New views on strand asymmetry in insect mitochondrial genomes

Abstract

Strand asymmetry in nucleotide composition is a remarkable feature of animal mitochondrial genomes. Understanding the mutation processes that shape strand asymmetry is essential for comprehensive knowledge of genome evolution, demographical population history and accurate phylogenetic inference. Previous studies found that the relative contributions of different substitution types to strand asymmetry are associated with replication alone or both replication and transcription. However, the relative contributions of replication and transcription to strand asymmetry remain unclear. Here we conducted a broad survey of strand asymmetry across 120 insect mitochondrial genomes, with special reference to the correlation between the signs of skew values and replication orientation/gene direction. The results show that the sign of GC skew on entire mitochondrial genomes is reversed in all species of three distantly related families of insects, Philopteridae (Phthiraptera), Aleyrodidae (Hemiptera) and Braconidae (Hymenoptera); the replication-related elements in the A+T-rich regions of these species are inverted, confirming that reversal of strand asymmetry (GC skew) was caused by inversion of replication origin; and finally, the sign of GC skew value is associated with replication orientation but not with gene direction, while that of AT skew value varies with gene direction, replication and codon positions used in analyses. These findings show that deaminations during replication and other mutations contribute more than selection on amino acid sequences to strand compositions of G and C, and that the replication process has a stronger affect on A and T content than does transcription. Our results may contribute to genome-wide studies of replication and transcription mechanisms.

Figure 1. Scatterplots of skews values calculated for whole majority strand of 120 insect mitochondrial genomes.

Reversal of both AT and GC skew are found in all species with a sequenced mitochondrial genome of in the families Philopteridae (Bothriometopus macrocnemis, Campanulotes bidentatus), Aleyrodidae (Aleurochiton aceris, Aleurodicus dugesii, Bemisia tabaci, Neomaskellia andropogonis, Tetraleurodes acaciae, Trialeurodes vaporariorum) and Braconidae (Cotesia vestalis, Spathius agrili). Reversal of AT skew was found in 10 unrelated species: Onychiurus orientalis (Collembola: Onychiuridae), Bilobella aurantiaca (Collembola: Neanuridae), Heterodoxus macropus (Phthiraptera: Boopidae), Antheraea pernyi (Lepidoptera: Saturniidae), Coreana raphaelis (Lepidoptera: Lycaenidae), Manduca sexta (Lepidoptera: Sphingidae), Saturnia boisduvalii (Lepidoptera: Saturniidae), Simosyrphus grandicornis (Diptera: Syrphidae), Polystoechotes punctatus (Neuroptera: Polystoechotidae) and Abispa ephippium (Hymenoptera: Eumenidae).

Figure 2. Predicted structural elements for A+T-rich region of 10 species with reversal of strand asymmetry.

Figure 3. Gene arrangement of the mitochondrial genome of 10 species with reversal of strand asymmetry.

Genes are showed in boxes. Box with underscore indicates that the gene is encoded on minority strand while box without underscore indicates that the gene is encoded on majority strand. Rearranged genes compared to the ancestral mitochondrial genome arrangement were marked with colours. Green indicates that the gene was inverted or remotely inverted, while brown indicates that the gene was translocated or shuffled. AT indicates the A+T-rich region. A+T-rich regions of all species were inverted and marked in green. AN: Ancestral arrangement; CV: Cotesia vestalis; SA: Spathius agrili; BM: Bothriometopus macrocnemis; CB: Campanulotes bidentatus; AA: Aleurochiton aceris; AD: Aleurodicus dugesii; BT: Bemisia tabaci; NA: Neomaskellia andropogonis; TA: Tetraleurodes acacia; TV: Trialeurodes vaporariorum.

Figure 4. Scatterplots of skews values calculated for third codon positions of individual protein-coding genes.

(A) Relationship of AT skew on third codon position of individual gene and gene direction in 120 insect species. (B) Relationship of GC skew on individual gene and gene direction in 110 insect mitochondrial genomes with normal replication origin. (C) Relationship of GC skew on individual gene and gene direction in 10 insect mitochondrial genomes with inverted replication origin. Gene name with minus indicates that the gene is encoded on minority strand, while without minus indicates on majority strand.