Abstract
Integrated linkage maps are a valuable tool for comparative mapping between and within genus and species. Novel single-nucleotide polymorphism (SNP) linkage maps integrated with simple sequence repeats (SSRs) based on pseudo-chromosomes of the Chinese pear reference genome of ‘Dangshansuli’ (Pyrus bretschneideri) were constructed. In total, 4801 qualified SNP markers were obtained using a customized pipeline. The consensus map for ‘Whangkeumbae’ and ‘Minibae’ contained 321 SNP and 30 SSR markers spanning 1511.1 cM with an average genetic distance of 4.3 cM. A total of 30 SSR markers made it possible to compare our consensus map to other pear and apple maps. SSR markers originating from pear and apple maps showed high co-linearity. SNPs coordinated with pseudo-chromosomes, provide information on physical length coverage for 17 corresponding linkage groups, and enable easier genome annotation for genomic regions detected by quantitative trait loci analysis. Genotyping-by-sequencing-based SNP maps integrated with SSRs in the interspecific mapping population illustrate the genomic structure of Korean pear resources and will be used as our reference maps for tribe Maleae.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Ahn YH (2001) Distribution and characteristics of plant resources of native Pyrus sp. Plant Res 4:157–160
Bielenberg DG, Rauh B, Fan S, Gasic K, Abbott AG, Reighard GL, Okie WR, Wells CE (2015) Genotyping by sequencing for SNP-based linkage map construction and QTL analysis of chilling requirement and bloom date in peach [Prunus persica (L.) Batsch]. PLoS ONE 10:e0139406. https://doi.org/10.1371/journal.pone.0139406
Cao Y, Tian L, Gao Y, Liu F (2012) Genetic diversity of cultivated and wild Ussurian Pear (Pyrus ussuriensis Maxim.) in China evaluated with M13-tailed SSR markers. Genet Resour Crop Evol 59:9–17. https://doi.org/10.1007/s10722-011-9661-1
Celton JM, Tustin DS, Chagné D, Gardiner SE (2009) Construction of a dense genetic linkage map for apple rootstocks using SSRs developed from Malus ESTs and Pyrus genomic sequences. Tree Genet Genomes 5:93–107. https://doi.org/10.1007/s11295-008-0171-z
Chagné D, Crowhurst RN, Pindo M, Thrimawithana A, Deng C, Ireland H, Fiers M, Dzierzon H, Cestaro A, et al (2014) The draft genome sequence of European pear (Pyrus communis L. 'Bartlett'). PLoS ONE 9:e92644. https://doi.org/10.1371/journal.pone.0092644
Chen H, Song Y, Li LT, Awais Khan M, Li XG, Korban SS, Wu J, Zhang SL (2015) Construction of a high-density simple sequence repeat consensus genetic map for pear (Pyrus spp.). Plant Mol Biol Rep 33:316–325. https://doi.org/10.1007/s11105-014-0745-x
Cho HM, Cho KS, Kang SS, Koh GC, Hong KH, Kim WC, Kim KY (2002) Breeding of early summer pear cultivar ‘Minibae’. Kor J Hortic Sci Technol 20:238–241
Choi JK, Na DY, Kim D, Shin IS, Kim MY, Lee HJ (2010) Genetic linkage mapping using interspecific hybrid population between Korean wild pear (Pyrus ussuriensis) and Japanese pear (P. pyrifolia). Hortic Environ Biotechnol 51:319–325
Cox MP, Peterson DA, Biggs PJ (2010) SolexaQA: At-a-glance quality assessment of Illumina second-generation sequencing data. BMC Bioinformatics 11:485. https://doi.org/10.1186/1471-2105-11-485
Danecek P, Auton A, Abecasis G, Albers CA, Banks E, DePristo MA, Handsaker RE, Lunter G, Marth GT et al (2011) The variant call format and VCFtools. Bioinformatics 27:2156–2158. https://doi.org/10.1093/bioinformatics/btr330
Elshire RJ, Glaubitz JC, Poland JA, Kawamoto K, Buckler ES (2011) A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS ONE 6:e19379. https://doi.org/10.1371/journal.pone.0019379
Gabay G, Dahan Y, Izhaki Y, Faigenboim A, Ben-Ari G, Elkind Y, Flaishman MA (2018) High-resolution genetic linkage map of European pear (Pyrus communis) and QTL fine-mapping of vegetative budbreak time. BMC Plant Biol 18:175. https://doi.org/10.1186/s12870-018-1386-2
