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Phylogeography of Chinese Cherry (Prunus Pseudocerasus Lindl

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Phylogeography of Chinese Cherry (Prunus Pseudocerasus Lindl Plant Biology ISSN 1435-8603 RESEARCH PAPER Phylogeography of Chinese cherry (Prunus pseudocerasus Lindl.) inferred from chloroplast and nuclear DNA: insights into evolutionary patterns and demographic history T. Chen1, Q. Chen1, Y. Luo1, Z.-L. Huang1, J. Zhang1, H.-R. Tang1,2, D.-M. Pan3 & X.-R. Wang2 1 College of Horticulture, Sichuan Agricultural University, Ya’an, China 2 Institute of Pomology and Olericulture, Sichuan Agricultural University, Chengdu, China 3 College of Horticulture, Fujian Agriculture and Forestry University, Fuzhou, China Keywords ABSTRACT Chinese cherry (Prunus pseudocerasus Lindl.); Prunus pseudocerasus cpDNA; nrDNA; phylogeography. Chinese cherry ( Lindl.) is a commercially valuable fruit crop in China. In order to obtain new insights into its evolutionary history and provide valu- Correspondence able recommendations for resource conservation, phylogeographic patterns of 26 nat- X.-R. Wang, Institute of Pomology and ural populations (305 total individuals) from six geographic regions were analyzed Olericulture, Sichuan Agricultural University, using chloroplast and nuclear DNA fragments. Low levels of haplotype and nucleotide Chengdu 611130, China. diversity were found in these populations, especially in landrace populations. It is E-mail: [email protected] likely that a combined effect of botanical characteristics impact the effective popula- tion size, such as inbreeding mating system, long life span, as well as vegetative repro- Editor duction. In addition, strong bottleneck effect caused by domestication, together with X. Wang founder effect after dispersal and subsequent demographic expansion, might also accelerate the reduction of the genetic variation in landrace populations. Interestingly, Received: 5 October 2014; Accepted: 10 populations from Longmen Mountain (LMM) and Daliangshan Mountain (DLSM) December 2014 exhibited relatively higher levels of genetic diversity, inferring the two historical genetic diversity centers of the species. Moreover, moderate population subdivision doi:10.1111/plb.12294 was also detected by both chloroplast DNA (GST = 0.215; NST = 0.256) and nuclear DNA (GST = 0.146; NST = 0.342), respectively. We inferred that the episodes of effi- cient gene flow through seed dispersal, together with features of long generation cycle and inbreeding mating system, were likely the main contributors causing the observed phylogeographic patterns. Finally, factors that led to the present demographic pat- terns of populations from these regions and taxonomic varieties were also discussed. this species inhabit wide eco-geographic regions in China INTRODUCTION (from North China Plain to Yungui Plateau) (Fig. 1). Consid- Rosaceae consists of over 100 genera and 3000 species, includ- erable genetic variation associated with multiple favorable ing many important fruit crops with diverse growth habits characters have been accumulated in these populations, such as (herbaceous, liana, bush and tree forms) and fruit types (pome, intensive pest/disease resistance, outstanding nutritional values, drupe, achene, hip, follicle and capsule) (Hummer & Janick unique flavor and remarkable abiotic adaptation (Huang et al. 2009; Janick 2005; Potter et al. 2007). The members of Rosa- 2013), thereby providing the promising opportunities for ceae such as Fragaria, Rosa, Rubus, and Prunus provide high- cherry breeding (Gutierrez-Pesce et al. 1998; Rugini 2004). value nutritional foods and contribute desirable aesthetic and Phylogeography has recently emerged as a powerful method commercial products. Chinese cherry (Prunus pseudocerasus for understanding population structure and evolutionary his- Lindl.) is an endemic tetraploid species (Iwatsubo et al. 2004; tory of plant species by synthesizing the influence of both his- Oginuma 1988), distributing throughout the temperate and torical and current genetic exchange (Petit et al. 2005; Schaal warm-temperate forests in China (Yu€ 1979). As an important et al. 1998). A large number of reports have witnessed increas- fruit crop of Rosaceae, Chinese cherry has been domesticated ing applications of phylogeography in economically important and cultivated for more than 3000 years (Liu & Liu 1993; Yu€ plants and their wild relatives, such as Oryza rufipogon (Huang 1979). It is a hermaphrodite, perennial woody plant with high et al. 2012), Spartina pectinata (Kim et al. 2013), Medicago sati- levels of inbreeding rate, strong animal or gravity seed dispersal va (Sakiroglu & Brummer 2013), Camellia taliensis (Liu et al. ability as well as long intergeneration period of 3–6 years (Yu€ 2012), Triticum monococcum (Oliveira et al. 2011), Miscanthus 1979). The drupe fruit contains