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Construction of high-resolution genetic linkage map in pear pseudo-BC1 ((Pyrus pyrifolia × P. communis) × P. pyrifolia) using GBS-SNPs and SSRs

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Abstract

Genetic linkage map of pear ((Pyrus pyrifolia × P. communis) × P. pyrifolia) was constructed to validate the effectiveness of the two-enzyme approach in GBS library preparation. In addition, allele inheritance was analyzed to investigate the usefulness of the pear pseudo-BC1 in genetic analysis. A total of 905 GBS-SNPs and 69 SSRs were anchored in 17 linkage groups with total genetic distance of 1760.1 cM and average marker distance of 1.88 cM. The genetic linkage map represents 80.5% of pear genome. GBS two-enzyme approach improved marker density and genome coverage compared to the single-enzyme approach. In addition, the inheritance analysis of SSR alleles demonstrated that pseudo-BC could allow genetic dissection of donor parent specific trait segregating in the F2. The high-resolution genetic linkage map of pear pseudo-BC1 will be used for candidate gene identification. Moreover, genetic analysis of donor parent specific traits segregating in the pseudo-BC1 hybrids will promote marker development for molecular breeding in pear.

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References

  • Abe K, Kotobuki K (1998) Inheritance of high resistance to Venturia nashicola Tanaka et Yamamoto in Japanese pear (Pyrus pyrifolia Nakai) and Chinese pear (P. ussuriensis Maxim.). J Jpn Soc Hortic Sci 67:677–680

    Google Scholar 

  • Abe K, Kotobuki K, Saito T, Terai O (2000) Inheritance of resistance to pear scab from European pears to Asian pears. J Jpn Soc Hortic Sci 69:1–8

    Google Scholar 

  • Ban SH, Choi C (2018) Development of an apple F1 segregating population genetic linkage map using genotyping-by-sequencing. Plant Breed Biotechnol 6:434–443

    Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bouquet A (1986) Introduction dans l’espece Vitis vinifera L. d’un caractere de resistance àl’oidium (Uncinula necator Schw. Burr.) issu de l’espèce Muscadinia rotundifolia (Michx.) Small. Vignevini 13:141–146

    Google Scholar 

  • Chen H, Song Y, Li LT, Khan A, 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

    CAS  Google Scholar 

  • Chevreau E, Leuliette S, Gallet M (1997) Inheritance and linkage of isozyme loci in pear (Pyrus communis L.). Theor Appl Genet 94:498–506

    CAS  Google Scholar 

  • Chung YS, Jun T, Kim C (2017) Digestion efficiency differences of restriction enzymes frequently used for genotyping-by-sequencing technology. Korean J Agric Sci 44:318–323

    CAS  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dettori MT, Quarta R, Verde I (2001) A peach linkage map integrating RFLPs, SSRs, RAPDs, and morphological markers. Genome 44:783–790

    CAS  PubMed  Google Scholar 

  • Elshire RJ, Glaubitz JC, Sun Q, Poland JA, Kawamoto K, Buckler ES, Mitchell SE (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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Flachowsky H, Le Roux PM, Peil A, Patocchi A, Richter K, Hanke MV (2011) Application of a high-speed breeding technology to apple (Malus × domestica) based on transgenic early flowering plants and marker-assisted selection. New Phytol 192:364–377

    CAS  PubMed  Google Scholar 

  • 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 4:1681–1686

    Google Scholar 

  • Gonai T, Terakami S, Nishitani C, Yamamoto T, Kasumi M (2009) The validity of marker-assisted selection using DNA markers linked to a pear scab resistance gene (Vnk) in two populations. J Jpn Soc Hortic Sci 78:49–54

    CAS  Google Scholar 

  • Grattapaglia D, Sederoff R (1994) Genetic linkage maps of Eucalyptus grandis and Eucalyptus urophylla using a pseudo-testcross: mapping strategy and RAPD markers. Genetics 137:1121–1137

    CAS  PubMed  PubMed Central  Google Scholar 

  • Guilford P, Prakash S, Zhu JM, Rikkerink E, Gardiner S, Bassett H, Forster R (1997) Microsatellites in Malus × domestica (apple): abundance, polymorphism and cultivar identification. Theor Appl Genet 94:249–254

    CAS  Google Scholar 

  • Hamblin MT, Rabbi IY (2014) The effects of restriction-enzyme choice on properties of genotyping-by-sequencing libraries: a study in cassava (Manihot esculenta). Crop Sci 54:2603–2608

