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Phylogeography and Conservation Genetics of the Rare and Relict Bretschneidera Sinensis (Akaniaceae)

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Phylogeography and Conservation Genetics of the Rare and Relict Bretschneidera Sinensis (Akaniaceae) RESEARCH ARTICLE Phylogeography and conservation genetics of the rare and relict Bretschneidera sinensis (Akaniaceae) Mei-Na Wang1,2☯, Lei Duan1☯, Qi Qiao1,3, Zheng-Feng Wang1, Elizabeth A. Zimmer4, Zhong-Chao Li1, Hong-Feng Chen1* 1 Key Laboratory of Plant Resources Conservation and Sustainable Utilization, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou, China, 2 Shenzhen Key Laboratory for Orchid a1111111111 Conservation and Utilization, The National Orchid Conservation Center of China and The Orchid a1111111111 Conservation & Research Center of Shenzhen, Shenzhen, China, 3 College of Agriculture, Henan University a1111111111 of Science and Technology, Luoyang, China, 4 Department of Botany, National Museum of Natural History, a1111111111 MRC 166, Smithsonian Institution, Washington, D.C., United States of America a1111111111 ☯ These authors contributed equally to this work. * [email protected] OPEN ACCESS Abstract Citation: Wang M-N, Duan L, Qiao Q, Wang Z-F, Bretschneidera sinensis, a class-I protected wild plant in China, is a relic of the ancient Ter- Zimmer EA, Li Z-C, et al. (2018) Phylogeography tiary tropical flora endemic to Asia. However, little is known about its genetics and phylogeo- and conservation genetics of the rare and relict Bretschneidera sinensis (Akaniaceae). PLoS ONE graphy. To elucidate the current phylogeographic patterns and infer the historical population 13(1): e0189034. https://doi.org/10.1371/journal. dynamics of B. sinensis, and to make recommendations for its conservation, three non-cod- pone.0189034 ing regions of chloroplast DNA (trnQ-rps16, rps8-rps11, and trnT-trnL) were amplified and Editor: Tzen-Yuh Chiang, National Cheng Kung sequenced across 256 individuals from 23 populations of B. sinensis, spanning 10 prov- University, TAIWAN inces of China. We recognized 13 haplotypes, demonstrating relatively high total haplotype Received: April 19, 2017 diversity (hT = 0.739). Almost all of the variation existed among populations (98.09%, P < Accepted: November 19, 2017 0.001), but that within populations was low (1.91%, P < 0.001). Strong genetic differentiation was detected among populations (GST = 0.855, P < 0.001) with limited estimations of seed Published: January 12, 2018 flow (Nm = 0.09), indicating that populations were strongly isolated from one another. Copyright: This is an open access article, free of all According to SAMOVA analysis, populations of B. sinensis in China could be divided into copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or five geographic groups: (1) eastern Yunnan to western Guangxi; (2) Guizhou-Hunan-Hubei; otherwise used by anyone for any lawful purpose. (3) central Guangdong; (4) northwestern Guangdong; and (5) the Luoxiao-Nanling-Wuyi The work is made available under the Creative -Yangming Mountain. Network analysis showed that the most ancestral haplotypes were Commons CC0 public domain dedication. located in the first group, i.e., the eastern Yungui Plateau and in eastern Yunnan, which is Data Availability Statement: All relevant data are regarded as a putative glacial refugia for B. sinensis in China. B. sinensis may have from GenBank (accession numbers JF448503- expanded its range eastward from these refugia and experienced bottleneck or founder JF448506, JF448492-JF448494, KF849804- KF849814). effects in southeastern China. Populations in Liping (Guizhou Province), Longsheng (Guangxi Province), Huizhou (Guangdong Province), Chongyi (Jiangxi Province), Dong-an Funding: This work was supported by grants from the National Natural Science Foundation of China (Hunan Province), Pingbian (Yunnan Province) and Xinning (Hunan Province) are proposed (31570337, 31170196). The funders had no role in as the priority protection units. study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing interests: The authors have declared that no competing interests exist. PLOS ONE | https://doi.org/10.1371/journal.pone.0189034 January 12, 2018 1 / 17 Phylogeography of Bretschneidera sinensis Introduction Bretschneidera sinensis Hemsl., a relict tree of the Tertiary tropical flora, occurs in evergreen broad-leaved or mixed evergreen and deciduous forests in montane areas at altitudes of 300±1700 m. Historically, B. sinensis was a heliophilous volunteer species and a long-term resident in the eastern Palearctic [1, 2]. B. sinensis is listed as a Category-I species in the ªStatute of Protection of Wild Plants in Chinaº [3], and is flagged as ªNTº (Near Threat- ened) in the Chinese Species Red List [4], indicating that it requires urgent protection and restoration. Its rare and endangered status is exemplified by its greatly diminished popula- tion size in recent decades, probably due to scarcity of flowering individuals, low seed pro- duction, weak germination, deforestation, and destructive collection of seedlings [5]. According to Wu's Angiosperm taxonomic system [2,6], Bretschneidera sinensis