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Plastome Structure and Phylogenetic Relationships of Styracaceae (Ericales) Xiu‑Lian Cai1, Jacob B

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Plastome Structure and Phylogenetic Relationships of Styracaceae (Ericales) Xiu‑Lian Cai1, Jacob B Cai et al. BMC Ecol Evo (2021) 21:103 BMC Ecology and Evolution https://doi.org/10.1186/s12862-021-01827-4 RESEARCH ARTICLE Open Access Plastome structure and phylogenetic relationships of Styracaceae (Ericales) Xiu‑Lian Cai1, Jacob B. Landis2,3, Hong‑Xin Wang1, Jian‑Hua Wang1, Zhi‑Xin Zhu1 and Hua‑Feng Wang1* Abstract Background: The Styracaceae are a woody, dicotyledonous family containing 12 genera and an estimated 160 spe‑ cies. Recent studies have shown that Styrax and Sinojackia are monophyletic, Alniphyllum and Bruinsmia cluster into a clade with an approximately 20‑kb inversion in the Large Single‑Copy (LSC) region. Halesia and Pterostyrax are not supported as monophyletic, while Melliodendron and Changiostyrax always form sister clades. Perkinsiodendron and Changiostyrax are newly established genera of Styracaceae. However, the phylogenetic relationship of Styracaceae at the generic level needs further research. Results: We collected 28 complete plastomes of Styracaceae, including 12 sequences newly reported here and 16 publicly available sequences, comprising 11 of the 12 genera of Styracaceae. All species possessed the typical quadri‑ partite structure of angiosperm plastomes, with sequence diferences being minor, except for a large 20‑kb (14 genes) inversion found in Alniphyllum and Bruinsmia. Seven coding sequences (rps4, rpl23, accD, rpoC1, psaA, rpoA and ndhH) were identifed to possess positively selected sites. Phylogenetic reconstructions based on seven data sets (i.e., LSC, SSC, IR, Coding, Non‑coding, combination of LSC SSC and concatenation of LSC SSC one IR) produced similar topologies. In our analyses, all genera were strongly+ supported as monophyletic. Styrax+ was+ sister to the remaining genera. Alniphyllum and Bruinsmia form a clade. Halesia diptera does not cluster with Perkinsiodendron, while Perkinsio- dendron and Rehderodendron form a clade. Changiostyrax is sister to a clade of Pterostyrax and Sinojackia. Conclusion: Overall, our results demonstrate the power of plastid phylogenomics in improving estimates of phylo‑ genetic relationships among genera. This study also provides insight into plastome evolution across Styracaceae. Keywords: Styracaceae, Plastome, Genome structure, Phylogeny, Positive selection Background actinomorphic fowers with varying degrees of synsepaly Te Styracaceae DC. & Spreng (Ericales) comprise and sympetaly [2]. Te fruit of Styracaceae is a drupe an angiosperm clade of 12 genera and over 160 spe- or capsule, with persistent calyx, surrounding or united cies, mainly distributed in regions of Asia, as well as with the fruit. Te Styracaceae have been included in a tropical and temperate America, and the Mediterra- number of morphological studies, analyzing leaf anat- nean [1]. Te family consists of shrubs or trees, usually omy [3], wood anatomy [4], pollen morphology [5] and having stellate pubescent or epidermal scales, simple foral morphology and anatomy [2], but distinguishing leaves, with raceme, cyme or panicle inforescence, and between genera in the family primarily involves varia- tion in fruit morphological characters (e.g. hypanthium at maturity). On one hand the ovary is inferior with a *Correspondence: [email protected] persistent hypanthium combined with the fruit at matu- 1 Hainan Key Laboratory for Sustainable Utilization of Tropical Bioresources, College of Tropical Crops, Hainan University, Haikou 570228, rity [(i.e., Changiostyrax C.T. Chen (one species), Halesia China J. Ellis ex L (two species), Melliodendron Hand.-Mazz Full list of author information is available at the end of the article (one species), Parastyrax Siebold & Zucc. (two species), © 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. Cai et al. BMC Ecol Evo (2021) 21:103 Page 2 of 16 Perkinsiodendron P. W. Fritsch (one species), Pterostyrax was polyphyletic with Styrax and Clethra Gronov. ex W.W. Sm.