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Developing DNA Barcodes for Species Identification In Journal of Systematics and Evolution 9999 (9999): 1–13 (2014) doi: 10.1111/jse.12076 Research Article Developing DNA barcodes for species identification in Podophylloideae (Berberidaceae) 1Yun‐Rui MAO 1Yong‐Hua ZHANG 2Koh NAKAMURA 3Bi‐Cai GUAN 1Ying‐Xiong QIU* 1(Key Laboratory of Conservation Biology for Endangered Wildlife of the Ministry of Education, and Laboratory of Systematic and Evolutionary Botany and Biodiversity, College of Life Sciences, Zhejiang University, Hangzhou 310058, China) 2(Herbarium (HAST), Biodiversity Research Center, Academia Sinica, Taipei 115, Nangang, Taiwan, China) 3(College of Life Sciences and Food Engineering, Nanchang University, Nanchang 310031, China) Abstract Species of Podophyllum, Dysosma, Sinopodophyllum, and Diphylleia, genera from Podophylloideae of Berberidaceae, have long been used in traditional herbal medicine in East Asia and/or North America. Accurate identification of the species of these four genera is crucial to their medicinal uses. In this study, we tested the utility of nine barcodes (matK, rbcL, atpH‐atpI, rpl32‐trnLUAG, rps18‐clpp, trnL‐trnF, trnL‐ndhJ, trnS‐trnfM, and internal transcribed spacer (ITS)) to discriminate different species of Podophylloideae. Thirty‐six individuals representing 12 species of Podophylloideae were collected from different locations in China, Japan, and North America. We assessed the feasibility of amplification and sequencing of all markers, examined the levels of the barcoding gap based on DNA sequence divergence between ranges of intra‐ and interspecific variation using pairwise distances, and further evaluated successful identifications using each barcode by similarity‐based and tree‐based methods. Results showed that nine barcodes, except rps18‐clpp, have a high level of primer universality and sequencing success. As a single barcode, ITS has the most variable sites, greater intra‐ and interspecific divergences, and the highest species discrimination rate (83%), followed by matK which has moderate variation and also high species discrimination rates. However, these species can also be discriminated by ITS alone, except Dysosma versipellis (Hance) M. Cheng ex T. S. Ying and D. pleiantha (Hance) Woodson. The combination of ITS þ matK did not improve species resolution over ITS alone. Thus, we propose that ITS may be used as a sole region for identification of most species in Podophylloideae. The failure of ITS to distinguish D. versipellis and D. pleiantha is likely attributed to incomplete lineage sorting due to recent divergence of the two species. Key words DNA barcoding, Podophylloideae, species identification, traditional Chinese medicine. Podophylloideae Eaton is a small subfamily of 12 idaceae, and also confirmed that Sinopodophyllum species belonging to Berberidaceae, which comprises hexandrum (Royle) T. S. Ying was sister to the ENA Sinopodophyllum (Royle) Ying (1 sp.), Dysosma Podophyllum peltatum L. (Loconte & Estes, 1989; Woodson (7 spp.), Podophyllum L. (1 sp.), and Nickol, 1995; Kim & Jansen, 1998; Liu et al., 2002; Diphylleia Michaux (3 spp.) (Loconte, 1993; Ying Wang et al., 2009), which was sister to Dysosma et al., 1993). Dysosma is restricted to China. Diphylleia versipellis (Hance) M. Cheng ex T. S. Ying; species of has an intercontinental disjunct distribution in eastern Diphylleia formed a basal clade in Podophylloideae with North America (ENA) (Diphylleia cymosa Michaux) Diphylleia cymosa from ENA, sister to Diphylleia and East Asia (Diphylleia grayi F. Schmidt and grayi–Diphylleia sinensis from East Asia (Wang Diphylleia sinensis H. L. Li). Both Sinopodophyllum et al., 2007, 2009). However, in all previous studies, and Podophyllum are monotypic, and native to the most species of Dysosma were missing except Himalaya–Hengduan Mountains and ENA, respectively D. versipellis; thus the detailed picture of species (Ying et al., 1993). Previous phylogenetic analyses relationships within the subfamily has remained unclear. using morphological and molecular data revealed that Podophylloideae species are rich sources of Podophylloideae was a monophyletic group in Berber- podophyllotoxin, an aryltetralin lignan that has impor- tant biological activities and is the precursor of semisynthetic chemotherapeutic drugs such as etopo- Received: 19 June 2013 Accepted: 19 December 2013 Ã Author for correspondence. E‐mail: [email protected]. Tel./Fax: side and teniposide (Broomhead & Dewick, 1990; 86‐571‐86432273. Stähelin & von Wartburg, 1991). However, the © 2014 Institute of Botany, Chinese Academy of Sciences 2 Journal of Systematics and Evolution Vol. 9999 No. 9999 2014 phytochemical compounds in quality and effect differ phyllum, Podophyllum, and Dysosma) of Podophylloi- greatly between genera and species