Parallel origins of duplications and the formation of pseudogenes in mitochondrial DNA from parthenogenetic lizards (Heteronotia binoei; Gekkonidae)

Abstract

Analysis of mitochondrial DNAs (mtDNAs) from parthenogenetic lizards of the Heteronotia binoei complex with restriction enzymes revealed an approximately 5-kb addition present in all 77 individuals. Cleavage site mapping suggested the presence of a direct tandem duplication spanning the 16S and 12S rRNA genes, the control region and most, if not all, of the gene for the subunit 1 of NADH dehydrogenase (ND1). The location of the duplication was confirmed by Southern hybridization. A restriction enzyme survey provided evidence for modifications to each copy of the duplicated sequence, including four large deletions. Each gene affected by a deletion was complemented by an intact version in the other copy of the sequence, although for one gene the functional copy was heteroplasmic for another deletion. Sequencing of a fragment from one copy of the duplication which encompassed the tRNA(leu)(UUR) and parts of the 16S rRNA and ND1 genes, revealed mutations expected to disrupt function. Thus, evolution subsequent to the duplication event has resulted in mitochondrial pseudogenes. The presence of duplications in all of these parthenogens, but not among representatives of their maternal sexual ancestors, suggests that the duplications arose in the parthenogenetic form. This provides the second instance in H. binoei of mtDNA duplication associated with the transition from sexual to parthenogenetic reproduction. The increased incidence of duplications in parthenogenetic lizards may be caused by errors in mtDNA replication due to either polyploidy or hybridity of their nuclear genomes.

Novel features of metazoan mtDNA revealed from sequence analysis of three mitochondrial DNA segments of the land snail Albinaria turrita (Gastropoda: Clausiliidae)

“…No apparent correlation between size and taxonomic relationship has been documented (Gjetvaj et al 1992). Relatively small size variations among metazoan mtDNAs usually arise from differences in gene lengths and in the noncoding or control regions, whereas larger size variations can be additionally attributed to the presence of repeats arising from duplications of different parts of the mtDNA molecule Snyder et al 1987;Hyman et al 1988;LaRoche et al 1990;Zevering et al 1991;Gjetvaj et al 1992).…”

Origin and Evolution of Parthenogenetic Genomes in Lizards: Current State and Future Directions

“…Hybrid disruption of coadapted mtDNA replication machinery may cause these mutations to occur more frequently in parthenogenetic lizards, and thus their presence may merely reflect an increased duplication mutation rate [Zevering et al, 1991;Fujita et al, 2007]. For example, such a situation has been documented in hybrid copepods (Tigriopus californicus) , where disruption of cytonuclear complexes has caused a reduction in mitochondrial transcription rates ].…”

“…More than just a marker, mitochondrial genomes of parthenogenetic lizards have an interesting biology of their own, and their features provide unique opportunities to learn about basic mtDNA evolution in all animals. The mitochondrial genomes of parthenogenetic lizards often contain large, tandem duplications that contain tRNA, rRNA, protein-coding genes, and often the control region Moritz, 1991;Zevering et al, 1991] ( fig. 3 A).…”

Stable heteroplasmy for a large-scale deletion in the coding region of Drosophila subobscura mitochondrial DNA.

“…Consequently, they are conserved across taxa, with the exception of the ATPase 8 gene, which is missing in nematodes (17). In some species of lizards, individuals with large duplications have been observed (18,19). However, large deletions involving the coding region are found only in the heteroplasmic state.…”