is endemic to China, mainly distributed in areas south of the Yangtze River, with rare appearances in Vietnam and Laos. Previously, it was generally believed that Bretschneideraceae was an independent monotypic family closely related to Sapindaceae and Hippocastanaceae [7, 8, 9]. However, based on recent morphological and molecular phylogenetic studies [10], the IV Angiosperm Phylogeny Group [11] classified B. sinensis in the family Akaniaceae, which contains one other monotypic genus endemic to eastern Australia (Akania) Hook.f.). Aka- niaceae appears most related to Caricaceae, Capparaceae and Moringaceae in Brassicales [11]. As a relict and endemic tree from a monotypic genus, B. sinensis has attracted the attention of various workers on phylogeny, ancient geography, and climate research [12, 13]. However, little is known about its genetics and phylogeography. The geographic distribution, demographic history, and patterns of genetic diversification of many plant and animal species are assumed to have been greatly influenced by climatic oscilla- tions during the Pleistocene [14, 15], when at least four major glaciations are thought to have occurred in Asia [16]. Although the glacial advance in Asia was not as extensive as that in Europe and North America, the flora and fauna of Asia are believed to have been affected by the climatic oscillations [17, 18]. Pollen and other fossil records have traditionally provided evidence for inferring biogeographic histories and signatures of glacial refugia [19]. However, in most of the relevant studies on B. sinensis, either the fossil records were poor or data prior to the Quaternary period were not available [20]. Phylogeography, an interdiscipline of phylogeny and biogeography, disentangles historical changes in patterns of gene flow, isolation, and secondary contact among divergent popula- tions at various spatiotemporal scales [21±23] and helps to identify biodiversity hotspots and to inform conservation policies [14, 15, 24]. It is a powerful tool for inferring the processes that determine the genetic composition of species or species groups [14, 23], and can shed light on the association between climate cycles and species distributions [25]. Owing to their non-recombining nature, moderate evolutionary rates, and generally maternal inheritance, the genomes of angiosperm organelles, particularly those of non-cod- ing regions of chloroplast DNA, have enabled resolution of some phylogeographic ques- tions in angiosperms [14, 18, 19, 22, 26±29]. These regions are sensitive to the effects of habitat fragmentation due to their smaller effective population size relative to nuclear genes, and because of the limits of seed-mediated gene dispersal compared to pollen-medi- ated gene flow [27, 30]. In the present study, we aimed to clarify the phylogeography of B. sinensis using three chlo- roplast DNA markers. Our specific objectives were as follows: (1) to understand the historical processes that have affected the distribution of B. sinensis; (2) to identify refugia of the species; and (3) to make recommendations for future conservation activities. PLOS ONE | https://doi.org/10.1371/journal.pone.0189034 January 12, 2018 2 / 17 Phylogeography of Bretschneidera sinensis Methods Sampling and DNA extraction Leaf materials were collected throughout the range of B. sinensis, from 10 provinces in China. No specific permissions were required by authorities of the collecting areas, on the condition that there be no harm to the target plants. It is not illegal to remove only a few leaves from a protected tree species for the purpose of scientific research. For each population, leaves were collected from individuals that were separated over 30 m. In total, 256 individuals from 23 populations were investigated (Table 1, Fig 1A). Unfortunately, due to habitat loss, only one population (PB, see Fig 1A) was found in Yunnan. However, our collecting area did not cover all the recorded localities of B. sinensis in this province, e.g. Hengduan Mtn. Another trip is planned for other populations. Total genomic DNA was extracted from leaf tissue dried in silica gel using a slightly modi- fied protocol of the CTAB method [31]. DNA was finally dissolved in 100 μL TE-buffer for long-term storage at -20ÊC. Table 1. Sampling sites, sample sizes (n), haplotype diversity (h), and nucleotide diversity (π) of the 23 Bretschneidera sinensis populations investigated in this study. Standard errors are given in parentheses. Population Sample Mountain region Latitude Longitude (ÊE) n Hap- h (sd.) π×10−3 (sd.) location (ÊN) lotype 1. ES Enshi, Hubei Xingdo-u Mtn. 30Ê2'54" 109Ê8'1" 12 M 0(0) 0(0) 2. GD Guidong, Hunan Bamian Mtn. 25Ê56'22" 113Ê40'48" 12 A 0(0) 0(0) 3. DA Dong-an, Hunan Shunhu-ang Mtn. 26Ê23'51" 111Ê17'59" 12 D 0(0) 0(0) 4. XN Xinning, Ziyun Mtn. 26Ê36'31" 111Ê05'26" 12 D 0(0) 0(0) Hunan 5. JN Jingning, Zhejiang Donggo-ng Mtn. 27Ê58'24" 119Ê38'9" 12 A 0(0) 0(0) 6. LQ Longquan, Zhejiang Fengyan-g, Mtn. 28Ê4'29" 119Ê8'29" 12 A 0(0) 0(0) 7. CY Chongyi, Qiyun Mtn. 25Ê40'55" 114Ê18'30" 11 A, B 0.5091 0(0) Jiangxi (0.1008) 8. LN Longnan, Jiangxi Jiulian Mtn. 24Ê54'40" 114Ê47'23" 12 A 0(0) 0(0) 9.
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