Gardner KM, Brown P, Cooke TF, Cann S, Costa F, Bustamante C, Velasco R, Troggio M, Myles S (2014) Fast and cost-effective genetic mapping in apple using next-generation sequencing. G3 Genes Genomes Genet 4:1681–1687. https://doi.org/10.1534/g3.114.011023
Guajardo V, Simón S, Sagredo B, Gainza F, Carlos M, Gasic K, Hinrichsen P (2015) Construction of high density sweet cherry (Prunus avium L.) linkage maps using microsatellite markers and SNPs detected by genotyping-by-sequencing (GBS). PLoS ONE 10:e0127750. https://doi.org/10.1371/journal.pone.0127750
He J, Zhao X, Laroche A, Lu ZX, Liu H, Li Z (2014) Genotyping-by-sequencing (GBS), an ultimate marker-assisted selection (MAS) tool to accelerate plant breeding. Front Plant Sci 5:484. https://doi.org/10.3389/fpls.2014.00484
Hong J, Shim E, Kwon Y (2017) Construction of a microsatellite DNA profile database for pear cultivars and germplasm. Hortic Sci Technol 35:98–107. https://doi.org/10.12972/kjhst.20170011
Hummer KE, Janick J (2009) Rosaceae: taxonomy, economic importance, genomics. In: Gardiner SE, Folta KM (eds) Genetics and genomics of Rosaceae, vol 6. Springer, New York, pp 1–17
Joobeur T, Viruel MA, de Vicente MC, Juregui B, Ballester J, Dettori MT, Verde I, Truco MJ, Batlle RI et al (1998) Construction of a saturated linkage map for Prunus using an almond×peach F2 progeny. Theor Appl Genet 97:1034–1041
Khan MA, Han Y, Zhao YF, Troggio M, Korban SS (2012) A multi-population consensus genetic map reveals inconsistent marker order among maps likely attributed to structural variations in the apple genome. PLoS ONE 7:e47864. https://doi.org/10.1371/journal.pone.0047864
Kim YS, Kim WC, Hong KH, Kim JB, Kim UJ, Hong SB, Kim JH, Kim YK, Moon JY et al (1985) A new mid-season pear cultivar, ‘Whangkeumbae’ with high soluble solids content and beautiful appearance. Res Rpt RDA Hortic 27:103–106
Kim HJ, Lee JN, Cho KS, Won HS, Suh JT (2019) Genetic diversity and population structure analysis of ever-bearing and June-bearing strawberry cultivars using SSR markers. Hortic Sci Technol 37:108–118. https://doi.org/10.12972/kjhst.20190010
Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754–1760. https://doi.org/10.1093/bioinformatics/btp324
Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079. https://doi.org/10.1093/bioinformatics/btp352
Liebhard R, Gianfranceschi L, Koller B, Ryder CD, Tarchini R, Van De Weg E, Gessler C (2002) Development and characterization of 140 new microsatellites in apple (Malus × domestica Borkh.). Mol Breed 4:217–241. https://doi.org/10.1023/A:1020525906332
Liebhard R, Kellerhals M, Pfammater W, Jertmini M, Gessler C (2003) Mapping quantitative physiological traits in apple (Malus × domestica Borkh.). Plant Mol Biol 52:511–526. https://doi.org/10.1023/A:1024886500979
Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J 17:10–12. https://doi.org/10.14806/ej.17.1.200
Martínez-García PJ, Parfitt DE, Ogundiwin EA, Fass J, Chan HM, Ahmad R, Lurie S, Dandekar A, Gradziel TM et al (2013) High density SNP mapping and QTL analysis for fruit quality characteristics in peach (Prunus persica L.). Tree Genet Genomes 9:19–36. https://doi.org/10.1007/s11295-012-0522-7
McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altshuler D, Gabriel S et al (2010) The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20:1297–1303. https://doi.org/10.1101/gr.107524.110
Nguyen TK, Yu J, Choi HW, In BC, Lim JH (2018) Optimization of genotyping-by-sequencing (GBS) in Chrysanthemums: selecting proper restriction enzymes for GBS library construction. Hortic Sci Technol 36:108–114. https://doi.org/10.12972/kjhst.20180012
Sabre-barcode-demultiplexing. Available via https://github.com/najoshi/sabre. Accessed 27 Sept 2013
Semagn K, Bjørnstad Å, Ndjiondjop MN (2006) An overview of molecular marker methods for plants. Afr J Biotechnol 5:2540–2568. http://www.academicjournals.org/AJB
