Theoretical and Applied Genetics

, Volume 125, Issue 2, pp 311–327 | Cite as

Construction of black (Rubus occidentalis) and red (R. idaeus) raspberry linkage maps and their comparison to the genomes of strawberry, apple, and peach

  • J. M. Bushakra
  • M. J. Stephens
  • A. N. Atmadjaja
  • K. S. Lewers
  • V. V. Symonds
  • J. A. Udall
  • D. Chagné
  • E. J. Buck
  • S. E. Gardiner
Original Paper

Abstract

The genus Rubus belongs to the Rosaceae and is comprised of 600–800 species distributed world-wide. To date, genetic maps of the genus consist largely of non-transferable markers such as amplified fragment length polymorphisms. An F1 population developed from a cross between an advanced breeding selection of Rubus occidentalis (96395S1) and R. idaeus ‘Latham’ was used to construct a new genetic map consisting of DNA sequence-based markers. The genetic linkage maps presented here are constructed of 131 markers on at least one of the two parental maps. The majority of the markers are orthologous, including 14 Rosaceae conserved orthologous set markers, and 60 new gene-based markers developed for raspberry. Thirty-four published raspberry simple sequence repeat markers were used to align the new maps to published raspberry maps. The 96395S1 genetic map consists of six linkage groups (LG) and covers 309 cM with an average of 10 cM between markers; the ‘Latham’ genetic map consists of seven LG and covers 561 cM with an average of 5 cM between markers. We used BLAST analysis to align the orthologous sequences used to design primer pairs for Rubus genetic mapping with the genome sequences of Fragaria vesca ‘Hawaii 4’, Malus × domestica ‘Golden Delicious’, and Prunus ‘Lovell’. The alignment of the orthologous markers designed here suggests that the genomes of Rubus and Fragaria have a high degree of synteny and that synteny decreases with phylogenetic distance. Our results give unprecedented insights into the genome evolution of raspberry from the putative ancestral genome of the single ancestor common to Rosaceae.

Supplementary material

122_2012_1835_MOESM1_ESM.pdf (210 kb)
Supplemental Fig. 1: Comparison between Rubus idaeus ‘Latham’ genetic map and Fragaria physical map constructed using BLAST analysis. ‘Latham’ map distance is measured in centimorgans (cM); Fragaria map distance is measured in megabase pairs (Mbp). ‘Latham’ LG arranged in proposed order (RLG) with original numbering (OLG) in parentheses. (PDF 210 kb)
122_2012_1835_MOESM2_ESM.pdf (230 kb)
Supplemental Fig. 2: Comparison between Rubus idaeus ‘Latham’ genetic map and Malus physical map constructed using BLAST analysis. ‘Latham’ map distance is measured in cM; Malus map distance is measured in Mbp. ‘Latham’ LG arranged in proposed order (RLG) with original numbering (OLG) in parentheses. (PDF 229 kb)
122_2012_1835_MOESM3_ESM.pdf (201 kb)
Supplemental Fig. 3: Comparison between Rubus idaeus ‘Latham’ genetic map and Prunus physical map constructed using BLAST analysis. ‘Latham’ map distance is measured in cM; Prunus map distance is measured in Mbp. ‘Latham’ LG arranged in proposed order (RLG) with original numbering (OLG) in parentheses. (PDF 201 kb)
122_2012_1835_MOESM4_ESM.pdf (163 kb)
Supplemental Table 1: Redesigned and newly designed primer pair sequences of markers polymorphic in Rubus occidentalis 96395S1 × R. idaeus ‘Latham’ progeny. (PDF 162 kb)
122_2012_1835_MOESM5_ESM.pdf (755 kb)
Supplemental Table 2: Marker design information. Information on origin and type of sequence, locations in strawberry, apple and peach genomes, expected values (E-values), and percent identity for each marker mapped in Rubus occidentalis 96395S1 × R. idaeus ‘Latham’. (PDF 754 kb)

