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Homologs of the FB_MR5 fire blight resistance gene of Malus ×robusta 5 are present in other Malus wild species accessions

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Abstract

Breeding for fire blight resistance is a major goal of nearly all apple breeding programs worldwide. Resources for resistance can be found in Malus wild species accession such as Malus ×robusta 5 (Mr5) which carries the FB_MR5 CC-NBS-LRR fire blight resistance gene. To study the occurrence of FB_MR5 in other genetic resources of Malus, a total of 394 wild species accessions of three international germplasm collections were screened using the markers CH03e03 and FEM18 that flank the FB_MR5 locus of Mr5. Five accessions exhibited the allele sizes linked to FB_MR5 for both markers. All five accessions belong to the species M. ×robusta (Carrière) Rehder. In addition, several accessions of other closely related Malus wild species amplified the 224 bp fragment linked to FEM18 and a slightly larger fragment for CH03e03. The presence and expression of FB_MR5 and homologs in M. ×robusta and four more accessions were further tested using gene-specific primers. Fragments of identical size could be detected in six different genotypes of M. ×robusta. Sequence analysis revealed the presence of alleles of FB_MR5 in the accessions ‘Korea’ and ‘Leucocarpa’. Homologs of FB_MR5 were found in different accessions of Malus prunifolia and Malus baccata, two Malus species closely related to M. ×robusta. Their functionality is suggested by results obtained by artificial shoot inoculation with the pathogen. Based on the results using the simple sequence repeat (SSR) markers CH03e03 and FEM18, the gene-specific primers and the analysis of the ‘Golden Delicious’ whole genome sequence, we assume that FB_MR5 is a unique gene which most likely evolved from M. baccata as the common ancestor of M. ×robusta and M. prunifolia.

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References

  • Aldwinkle H, Gustafson H, Forsline P (1999) Evaluation of the core subset of the USDA apple germplasm collection for resistance to fire blight. Acta Horticult 489:269–272

    Article  Google Scholar 

  • Bertani G (2004) Lysogeny at mid-twenthieth century: P1, P2, and other experimental systems. J Bateriol 186(3): 595–600

  • Broggini GAL, Woehner T, Fahrentrapp J, Kost TD, Flachowsky H, Peil A, Hanke MV, Richter K, Patocchi A, Gessler C (2014) Engineering fire blight resistance into the apple cultivar 'Gala' using the FB_MR5 CC-NBS-LRR resistance gene of Malus x robusta 5. Plant Biotechnol J 12:728–733

    Article  CAS  PubMed  Google Scholar 

  • Calenge F, Drouet D, Denance C, van de Weg W, Brisset M, Paulin J-P, Durel C-E (2005) Identification of a major QTL together with several minor additive or epistatic QTLs for resistance to fire blight in apple in two related progenies. Theor Appl Genet 111:128–135

    Article  CAS  PubMed  Google Scholar 

  • Doyle J, Doyle J (1987) A rapid DNA isolation procedure for small quantities of fresh leafs. Phytochem Bull 19:11–15

    Google Scholar 

  • Durel C-E, Denancé C, Brisset M-N (2009) Two distinct major QTL for resistance to fire blight co-localize on linkage group 12 in apple genotypes ‘Evereste’ and Malus floribunda clone 821. Genome 52(2):139–147

    Article  CAS  PubMed  Google Scholar 

  • Eldin MAS (2011) Genotypic and phenotypic evaluation of the wild apple collection of the JKI. Martin-Luther-Universität Halle-Wittenberg, pp. 224

  • Emeriewen O, Richter K, Kilian A, Zini E, Hanke M-V, Malnoy M, Peil A (2014) Identification of a major quantitative trait locus for resistance to fire blight in the wild apple species Malus fusca. Mol Breed 34(2):407–419

    Article  CAS  Google Scholar 

  • Emeriewen OF, Richter K, Hanke M-V, Malnoy M, Peil A (2015) The fire blight resistance QTL of Malus fusca (Mfu10) is affected but not broken down by the highly virulent Canadian Erwinia amylovora strain E2002A. Eur J Plant Pathol 141(3):631–635

