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Evolutionary Directions of Single Nucleotide Substitutions And Dong et al. BMC Evolutionary Biology (2020) 20:96 https://doi.org/10.1186/s12862-020-01661-0 RESEARCH ARTICLE Open Access Evolutionary directions of single nucleotide substitutions and structural mutations in the chloroplast genomes of the family Calycanthaceae Wenpan Dong1,2, Chao Xu1, Jun Wen1,3 and Shiliang Zhou1,4* Abstract Background: Chloroplast genome sequence data is very useful in studying/addressing the phylogeny of plants at various taxonomic ranks. However, there are no empirical observations on the patterns, directions, and mutation rates, which are the key topics in chloroplast genome evolution. In this study, we used Calycanthaceae as a model to investigate the evolutionary patterns, directions and rates of both nucleotide substitutions and structural mutations at different taxonomic ranks. Results: There were 2861 polymorphic nucleotide sites on the five chloroplast genomes, and 98% of polymorphic sites were biallelic. There was a single-nucleotide substitution bias in chloroplast genomes. A → TorT→ A(2.84%)and G → CorC→ G (3.65%) were found to occur significantly less frequently than the other four transversion mutation types. Synonymous mutations kept balanced pace with nonsynonymous mutations, whereas biased directions appeared between transition and transversion mutations and among transversion mutations. Of the structural mutations, indels and repeats had obvious directions, but microsatellites and inversions were non-directional. Structural mutations increased the single nucleotide mutations rates. The mutation rates per site per year were estimated to be 0.14–0.34 × 10− 9 for nucleotide substitution at different taxonomic ranks, 0.64 × 10− 11 for indels and 1.0 × 10− 11 for repeats. Conclusions: Our direct counts of chloroplast genome evolution events provide raw data for correctly modeling the evolution of sequence data for phylogenetic inferences. Keywords: Chloroplast genome, Calycanthaceae, Structural mutations, Substitution rate, Indels Background genome structure mutations and nucleotide substitu- Genome evolution is a major theme of biology in the tions. The mutations of genome structure include inser- genomics era. The topics cover patterns, directions and tions/deletions (indels) and inversions. The nucleotide rates of substitutions, repeats, rearrangements and re- substitutions are classified into transition (Ts) and trans- combinations, hybridization and polyploidy, lateral gene version (Tv). A genome consists of coding regions and transfer, gene families, etc., with varying depth and scope noncoding regions (including introns and intergenic [1, 2]. Genome evolution can be easily demonstrated by spacers). The nuclear genome is usually very large and complicate. Moreover, plant nuclear genome sequencing * Correspondence: [email protected] is still a bottle-neck due to high costs, bacteria or fungi 1 State Key Laboratory of Systematic and Evolutionary Botany, Institute of contaminations, high heterozygosity, etc. [3, 4]. Only Botany, Chinese Academy of Sciences, Beijing 100093, China 4University of Chinese Academy of Sciences, Beijing 100049, China economically important or model plants have their Full list of author information is available at the end of the article © The Author(s). 2020 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://creativecommons.org/licenses/by/4.0/. 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 in a credit line to the data. Dong et al. BMC Evolutionary Biology (2020) 20:96 Page 2 of 12 complete nuclear genomes sequenced. Instead, the subfamilies (see below for more details). The phylogen- chloroplast genomes unique to plants are very much etic topology of the family has only one possibility at smaller and easier to manipulate, and it is more likely to subfamily, genus and species ranks (Fig. 1), which en- give a complete picture of plant genome evolution. ables us to infer the chloroplast genome evolution in this Therefore, chloroplast genomes are currently a right family at different taxonomic ranks. In this study, we use choice for genome evolution studies. Calycanthaceae as a model to empirically observe the di- Considerable attention has been paid to the evolution rections and to estimate the rates of different mutations rate variations among genes or lineages [5, 6]. The