rich nutritional ingredients sinensis (Shimono et al. 2013). However, most of these studies and trace elements, such as vitamins, minerals, fiber and anti- only focused on domesticated annual crops, phylogeographic oxidant compounds for healthy diets, and its flower is also studies of perennial fruit crops were scarcely reported, including endowed with well-known ornamental value (Huang et al. Rosaceae species (Bai et al. 2014; Zong et al. 2014). As for 2013; Yu€ et al. 1986). Both landrace and wild populations of Chinese cherry, although our previous study has provided Plant Biology 17 (2015) 787–797 © 2014 German Botanical Society and The Royal Botanical Society of the Netherlands 787 Phylogeographic study of Prunus pseudocerasus Chen, Chen, Luo, Huang, Zhang, Tang, Pan & Wang A B C Fig. 1. Sampling locations and haplotypes distribution of P. pseudocerasus. A: The geographic distribution of sampled populations. The landrace and wild populations are represented with circles and triangles, respectively. The dotted circles with different colors delimit different geographic regions, as shown in the key. The six geographic regions are: Daliangshan Mountain (DLSM), Sichuan Basin (SCB), Longmen Mountain (LMM), Qinba Mountain (QBM), North China Plain (NCP) and Yungui Plateau (YGP). B: The geographic distribution and frequencies of cpDNA haplotypes. C: The geographic distribution and frequencies of nrDNA haplotypes. Colors represent the different haplotypes, as shown in the key. preliminary information about the genetic variation and popu- markers, elucidate the population structure patterns, and iden- lation structure, based on a single chloroplast DNA (cpDNA) tify hot-spots of diversity to define more accurate conservation fragment (Chen et al. 2013), more data are also critical for fur- criteria; (ii) clarify the usability of ITS polymorphism status in ther understanding the phylogeographic patterns of this species. population genetic studies in the tetraploid species; and (iii) DNA sequences derived from nuclear and cytoplasmic ge- explore the long-term population dynamics that have shaped nomes play a vital role in plant phylogeographic analyses (Soltis the current population structure, determine its demographic & Soltis 1998; Zheng et al. 2008). It was reported that intergenic and evolutionary history, as well as investigate recently colo- spacers of cpDNA such as rpl32-trnL and rps16-trnQ could nized areas throughout its distribution. offer higher levels of variation, thereby frequently used to inves- tigate intraspecific genetic diversity, population genetic struc- ture and phylogeography (Shaw et al. 2005, 2007; Small et al. MATERIALS AND METHODS 2005). In addition, internal transcribed spacer (ITS) region Sampling strategy from nuclear ribosomal DNA (nrDNA) was also widely applied in plant phylogeographic and evolutionary studies (Alvarez & A total of 305 individuals from 26 natural populations were Wendel 2003). Although intra-individual ITS polymorphism collected in six geographic regions (from southwest to north of were found in non-hybrid diploid taxa, even in the same gen- China), representing almost the entire distribution range of the ome (Alvarez & Wendel 2003; Zheng et al. 2008), homogenous species in China (Fig. 1 and Table 1). These populations con- nrDNA arrays within individuals were identified in many sisted of 17 landraces and nine wild populations, with 139 and reports (Bailey et al. 2003; Zheng et al. 2008) and successfully 166 individuals, respectively. All the landraces were primarily used in many species (Wissemann & Ritz 2005; Yang et al. domesticated to best-fit local climatic, soil conditions and the 2012), including Malus (Robinson et al. 2001) and Maloideae taste preferences of the consumers over centuries. For each (Campbell et al. 2007). These markers might provide unprece- population, young and healthy leaves were randomly sampled dented opportunities to investigate genetic structure and popu- from 2 to 49 individual trees, based on available population lation history of species, particularly by means of a combined size and reproductive modes. In order to ensure adequate pop- analysis of biparentally inherited nuclear and maternally inher- ulation coverage, samples were randomly taken from about 50 ited organelle ones (Liu et al. 2012; Petit et al. 2005; Schaal et al. to 1000 m intervals in each population. Leaves were individu- 1998; Turchetto-Zolet et al. 2012; Yuan et al. 2010). ally collected in field and silica-dried instantly for subsequent In this study, a total of 26 populations from six geographical DNA extraction. regions (defined based on geographical characteristics and sub- sequent ecological and climatic types, Fig. 1 and Table 1) were DNA isolation, PCR amplification, and sequencing screened and comprehensively analyzed using biparentally inherited nuclear
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