References

  1. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410PubMedGoogle Scholar
  2. Amsellem L, Dutech C, Billotte N (2001) Isolation and characterization of polymorphic microsatellite loci in Rubus alceifolius Poir. (Rosaceae), an invasive weed in La Réunion Island. Mol Ecol Notes 1:33–35CrossRefGoogle Scholar
  3. Bassil N, Hummer K, Postman J, Fazio G, Baldo A, Armas I, Williams R (2009) Nomenclature and genetic relationships of apples and pears from Terceira Island. Genet Resour Crop Evol 56:339–352CrossRefGoogle Scholar
  4. Bushakra JM, Sargent DJ, Cabrera A, Crowhurst RN, Lopez Girona E, Velasco R, Symonds VV, van der Knaap E, Troggio M, Gardiner SE, Chagné D (2012) Rosaceae conserved orthologous set (RosCOS) markers as a tool to assess genome synteny between Malus and Fragaria. Tree Genet Genomes. doi:10.1007/s11295-011-0450-y Google Scholar
  5. Cabrera A, Kozik A, Howad W, Arus P, Iezzoni A, van der Knaap E (2009) Development and bin mapping of a Rosaceae Conserved Ortholog Set (COS) of markers. BMC Genomics 10:562PubMedCrossRefGoogle Scholar
  6. Castillo NRF, Reed BM, Graham J, Fernandez–Fernandez F, Bassil NV (2010) Microsatellite markers for raspberry and blackberry. J Amer Soc Hort Sci 135:271–278Google Scholar
  7. Celton J-M, 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 5:93–107CrossRefGoogle Scholar
  8. Chagné D, Gasic K, Crowhurst RN, Han Y, Bassett HC, Bowatte DR, Lawrence TJ, Rikkerink EHA, Gardiner SE, Korban SS (2008) Development of a set of SNP markers present in expressed genes of the apple. Genomics 92(5):353–358 PubMedCrossRefGoogle Scholar
  9. Dale A, Moore PP, McNicol RJ, Sjulin TM, Burmistrov LA (1993) Genetic diversity of red raspberry varieties throughout the world. J Amer Soc Hort Sci 118:119–129Google Scholar
  10. Dirlewanger E, Graziano E, Joobeur T, Garriga-Caldera F, Cosson P, Howad W, Arús P (2004) Comparative mapping and marker-assisted selection in Rosaceae fruit crops. Proc Natl Acad Sci USA 101:9891–9896PubMedCrossRefGoogle Scholar
  11. Eriksson T, Hibbs MS, Yoder AD, Delwiche CF, Donoghue MJ (2003) The phylogeny of Rosoideae (Rosaceae) based on sequences of the internal transcribed spacers (ITS) of nuclear ribosomal DNA and the TrnL/F region of chloroplast DNA. Int J Plant Sci 164:197–211CrossRefGoogle Scholar
  12. Falconer DS, Mackay TFC (1996) Introduction to quantitative genetics, 4th edn. Pearson Education Limited, Longmans GreenGoogle Scholar
  13. Graham J, Smith K, MacKenzie K, Jorgenson L, Hackett C, Powell W (2004) The construction of a genetic linkage map of red raspberry (Rubus idaeus subsp. idaeus) based on AFLPs, genomic-SSR and EST-SSR markers. Theor Appl Genet 109:740–749PubMedCrossRefGoogle Scholar
  14. Graham J, Smith K, Tierney I, MacKenzie K, Hackett C (2006) Mapping gene H controlling cane pubescence in raspberry and its association with resistance to cane botrytis and spur blight, rust and cane spot. Theor Appl Genet 112:818–831PubMedCrossRefGoogle Scholar
  15. Graham J, Hackett C, Smith K, Woodhead M, Hein I, McCallum S (2009) Mapping QTLs for developmental traits in raspberry from bud break to ripe fruit. Theor Appl Genet 118:1143–1155PubMedCrossRefGoogle Scholar
  16. Grattapaglia D, Sederoff R (1994) Genetic linkage maps of Eucalyptus grandis and Eucalyptus urophylla using a pseudo-testcross: mapping strategy and RAPD markers. Genetics 137:1121–1137PubMedGoogle Scholar
  17. Gygax M, Gianfranceschi L, Liebhard R, Kellerhals M, Gessler C, Patocchi A (2004) Molecular markers linked to the apple scab resistance gene Vbj; derived from Malus baccata jackii. Theor Appl Genet 109:1702–1709PubMedCrossRefGoogle Scholar
  18. Illa E, Sargent D, Lopez Girona E, Bushakra J, Cestaro A, Crowhurst R, Pindo M, Cabrera A, van der Knaap E, Iezzoni A, Gardiner S, Velasco R, Arus P, Chagne D, Troggio M (2011) Comparative analysis of rosaceous genomes and the reconstruction of a putative ancestral genome for the family. BMC Evol Biol 11:9PubMedCrossRefGoogle Scholar
