Abstract
Pear (Pyrus) is an important temperate fruit, which originates in the southwestern region of China and has more than 3000 year’s cultivation history. However, the historic routes of pear dissemination in China have not been fully elucidated. In this study, a total of 2,412,930 single nucleotide polymorphisms (SNPs) at a density of 4.74 SNP/kb were identified by resequencing. The SNP-based phylogenetic analysis revealed that 102 pear samples from 23 provinces in China were divided into two major clades and eight geographic groups, and these divisions were supported by results of a population structure analysis and principal component analysis (PCA). Combined with the results of population diversity and identity-by-descent (IBD) analysis, it was revealed that the dissemination direction of pear was from southwest to southeast and from south to north. In the southern region, the dispersal pattern of pear spreading from west to east was generally in line with the course of the Yangtze River and Pearl River. The southern pear spread by multiple routes to its north neighboring areas, and regions in the middle and lower reaches of the Yellow River played important roles in the further dissemination of pear in the northern region of China. Moreover, we identified comparative higher genetic diversity of Ussurian pear than other populations, which might be due to low degree of domestication and closely resembled the high diversity of its wild counterpart. Our study provides new information to further our understanding of pear evolution in China, while laying a foundation of data for population genetic research, germplasm protection, and utilization for pear breeding in the future.
Similar content being viewed by others
Data availability
The datasets generated and analyzed during the current study are available from the corresponding author upon request. Raw genome resequencing reads have been deposited into the NCBI sequence read archive (SRA) under BioProject accession PRJNA782471.
Code availability
The software application during the current study is downloaded from its official website, and custom codes are available from the corresponding author upon request.
References
Alexander DH, Novembre J, Lange K (2009) Fast model-based estimation of ancestry in unrelated individuals. Genome Res 19:1655–1664
Andari MVC, Bussamra SLC, Tedesco TGD, Peixoto PAB, Pares P, Braga A, Araujo Júnior E, Aoki T (2020) Noninvasive prenatal testing: benefits and limitations of the available tests. Ceska Gynekol 85:41–48
Bell RL (1984) Evaluation of Pyrus germplasm for resistance to pear Psylla in the orchard. Acta Hortic 161:133–134
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120
Browning SR, Browning BL (2007) Rapid and accurate haplotype phasing and missing-data inference for whole-genome association studies by use of localized haplotype clustering. Amer J Human Genet 81:1084–1097
Campbell CL, Palamara PF, Dubrovsky M, Botigue LR, Fellous M, Atzmon G, Oddoux C, Pearlman A, Hao L, Henn BM (2012) North African Jewish and non-Jewish populations form distinctive, orthogonal clusters. P Natl Acad Sci USA 109:13865–13870
Cao K, Li Y, Deng CH, Gardiner SE, Zhu GR, Fang WC, Chen CW, Wang XW, Wang LR (2019) Comparative population genomics identified genomic regions and candidate genes associated with fruit domestication traits in peach. Plant Biotechnol J 17:1954–1970
Catchen J, Hohenlohe PA, Bassham S, Amores A, Cresko WA (2013) Stacks: an analysis tool set for population genomics. Mol Ecol 22:3124–3140
Challice JS, Westwood MN (1973) Numerical taxonomic studies of the genus Pyrus using both chemical and botanical characters. Bot J Linn Soc: 121–48
Chang YJ, Cao YF, Zhang JM, Tian LM, Dong XG, Zhang Y, Qi D, Zhang XS (2017) Study on chloroplast DNA diversity of cultivated and wild pears (Pyrus L) in Northern China. Tree Genet Genomes 13: 44
Danecek P, Auton A, Abecasis G, Albers CA, Banks E, DePristo MA, Handsaker RE, Lunter G, Marth GT, Sherry ST, McVean G, Durbin R (2011) The variant call format and VCFtools. Bioinformatics 27:2156–2158
