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New Views on Strand Asymmetry in Insect Mitochondrial Genomes Shu-Jun Wei Zhejiang University, China University of Kentucky UKnowledge Entomology Faculty Publications Entomology 9-15-2010 New views on strand asymmetry in insect mitochondrial genomes Shu-Jun Wei Zhejiang University, China Min Shi Zhejiang University, China Xue-Xin Chen Zhejiang University, China Michael J. Sharkey University of Kentucky, [email protected] Cornelis van Achterberg Nationaal Natuurhistorisch Museum, Netherlands See next page for additional authors Right click to open a feedback form in a new tab to let us know how this document benefits oy u. Follow this and additional works at: https://uknowledge.uky.edu/entomology_facpub Part of the Entomology Commons Repository Citation Wei, Shu-Jun; Shi, Min; Chen, Xue-Xin; Sharkey, Michael J.; van Achterberg, Cornelis; Ye, Gong-Yin; and He, Jun-Hua, "New views on strand asymmetry in insect mitochondrial genomes" (2010). Entomology Faculty Publications. 27. https://uknowledge.uky.edu/entomology_facpub/27 This Article is brought to you for free and open access by the Entomology at UKnowledge. It has been accepted for inclusion in Entomology Faculty Publications by an authorized administrator of UKnowledge. For more information, please contact [email protected]. Authors Shu-Jun Wei, Min Shi, Xue-Xin Chen, Michael J. Sharkey, Cornelis van Achterberg, Gong-Yin Ye, and Jun- Hua He New views on strand asymmetry in insect mitochondrial genomes Notes/Citation Information Published in PLoS ONE, v. 5, no. 9, e12708. © 2010 Wei et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Digital Object Identifier (DOI) http://dx.doi.org/10.1371/journal.pone.0012708 This article is available at UKnowledge: https://uknowledge.uky.edu/entomology_facpub/27 New Views on Strand Asymmetry in Insect Mitochondrial Genomes Shu-Jun Wei1,2, Min Shi1, Xue-Xin Chen1*, Michael J. Sharkey3, Cornelis van Achterberg4, Gong-Yin Ye1, Jun-Hua He1 1 State Key Laboratory of Rice Biology and Ministry of Agriculture Key Laboratory of Molecular Biology of Crop Pathogens and Insects, Institute of Insect Sciences, Zhejiang University, Hangzhou, China, 2 Institute of Plant and Environmental Protection, Beijing Academy of Agriculture and Forestry Sciences, Beijing, China, 3 Department of Entomology, University of Kentucky, Lexington, Kentucky, United States of America, 4 Department of Entomology, Nationaal Natuurhistorisch Museum, Leiden, The Netherlands 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. Citation: Wei S-J, Shi M, Chen X-X, Sharkey MJ, van Achterberg C, et al. (2010) New Views on Strand Asymmetry in Insect Mitochondrial Genomes. PLoS ONE 5(9): e12708. doi:10.1371/journal.pone.0012708 Editor: M. Thomas P. Gilbert, Natural History Museum of Denmark, Denmark Received October 5, 2009; Accepted August 20, 2010; Published September 15, 2010 Copyright: ß 2010 Wei et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: Funding for this study was provided jointly by the National Science Fund for Distinguished Young Scholars (30625006), the 973 Program (2006CB102005), the National Science Foundation of China (30970384, 30700063 and 30499341), the National Special Basic Research Funds (2006FY110500-3, 2006FY120100), Special Fund for Agro-Scientific Research of the Public Interest (200803005-04) and Zhejiang Key Program of Agriculture (2009C12048) to XXC, and the NSF (EF-0337220) to MJS. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * E-mail: [email protected] Introduction genomes, the two DNA strands are referred to as the majority strand (light strand in mammal mitochondrial genomes), on which Most animal mitochondrial genomes are about 16 Kb in size more genes are coded, and the minority strand (heavy strand in and contain 37 genes: 13 protein-coding genes, 22 transfer RNA mammal mitochondrial genomes) [7]. Additionally, there is genes (tRNA) and two ribosomal RNA genes (rRNA) [1]. usually more A than T and more C than G on the majority Additionally, there is an A+T-rich region which contains essential strand. However, in some arthropods [8,9,10,11,12], flatworms regulatory elements for the initiation of transcription and [13], brachiopods [14], echinoderms [15] and fish [16], strand replication, and is therefore referred to the control region [2]. asymmetry is reversed and there is less A than T and less C than G Features of highly economized organization, lack of recombina- on the majority strand. tion, maternal inheritance and a high mutation rate relative to the Replication and transcription processes, during which one nuclear genome have resulted in the wide use of mitochondrial strand is transiently in a single-stranded state and thereby exposed genomes in studies of genome evolution, population genetic to more DNA damage, has been widely considered to bias the structure and phylogenetic inference [3]. occurrence of mutations between the two complementary DNA A remarkable feature of mitochondrial DNA is the violation of strands [9,17]. Therefore, inversion of the replication origin Chargaff’s second parity rule, called strand asymmetry (strand located in the A+T-rich region would change the replication order compositional bias) [4,5]. Strand asymmetry is usually reflected by of two mitochondrial DNA strands and consequently lead to AT skew, as expressed by (A2T)/(A+T), and GC skew, as reversal of strand asymmetry [9]. It has been demonstrated in a expressed by (G2C)/(G+C) [6]. Positive AT skew values indicate crustacean [10] and in two vertebrates that replication order is more A than T on the target strand, and positive GC skew values responsible for the reversal of strand asymmetry [18]. Moreover, it indicate more G than C, and vice versa. In insect mitochondrial has been demonstrated in experiments that rates of spontaneous PLoS ONE | www.plosone.org 1 September 2010 | Volume 5 | Issue 9 | e12708 Mt DNA Strand Asymmetry deamination of A and C nucleotides are higher in single-stranded Here, we conduct a broad survey of strand asymmetry in 120 DNA than in double-stranded DNA [19,20,21]. Deamination of A insect mitochondrial genomes, with special reference to the yields a base, hypoxanthine, that pairs with C rather than T, while correlation between skew values and gene direction/replication deamination of C yields a base, uracil, that pairs with A instead of orientation. G [22]. In order to decipher the underlying mutation processes causing Results strand asymmetry in mitochondrial genomes, much research has gone into assessing the contributions of different substitution types Reversal of strand asymmetry in insect mitochondrial associated with replication. C deamination that promotes C:G to genomes T:A transitions was shown to be the major source of mutation in We calculated the AT and GC skews for the entire majority vertebrate mitochondrial DNA [23,24,25]. Additionally, genes strand of 120 insect mitochondrial genomes. Most species have closer to the replication origin of leading strands remain exposed positive AT skews and negative GC skews, i.e., most have a strand to mutation for a longer period of time during replication and this asymmetry characterized by an excess of A relative to T and an should result in a positive correlation between strand asymmetry excess of C relative to G. However, ten species, i.e., two species in and duration of time spent in the single-stranded
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