Theoretical and Applied Genetics

, Volume 129, Issue 6, pp 1191–1201 | Cite as

FaRXf1: a locus conferring resistance to angular leaf spot caused by Xanthomonas fragariae in octoploid strawberry

  • Jack A. Roach
  • Sujeet Verma
  • Natalia A. Peres
  • Andrew R. Jamieson
  • W. Eric van de Weg
  • Marco C. A. M. Bink
  • Nahla V. Bassil
  • Seonghee Lee
  • Vance M. Whitaker
Original Article


Key message

Angular leaf spot is a devastating bacterial disease of strawberry. Resistance from two wild accessions is highly heritable and controlled by a major locus on linkage group 6D.


Angular leaf spot caused by Xanthomonas fragariae is the only major bacterial disease of cultivated strawberry (Fragaria ×ananassa). While this disease may cause reductions of up to 8 % of marketable yield in Florida winter annual production, no resistant cultivars have been commercialized. Wild accessions US4808 and US4809 were previously identified as resistant to the four genetic clades of X. fragariae, and introgression of the trait into commercial quality perennial-type germplasm was initiated. Previous reports indicated high heritability for the trait but proposed both single-locus and multi-locus inheritance models. The objective of this study was to determine the mode of inheritance of resistance, to identify causal loci, and to begin introgression of resistance into Florida-adapted germplasm. Resistance was observed in two years of field trials with inoculated plants that assayed four full-sib families descended from US4808 to US4809. Resistance segregated 1:1 in all families indicating control by a dominant allele at a single locus. Using a selective genotyping approach with the IStraw90 Axiom® SNP array and pedigree-based QTL detection, a single major-effect QTL was identified in two full-sib families, one descended from each resistant accession. High-resolution melt curve analysis validated the presence of the QTL in separate populations. The QTL was delimited to the 33.1–33.6 Mbp (F. vesca vesca v1.1 reference) and 34.8–35.3 Mbp (F. vesca bracteata v2.0 reference) regions of linkage group 6D for both resistance sources and was designated FaRXf1. Characterization of this locus will facilitate marker-assisted selection toward the development of resistant cultivars.


Selective Genotyping Angular Leaf Spot Diseased Leaf Area Resistant Progeny Overhead Irrigation 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



The authors acknowledge Tomas Hasing, Dr. James Mertely, and Teresa Seijo for their assistance and guidance. This work was funded in part by the National Institute of Food and Agriculture, U.S. Department of Agriculture Specialty Crop Research Initiative project “RosBREED: Combining disease resistance with horticultural quality in new rosaceous cultivars” under award No 2014-51181-22378.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

122_2016_2695_MOESM1_ESM.pdf (65 kb)
Supplementary material 1 (PDF 65 kb)
122_2016_2695_MOESM2_ESM.pdf (453 kb)
Supplementary material 2 (PDF 452 kb)
122_2016_2695_MOESM3_ESM.pdf (125 kb)
Supplementary material 3 (PDF 125 kb)