imprinted in the chloroplast genomes at different taxo- chloroplast genes such as ndhF, matK, rbcL and trnL-F nomic ranks. More specifically, we are going to answer have been well studied [7, 8]. Chloroplast DNA shows a (1) if there are significant mutation rate differences be- biased transition (Ts) mutation toward A and T. For ex- tween the two subfamilies, between the two genera ample, the frequency of A and T at the 3rd codon pos- within subfamily Calycanthoideae, and among species ition is fourfold of other nucleotides in the rbcL gene of within Calycanthus and within Chimonanthus; and (2) angiosperms [8]. This explains why the chloroplast ge- what the evolutionary patterns, directions of nucleotide nomes are usually A/T rich. The rates of the single nu- substitutions and structural mutations in the Caly- cleotide mutations are not uniform among different canthaceae chloroplast genomes are like. Such kind of genes. Transition/transversion ratios (Ts/Tv) are 0.9 for empirical data is of values for precisely modeling the rbcL and 1.4 for matK [9, 10]. Among the eight transver- chloroplast genome evolution. sion mutation possibilities, from A to T and C to G are significantly less frequent than the other four possibil- Methods ities [11–13]. Whether this observation is a general pat- The family Calycanthaceae and sampling strategies tern or only a special case remains to be tested at Calycanthaceae holds a basal position in Laurales [26]. genome level. The family is subdivided into two subfamilies: subfamily Structural mutations of genomes convey important Idiospermoideae [one genus, one species, Idiospermum evolution information of organisms. The indels and in- australiense (Diels) S. T. Blake] and subfamily Caly- versions are rich in chloroplast genomes and can be reli- canthoideae (two genera, ca. nine species). Subfamily ably identified and used to reveal the evolution of Idiospermoideae was sometimes considered a distinct organisms [14, 15]. Structural mutations are not ran- family [27] but it is more natural in Calycanthaceae. domly distributed throughout the chloroplast genome There are three species in Calycanthus, one in China (C. [14]. Tandem repeat-induced indels showed a statisti- chinensis Cheng & S. Y. Chang) and two in USA (C. flor- cally significant bias towards A/T-rich and the indel mu- idus L. and C. occidentalis Hook. & Arn.). Calycanthus tation rate was estimated to be approximately 0.8 ± chinensis was once separated and put in the monotypic − 0.04 × 10 9 per site per year in Poaceae [16]. Short in- genus Sinocalycanthus. There are about six species in versions also have a widespread occurrence in chloro- Chimonanthus. There are deciduous species like Ch. plast genomes and often form stem-loop structures [17– praecox L., and evergreen species like Ch. nitens Oliv. 19]. Understanding the evolution of such structural mu- (see Zhou et al. 2006 for details). tations is crucial for making full and correct use of the We selected five species, C. chinensis, C. floridus, Ch. genome information [20]. nitens, Ch. praecox and Idiospermum australiense,to The rates of DNA mutation is one of the core ques- represent two subfamilies, three genera and deciduous tions in molecular evolution [5]. The mutation rates can and evergreen species within Chimonanthus. Thus their be estimated from either mutation accumulation (MA) phylogenetic relationships are intuitively quite clear lines [21, 22] or phylogenetic inference [23]. For the lat- (Fig. 1). The chloroplast genome of C. floridus has been ter method, if the branch age is known, the absolute determined [28] and the genomes of other four species substitution rate can be calculated. The branch age is need to be determined. Young and healthy leaves of usually dated using calibrated molecular clocks. It is a these species were collected. The voucher details of the common practice to infer the directions of mutations ac- samples are given in Supplementary Table S1. According cording to a phylogeny which, unfortunately, is usually to APG IV [29], more basal species Liriodendron tulipi- based on the same dataset. It would be better if the phyl- fera L. and Magnolia kwangsiensis Figlar & Noot. are ogeny is independent to dataset [24]. The family Caly- used as outgroups. canthaceae serves as an ideal reference because the phylogenetic relationships within the
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