  19. Joobeur T, Viruel MA, de Vicente MC, Jáuregui B, Ballester J, Dettori MT, Verde I, Truco MJ, Messeguer R, Batlle I, Quarta R, Dirlewanger E, Arús P (1998) Construction of a saturated linkage map for Prunus using an almond × peach F2 progeny. Theor Appl Genet 97:1034–1041CrossRefGoogle Scholar
  20. Kassim A, Poette J, Paterson A, Zait D, McCallum S, Woodhead M, Smith K, Hackett C, Graham J (2009) Environmental and seasonal influences on red raspberry anthocyanin antioxidant contents and identification of quantitative traits loci (QTL). Mol Nutr Food Res 53:625–634PubMedCrossRefGoogle Scholar
  21. Kobayashi N, Horikoshi T, Katsuyama H, Handa T, Takayanagi K (1998) A simple and efficient DNA extraction method for plants, especially woody plants. Plant Tissue Culture Biotechnol 4:76–80Google Scholar
  22. Lansari A, Kester DE, Iezzoni AF (1994) Inbreeding, coancestry, and founding clones of almonds of California, Mediterranean shores, and Russia. J Amer Soc Hort Sci 119:1279–1285Google Scholar
  23. Lewers KS, Styan SMN, Hokanson SC, Bassil NV (2005) Strawberry GenBank-derived and genomic simple sequence repeat (SSR) markers and their utility with strawberry, blackberry, and red and black raspberry. J Amer Soc Hort Sci 130:102–115Google Scholar
  24. Lewers K, Saski C, Cuthbertson B, Henry D, Staton M, Main D, Dhanaraj A, Rowland L, Tomkins J (2008) A blackberry (Rubus L.) expressed sequence tag library for the development of simple sequence repeat markers. BMC Plant Biol 8:69–76PubMedCrossRefGoogle Scholar
  25. Lopes MS, Maciel GB, Mendonça D, Gil FS, Da Machado Câmara A (2006) Isolation and characterization of simple sequence repeat loci in Rubus hochstetterorum and their use in other species from the Rosaceae family. Mol Ecol Notes 6:750–752CrossRefGoogle Scholar
  26. McCallum S, Woodhead M, Hackett C, Kassim A, Paterson A, Graham J (2010) Genetic and environmental effects influencing fruit colour and QTL analysis in raspberry. Theor Appl Genet 121:611–627PubMedCrossRefGoogle Scholar
  27. Montgomery J, Wittwer CT, Palais R, Zhou L (2007) Simultaneous mutation scanning and genotyping by high-resolution DNA melting analysis. Nat Protoc 2:59–66PubMedCrossRefGoogle Scholar
  28. Potter D, Eriksson T, Evans RC, Oh S, Smedmark JEE, Morgan DR, Kerr M, Robertson KR, Arsenault M, Dickinson TA, Campbell CS (2007) Phylogeny and classification of Rosaceae. Plant Syst Evol 266:5–43CrossRefGoogle Scholar
  29. Reed GH, Wittwer CT (2004) Sensitivity and specificity of single-nucleotide polymorphism scanning by high-resolution melting analysis. Clin Chem 50:1748–1754PubMedCrossRefGoogle Scholar
  30. Sargent DJ, Clarke J, Simpson DW, Tobutt KR, Arús P, Monfort A, Vilanova S, Denoyes-Rothan B, Rousseau M, Folta KM, Bassil NV, Battey NH (2006) An enhanced microsatellite map of diploid Fragaria. Theor Appl Genet 112:1349–1359PubMedCrossRefGoogle Scholar
  31. Sargent DJ, Fernández-Fernández F, Rys A, Knight VH, Simpson DW, Tobutt KR (2007) Mapping of A 1 conferring resistance to the aphid Amphorophora idaei and dw (dwarfing habit) in red raspberry (Rubus idaeus L.) using AFLP and microsatellite markers. BMC Plant Biol 7:15Google Scholar
  32. Sargent DJ, Davis TM, Simpson DW (2009) Strawberry (Fragaria spp.) Structural Genomics. In: Folta KM, Gardiner SE (eds) Genetics and genomics of Rosaceae. Springer, New York, pp 437–456Google Scholar
  33. Shulaev V, Sargent DJ, Crowhurst RN, Mockler TC, Folkerts O, Delcher AL, Jaiswal P, Mockaitis K, Liston A, Mane SP, Burns P, Davis TM, Slovin JP, Bassil N, Hellens RP, Evans C, Harkins T, Kodira C, Desany B, Crasta OR, Jensen RV, Allan AC, Michael TP, Setubal JC, Celton J-M, Rees DJG, Williams KP, Holt SH, Rojas JJR, Chatterjee M, Liu B, Silva H, Meisel L, Adato A, Filichkin SA, Troggio M, Viola R, Ashman T-L, Wang H, Dharmawardhana P, Elser J, Raja R, Priest HD, Bryant DW, Fox SE, Givan SA, Wilhelm LJ, Naithani S, Christoffels A, Salama DY, Carter J, Girona EL, Zdepski A, Wang W, Kerstetter RA, Schwab W, Korban SS, Davik J, Monfort A, Denoyes-Rothan B, Arus P, Mittler R, Flinn B, Aharoni A, Bennetzen JL, Salzberg SL, Dickerman AW, Velasco R, Borodovsky M, Veilleux RE, Folta KM (2011) The genome of woodland strawberry (Fragaria vesca). Nat Genet 43:109–116PubMedCrossRefGoogle Scholar