  1. Bassil NV, Davis TM, Zhang H, Ficklin S, Mittmann M, Webster T, Mahoney L, Wood D, Alperin ES, Rosyara UR, Koehorst-vanc Putten H, Monfort A, Sargent DJ, Amaya I, Denoyes B, Bianco L, van Dijk T, Pirani A, Iezzoni A, Main D, Peace C, Yang Y, Whitaker V, Verma S, Bellon L, Brew F, Herrera R, van de Weg WE (2015) Development and preliminary evaluation of a 90 K Axiom® SNP array for the allo-octoploid cultivated strawberry Fragaria ×ananassa. BMC Genom 16:155CrossRefGoogle Scholar
  2. Bink MCAM, Uimari P, Sillanpaa J, Janss LLG, Jansen RC (2002) Multiple QTL mapping in related plant populations via a pedigree-analysis approach. Theor Appl Genet 104:751–762CrossRefPubMedGoogle Scholar
  3. Bink MCAM, Boer MP, ter Braak CJF, Jansen J, Voorrips RE, van de Weg WE (2008) Bayesian analysis of complex traits in pedigreed plant populations. Euphytica 161:85–96CrossRefGoogle Scholar
  4. Bink MCAM, Jansen J, Madduri M, Voorrips RE, Durel CE, Kouassi AB, Laurens F, Mathis F, Gessler C, Gobbin D, Rezzonico F, Patocchi A, Kellerhals M, Boudichevskaia A, Dunemann F, Peil A, Nowicka A, Lata B, Stankiewicz-Kosyl M, Jeziorek K, Pitera E, Soska A, Tomala K, Evans KM, Fernandez-Fernandez F, Guerra W, Korbin M, Keller S, Lewandowski M, Plocharski W (2014) Baysian QTL analyses using pedigreed families of an outcrossing species, with application to fruit firmness in apple. Theor Appl Genet 127:1073–1090PubMedGoogle Scholar
  5. CABI/EPPO (1997) Quarantine pests for Europe. Smith IM, McNamara DG, Scott PR, Holderness M (eds), 2nd edn. CABI International, WallingfordGoogle Scholar
  6. Clark MD, Schmitz CA, Rosyara UR, Luby JJ, Bradeen JM (2014) A consensus ‘Honeycrisp’ apple (Malus × domestica) genetic linkage map from three full-sib progeny populations. Tree Genet Genomes 10:627–639CrossRefGoogle Scholar
  7. Darvasi A, Soller M (1992) Selective genotyping for determination of linkage between a marker locus and a quantitative trait locus. Theor Appl Genet 85:353–359PubMedGoogle Scholar
  8. de Mendiburu F (2010) Agricolae: statistical procedures for agricultural research using R (Online) Accessed date 16 Oct 2015
  9. Epstein AH (1966) Angular leaf spot of strawberry. Plant Dis Report 50:167Google Scholar
  10. Guan Y, Peace C, Rudell Dm Verma S, Even K (2015) QTLs detected for individual sugars and soluble solids content in apple. Mol Breed 35:135CrossRefGoogle Scholar
  11. Hartung JS, Gouin CC, Lewers KS, Maas JL, Hokanson S (2003) Identification of sources of resistance to bacterial angular leafspot disease of strawberry. Acta Hortic 626:155–159CrossRefGoogle Scholar
  12. Haymes KM (1996) Mini-prep method suitable for a plant breeding program. Plant Mol Biol Report 14:280–284CrossRefGoogle Scholar
  13. Hildebrand PD, Braun PG, Renderos WE, Jamieson AR, McRae KB, Binns MR (2005) A quantitative method for inoculating strawberry leaves with Xanthomonas fragariae, factors affecting infection, and cultivar reactions. Can J Plant Pathol 27:16–24CrossRefGoogle Scholar
  14. Jamieson AR, Hildebrand PD, Renderos WE (2013) Breeding strawberry plants resistant to angular leaf spot disease. Int J Fruit Sci 13:28–35CrossRefGoogle Scholar
  15. Jamieson AR, Hildebrand PD, Renderos WE, Fillmore SAE (2014) Resistance to angular leafspot disease of strawberry: influence of seedling age. Acta Hortic 1049:187–192CrossRefGoogle Scholar
  16. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Mentjies P, Drummond A (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649CrossRefPubMedPubMedCentralGoogle Scholar
  17. Kennedy BW, King TH (1960) Angular leafspot, a new disease of strawberry. Phytopathology 50:641–642Google Scholar
  18. Kennedy BW, King TH (1962a) Angular leaf spot of strawberry caused by Xanthomonas fragariae sp. nov. Phytopathology 52:873–875Google Scholar
  19. Kennedy BW, King TH (1962b) Studies on epidemiology of bacterial angular leafspot on strawberry. Plant Dis Report 46:360–363Google Scholar
  20. Koike H (1965) The aluminum-cap method for testing sugarcane varieties against leaf scald disease. Phytopathology 55:317–319Google Scholar
  21. Lebowitz RJ, Soller M, Beckmann JS (1987) Trait-based analyses for the detection of linkage between marker loci and quantitative trait loci in crosses between inbred lines. Theor Appl Genet 73:556–562CrossRefPubMedGoogle Scholar
  22. Lewers KS, Maas JL, Hokanson SC, Gouin C, Hartung JS (2003) Inheritance of resistance in strawberry to bacterial angular leafspot disease caused by Xanthomonas fragariae. J Amer Soc Hortic Sci 128:209–212Google Scholar
  23. 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 25:2078–2079CrossRefPubMedPubMedCentralGoogle Scholar
  24. Maas JL (1984) Compendium of strawberry diseases. American Phytopathological Society, St. PaulGoogle Scholar
  25. Maas JL, Gouin-Behe C, Hartung JS, Hokanson SC (2000) Sources of resistance for two differentially pathogenic strains of Xanthomonas fragariae in Fragaria genotypes. HortScience 35:128–131Google Scholar
