Upon this discovery, we decided to investigate the diversity and evolutionary implications of these palindromic elements by sequencing and characterizing large portions of mtDNA and ptDNA and then comparing these data to the V. carteri draft nuclear genome sequence. Results: We sequenced 30 and 420 kilobases (kb) of the mitochondrial and plastid genomes of V. carteri, respectively- resulting in partial assemblies of these genomes. The mitochondrial genome is the most bloated green-algal mtDNA observed to date: similar to 61% of the sequence is noncoding, most of which is comprised of short palindromic repeats spread throughout the intergenic and intronic regions. The plastid genome is the largest (> 420 kb) and most expanded (> 80% noncoding) ptDNA sequence yet discovered, with a myriad of palindromic repeats in the noncoding regions, which have a similar size and secondary structure to those of the mtDNA. We found that 15 kb (similar to 0.01%) of the nuclear genome are homologous to the palindromic elements of the mtDNA, and 50 kb (similar to 0.05%) are homologous to those of the ptDNA. Conclusion: Selfish elements in the form of short palindromic repeats have propagated in the V. carteri mtDNA and ptDNA, resulting in the distension of these genomes. Copies of these same repeats are also found in a small fraction of the nucDNA, but appear to be inert in this compartment. We conclude that the palindromic repeats in V. carteri represent a single class of selfish DNA and speculate that the derivation of this element involved the lateral gene transfer of an organelle intron that first appeared in the mitochondrial genome, spreading to the ptDNA through mitochondrion-to-plastid DNA migrations, and eventually arrived in the nucDNA through organelle-to-nucleus DNA transfer events. The overall implications of palindromic repeats on the evolution of chlorophyte organelle genomes are discussed.