Dolatowski J, Zych M, Podyma W, Nowosielski J, Szymańska M (2004) Molecular studies on the variability of Polish semi-wild pears (Pyrus) using AFLP. J Fruit Ornam Plant Res 12:331–337
Duan NB, Bai Y, Sun HH, Wang N, Ma YM, Li MJ, Wang X, Jiao C, Legall N, Mao LY, Wan SB, Wang K, He TM, Feng SQ, Zhang ZY, Mao ZQ, Shen X, Chen XL, Jiang YM, Wu SJ, Yin CM, Ge SF, Yang L, Jiang SH, Xu HF, Liu JX, Wang DY, Qu CZ, Wang YC, Zuo WF, Xiang L, Liu C, Zhang DY, Gao Y, Xu YM, Xu KN, Chao T, Fazio G, Shu HR, Zhong GY, Cheng LL, Fei ZJ, Chen XS (2017) Genome re-sequencing reveals the history of apple and supports a two-stage model for fruit enlargement. Nat Commun 8:1–11
Emanuelli F, Lorenzi S, Grzeskowiak L, Catalano V, Stefanini M, Troggio M, Myles S, Martinez-Zapater JM, Zyprian E, Moreira FM, Grando MS (2013) Genetic diversity and population structure assessed by SSR and SNP markers in a large germplasm collection of grape. BMC Plant Biol 13:39
Erfani J, Ebadi A, Abdollahi H, Fatahi R (2012) Genetic diversity of some pear cultivars and genotypes using simple sequence repeat (SSR) markers. Plant Mol Biol Rep 30:1065–1072
Ferradini N, Lancioni H, Torricelli R, Russi L, Ragione ID, Cardinali I, Marconi G, Gramaccia M, Concezzi L, Achilli A, Veronesi F, Albertini E (2017) Characterization and phylogenetic analysis of ancient Italian landraces of pear. Front Plant Sci 8
Fischer MC, Rellstab C, Leuzinger M, Roumet M, Gugerli F, Shimizu KK, Holderegger R, Widmer A (2017) Estimating genomic diversity and population differentiation - an empirical comparison of microsatellite and SNP variation in Arabidopsis halleri. BMC Genomics 18:69
Ginestet C (2011) ggplot2: elegant graphics for data analysis. J Roy Stat Soc 174:245–246
Gupta PK, Rustgi S, Kulwal PL (2005) Linkage disequilibrium and association studies in higher plants: present status and future prospects. Plant Mol Biol 57:461–485
Gusev A, Palamara PF, Aponte G, Zhuang Z, Darvasi A, Gregersen P, Pe’er I (2012) The architecture of long-range haplotypes shared within and across populations. Mol Biol Evol 29:473–86
Han Z, Hu Y, Tian Q, Cao Y, Si A, Si Z, Zang Y, Xu C, Shen W, Dai F (2020) Genomic signatures and candidate genes of lint yield and fibre quality improvement in Upland cotton in Xinjiang. Plant Biotechnol J 18:1–13
He Q (2005) Collation and interpretation of panoramic maps of the three county level administrative districts in Qin and Han Dynasties (in Chinese). ZhongHua Book Company, Beijing
Iketani H, Katayama H, Uematsu C, Mase N, Sato Y, Yamamoto T (2012) Genetic structure of East Asian cultivated pears (Pyrus spp.) and their reclassification in accordance with the nomenclature of cultivated plants. Plant Syst Evol 298:1689–1700
Iketani H, Manabe T, Matsuta N, Akihama T, Hayashi T (1998) Incongruence between RFLPs of chloroplast DNA and morphological classification in east Asian pear (Pyrus spp). Genet Resour Crop Ev 45:533–539
Kalinowski ST (2004) Counting alleles with rarefaction: private alleles and hierarchical sampling designs. Conserv Genet 5:539–543
Kumar S, Kirk C, Deng C, Wiedow C, Knaebel M, Brewer L (2017) Genotyping-by-sequencing of pear (Pyrus spp.) accessions unravels novel patterns of genetic diversity and selection footprints. Hortic Res 4
Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754–1760
Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, Subgroup GPDP (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079
Li XL, Singh J, Qi MF, Li SW, Zhang X, Zhang MY, Khan A, Zhang SL, Wu J (2019) Development of an integrated 200K SNP genotyping array and application for genetic mapping, genome assembly improvement and genome wide association studies in pear (Pyrus). Plant Biotechnol J 17:1582–1594
Lijavetzky D, Cabezas JA, Ibanez A, Rodriguez V, Martinez-Zapater JM (2007) High throughput SNP discovery and genotyping in grapevine (Vitis vinifera L.) by combining a re-sequencing approach and SNPlex technology. BMC Genomics 8
Liu QW, Song Y, Liu L, Zhang MY, Sun JM, Zhang SL, Wu J (2015) Genetic diversity and population structure of pear (Pyrus spp.) collections revealed by a set of core genome-wide SSR markers. Tree Genet Genomes 11:1–22
