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Molecular Breeding

, Volume 33, Issue 4, pp 835–849 | Cite as

The use of genotyping by sequencing in blackcurrant (Ribes nigrum): developing high-resolution linkage maps in species without reference genome sequences

  • Joanne Russell
  • Christine Hackett
  • Pete Hedley
  • Hui Liu
  • Linda Milne
  • Micha Bayer
  • David Marshall
  • Linzi Jorgensen
  • Sandra Gordon
  • Rex BrennanEmail author
Article

Abstract

A genotyping by sequencing (GbS) approach is reported in blackcurrant (Ribes nigrum L.) using a de novo read assembly method developed because of the current absence of a reference genome sequence for this species. A new approach to single nucleotide polymorphism (SNP) genotype calling is described, where individual genotypes for a large number of SNPs were characterised from the GbS counts using a novel method based on a functional regression of major and minor allele read counts. The high-quality GbS SNPs were combined with SNPs and simple sequence repeats generated from other technologies to develop a linkage map with increased marker density and improved genome coverage, containing up to 204 SNPs on each linkage group. SNPs of lower quality were then located on the map using quantitative trait locus (QTL) interval mapping of the proportion of the major allele. Two QTL each for 100-berry weight and Brix scores, measured over three years, were identified using the map. The use of this approach to identify and map a significant number of novel SNPs in a woody species with hitherto limited genomic resources may have generic application to other under-resourced and minor species in the development of cost-effective and efficient high-density genetic maps.

Keywords

Genotyping by sequencing Ribes Woody perennial SNP discovery Linkage map 

Abbreviations

GbS

Genotyping by sequencing

SNP

Single nucleotide polymorphism

SSR

Simple sequence repeat

AFLP

Amplified fragment length polymorphism

QTL

Quantitative trait locus

2GS

Second-generation sequencing

SbG

Sequencing-based genotyping

RRL

Reduced representation libraries

RAD

Restriction site associated DNA

HBW

100-Berry weight

Notes

Acknowledgments

Support for this work from the Scottish Government’s Rural and Environment Science and Analytical Services Division (RESAS) and the EU FP7 EUBerry project is gratefully acknowledged.

