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Comparative Analysis of the Mitochondrial Genomes of Oriental Spittlebug Trible Cosmoscartini: Insights Into the Relationships A

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Comparative Analysis of the Mitochondrial Genomes of Oriental Spittlebug Trible Cosmoscartini: Insights Into the Relationships A Su et al. BMC Genomics (2018) 19:961 https://doi.org/10.1186/s12864-018-5365-7 RESEARCHARTICLE Open Access Comparative analysis of the mitochondrial genomes of oriental spittlebug trible Cosmoscartini: insights into the relationships among closely related taxa Tianjuan Su1,2 ,BoHe3, Kui Li1,2 and Aiping Liang1,2* Abstract Background: Cosmoscartini (Hemiptera: Cercopoidea: Cercopidae) is a large and brightly colored Old World tropical tribe, currently containing over 310 phytophagous species (including some economically important pests of eucalyptus in China) in approximately 17 genera. However, very limited information of Cosmoscartini is available except for some scattered taxonomic studies. Even less is known about its phylogenetic relationship, especially among closely related genera or species. In this study, the detailed comparative genomic and phylogenetic analyses were performed on nine newly sequenced mitochondrial genomes (mitogenomes) of Cosmoscartini, with the purpose of exploring the taxonomic status of the previously defined genus Okiscarta and some closely related species within the genus Cosmoscarta. Results: Mitogenomes of Cosmoscartini display similar genomic characters in terms of gene arrangement, nucleotide composition, codon usage and overlapping regions. However, there are also many differences in intergenic spacers, mismatches of tRNAs, and the control region. Additionally, the secondary structures of rRNAs within Cercopidae are inferred for the first time. Based on comparative genomic (especially for the substitution pattern of tRNA secondary structure) and phylogenetic analyses, the representative species of Okiscarta uchidae possesses similar structures with other Cosmoscarta species and is placed consistently in Cosmoscarta. Although Cosmoscarta bimacula is difficult to be distinguished from Cosmoscarta bispecularis by traditional morphological methods, evidence from mitogenomes highly support the relationships of (C. bimacula + Cosmoscarta rubroscutellata)+(C. bispecularis + Cosmoscarta sp.). Conclusions: This study presents mitogenomes of nine Cosmoscartini species and represents the first detailed comparative genomic and phylogenetic analyses within Cercopidae. It is indicated that knowledge of mitogenomes can be effectively used to resolve phylogenetic relationships at low taxonomic levels. Sequencing more mitogenomes at various taxonomic levels will also improve our understanding of mitogenomic evolution and phylogeny in Cercopidae. Keywords: Mitochondrial genome, Spittlebug, Cosmoscartini, Phylogeny * Correspondence: [email protected] 1Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China 2College of Life Sciences, University of Chinese Academy of Sciences, Beijing 100049, China Full list of author information is available at the end of the article © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Su et al. BMC Genomics (2018) 19:961 Page 2 of 13 Background less is understood about the phylogenetic relationship The mitochondrial genome (mitogenome) of most meta- within Cosmoscartini, especially among closely related zoan is circular and compact with relatively conserved genera or species. There is a controversy related to gene organization, order and direction. It varies from 14 whetherornotOkiscarta should be raised to genus to 20 kb and contains 13 protein-coding genes (PCGs), level [ 18–20]. Therefore, detailed molecular data is re- two ribosomal RNA genes (rRNAs), 22 transfer RNA quired for a comprehensive phylogenetic analysis of the genes (tRNAs), and a large non-coding region (also re- tribe Cosmoscartini. ferred to as the control region) [1–3]. Owing to some To date, only one complete mitogenome of Cosmos- unique features like small size, high copy numbers, ma- cartini has been sequenced (GenBank accession number ternal inheritance, strict orthologous genes, low rate of KP064511), which is quite limited and restricts our un- recombination, and accelerated rate of nucleotide substi- derstanding of the phylogeny of Cosmoscartini. In the tution [4, 5], the mitogenome has been extensively used present study, we sequenced mitogenomes of nine Cos- in various study areas, including species identification, moscartini species, including one Ectemnonotum, one population genetics, phylogeny and evolution [6–9]. Okiscarta (this genus has only two species totally), and Genome-level characters, including nucleotide compos- seven Cosmoscarta species, respectively. The aims of this ition, structural genomic features, and gene rearrange- study were to: 1) provide a detailed comparative analysis ment, have also been widely used for comparative and of these mitogenomes, including nucleotide compos- evolutionary genomics, and phylogenetic inference at ition, codon usage, secondary structures of RNAs, and different taxonomic levels [7, 10, 11]. TRNAs with dif- novel features of the control region; 2) investigate the ferent patterns in base composition, gene rearrange- phylogenetic relationships among three genera of Cos- ment, and secondary structure are proposed as useful moscartini, especially for the taxonomic status of the ways to study the evolution of mitogenomes and can be previously defined genus Okiscarta; 3) explore the rela- used as powerful phylogenetic markers [12–15]. Further- tionships among some closely related species, which more, mitogenomes, especially in intergenic spaces, usu- were difficult to distinguish from traditional morpho- ally present higher mutation rates than nuclear genes logical methods. and may provide valuable information for phylogenetic analyses among closely related taxa [10, 16, 17]. Cosmoscartini (Hemiptera: Cercopoidea: Cercopidae) Results is a large and brightly colored Old World tropical tribe, Genome structure including more than 310 described species in approxi- This study presented five complete and four nearly mately 17 genera [18–20]. Just as other spittlebugs, dur- complete mitogenomes with the absence of the con- ing the nymphal period, they present the habit of trol region (Fig. 1). The total length of each complete producing copious spittle masses to cover themselves in- mitogenome ranged from 15,024 bp in Cosmoscarta side through continuously sucking the liquid and nutri- bimacula to 15,677 bp in Cosmoscarta rubroscutellata ents contained in xylem tissue, which may cause serious (Additional file 1: Table S1). The sequenced mitogen- economic damage to host plants [21, 22]. In terms of omes contained the entire set of 37 genes. The J-strand ecological function, spittle mass has traditionally been carried most of the genes (9 PCGs and 14 tRNAs), while seen as an effective barrier against predation, parasit- the remaining genes (4 PCGs, 8 tRNAs and two rRNAs) ism, and desiccation [21, 23]. In addition, the spittle were located on the N-strand (Fig. 1). Gene arrangement mass functions as a light attenuator, which could re- was identical within Cosmoscartini and was consistent duce potentially damaging solar radiation [24]. Further- with the putative ancestral type of insects [2, 7]. All the se- more, nymphs of many spittlebug species are known to quenced genomes were relatively compact with genes aggregate in one spittle mass and inflict more serious overlapping at 12–15 locations, in which the longest over- economic damage [25]. Some species of Cosmoscarta lap (8 bp) was between trnW and trnC. These overlapping are reported as economically important pests of euca- sequences were highly conserved in length among all se- lyptus in China [26]. Therefore, it is very important to quenced Cosmoscartini mitogenomes. Two PCG pairs, in- accurately elucidate the taxonomic status and phylo- cluding atp8-atp6 and nad4-nad4l, both overlapped 7 bp genetic relationships of Cosmoscartini species. How- and shared the similar sequence (ATGNTAA), which had ever, only very limited studies about Cosmoscartini are also been reported in many other insect mitogenomes [29, available except for some scattered taxonomic studies 30].Therewerealso5–7 intergenic spacers (in addition to [27, 28] and the detailed biology of Cosmoscartini spe- the control region), with the longest intergenic spacer lo- cies is likewise scattered. Additionally, some taxa are cated between trnS2 and nad1. In addition, 14–19 pairs of difficult to identify to species due to a lack of sufficient genes were directly adjacent with one another including diagnostic characters to illustrate distinctions [21]. Even the pairs of rrnL-trnV, trnV-rrnS, rrnS-CR, and CR-trnI. Su et al. BMC Genomics (2018) 19:961 Page 3 of 13 Fig. 1 Circular diagram of the nine Cosmoscartini mitogenomes. Different color is performed to show the nucleotide identity of BLAST hits, with the reference genome represented by C. bimacula. The rings are arranged in an order that the most similar genome is placed closest to the outer edge of the circle To better visualize the sequence identity in Cosmos- generally higher
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