Silfverberg-Dilworth E, Matasci CL, Van de Weg WE, Van Kaauwen MPW, Walser M, Kodde LP, Soglio V, Gianfranceschi L, Durel CE et al (2006) Microsatellite markers spanning the apple (Malus × domestica Borkh.) genome. Tree Genet Genomes 2:202–224. https://doi.org/10.1007/s11295-006-0045-1
Tanksley SD, Young ND, Paterson AH, Bonierbale MW (1989) RFLP mapping in plant breeding: new tools for an old science. Nat Biotechnol 7:257–264. https://doi.org/10.1038/nbt0389-257
Terakami S, Kimura T, Nishitani C, Sawamura Y, Saito T, Hirabayashi T, Yamamoto T (2009) Genetic linkage map of the Japanese pear ‘Housui’ identifying three homozygous genomic regions. J Jpn Soc Hortic Sci 78:417–424. https://doi.org/10.2503/jjshs1.78.417
Terakami S, Nishitani C, Kunihisa M, Shirasawa K, Sato S, Tabata S, Kurita K, Kanamori H, Katayose Y et al (2014) Transcriptome-based single nucleotide polymorphism markers for genome mapping in Japanese pear (Pyrus pyrifolia Nakai). Tree Genet Genomes 10:853–863. https://doi.org/10.1007/s11295-014-0726-0
Tokamaneh D, Laroche J, Bastien M, Abed A, Belzile F (2017) Fast-GBS: a new pipeline for the efficient and highly accurate calling of SNPs from genotyping by-sequencing data. BMC Bioinformatics 18:5. https://doi.org/10.1186/s12859-016-1431-9
Van Ooijen JW (2006) JoinMap 4. Software for the calculation of genetic linkage maps in experimental populations, Kyazma BV, Wageningen
Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78
Ward JA, Bhangoo J, Fernández-Fernández F, Moore P, Swanson JD, Viola R, Velasco R, Bassil N, Weber CA et al (2013) Saturated linkage map construction in Rubus idaeus using genotyping by sequencing and genome-independent imputation. BMC Genomics 14:2. https://doi.org/10.1186/1471-2164-14-2
Wu J, Wang Z, Shi Z, Zhang S, Ming R, Zhu S, Khan MA, Tao S, Korban SS et al (2013) The genome of the pear (Pyrus bretschneideri Rehd.). Genome Res 23:396–408. https://doi.org/10.1101/gr.144311.112
Wu J, Li LT, Li M, Khan MA, Li XG, Chen H, Yin H, Zhang SL (2014) High-density genetic linkage map construction and identification of fruit-related QTLs in pear using SNP and SSR markers. J Exp Bot 65:5771–5781. https://doi.org/10.1093/jxb/eru311
Yamamoto T, Terakami S (2016) Genomics of pear and other Rosaceae fruit trees. Breed Sci 66:149–159. https://doi.org/10.1270/jsbbs.66.148
Yamamoto T, Kimura T, Shoda M, Ban Y, Hayashi T, Matsuta N (2002) Development of microsatellite markers in the Japanese pear (Pyrus pyrifolia Nakai). Mol Ecol Notes 2:14–16. https://doi.org/10.1046/j.1471-8286.2002.00128.x
Yang Z, Yoder AD (1999) Estimation of the transition/transversion rate bias and species sampling. J Mol Evol 48:274–283. https://doi.org/10.1007/PL00006470
Zhang S, Chen W, Xin L, Gao Z, Hou Y, Yu X, Zhang Z, Qu S (2014) Genomic variants of genes associated with three horticultural traits in apple revealed by genome re-sequencing. Hortic Res 1:14045. https://doi.org/10.1038/hortres.2014.45
Acknowledgements
This work was supported by a Grant from the Next-Generation BioGreen 21 Program (No. PJ01311501), Rural Development Administration, Republic of Korea.
Author information
Authors and Affiliations
Contributions
HH performed the overall data analysis including SNP calling and compared the linkage map with published pear and apple maps. YO constructed the linkage map using SNP and SSR markers. HH and YO drafted the manuscript together. KK, SO, and SC contributed SSR marker analysis including sample preparation and marker detection. YK generated and maintained the plant materials. DK designed and managed whole experiments and finalized the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by Heakeun Yun, Ph.D.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Han, H., Oh, Y., Kim, K. et al. Integrated genetic linkage maps for Korean pears (Pyrus hybrid) using GBS-based SNPs and SSRs. Hortic. Environ. Biotechnol. 60, 779–786 (2019). https://doi.org/10.1007/s13580-019-00171-3
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13580-019-00171-3