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.
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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
References
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:e3376
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 23:2633–2635
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 191–295
Brennan R, Jorgensen L, Woodhead M, Russell J (2002) Development and characterisation of SSR markers in Ribes species. Mol Ecol Notes 2:327–330
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 161:19–34
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 118:205–212
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:e57438
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 81:1049–1057
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 99:291–311
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 12:499–510
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:e62137
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 3:53–68
Eckert AJ, Dyer RJ (2012) Defining the landscape of adaptive genetic diversity. Mol Ecol 21:2836–2838
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
Garrison E, Marth G (2012) Haplotype-based variant detection from short-read sequencing. http://arxiv.org/abs/1207.3907
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 2:121–133
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):644–652
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 10:202
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):38
International Barley Genome Sequencing Consortium (2012) A physical, genetic and functional sequence assembly of the barley genome. Nature 491:711–717
Kosambi D (1944) The estimation of map distances from recombination values. Ann Eugen 12:172–175
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:R25
Lanham PG, Brennan RM (1999) Genetic characterisation of gooseberry (Ribes subgenus Grossularia) germplasm using RAPD, ISSR and AFLP markers. J Hort Sci Biotechnol 74:361–366
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 75:371–375
Payne RW, Murray DA, Harding SA, Baird D, Soutar D (2012) Introduction to GenStat for windows, 15th edn. VSN International, Hemel Hempstead
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 13:179–195
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 122:1467–1480
Poland JA, Rife TW (2012) Genotyping-by-sequencing for plant breeding and genetics. Plant Genome 5:92–102
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
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 11:147
Sokal RR, Rohlf FJ (1995) Biometry: the principles and practice of statistics in biological research, 3rd edn. WH Freeman, New York
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
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
Van Ooijen JW (2004) MapQTL® 5, Software for the mapping of quantitative trait loci in experimental populations. Kyazma BV, Wageningen, Netherlands
Van Ooijen JW (2006) JoinMap® 4, Software for the calculation of genetic linkage maps in experimental populations. Kyazma BV, Wageningen, Netherlands
Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93(1):77–78
Wang S, Meyer E, McKay JK, Matz MV (2012) 2b-RAD: a simple and flexible method for genome-wide genotyping. Nat Methods 9:808–810
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 14:2
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.
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Russell, J., Hackett, C., Hedley, P. et al. The use of genotyping by sequencing in blackcurrant (Ribes nigrum): developing high-resolution linkage maps in species without reference genome sequences. Mol Breeding 33, 835–849 (2014). https://doi.org/10.1007/s11032-013-9996-8
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DOI: https://doi.org/10.1007/s11032-013-9996-8