    Google Scholar 

  • Han K, Lee HY, Ro NY, Hur OS, Lee JH, Kwon JK, Kang BC (2018) QTL mapping and GWAS reveal candidate genes controlling capsaicinoid content in Capsicum. Plant Biotechnol J 16:1546–1558

    CAS  PubMed Central  Google Scholar 

  • Han H, Oh Y, Kim K, Oh S, Cho S, Kim YK, Kim D (2019) Integrated genetic linkage maps for Korean pears (Pyrus hybrid) using GBS-based SNPs and SSRs. Hortic Environ Biotechnol 60:779–786

    CAS  Google Scholar 

  • Huang N, Angeles ER, Domingo J, Magpantay G, Singh S, Zhang G, Kumaravadivel N, Bennett J, Khush GS (1997) Pyramiding of bacterial blight resistance genes in rice: marker-assisted selection using RFLP and PCR. Theor Appl Genet 95:313–320

    CAS  Google Scholar 

  • Hwang K, Oh S, Kim K, Han H, Oh Y, Lim H, Kim YK, Kim D (2019) Genotyping-by-sequencing approaches using optimized two-enzyme combinations in Asian pears (Pyrus spp.). Mol Breed 39:161. https://doi.org/10.1007/s11032-019-1071-7

    Article  CAS  Google Scholar 

  • Iketani H, Abe K, Yamamoto T, Kotobuki K, Sato Y, Saito T, Terai O, Matsuta N, Hayashi T (2001) Mapping of disease-related genes in Japanese pear using a molecular linkage map with RAPD markers. Breed Sci 51:179–184

    CAS  Google Scholar 

  • Kim YK, Kang SS, Won KH, Shin IS, Cho KS, Ma KB, Kim MS, Choi JJ, Choi JH (2016) Breeding of the scab-resistant pear cultivar ‘Greensis’. Korean J Hortic Sci Technol 34:655–661

    Google Scholar 

  • Kullan ARK, Van Dyk MM, Jones N, Kanzler A, Bayley A, Myburg AA (2012) High-density genetic linkage maps with over 2,400 sequence-anchored DArT markers for genetic dissection in an F2 pseudo-backcross Eucalyptus grandis × E. urophylla. Tree Genet Genomes 8:163–175

    Google Scholar 

  • Kumar S, Kirk C, Deng CH, Wiedow C, Qin M, Espley R, Wu J, Brewer L (2019) Fine-mapping and validation of the genomic region underpinning pear red skin colour. Hortic Res 6:29. https://doi.org/10.1038/s41438-018-0112-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li H, Durbin R (2009) Fast and accurate short read alignment with burrows-wheeler transform. Bioinformatics 25:1754–1760

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, 1000 Genome Project Data Processing Subgroup (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079

    PubMed  PubMed Central  Google Scholar 

  • Li G, Wang Y, Chen MS, Edae E, Poland J, Akhunov E, Chao S, Bai G, Carver BF, Yan L (2015) Precisely mapping a major gene conferring resistance to Hassian fly in bread wheat using genotyping-by-sequencing. BMC Genom 16:108. https://doi.org/10.1186/s12864-015-1297-7

    Article  Google Scholar 

  • 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 10:217–241

    CAS  Google Scholar 

  • Liu N, Li M, Hu X, Ma Q, Mu Y, Tan Z, Xia Q, Zhang G, Nian H (2017) Construction of high-density genetic map and QTL mapping of yield-related and two quality traits in soybean RILs population by RAD-sequencing. BMC Genom 18:466. https://doi.org/10.1186/s12864-017-3854-8

    Article  CAS  Google Scholar 

  • Luby JJ, Shaw DV (2001) Does marker-assisted selection make dollars and sense in a fruit breeding program? HortScience 36:872–879

    Google Scholar 

  • Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J 17:10–12

    Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Molnár S, Galbács Z, Halász G, Hoffmann S, Kiss E, Kozma P, Veres A, Galli Z, Szõke A, Heszky L (2007) Marker assisted selection (MAS) for powdery mildew resistance in a grapevine hybrid family. Vitis 46:212–213

    Google Scholar 

  • Montoya C, Cochard B, Flori A, Cros D, Lopes R, Cuellar T, Espeout S, Syaputra I, Villeneuve P et al (2014) Genetic architecture of palm oil fatty acid composition in cultivated oil palm (Elaeis guineensis Jacq.) compared to its wild relative E. oleifera (H.B.K) cortés. PLoS ONE 9:e95412. https://doi.org/10.1371/journal.pone.0095412