Liu X (2006) Miscellany of the western capital (in Chinese). Xi’an: SANQIN Publishing House, Xi’an
Ma H, Wang S, Zeng G, Guo J, Guo M, Dong X, Hua G, Liu Y, Wang M, Ling Y, Ding X, Zhao C, Wu C (2019) The origin of a coastal indigenous horse breed in China revealed by genome-wide SNP data. Genes 10
McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altshuler D, Gabriel S, Daly M, DePristo MA (2010) The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20:1297–1303
Millar CI, Westfall RD (1992) Allozyme markers in forest genetic conservation. Populat Genet Forest Trees 42:347–371
Montanari S, Bianco L, Allen BJ, Martinez-Garcia PJ, Bassil NV, Postman J, Knabel M, Kitson B, Deng CH, Chagne D, Crepeau MW, Langley CH, Evans K, Dhingra A, Troggio M, Neale DB (2019) Development of a highly efficient AxiomTM 70 K SNP array for Pyrus and evaluation for high-density mapping and germplasm characterization. BMC Genomics 20:1–18
Moritz C (1994) Applications of mitochondrial DNA analysis in conservation: a critical review. Mol Ecol 3:401–411
Newton AC, Allnutt TR, Gillies ACM, Lowe AJ, Ennos RA (1999) Molecular phylogeography, intraspecific variation and the conservation of tree species. Trends Ecol Evol 14:140–145
Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 32:268–274
Park B, Burke JM (2020) Phylogeography and the evolutionary history of sunflower (Helianthus annuus L.): wild diversity and the dynamics of domestication. Genes 11:1–18
Pu F, Wang Y (1963) Pomology of China pears (in Chinese). Shanghai Scientific and Technical Publishers, Shanghai
Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MAR, Bender D, Maller J, Sklar P, de Bakker PIW, Daly MJ, Sham PC (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 81:559–575
Ralph P, Coop G (2013) The geography of recent genetic ancestry across Europe. Plos Biol 11: e1001555
Rubtsov GA (1944) Geographical distribution of the genus Pyrus and trends and factors in its evolution. Amer Naturalist 78:358–366
Shen Z (1965) Records of Kuaiji (in Chinese). Nanjing: manuscripts of China Agricultural Heritage Museum, Nanjing
Shi S, Li J, Sun J, Yu J, Zhou S (2013) Phylogeny and classification of Prunus sensu lato (Rosaceae). J Integr Plant Biol 55:1069–1079
Shuang J, Zheng X, Yu P, Yue X, Maqsood A, Cai D, Teng Y, Takaya MJPO (2016) Primitive genepools of Asian pears and their complex hybrid origins inferred from fluorescent sequence-specific amplification polymorphism (SSAP) markers based on LTR retrotransposons. Plos One 11: e0149192
Song Y, Fan L, Chen H, Zhang M, Ma Q, Zhang S, Wu J (2014) Identifying genetic diversity and a preliminary core collection of Pyrus pyrifolia cultivars by a genome-wide set of SSR markers. Sci Hortic 167:5–16
Tam NT, Dwiyanti MS, Koide Y, Nagano AJ, Ky H, Tin HQ, Hien NL, Dung LV, Kishima Y (2019) Profiling SNP and nucleotide diversity to characterize Mekong Delta rice landraces in Southeast Asian populations. Plant Genome 12:1–11
Teng YW, Tanabe K, Tamura F, Itai A (2002) Genetic relationships of Pyrus species and cultivars native to East Asia revealed by randomly amplified polymorphic DNA markers. J Am Soc Hortic Sci 127:262–270
Vavilov NI (1951) The origin, variation, immunity and breeding of cultivated plants. Ronald Press, New York
Wang X, Feng H, Chang Y, Ma C, Wang L, Hao X, Al Li, Cheng H, Wang L, Cui P, Jin J, Wang X, Wei K, Ai C, Zhao S, Wu Z, Li Y, Liu B, Wang G-D, Chen L, Ruan J, Yang Y (2020) Population sequencing enhances understanding of tea plant evolution. Nat Commun 11:1–10
Warschefsky EJ, von Wettberg EJB (2019) Population genomic analysis of mango (Mangifera indica) suggests a complex history of domestication. New Phytol 222:2023–2037
Wu J, Wang YT, Xu JB, Korban SS, Fei ZJ, Tao ST, Ming R, Tai SS, Khan AM, Postman JD, Gu C, Yin H, Zheng DM, Qi KJ, Li Y, Wang RZ, Deng CH, Kumar S, Chagne D, Li XL, Wu JY, Huang XS, Zhang HP, Xie ZH, Li X, Zhang MY, Li YH, Yue Z, Fang XD, Li JM, Li LT, Jin C, Qin MF, Zhang JY, Wu X, Ke YQ, Wang J, Yang HM, Zhang SL (2018) Diversification and independent domestication of Asian and European pears. Genome Biol 19
