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Mitochondrial Genome of the Stonefly Kamimuria Wangi (Plecoptera: Perlidae) and Phylogenetic Position of Plecoptera Based on Mitogenomes

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Mitochondrial Genome of the Stonefly Kamimuria Wangi (Plecoptera: Perlidae) and Phylogenetic Position of Plecoptera Based on Mitogenomes Mitochondrial Genome of the Stonefly Kamimuria wangi (Plecoptera: Perlidae) and Phylogenetic Position of Plecoptera Based on Mitogenomes Qian Yu-Han1,2, Wu Hai-Yan1, Ji Xiao-Yu1, Yu Wei-Wei1, Du Yu-Zhou1* 1 School of Horticulture and Plant Protection and Institute of Applied Entomology, Yangzhou University, Yangzhou, Jiangsu, China, 2 College of Forestry, Southwest Forestry University, Kunming, Yunnan, China Abstract This study determined the mitochondrial genome sequence of the stonefly, Kamimuria wangi. In order to investigate the relatedness of stonefly to other members of Neoptera, a phylogenetic analysis was undertaken based on 13 protein-coding genes of mitochondrial genomes in 13 representative insects. The mitochondrial genome of the stonefly is a circular molecule consisting of 16,179 nucleotides and contains the 37 genes typically found in other insects. A 10-bp poly-T stretch was observed in the A+T-rich region of the K. wangi mitochondrial genome. Downstream of the poly-T stretch, two regions were located with potential ability to form stem-loop structures; these were designated stem-loop 1 (positions 15848– 15651) and stem-loop 2 (15965–15998). The arrangement of genes and nucleotide composition of the K. wangi mitogenome are similar to those in Pteronarcys princeps, suggesting a conserved genome evolution within the Plecoptera. Phylogenetic analysis using maximum likelihood and Bayesian inference of 13 protein-coding genes supported a novel relationship between the Plecoptera and Ephemeroptera. The results contradict the existence of a monophyletic Plectoptera and Plecoptera as sister taxa to Embiidina, and thus requires further analyses with additional mitogenome sampling at the base of the Neoptera. Citation: Yu-Han Q, Hai-Yan W, Xiao-Yu J, Wei-Wei Y, Yu-Zhou D (2014) Mitochondrial Genome of the Stonefly Kamimuria wangi (Plecoptera: Perlidae) and Phylogenetic Position of Plecoptera Based on Mitogenomes. PLoS ONE 9(1): e86328. doi:10.1371/journal.pone.0086328 Editor: Patrick C. Y. Woo, The University of Hong Kong, China Received July 17, 2013; Accepted December 9, 2013; Published January 23, 2014 Copyright: ß 2014 Yu-Han 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: This work was supported by National Natural Science Foundation of China (No. 31071958). 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 basal group, diverging early after the split between the Paleoptera and Neopteran ancestors, and before other Neopteran diversifi- The order Plecoptera is comprised of 16 families and includes cation [11,12]. At the same time, the relationship about 3,497 species [1]; these occur on all continents except Antarctica Styloperlidae, Peltoperlidae, Chloroperlidae, Perlidae and Perlo- [2]. Plecoptera is a small order of hemimetabolous insects that are didae was controversial [13,14]. The aim of this study was to primarily associated with clean, cool, running water and cool, discuss the phylogenetic position of Plecoptera based on mtDNA. damp terrestrial environments [3]. The nymphs generally have In this work, we present the complete mitochondrial genome of their highest density in riffle areas of streams where rocks, gravel, the stonefly, Kamimuria wangi Du, 2012 (Perlidae) and reconstructed snags, and accumulated leaves are abundant. Their potential use phylogenies of 17 major basal Pterygote lineages based on 13 as biological indicators of water quality is well-known [4]. PCGs obtained from mitochondrial genomes. The insects mitochondrial genome is a circular molecule ranging from 15 to 20 kp; it generally encodes two rRNA genes, 22 tRNA genes, 13 protein-coding genes (PCGs), and an A+T-rich Results and Discussion region varying in length among taxa [5,6]. Recently, whole Genome organization, structure and composition mitochondrial DNA (mtDNA) sequences have been used in The full-length mtDNA of K. wangi is a circular molecule of phylogenetic analyses of various insect orders. After the complete 16,179 nucleotides, just slightly longer than that of P. princeps mitochondrial genome of Pteronarcys princeps was published [7], (16004 bp). The K. wangi mtDNA contains 37 genes (13 PCGs, 22 increasing numbers of researchers used this data for phylogenetic tRNA genes, two rRNA genes) and an AT-rich control region. analyses, which resulted in various theories on the phylogenetic