Skip to main content
SpringerLink
Log in

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

  • Original Paper
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    PubMed  CAS  Google Scholar 

  • 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 1:33–35

    Article  CAS  Google Scholar 

  • 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 56:339–352

    Article  Google Scholar 

  • 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 

  • 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 10:562

    Article  PubMed  Google Scholar 

  • Castillo NRF, Reed BM, Graham J, Fernandez–Fernandez F, Bassil NV (2010) Microsatellite markers for raspberry and blackberry. J Amer Soc Hort Sci 135:271–278

    Google Scholar 

  • 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 5:93–107

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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 118:119–129

    Google Scholar 

  • 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 101:9891–9896

    Article  PubMed  CAS  Google Scholar 

  • 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 164:197–211

    Article  CAS  Google Scholar 

  • Falconer DS, Mackay TFC (1996) Introduction to quantitative genetics, 4th edn. Pearson Education Limited, Longmans Green

    Google Scholar 

  • 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 109:740–749

    Article  PubMed  CAS  Google Scholar 

  • 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 112:818–831

    Article  PubMed  CAS  Google Scholar 

  • 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 118:1143–1155

    Article  PubMed  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

    PubMed  CAS  Google Scholar 

  • 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 109:1702–1709

    Article  PubMed  CAS  Google Scholar 

  • 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 11:9

    Article  PubMed  Google Scholar 

  • 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 97:1034–1041

    Article  CAS  Google Scholar 

  • 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 53:625–634

    Article  PubMed  CAS  Google Scholar 

  • 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 4:76–80

    Google Scholar 

  • 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 119:1279–1285

    Google Scholar 

  • 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 130:102–115

    CAS  Google Scholar 

  • 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 8:69–76

    Article  PubMed  Google Scholar 

  • 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 6:750–752

    Article  CAS  Google Scholar 

  • 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 121:611–627

    Article  PubMed  CAS  Google Scholar 

  • Montgomery J, Wittwer CT, Palais R, Zhou L (2007) Simultaneous mutation scanning and genotyping by high-resolution DNA melting analysis. Nat Protoc 2:59–66

    Article  PubMed  CAS  Google Scholar 

  • 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 266:5–43

    Article  Google Scholar 

  • Reed GH, Wittwer CT (2004) Sensitivity and specificity of single-nucleotide polymorphism scanning by high-resolution melting analysis. Clin Chem 50:1748–1754

    Article  PubMed  CAS  Google Scholar 

  • 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 112:1349–1359

    Article  PubMed  CAS  Google Scholar 

  • 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 7:15

  • 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 437–456

  • 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 43:109–116

    Article  PubMed  CAS  Google Scholar 

  • Sosinski B, Verde I, Rokhsar DS (2010) International peach genome initiative peach genome v1.0

  • Stafne ET, Clark JR (2004) Genetic relatedness among eastern North American blackberry cultivars based on pedigree analysis. Euphytica 139:95–104

    Article  Google Scholar 

  • Thompson MM (1995a) Chromosome numbers of Rubus cultivars at the National Clonal Germplasm Repository. HortSci 30:1453–1456

    Google Scholar 

  • Thompson MM (1995b) Chromosome numbers of Rubus species at the National Clonal Germplasm Repository. HortSci 30:1447–1452

    Google Scholar 

  • van Ooijen JW, Voorrips RE (2001) JoinMap(R) 3.0, Software for the calculation of genetic linkage maps. Plant Res Int, Wageningen, The Netherlands

  • 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 42:833–839

    Article  PubMed  CAS  Google Scholar 

  • 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 8:67

    Article  PubMed  Google Scholar 

  • Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78

    Article  PubMed  CAS  Google Scholar 

  • Wittwer CT, Reed GH, Gundry CN, Vandersteen JG, Pryor RJ (2003) High-resolution genotyping by amplicon melting analysis using LCGreen. Clin Chem 49:853–860

    Article  PubMed  CAS  Google Scholar 

  • 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 22:555–563

    Article  CAS  Google Scholar 

  • Woodhead M, Weir A, Smith K, McCallum S, MacKenzie K, Graham J (2010) Functional markers for red raspberry. J Amer Soc Hort Sci 135:418–427

    Google Scholar 

  • 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 27:137–156

    Article  Google Scholar 

Download references

Acknowledgments

This work was part of a Ph.D. thesis and supported in part by the PFR Excellence Program (JMB), the “New Berries” FRST Programme (CO6XO807) (EJB, MJS), PFR funding (MJS), and USDA-ARS Project 1275-21220-185-00D (KSL). The authors would like to thank Jared C. Price of Brigham Young University, Computer Science Department for his assistance with the Rubus genome; the International Peach Genome Initiative for access to the Prunus genome; Dr Ross Crowhurst and Roy Storey of PFR for bioinformatic support; Tony Corbett of PFR for graphic design of all figures; the Editor and two anonymous reviewers for helpful suggestions on the original manuscript. Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by any of the agencies referenced.

Author information

Authors and Affiliations

  1. The New Zealand Institute for Plant & Food Research Limited (PFR), Batchelar Road, Private Bag 11600, Palmerston North, 4442, New Zealand

    J. M. Bushakra, A. N. Atmadjaja, D. Chagné, E. J. Buck & S. E. Gardiner

  2. Institute of Molecular Biosciences, Massey University, Private Bag 11222, Palmerston North, 4442, New Zealand

    J. M. Bushakra & V. V. Symonds

  3. PFR, Old Mill Road, RD3, Motueka, 7198, New Zealand

    M. J. Stephens

  4. USDA-ARS, Genetic Improvement of Fruits and Vegetables Laboratory, Bldg. 010A, BARC-W, 10300 Baltimore Avenue, Beltsville, MD, 20705, USA

    K. S. Lewers

  5. Plant and Wildlife Science Department, Brigham Young University, Provo, UT, 84602, USA

    J. A. Udall

Authors
  1. J. M. Bushakra
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. J. Stephens
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. N. Atmadjaja
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. K. S. Lewers
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. V. V. Symonds
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. J. A. Udall
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. D. Chagné
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. E. J. Buck
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. S. E. Gardiner
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to D. Chagné.

Additional information

Communicated by H. Nybom.

Electronic supplementary material

Below is the link to the electronic supplementary material.

122_2012_1835_MOESM1_ESM.pdf

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

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

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

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

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)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bushakra, J.M., Stephens, M.J., Atmadjaja, A.N. et al. Construction of black (Rubus occidentalis) and red (R. idaeus) raspberry linkage maps and their comparison to the genomes of strawberry, apple, and peach. Theor Appl Genet 125, 311–327 (2012). https://doi.org/10.1007/s00122-012-1835-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-012-1835-5

Keywords

Search

Navigation