Wu J, Wang Z, Shi Z, Zhang S, Ming R, Zhu S, Khan MA, Tao S, Korban SS, Wang H, Chen NJ, Nishio T, Xu X, Cong L, Qi K, Huang X, Wang Y, Zhao X, Wu J, Deng C, Gou C, Zhou W, Yin H, Qin G, Sha Y, Tao Y, Chen H, Yang Y, Song Y, Zhan D, Wang J, Li L, Dai M, Gu C, Wang Y, Shi D, Wang X, Zhang H, Zeng L, Zheng D, Wang C, Chen M, Wang G, Xie L, Sovero V, Sha S, Huang W, Zhang S, Zhang M, Sun J, Xu L, Li Y, Liu X, Li Q, Shen J, Wang J, Paull RE, Bennetzen JL, Wang J, Zhang S (2013) The genome of the pear (Pyrus bretschneideri Rehd.). Genome Res 23:396–408
Wuyun T, Amo H, Xu JS, Ma T, Uematsu C, Katayama H (2015) Population structure of and conservation strategies for wild Pyrus ussuriensis Maxim. in China. PLoS ONE 10:1–20
Xue L, Liu QW, Hu HJ, Song Y, Fan J, Bai B, Zhang MY, Wang RZ, Qin MF, Li XL, Wu J (2018) The southwestern origin and eastward dispersal of pear (Pyrus pyrifolia) in East Asia revealed by comprehensive genetic structure analysis with SSR markers. Tree Genet Genomes 14:1–12
Xue L, Liu QW, Qin MF, Zhang MY, Wu X, Wu J (2017) Genetic variation and population structure of “Zangli” pear landraces in Tibet revealed by SSR markers. Tree Genet Genomes 13:1–11
Yu D (1979) Taxonomy of the fruit tree in China. China Agr Press, Beijing
Yu P, Shuang J, Wang X, Bai S, Teng Y (2016) Retrotransposon-based sequence-specific amplification polymorphism markers reveal that cultivated Pyrus ussuriensis originated from an interspecific hybridization. Eur J Hortic Sci 81:264–272
Yuan K (1993) Proofreading and annotation of Shanhaijing (in Chinese). Bashu Publishing House, Sichuan
Yue XY, Zheng XY, Zong Y, Jiang S, Hu CY, Yu PY, Liu GQ, Cao YF, Hu HJ, Teng YW (2018) Combined analyses of chloroplast DNA haplotypes and microsatellite markers reveal new insights into the origin and dissemination route of cultivated pears native to East Asia. Front Plant Sci 9
Zhang MY, Xue C, Hu H, Li J, Xue Y, Wang R, Fan J, Zou C, Tao S, Qin M (2021) Genome-wide association studies provide insights into the genetic determination of fruit traits of pear. Nat Commun 12:1–10
Zhao H (1965) General annals of Jiangnan (in Chinese) Nanjing: manuscripts of China Agricultural Heritage Museum, Nanjing
Zhukovsky PM (1965) Main gene centres of cultivated plants and their wild relatives within the territory of the U.S.S.R. Euphytica 14:177–188
Zimmerman SJ, Aldridge CL, Oyler-McCance SJ (2020) An empirical comparison of population genetic analyses using microsatellite and SNP data for a species of conservation concern. BMC Genomics 21:382
Zong Y, Sun P, Liu J, Yue XY, Niu QF, Teng YW (2014) Chloroplast DNA-based genetic diversity and phylogeography of Pyrus betulaefolia (Rosaceae) in Northern China. Tree Genet Genomes 10:739–749
Acknowledgements
This project was supported by the Bioinformatics Center of Nanjing Agricultural University.
Funding
This work was funded by the Earmarked Fund for Jiangsu Agricultural Industry Technology System (JATS [2020]401]), the National Science Foundation of China (31820103012, 31725024, 31801835, 31901983), and China Agriculture Research System of MOF and MARA.
Author information
Authors and Affiliations
Contributions
JW designed this project. XNC and MYZ drafted the manuscript. XNC collected the public dataset and performed bioinformatics analysis. MYZ and MYS contributed to results analysis. BBS contributed to data analysis. SNL worked with data collection. YYL and MYL reviewed the manuscript. SLZ provided help to the platform. RZW, JML, and KJZ provided the suggestion to do this study. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Additional information
Responsible Editor: D. Chagné
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Chen, X., Zhang, M., Sun, M. et al. Genome-wide genetic diversity and IBD analysis reveals historic dissemination routes of pear in China. Tree Genetics & Genomes 18, 1 (2022). https://doi.org/10.1007/s11295-021-01530-x
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11295-021-01530-x