Supplementary material

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References

  1. Baird NA, Etter PD, Atwood TS, Currey MC, Shiver AL, Lewis ZA, Selker EU, Cresko WA, Johnson EA (2008) Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLoS ONE 3:e3376PubMedCentralPubMedCrossRefGoogle Scholar
  2. Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23:2633–2635PubMedCrossRefGoogle Scholar
  3. Brennan RM (1996) Currants and gooseberries. In: Janick J, Moore JN (eds) Fruit breeding, vol II. Small fruits and vine crops. Wiley, New York, pp 191–295Google Scholar
  4. Brennan R, Jorgensen L, Woodhead M, Russell J (2002) Development and characterisation of SSR markers in Ribes species. Mol Ecol Notes 2:327–330CrossRefGoogle Scholar
  5. Brennan R, Jorgensen L, Hackett C, Woodhead M, Gordon SL, Russell J (2008) The development of a genetic linkage map of blackcurrant (Ribes nigrum L.) and the identification of regions associated with key fruit quality and agronomic traits. Euphytica 161:19–34CrossRefGoogle Scholar
  6. Brennan R, Jorgensen L, Gordon SL, Loades K, Hackett C, Russell J (2009) The development of a PCR-based marker linked to resistance to the blackcurrant gall mite (Cecidophyopsis ribis Acari: Eriophyidae). Theor Appl Genet 118:205–212PubMedCrossRefGoogle Scholar
  7. Byrne S, Czaban A, Studer B, Panitz F, Bendixen C, Asp T (2013) Genome wide allele frequency fingerprints (GWAFFs) of populations via genotyping by sequencing. PLoS ONE 8:e57438PubMedCentralPubMedCrossRefGoogle Scholar
  8. Chiche J, Brown SC, Leclerc J-L, Siljak-Yacovlev S (2003) Genome size, heterochromatin organisation and ribosomal gene mapping in four species of Ribes. Can J Bot 81:1049–1057CrossRefGoogle Scholar
  9. Cronn R, Knaus BJ, Liston A, Maughan PJ, Parks M, Syring JV, Udall J (2012) Targeted enrichment strategies for next-generation plant biology. Am J Bot 99:291–311PubMedCrossRefGoogle Scholar
  10. Davey JW, Hohenloe PA, Etter PD, Boone JQ, Catchen JM, Blaxter ML (2011) Genome-wide genetic marker discovery and genotyping using next-generation sequencing. Nat Genet 12:499–510CrossRefGoogle Scholar
  11. De Donato M, Peters SO, Mitchell SE, Hussain T, Imumorin IG (2013) Genotyping by sequencing (GBS): a novel, efficient and cost-effective method for cattle using next-generation sequencing. PLoS ONE 8:e62137PubMedCentralPubMedCrossRefGoogle Scholar
  12. Deschamps S, la Rota M, Ratashak JP, Biddle P, Thureen D, Farmer A, Luck S, Beatty M, Nagasawa N, Michael L, Llaca V, Sakai H, May G, Lightner J, Campbell MA (2010) Rapid genome-wide single nucleotide polymorphism discovery in soybean and rice via deep resequencing of reduced representation libraries with the Illumina genome analyser. Plant Genome 3:53–68CrossRefGoogle Scholar
  13. Eckert AJ, Dyer RJ (2012) Defining the landscape of adaptive genetic diversity. Mol Ecol 21:2836–2838PubMedCrossRefGoogle Scholar
  14. Elshire RJ, Glaubitz JC, Qi S, Poland JA, Kawamoto K, Buckler E, Mitchell SE (2011) A robust, simple genotyping by sequencing (GbS) approach for high diversity species. PLoS ONE 6(5):e19379. doi: 10.1371/journal.pone.0019379 PubMedCentralPubMedCrossRefGoogle Scholar
  15. Garrison E, Marth G (2012) Haplotype-based variant detection from short-read sequencing. http://arxiv.org/abs/1207.3907
  16. Gore MA, Wright MH, Ersoz ES, Bouffard P, Szekeres ES, Jarvie TP, Hurwitz BL, Narechania A, Harkins TT, Grills GS, Ware DH, Buckler ES (2009) Large-scale discovery of gene-enriched SNPs. Plant Genome 2:121–133CrossRefGoogle Scholar
  17. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palm F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29(7):644–652PubMedCentralPubMedCrossRefGoogle Scholar
  18. Hedley PE, Russell JR, Jorgensen L, Gordon S, Morris JA, Hackett CA, Cardle L, Brennan RM (2010) Candidate genes associated with bud dormancy release in blackcurrant (Ribes nigrum L.). BMC Genomics 10:202Google Scholar
  19. Hyten DL, Cannon SB, Song Q, Weeks N, Fickus EW, Shoemaker RC, Specht JE, Farmer AD, May GD, Cregan PB (2010) High-throughput SNP discovery through deep resequencing of a reduced representation library to anchor and orient scaffolds in the soybean whole genome sequence. BMC Genomics 11(1):38PubMedCentralPubMedCrossRefGoogle Scholar