  34. Sosinski B, Verde I, Rokhsar DS (2010) International peach genome initiative peach genome v1.0Google Scholar
  35. Stafne ET, Clark JR (2004) Genetic relatedness among eastern North American blackberry cultivars based on pedigree analysis. Euphytica 139:95–104CrossRefGoogle Scholar
  36. Thompson MM (1995a) Chromosome numbers of Rubus cultivars at the National Clonal Germplasm Repository. HortSci 30:1453–1456Google Scholar
  37. Thompson MM (1995b) Chromosome numbers of Rubus species at the National Clonal Germplasm Repository. HortSci 30:1447–1452Google Scholar
  38. van Ooijen JW, Voorrips RE (2001) JoinMap(R) 3.0, Software for the calculation of genetic linkage maps. Plant Res Int, Wageningen, The NetherlandsGoogle Scholar
  39. Velasco R, Zharkikh A, Affourtit J, Dhingra A, Cestaro A, Kalyanaraman A, Fontana P, Bhatnagar SK, Troggio M, Pruss D, Salvi S, Pindo M, Baldi P, Castelletti S, Cavaiuolo M, Coppola G, Costa F, Cova V, Dal Ri A, Goremykin V, Komjanc M, Longhi S, Magnago P, Malacarne G, Malnoy M, Micheletti D, Moretto M, Perazzolli M, Si-Ammour A, Vezzulli S, Zini E, Eldredge G, Fitzgerald LM, Gutin N, Lanchbury J, Macalma T, Mitchell JT, Reid J, Wardell B, Kodira C, Chen Z, Desany B, Niazi F, Palmer M, Koepke T, Jiwan D, Schaeffer S, Krishnan V, Wu C, Chu VT, King ST, Vick J, Tao Q, Mraz A, Stormo A, Stormo K, Bogden R, Ederle D, Stella A, Vecchietti A, Kater MM, Masiero S, Lasserre P, Lespinasse Y, Allan AC, Bus V, Chagne D, Crowhurst RN, Gleave AP, Lavezzo E, Fawcett JA, Proost S, Rouze P, Sterck L, Toppo S, Lazzari B, Hellens RP, Durel C-E, Gutin A, Bumgarner RE, Gardiner SE, Skolnick M, Egholm M, Van de Peer Y, Salamini F, Viola R (2010) The genome of the domesticated apple (Malus × domestica Borkh.). Nat Genet 42:833–839PubMedCrossRefGoogle Scholar
  40. Vilanova S, Sargent D, Arús P, Monfort A (2008) Synteny conservation between two distantly-related Rosaceae genomes: Prunus (the stone fruits) and Fragaria (the strawberry). BMC Plant Biol 8:67PubMedCrossRefGoogle Scholar
  41. Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78PubMedCrossRefGoogle Scholar
  42. Wittwer CT, Reed GH, Gundry CN, Vandersteen JG, Pryor RJ (2003) High-resolution genotyping by amplicon melting analysis using LCGreen. Clin Chem 49:853–860PubMedCrossRefGoogle Scholar
  43. Woodhead M, McCallum S, Smith K, Cardle L, Mazzitelli L, Graham J (2008) Identification, characterisation and mapping of simple sequence repeat (SSR) markers from raspberry root and bud ESTs. Mol Breed 22:555–563CrossRefGoogle Scholar
  44. Woodhead M, Weir A, Smith K, McCallum S, MacKenzie K, Graham J (2010) Functional markers for red raspberry. J Amer Soc Hort Sci 135:418–427Google Scholar
  45. Zorrilla-Fontanesi Y, Cabeza A, Torres A, Botella M, Valpuesta V, Monfort A, Sánchez-Sevilla J, Amaya I (2011) Development and bin mapping of strawberry genic-SSRs in diploid Fragaria and their transferability across the Rosoideae subfamily. Mol Breed 27:137–156CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • J. M. Bushakra
    • 1
    • 2
  • M. J. Stephens
    • 3
  • A. N. Atmadjaja
    • 1
  • K. S. Lewers
    • 4
  • V. V. Symonds
    • 2
  • J. A. Udall
    • 5
  • D. Chagné
    • 1
  • E. J. Buck
    • 1
  • S. E. Gardiner
    • 1
  1. 1.The New Zealand Institute for Plant & Food Research Limited (PFR)Palmerston NorthNew Zealand
  2. 2.Institute of Molecular BiosciencesMassey UniversityPalmerston NorthNew Zealand
  3. 3.PFRMotuekaNew Zealand
  4. 4.USDA-ARS, Genetic Improvement of Fruits and Vegetables LaboratoryBeltsvilleUSA
  5. 5.Plant and Wildlife Science DepartmentBrigham Young UniversityProvoUSA

Personalised recommendations