The number and arrangement of these genes is consistent with position of Plecoptera. Zhang et al. and Lin et al. [8,9] used 13 insect mitochondrial DNA [5,15] and identical to the P. princeps PCGs of mtDNA data to support relatedness between Ephemer- mitogenome (Figure 1). In 12 locations of the mtDNA, genes optera and Plecoptera within the Neoptera. overlapped by 1–47 bp (excluding the A+T-rich region; see The stoneflies are an ancient group of insects. Their fossil record Table 1). The mtDNA of K. wangi also contained intergenic regions extends into the Lower Permian [10]. But the phylogenetic (1–28 bp in length) in 13 locations. position of Plecoptera has long been under debate. Some of the competing evolutionary hypotheses place the stoneflies in a single PLOS ONE | www.plosone.org 1 January 2014 | Volume 9 | Issue 1 | e86328 Mitochondrial Genome and Phylogenetic of Stonefly Table 1. Annotation of the mitochondrial genome of K. wangi. a Feature Region Length Codon IGNb From To Start Stop tRNAIle(I) 16868 tRNAGln(Q) (69 137) 69 0 tRNAMet(M) 139 207 69 1 ND2 208 1245 1038 ATG TAA 0 tRNATrp(W) 1245 1311 67 21 tRNACys(C) (1304 1372) 69 28 tRNATyr(Y) (1372 1437) 66 21 COI 1397 2983 1587 ATA TAA 241 tRNALeu(UUR) 2939 3004 66 245 COII 3010 3705 686 ATG TAA 56 tRNALys(K) 3706 3776 71 0 tRNAAsp(D) 3778 3846 69 1 Figure 1. A map of the mitogenome of Kamimuria wangi. Transfer RNA genes are designated by single-letter amino acid codes. CR ATP8 3856 4005 150 ATA TAA 9 represents the A+T-rich region. The gene name without underline ATP6 3999 4676 678 ATG TAA 27 indicates the direction of transcription from left to right, and with underline indicates right to left. COIII 4676 5464 789 ATG TAA 21 doi:10.1371/journal.pone.0086328.g001 tRNAGly(G) 5467 5533 67 2 ND3 5534 5887 354 ATT TAA 0 tRNAAla(A) 5889 5953 65 1 Thirteen PCGs in K. wangi utilize the conventional translational Arg(R) start and stop codons for invertebrate mtDNA. For example, nine tRNA 5954 6017 64 0 PCGs (ND2, COII, ATP6, COIII, ND5, ND4, ND4L, ND6 and tRNAAsn(N) 6018 6084 67 0 CytB) contained ATG codons. Three PCGs (COI, ATP8 and tRNASer(AGN) 6085 6151 67 0 ND1) initiated with ATA codons, and one PCG (ND3) contained tRNAGlu(E) 6152 6217 66 0 ATT as the start site. However, in P. princeps, ND2 and ND5 tRNAPhe(F) (6224 6289) 66 6 initiated with GTG, ND6 and ATP8 with ATT, and ND1 gene ND5 (6273 8021) 1749 ATG TAA 217 initiated with TTG. Thirteen PCGs used the typical termination His(H) codons TAA and TAG in K. wangi. In contrast, only two PCGs tRNA (8022 8089) 68 0 encode conventional termination codons in P. princeps, e.g. TAA ND4 (8091 9455) 1365 ATG TAG 1 for ND4 and TAG for ND1. ND4L (9449 9745) 297 ATG TAA 27 The relative synonymous codon usage (RSCU) values showed a tRNAThr(T) 9748 9813 66 2 biased use of A and T nucleotides in K. wangi (Table 2). The high tRNAPro(P) (9814 9880) 67 0 incidence of anticodons NNA and NNU indicated partiality for ND6 9882 10397 516 ATG TAA 1 AT in the anticodon of PCGs. Ile (8.12%), Leu (11.61%), Ser (11.99%) and Thr (7.03%) were the most frequent amino acids in CYTB 10397 11536 1140 ATG TAG 21 K. wangi mtDNA PCGs, and Ser showed the highest incidence. In tRNASer(UCN) 11535 11604 70 22 P. princeps PCGs, Ile (7.51%), Leu (12.23%), Asn (7.48%) and Ser ND1 (11558 12541) 984 ATA TAA 247 (12.15%) were the most common amino acids, and Leu occurred tRNALeu(CUN) (12570 12636) 67 28 most frequently. lr RNA(16s) (12638 13982) 1345 1 The overall AT content in K. wangi mtDNA was 69.6%, which Val(V) was slightly lower than that of P. princeps (70.6%). The average AT tRNA (13991 14061) 71 8 content across all PCGs in K. wangi was 68.0%, which also lower sr RNA(12s) (14062 14928) 867 0 than that of P. princeps (70.5%). The nucleotide composition of the D-loop 14929 16179 1251 0 insect mitogenome was biased toward A and T nucleotides. The aPositions with parentheses indicate the genes encoded by N strand. AT content of the third codon (73.3%) was much higher than the bIGN: Intergenic nucleotide; minus (-) indicates overlap between genes. first (63.5%) and second codon positions (67.1%); this suggested doi:10.1371/journal.pone.0086328.t001 that both higher mutation rates and the increased AT occurrence are related and dependent on relaxed selection at the third codon by a total of 1484 nucleotides; tRNAs ranged from 64 to 71 bp position. However, the A+T% at the second codon (65.7%) was and the A+T content was 72.4%. Fourteen tRNAs were encoded lower than the first (71.0%) and third codon positions (74.9%) in P. by the H-strand and the remaining eight were encoded by the L- princeps. Furthermore, we present the detailed comparison in the strand.
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