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Quantification and Evolution of Mitochondrial Genome Zhang et al. BMC Ecol Evo (2021) 21:19 BMC Ecology and Evolution https://doi.org/10.1186/s12862-021-01755-3 RESEARCH ARTICLE Open Access Quantifcation and evolution of mitochondrial genome rearrangement in Amphibians Jifeng Zhang1,2,3,4,5* , Guopen Miao1, Shunjie Hu1, Qi Sun1, Hengwu Ding2, Zhicheng Ji6, Pen Guo7, Shoubao Yan1, Chengrun Wang1, Xianzhao Kan2* and Liuwang Nie2* Abstract Background: Rearrangement is an important topic in the research of amphibian mitochondrial genomes ("mitog- enomes" hereafter), whose causes and mechanisms remain enigmatic. Globally examining mitogenome rearrange- ments and uncovering their characteristics can contribute to a better understanding of mitogenome evolution. Results: Here we systematically investigated mitogenome arrangements of 232 amphibians including four newly sequenced Dicroglossidae mitogenomes. The results showed that our new sequenced mitogenomes all possessed a trnM tandem duplication, which was not exclusive to Dicroglossidae. By merging the same arrangements, the mitogenomes of ~ 80% species belonged to the four major patterns, the major two of which were typical vertebrate arrangement and typical neobatrachian arrangement. Using qMGR for calculating rearrangement frequency (RF) (%), we found that the control region (CR) (RF 45.04) and trnL2 (RF 38.79) were the two most frequently rearranged components. Forty-seven point eight percentage= of amphibians= possessed rearranged mitogenomes including all neobatrachians and their distribution was signifcantly clustered in the phylogenetic trees (p < 0.001). In addition, we argued that the typical neobatrachian arrangement may have appeared in the Late Jurassic according to possible occurrence time estimation. Conclusion: It was the frst global census of amphibian mitogenome arrangements from the perspective of quantity statistics, which helped us to systematically understand the type, distribution, frequency and phylogenetic character- istics of these rearrangements. Keywords: Mitogenomics, Amphibians, qMGR, Rearrangement score, Rearrangement frequency, Phylogenetic characteristics Background transduction and intermediary metabolism. Te content As semi-autonomous organelles, mitochondria retain of vertebrate mitogenomes is conservative, including 13 their own genomes and participate in many essential protein-coding genes (PCGs), 22 tRNA genes (trns), 2 biological processes in eukaryotic cells such as energy rRNA genes (rrns) and a control region (CR) with repli- cation and gene transcriptional regulatory signals [1, 2]. Because of the moderate evolutionary rate of the mitoge- *Correspondence: [email protected]; [email protected]; [email protected] nome, it has been an excellent molecular marker for phy- 1 School of Biological Engineering, Huainan Normal University, Huainan, logenetic studies [3–6]. Anhui 232001, People’s Republic of China Te gene order of vertebrate mitogenomes is as con- 2 College of Life Science, Anhui Normal University, Wuhu, Anhui 241000, People’s Republic of China servative as its content, such that human, mouse, clawed Full list of author information is available at the end of the article frog and zebrafsh all share the same gene arrangement © The Author(s) 2021. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creat iveco mmons .org/licen ses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creat iveco mmons .org/publi cdoma in/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Zhang et al. BMC Ecol Evo (2021) 21:19 Page 2 of 14 in their mitogenomes [7–10]. However, with an increas- in mitogenome rearrangements has been reported [34]. ing number of diferent species’ mitogenomes completely Tese fndings inspire us to further explore the landscape sequenced, gene rearrangements have been reported in of mitogenome rearrangements in amphibians. many diferent taxa. Generally, these rearrangements are Except for earlier studies on a few species of amphib- inferred to the results from events such as gene transpo- ians, most studies have focused only on a few lineages sition, gene inversion, gene duplication, and gene loss. rather than a more global and systematic analysis. Also, Summaries and comparisons of animal mitogenome rear- previous studies have paid little attention to the role of rangements have been reported [3, 11]. An initial