  26. Maas JL, Gouin CC, Hokanson SC, Hartung JS (2002) Strawberry parent clones US 4808 and US 4809 resistant to bacterial angular leafspot disease caused by Xanthomonas fragariae. HortScience 37:716–717Google Scholar
  27. Mertely J, Seijo T, Martin R, Moore DN, Peres NA (2010) Evaluation of products for angular leaf spot control in annual strawberry, 2009–10. Plant Dis Manag Rep 4:SMF052Google Scholar
  28. R Core Team (2013) R: a language and environment for statistical computer. R Foundation for Statistical Computing, Vienna. Accessed 15 Mar 2015
  29. Pooler MR, Ritchie DF, Hartung JS (1996) Genetic relationships among strains of Xanthomonas fragariae based on random amplified polymorphic DNA PCR, repetitive extragenic palindromic PCR, and enterobacterial repetitive intergenic consensus PCR data and generation of multiplexed PCR primers useful for identification of this phytopathogen. Appl Environ Microbiol 62:3121–3127PubMedPubMedCentralGoogle Scholar
  30. Roberts PD, Jones JB, Chandler CK, Stall RE, Berger RE (1996) Survival of Xanthomonas fragariae on strawberry in summer nurseries in Florida detected by specific primers and nested polymerase chain reaction. Plant Dis 80:1283–1288CrossRefGoogle Scholar
  31. Roberts PD, Berger RD, Jones JB, Chandler CK, Stall RE (1997) Disease progress, yield loss, and control of Xanthomonas fragariae on strawberry plants. Plant Dis 81:917–921CrossRefGoogle Scholar
  32. Roberts PD, Hodge NC, Bouzar H, Jones JB, Stall RE, Berger RD, Chase AR (1998) Relatedness of strains of Xanthomonas fragariae by restriction fragment length polymorphism, DNA-DNA reassociation, and fatty acid analyses. Appl Environ Microbiol 64:3961–3965PubMedPubMedCentralGoogle Scholar
  33. Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132:365–386PubMedGoogle Scholar
  34. Seijo T, Mertely J, Whitaker VM, Peres NA (2012) Evaluation of strawberry cultivars and advanced selections for resistance to anthracnose and Botrytis fruit rots and angular leaf spot, 2011–12. Plant Dis Manag Rep 6:SMF034Google Scholar
  35. 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 JM, Rees DJ, Williams KP, Holt SH, Ruiz Rojas JJ, Chatterjee M, Liu B, Silva H, Meisel L, Adato A, Filichkin SA, Troggio M, Viola R, Ashman TL, Wang H, Dharmawardhana P, Elser J, Raja R, Priest HD, Bryant DW Jr, Fox SE, Givan SA, Wilhelm LJ, Naithani S, Christoffels A, Salama DY, Carter J, Lopez Girona E, 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 43:109–116CrossRefPubMedPubMedCentralGoogle Scholar
  36. Tennessen JA, Govindarajulu R, Ashman T-L, Liston A (2014) Evolutionary origins and dynamics of octoploid strawberry subgenomes revealed by dense targeted capture linkage maps. Genome Biol Evol 6:3295–3313CrossRefPubMedGoogle Scholar
  37. Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG (2012) Primer3—new capabilities and interfaces. Nucl Acids Res 40:e115CrossRefPubMedPubMedCentralGoogle Scholar
  38. Van Ooijen JW (2006) JoinMap 4, software for the calculation of genetic linkage maps in experimental populations. Wageningen, Kyazma BVGoogle Scholar
  39. Van Ooijen JW (2011) Multipoint maximum likelihood mapping in a full-sib family of an outbreeding species. Genet Res 93:343–349CrossRefGoogle Scholar
  40. Welz HG, Schechert A, Pernet A, Pixley KV, Geiger HH (1998) A gene for resistance to the maize streak virus in the African CIMMYT maize inbred line CML202. Mol Breed 4:147–154CrossRefGoogle Scholar
  41. Whitaker VM, Chandler CK, Peres N, do Nascimento Nunes MC, Plotto A, Sims CA, Plotto A, Sims CA (2015) Sensation™ ‘Florida127’ strawberry. HortScience 50:1088–1091Google Scholar
  42. Wu TD, Nacu S (2010) Fast and SNP-tolerant detection of complex variants and splicing in short reads. Bioinformatics 26:873–881CrossRefPubMedPubMedCentralGoogle Scholar
  43. Wu TD, Watanabe CK (2005) GMAP: a genomic mapping and alignment program for mRNA and EST sequences. Bioinformatics 21:1859–1875CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Jack A. Roach
    • 1
  • Sujeet Verma
    • 1
  • Natalia A. Peres
    • 2
  • Andrew R. Jamieson
    • 3
  • W. Eric van de Weg
    • 4
  • Marco C. A. M. Bink
    • 5
  • Nahla V. Bassil
    • 6
  • Seonghee Lee
    • 1
  • Vance M. Whitaker
    • 1
  1. 1.Department of Horticultural Science, IFAS Gulf Coast Research and Education CenterUniversity of FloridaWimaumaUSA
  2. 2.Department of Plant Pathology, IFAS Gulf Coast Research and Education CenterUniversity of FloridaWimaumaUSA
  3. 3.Atlantic Food and Horticulture Research Centre, Agriculture and Agri-Food CanadaKentvilleCanada
  4. 4.Wageningen UR Plant BreedingWageningenThe Netherlands
  5. 5.Biometris, Wageningen University and Research CentreWageningenThe Netherlands
  6. 6.USDA-ARS, National Clonal Germplasm RepositoryCorvallisUSA

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