  20. International Barley Genome Sequencing Consortium (2012) A physical, genetic and functional sequence assembly of the barley genome. Nature 491:711–717Google Scholar
  21. Kosambi D (1944) The estimation of map distances from recombination values. Ann Eugen 12:172–175CrossRefGoogle Scholar
  22. Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10:R25PubMedCentralPubMedCrossRefGoogle Scholar
  23. Lanham PG, Brennan RM (1999) Genetic characterisation of gooseberry (Ribes subgenus Grossularia) germplasm using RAPD, ISSR and AFLP markers. J Hort Sci Biotechnol 74:361–366Google Scholar
  24. Lanham PG, Korycinska A, Brennan RM (2000) Genetic diversity within a secondary gene pool for Ribes nigrum L. revealed by RAPD and ISSR markers. J Hort Sci Biotechnol 75:371–375Google Scholar
  25. Payne RW, Murray DA, Harding SA, Baird D, Soutar D (2012) Introduction to GenStat for windows, 15th edn. VSN International, Hemel HempsteadGoogle Scholar
  26. Perez-de-Castro AM, Vilanova S, Canizares J, Pascual L, Blanca JM, Diez MJ, Prohens J, Pico B (2012) Application of genomic tools in plant breeding. Curr Genomics 13:179–195PubMedCentralPubMedCrossRefGoogle Scholar
  27. Pfender WF, Saha MC, Johnson EA, Slabaugh MB (2011) Mapping with RAD (restriction-site associated DNA) markers to rapidly identify QTL for stem rust resistance in Lolium perenne. Theor Appl Genet 122:1467–1480PubMedCrossRefGoogle Scholar
  28. Poland JA, Rife TW (2012) Genotyping-by-sequencing for plant breeding and genetics. Plant Genome 5:92–102CrossRefGoogle Scholar
  29. Poland JA, Brown PJ, Sorrells ME, Jannink J-L (2012) Development of high-density genetic maps for barley and wheat using a novel two-enzyme genotyping-by-sequencing approach. PLoS ONE 7(2):e32253. doi: 10.1371/journal.pone.0032253 PubMedCentralPubMedCrossRefGoogle Scholar
  30. Russell J, Bayer M, Booth C, Cardle L, Hackett C, Hedley PE, Jorgensen L, Brennan RM (2011) Identification, utilisation and mapping of novel transcriptome-based markers from blackcurrant (Ribes nigrum). BMC Plant Biol 11:147PubMedCentralPubMedCrossRefGoogle Scholar
  31. Sokal RR, Rohlf FJ (1995) Biometry: the principles and practice of statistics in biological research, 3rd edn. WH Freeman, New YorkGoogle Scholar
  32. Sonah H, Bastien M, Iquira E, Tardivel A, Légare G, Boyle B, Normandeau É, Laroche J, Larose S, Jean M, Belzile F (2013) An improved genotyping by sequencing (GBS) approach offering increased versatility and efficiency of SNP discovery and genotyping. PLoS ONE 8(1):e54603. doi: 10.1371/journal.pone.0054603 PubMedCentralPubMedCrossRefGoogle Scholar
  33. Truong HT, Ramos AM, Yalcin F, de Ruiter M, van der Poel HJA, Huvenaars KHJ, Hogers RCJ, van Enkevort LJG, Janssen A, van Orsouw NJ, van Eijk MJT (2012) Sequence-based genotyping for marker discovery and co-dominant scoring in germplasm and populations. PLoS ONE 7(5):e37565. doi: 10.1371/journal.pone.0037565 PubMedCentralPubMedCrossRefGoogle Scholar
  34. Van Ooijen JW (2004) MapQTL® 5, Software for the mapping of quantitative trait loci in experimental populations. Kyazma BV, Wageningen, NetherlandsGoogle Scholar
  35. Van Ooijen JW (2006) JoinMap® 4, Software for the calculation of genetic linkage maps in experimental populations. Kyazma BV, Wageningen, NetherlandsGoogle Scholar
  36. Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93(1):77–78PubMedCrossRefGoogle Scholar
  37. Wang S, Meyer E, McKay JK, Matz MV (2012) 2b-RAD: a simple and flexible method for genome-wide genotyping. Nat Methods 9:808–810PubMedCrossRefGoogle Scholar
  38. Ward JA, Bhangoo J, Fernández-Fernández F, Moore P, Swanson JD, Viola R, Velasco R, Bassil N, Weber C, Sargent DJ (2013) Saturated linkage map construction in Rubus idaeus using genotyping by sequencing and genome-independent imputation. BMC Genomics 14:2PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Joanne Russell
    • 1
  • Christine Hackett
    • 2
  • Pete Hedley
    • 1
  • Hui Liu
    • 3
  • Linda Milne
    • 1
  • Micha Bayer
    • 1
  • David Marshall
    • 1
  • Linzi Jorgensen
    • 1
  • Sandra Gordon
    • 1
  • Rex Brennan
    • 1
    Email author
  1. 1.The James Hutton InstituteInvergowrie, DundeeUK
  2. 2.Biomathematics and Statistics ScotlandInvergowrie, DundeeUK
  3. 3.Biomedical Sciences Research ComplexUniversity of St AndrewsFifeUK

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