(four species), Rehderodendron Hu (one spe- L. (Clethraceae) clustered in a clade, while Halesia, cies), and Sinojackia Hu (seven species)]. On the other Rehderodendron, and Sinojackia formed a clade that hand, the ovary is superior and a persistent hypanthium was sister to Diapensia L. and Galax Rafn. (Diapensi- forms only at the base of the fruit at maturity [Alniphyl- aceae). However, the interpretation of polyphyly does lum Matsum (three species), Bruinsmia Boerl. & Koord not always hold true. Olmstead et al. [24] inferred the (two species), and Styrax L (130 species)]. Moreover, the phylogeny of Asteridae based on the chloroplast gene ovary of Huodendron Rehder (four species) is semisu- ndhF, showing a strongly supported sister relationship perior with a persistent hypanthium extending from the between Styrax and Halesia. Albach et al. [25] came to base to about two-thirds of the fruit length [1, 2], a fea- the same conclusion based on the DNA gene sequences ture considered to be transitional. atpB, ndhF, rbcL and 18S [24] within the Asterids. In Te systematic position of Styracaceae and the gen- addition, the phylogeny of Styracaceae based on mor- era within have been unstable since the establishment phology plus three DNA sequences (chloroplast trnL of the family by Dumoritor in 1829 [6]. Early research- intron/trnL-trnF spacer and rbcL with the nuclear ers thought Styracaceae was positioned in the order Ebe- ribosomal DNA region ITS) recovered a monophyletic nales, along with the well-known Sapotaceae, Ebenaceae, relationship of Styracaceae [1]. Pterostyrax and Hale- and Symplocaceae, and the small family Lissocarpaceae sia were not supported as monophyletic, since Styrax [7–10]. However, Cronquist [10] showed that these fami- and Huodendron formed a clade that was sister to a lies have some original characteristics and some new clade of Alniphyllum and Bruinsmia, and a sister rela- evolutionary characters, which may have arisen via par- tionship was found between Halesia macgregorii and allel evolution. Based on embryological and anatomi- Rehderodendron macrocarpum [1]. Based on ITS, the cal studies, Herbert [11] suggested that Styracaceae and plastid psbA-trnH intergenic spacer, and microsatellite Teaceae may have originated from a common ances- data, Yao et al. [26] recovered Sinojackia as monophyl- tor, since the two share many common characteristics. etic and reported a similar topology as Fritsch et al. [1] According to molecular systematic studies, Styracaceae with weak support for six genera within Styracaceae. has been recognized as part of the order Ericales sensu Yan et al. [27] conducted phylogenetic analyses of Sty- lato [12]. racaceae based on 19 chloroplast genomes. Te results Within the family, phylogenetic resolution generally showed that Styrax was monophyletic, while Alniphyl- remains poor. At most 17 genera have been included lum and Bruinsmia clustered in a clade with an approx- in Styracaceae, with Symplocos L, Diclidanthera Mart, imate 20-kb inversion in the Large Single-Copy (LSC) Afrostyrax Perk et Gil, Foveolaria Ruiz et pav., Pamphilia region. Species of Pterostyrax were not supported as Mart. ex A. DC, Huapierre et De Wil, and Lissocarpa monophyletic, with Halesia carolina L and Pterostyrax Benth placed in the Styracaceae by various authors [13]. hispidus Siebold & Zucc forming a clade. Symplocos, Diclidanthera, and Lissocarpa were excluded Te chloroplast genomes of most angiosperms are from Styracaceae by Perkins [14]. Symplocos was treated maternally inherited. Te rate of evolution of genes in as an independent family (Symplocaceae Desf) [15]. the chloroplast is relatively slow overall, but diferences Diclidanthera was placed in Polygalaceae [7, 15], and Lis- have been observed across diferent regions of the plas- socarpa was placed in Ebenaceae [16]. Afrostyrax was tome, which can be applied to phylogenetic studies of once included in the genus Styrax [17], but was later various taxonomic scales. Signatures of selection (purify- reclassifed into Huaceae [7, 15, 18]. According to taxo- ing or positive/adaptive) have been observed in diferent nomic revisions, Pamphilia was classifed into Styrax regions of the plastome, including protein coding regions [19], while Fritsch [20] combined Foveolaria into Styrax involved in photosynthesis [28–30]. Several aspects have by implementing morphological phylogenetic analyses. led to the extensive use of plastomes for phylogenetic In addition, two new genera have been established: (1) inference such as a conserved structure, small efective Chen [21] segregated Sinojackia dolichocarpa
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