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nishitani C, Terakami S, Sawamura Y, Takada N, Yamamoto T (2009) Development of novel EST-SSR markers derived from Japanese pear (Pyrus pyrifolia). Breed Sci 59:391–400

    CAS  Google Scholar 

  • Novaes E, Osorio L, Drost DR, Miles BL, Boaventura-Novaes CR, Benedict C (2009) Quantitative genetic analysis of biomass and wood chemistry of Populus under different nitrogen levels. New Phytol 182:878–890

    CAS  PubMed  Google Scholar 

  • Padmarasu S, Sargent DJ, Jaensch M, Kellerhals M, Tartarini S, Velasco R, Troggio M, Patocchi A (2014) Fine-mapping of the apple scab resistance locus Rvi12 (Vb) derived from ‘Hansen’s baccata #2’. Mol Breed 34:2119–2129

    Google Scholar 

  • Pauquet J, Bouquet A, This P, Adam-Blondon AF (2001) Establishment of a local map of AFLP markers around the powdery mildew resistance gene Run1 in grapevine and assessment of their usefulness for marker assisted selection. Theor Appl Genet 103:1201–1210

    CAS  Google Scholar 

  • Pieratoni L, Dondini L, Cho KH, Shin IS, Gennari F, Chiodini R, Tartarini S, Kang SJ, Sansavini S (2007) Pear scab resistance QTLs via a European pear (Pyrus communis). Tree Genet Genomes 3:311. https://doi.org/10.1007/s11295-006-0070-0

    Article  Google Scholar 

  • Poland JA, Brown PJ, Sorrells ME, Jannink JL (2012) Development of high-density genetic maps for barley and wheat using a novel two-enzyme genotyping-by-sequencing approach. PLoS ONE 7:332253. https://doi.org/10.1371/journal.pone.0032253

    Article  CAS  Google Scholar 

  • Pootakham W, Sonthirod C, Naktang C, Jomchai N, Sangsrakru D, Tangphatsornruang S (2016) Effects of methylation-sensitive enzymes on the enrichment of genic SNPs and the degree of genome complexity reduction in a two-enzyme genotyping-by-sequencing (GBS) approach: a case study in oil palm (Elaeis guineensis). Mol Breed 36:154. https://doi.org/10.1007/s11032-016-0572-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rabbi I, Hamblin M, Gedil M, Kulakow P, Ferguson M, Ikpan AS, Ly D, Jannink JL (2014) Genetic mapping using genotyping-by-sequencing in the clonally propagated cassava. Crop Sci 54:1384–1396

    CAS  Google Scholar 

  • Rikkerink EHA, Oraguzie NC, Gardiner SE (2007) Prospects of association mapping in perennial horticultural crops. In: Orguzie NC, Rikkerink EHA, Gardiner SE, De Silva HN (eds) association mapping in plant. Springer, New York, pp 264–269

    Google Scholar 

  • Rubtsov GA (1944) Geographical distribution of the genus Pyrus and trends and factors in its evolution. Am Nat 78:358–366

    Google Scholar 

  • Schröder S, Mamidi S, Lee R, McKain MR, McClean PE, Osorno JM (2016) Optimization of genotyping by sequencing (GBS) data in common bean (Phaseolus vulgaris L.). Mol Breed 36:6. https://doi.org/10.1007/s11032-015-0431-1

    Article  CAS  Google Scholar 

  • Silfverberg-Dilworth E, Matasci CL, Van de Weg WE, Van Kaauwen MPW, Walser M, Kodde LP, Songlio V, Gianfranceschi L, Eurel CE et al (2006) Microsatellite markers spanning the apple (Malus × domestica Borkh.) genome. Tree Genet Genomes 2:202–224

    Google Scholar 

  • Soufflet-Freslon V, Gianfranceschi L, Patocchi A, Eurel CE (2008) Inheritance studies of apple scab resistance and identification of Rvi14, a new major gene that acts together with other broad-spectrum QTL. Genome 51:657–667

    CAS  PubMed  Google Scholar 

  • Sun W, Zhang Y, Le W, Zhang H (2009) Construction of a genetic linkage map and QTL analysis for some leaf traits in pear (Pyrus L.). Front Agric China 3:67–74

    Google Scholar 

  • Terakami S, Shoda M, Adachi Y, Gonai T, Kasumi M, Sawamura Y, Iketani H, Kotobuki K, Patocchi A et al (2006) Genetic mapping of the pear scab resistance gene Vnk of Japanese pear cultivar Kinchaku. Theor Appl Genet 113:743–752