impor- individual genes in rearrangement. Recently we proposed tant study undertaken by Boore summarized all gene a method, qMGR, for quantifying mitogenome rear- arrangements known for Metazoa, based on no more rangement and developed a web service (http://qmgr. than 100 mitogenomes available at that time [1]. Further hnnu.edu.cn/) that provides large-scale and accurate comparative studies of mitogenome arrangement have analysis of mitogenome rearrangement information [35]. subsequently been published (e.g., [12–15]). In addition, In this study, we newly determined mitogenomes for several possible rearrangement models were proposed four frogs in the neobatrachian frog family Dicroglossi- to explain mechanisms, including tandem duplication– dae, and found that they all had a tandem duplication of random loss (TDRL) [16, 17], tandem duplication and trnM (IQMM trn cluster), which was not a feature exclu- non-random loss (TDNL) [18, 19], intramitochondrial sive to this family [36, 37]. To identify common charac- recombination [20, 21], etc. Using the CREx and TreeREx teristics of mitogenome rearrangement in amphibians, programs, based on four rearrangement models, other we then focused on the study of gene rearrangement studies have tried to fnd common intermediate steps patterns of all known amphibian mitogenomes, quanti- (common intervals) in two or more gene orders being fed the rearrangement frequency (RF) for each single investigated to elucidate the evolution of mitogenome gene and the rearrangement score (RS) for each mitog- rearrangements in diferent lineages such as insects and emome by qMGR, detected phylogenetic characteristics crabs [22–25]. of species with identical mitogenome arrangements, and In general, most animals retain the conserved rather estimated possible time for rearrangement patterns. Our than rearranged mitogenome components and order. Te fndings contribute to understanding characteristics and conservative arrangement is called the “typical vertebrate evolution of mitogenome rearrangement in amphibians. (mitogenome) arrangement” in vertebrates and the “typi- cal invertebrate (mitogenome) arrangement” in inverte- Results brates [1, 26]. To date, the number of vertebrate species trnM tandem duplication of amphibian mitogenomes with typical vertebrate arrangement accounts for more Lengths of the four newly sequenced mitogenomes are than half of all species for which mitogenomes have been 18,520 bp (Quasipaa robertingeri), 16,640 bp (Limnon- determined. Among the amphibians, neobatrachians are ectes fragilis), 18,154 bp (Limnonectes fujianensis (Tai- the majority of frogs, accounting for ~ 92% of the total, wan)) and 18,293 bp (Limnonectes fujianensis (Fujian)), over 6600 species (AmphibiaWeb, http://www.Amphi respectively, and the full range of their GC contents biawe b.org/, accessed February, 2020). Most sequenced was relatively narrow (39.7–42.9%). Te four new neobatrachian frogs possess a derived mitogenome mitogenomes all contain a tandem duplication of trnM arrangement, “typical neobatrachian arrangement” [14, (IQMM trn cluster) that also occurs in other sequenced 27, 28]. Furthermore, there are some other types of rear- dicroglossids [14]. rangements in addition to typical neobatrachian arrange- Among the 35 amphibian mitogenomes presenting ment in amphibians. For example, the mitogenome of the evidence of duplication or loss of genes as well as CRs neobtrachian frog Limnonectes bannaensis lacks trnA, (excluding gene rearrangement with the same total num- trnN, trnC and trnE and contains a tandem duplication ber of genes), 19 species (including our four new mitog- of trnM [29], the mitogenome of the caecilian Crotapha- enomes) possess a tandem duplication of trnM (IQMM trema lamottei includes the duplications of trnF, trnP and trn cluster) (see Table 1). Tese 19 species represent 16 trnT and lack of trnK [30], and there are two CRs found species of Dicroglossidae, two species of Megophryidae in the mitogenomes of the neobatrachian frogs Mantella (the non-neobatrachian frog family), and one species madagascariensis [31] and Rhacophorus schlegelii [32]. of the neobatrachian Ceratobatrachidae. Tus, tandem In addition, while nad6 is located between nad5 and cob duplication of trnM is not exclusive to Dicroglossidae, genes within typical vertebrate mitogenome, it is rear- and more than one rearrangement
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