of the subfamily deae were included in this study (Table 1). Each species (Pandey et al., 2007; Kusari et al., 2010; Jiang was represented by two to five accessions collected et al., 2012). In addition, most species in Dysosma from different populations in China, Japan, or North and Diphylleia have been listed as “endangered” or America. The species were identified based on “rare” in the China Species Red List (Wang & descriptions and keys for this subfamily in the Flora Xie, 2004) or the IUCN (Ying et al., 2011), because of China (Ying et al., 2011). Fresh leaves were dried in of their small distributional ranges, few populations, silica gel at the time of collection. Voucher specimens and small sizes of the known populations. Therefore, a were deposited in the herbarium at the Kunming rapid and accurate method for species identification of Institute of Botany, Chinese Academy of Sciences Podophylloideae is needed not only to facilitate proper (KUN) (Table 1). medicinal uses (e.g., to guide correct introduction of Eight candidate barcoding markers of chloroplast wild resources for the pharmaceutical industry), but also genome (rbcL, matK, trnL‐trnF, trnL‐ndhJ, trnS‐trnfM, to aid conservation management. atpH‐atpI, rpl32‐trnLUAG, rps18‐clpp) plus the nuclear DNA barcoding is a well‐known technique that aims ITS region were chosen to be sequenced for the study. to facilitate rapid species identification based on short, All these DNA regions have been used in previous standardized DNA sequences in cases where convention- phylogenetic studies (Taberlet et al., 1991; Demesure al taxonomic identification is not feasible (Tautz et al., 1995; Fay et al., 1997; Grivet et al., 2001; Fu et al., 2002, 2003; Hebert et al., 2003; Kress et al., et al., 2005; Kress & Erickson, 2007; Shaw et al., 2007), 2005; Savolainen et al., 2005). The use of a combination which have shown that they could be directly sequenced of DNA sequences with existing morphological charac- from polymerase chain reaction (PCR) products (also ters can facilitate fast and reliable identification of species see below) without cloning, and possessed a reasonable (Smith et al., 2005; Will et al., 2005; DeSalle, 2006; number of variable sites. Hajibabaei et al., 2007). In plants, several single‐locus or multi‐loci candidate DNA barcodes have been tested and 1.2 DNA isolation, PCR amplification, and proven to be useful for plant identification sequencing procedures (Thomas, 2009; Gao, 2010; Li et al., 2011; Sun Total genomic DNA was extracted from the dried et al., 2012). These markers include the nuclear ribosomal leaf tissue using a DNeasy plant tissue kit (Qiagen, internal transcribed spacer (ITS) and plastid gene regions Valencia, CA, USA). The PCRs were carried out in 25‐ (rpoB, rpoC1, rbcL, matK) and plastid non‐coding mL reaction mixtures containing approximately 30 ng regions (atpH‐atpI, psbK‐psbI, trnH‐psbA). However, the genomic DNA template, PCR buffer (10 mmol/L Tris, utility of each region was found to vary among taxonomic 50 mmol/L KCl buffer, pH 8.0), 2.0 mmol/L MgCl2, groups. At present, the effectiveness of these DNA 0.5 mmol/L each primer, 0.2 mmol/L each dNTP, and regions as barcodes to identify species within Podophyl- 1.0 U Taq DNA polymerase (Takara, Dalian, China). loideae remains unknown. Sequences of all the primers and annealing temper- In this study, we tested eight plastid DNA markers atures are listed in Table S1. The PCR program was as (rbcL, matK, trnL‐trnF, trnL‐ndhJ, trnS‐trnfM, atpH‐ follows: 94 °C for 3 min, followed by 34 cycles of 94 °C atpI, rpl32‐trnLUAG, rps18‐clpp) and one nuclear DNA for 30 s; 53–60 °C annealing reaction for 30 s (depend- region (ITS) for their utility as barcodes for species ing on the primers); 72 °C for 2 min; with final identification of the Podophylloideae. Our major goal extension at 72 °C for 10 min. The PCR amplifications was to develop a reliable molecular system for were carried out on a GeneAmp 9700 DNA Thermal identification of Podophylloideae species that would Cycler (Perkin‐Elmer, Foster City, CA, USA). The benefit the pharmaceutical industry and conservation. A PCR products were visualized using electrophoresis on second goal of the study was to evaluate the 1.0% agarose gels. Purification and bidirectional morphology‐based species classification using the sequencing of PCR products were completed by Beijing DNA sequence data. Genomics Institute (Shenzhen, China) using the PCR primers. All sequences have been deposited in GenBank (see Table 1 for accession numbers). 1 Material and methods 1.3 Data analysis 1.1 Plant material and loci sampling Sequences were aligned and edited in GENEIOUS A total of 36 individual samples representing all 12 version 4.5.0 (Drummond et al., 2006). For each gene species of the four genera (i.e.,
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