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Wu S, Yang J, Huang Y, Li Y, Yin T, Wullschleger SD, Tuskan GA, Wu R (2010) An improved approach for mapping quantitative trait loci in a pseudo-testcross: revisiting a poplar mapping study. Bioinform Biol Insights 4:1–8

    PubMed  PubMed Central  Google Scholar 

  • Wu J, Wang Z, Shi Z, Zhang S, Ming R, Zhu S, Awais Khan M, Tao S, Korban SS et al (2013) The genome of the pear (Pyrus bretschneideri Rehd.). Genome Res 23:396–408

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wu J, Lu 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xue H, Wang S, Yao JL, Deng CH, Wang L, Su Y, Zhang H, Zhou H, Sun M et al (2018) Chromosome level high-density integrated genetic maps improve the Pyrus bretschneideri ‘DangshanSuli’ v1.0 genome. BMC Genom 19:833. https://doi.org/10.1186/s12864-018-5224-6

    Article  CAS  Google Scholar 

  • Yamamoto T, Kimura T, Shoda M, Imai T, Saito T, Sawamura Y, Kotobuki K, Hayashi T, Matsuta N (2002a) Genetic linkage maps constructed by using an interspecific cross between Japanese and European pears. Theor Appl Genet 106:9–18

    CAS  PubMed  Google Scholar 

  • Yamamoto T, Kimura T, Sawamura Y, Manabe T, Kotobuki K, Hayashi T, Ban Y, Matsuta N (2002b) Simple sequence repeats for genetic analysis in pear. Euphytica 124:129–137

    CAS  Google Scholar 

  • Yamamoto T, Kimura T, Shoda M, Ban Y, Hayashi T, Matsuta N (2002c) Development of microsatellite markers in the Japanese pear (Pyrus pyrifolia Nakai). Mol Ecol Notes 2:14–16

    CAS  Google Scholar 

  • Zhang RP, Wu J, Li XG, Khan MA, Chen H, Korban SS, Zhang SL (2013) An AFLP, SRAP, and SSR genetic linkage map and identification of QTLs for fruit traits in pear (Pyrus L.). Plant Mol Biol Rep 31:678–687

    CAS  Google Scholar 

  • Zhou G, Jian J, Wang P, Li C, Tao Y, Li X, Yang H (2018) Construction of an ultra-high density consensus genetic map, and enhancement of the physical map from genome sequencing in Lupinus angustifolius. Theor Appl Genet 131:209–223

    CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by a grant from the Next-generation BioGreen21 Program (No. PJ01311501), Rural Development Administration, Republic of Korea.

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  1. Sewon Oh and Youngjae Oh have contributed equally to this work.

Authors and Affiliations

  1. Department of Horticulture, Chungbuk National University, Cheongju, 28644, Korea

    Sewon Oh, Youngjae Oh, Keumsun Kim, Hyeondae Han, Yumi Kim & Daeil Kim

  2. Department of Horticultural Science, IFAS Gulf Coast Research and Education Center, University of Florida, 14625 County Road 672, Wimuama, FL, 33598, USA

    Youngjae Oh

  3. Pear Research Station, National Institute of Horticultural and Herbal Science, Rural Development Administration, Naju, 58216, Korea

    Keumsun Kim & Kyungho Won

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  1. Sewon Oh
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Contributions

SO performed the overall the experiment and data analysis. SO and YO wrote the manuscript together. KK and HH contributed SNP calling and data analysis. YK contributed SSR marker analysis. KW generated and maintained the plant materials. DK designed and managed whole experiments and finalized the manuscript.

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Correspondence to Daeil Kim.

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Communicated by Ali Sarkhosh.

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Supplementary Table 1

Description of SSR markers used for polymorphism test in the pseudo-BC1 ((Pyrus pyrifolia × P. communis) × P. pyrifolia) and the progenitors (P. pyrifolia cv. Whangkeumbae and P. communis cv. Bartlett) (DOCX 16 kb)

Supplementary Table 2

Summary of genotyping-by-sequencing including the number of reads, mapping rate, and depth of mapped region (DOCX 15 kb)

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Oh, S., Oh, Y., Kim, K. et al. Construction of high-resolution genetic linkage map in pear pseudo-BC1 ((Pyrus pyrifolia × P. communis) × P. pyrifolia) using GBS-SNPs and SSRs. Hortic. Environ. Biotechnol. 61, 745–753 (2020). https://doi.org/10.1007/s13580-020-00261-7

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