    Article  Google Scholar 

  • Fahrentrapp J, Broggini G, Kellerhals M, Peil A, Richter K, Zini E, Gessler C (2013) A candidate gene for fire blight resistance in Malus × robusta 5 is coding for a CC–NBS–LRR. Tree Genet Genomes, 1–15

  • Fiala JL (1994) Flowering crabapples: the genus Malus. Timber Press, Portland

    Google Scholar 

  • Fischer M, Fischer C (1999) Evaluation of Malus species and cultivars at the fruit genebank dresden-pillnitz and its use for apple resistance breeding. Genet Resour Crop Evol 46:235–241

    Article  Google Scholar 

  • Flachowsky H, Peil A, Sopanen T, Elo A, Hanke V (2007) Overexpression of BpMADS4 from silver birch (Betula pendula Roth.) induces early-flowering in apple (Malus x domestica Borkh.). Plant Breed 126:137–145

    Article  CAS  Google Scholar 

  • Forsline PL, Aldwinckle HS, Dickson EE, Luby JJ, Hokanson SC (2003) Collection, maintenance, characterization, and utilization of wild apples of Central Asia. Hortic Rev, 1–61

  • Gao ZS, van de Weg WE, Schaart JG, Schouten HJ, Tran DH, Kodde LP, van der Meer IM, van der Geest AHM, Kodde J, Breiteneder H, Hoffmann-Sommergruber K, Bosch D, Gilissen LJWJ (2005) Genomic cloning and linkage mapping of the Mal d 1 (PR-10) gene family in apple (Malus domestica). Theor Appl Genet 111:171–183

    Article  CAS  PubMed  Google Scholar 

  • Gardiner SE, Norelli JL, Silva N, Fazio G, Peil A, Malnoy M, Horner M, Bowatte D, Carlisle C, Wiedow C, Wan Y, Bassett CL, Baldo AM, Celton JM, Richter K, Aldwinckle HS, Bus VG (2012) Putative resistance gene markers associated with quantitative trait loci for fire blight resistance in Malus 'Robusta 5' accessions. BMC Genet 13:25

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gardner RG, Cummins JN, Aldwinckle HS (1980) Inheritance of fire blight resistance in Malus in relation to rootstock breeding. J Am Soc Hortic Sci 105:912–916

    Google Scholar 

  • Ignatov A, Bodishevskaya A (2011) Malus. In: Kole C (ed) Wild crop relatives: genomic and breeding resources. Springer Berlin, Heidelberg, pp 45–64. doi:10.1007/978-3-642-16057-8_3

    Chapter  Google Scholar 

  • Kellerhals M, Szalatnay D, Hunziker K, Duffy B, Nybom H, Afzadi MA, Hofer M, Richter K, Lateur M (2012) European pome fruit genetic resources evaluated for disease resistance. Trees-Struct Funct 26:179–189

    Article  Google Scholar 

  • Khan MA, Duffy B, Gessler C, Patocchi A (2006) QTL mapping of fire blight resistance in apple. Mol Breed 17:299–306

    Article  Google Scholar 

  • Khan M, Durel C-E, Duffy B, Drouet D, Kellerhals M, Gessler C, Patocchi A (2007) Development of molecular markers linked to the 'Fiesta' linkage group 7 major QTL for fire blight resistance and their application for marker-assisted selection. Genome 50:568–577

    Article  CAS  PubMed  Google Scholar 

  • Khan M, Zhao Y, Korban S (2012) Molecular mechanisms of pathogenesis and resistance to the bacterial pathogen Erwinia amylovora, causal agent of fire blight disease in Rosaceae. Plant Mol Biol Report 30:247–260

    Article  CAS  Google Scholar 

  • Korban SS, Ries SM, Klopmeyer MJ, Morrisey JF, Hattermann DR (1988) Genotypic responses of scab-resistant apple cultivars selections to 2 strains of Erwinia amylovora and the inheritance of resistance to fire blight. Ann Appl Biol 113:101–105

    Article  Google Scholar 

  • Kumar S, Bink MCAM, Volz RK, Bus VGM, Chagne D (2012) Towards genomic selection in apple (Malus x domestica Borkh.) breeding programmes: prospects, challenges and strategies. Tree Genet Genomes 8:1–14

    Article  Google Scholar 

  • Le Lezec M, Lecompte P, Laurens F, Michelesi JC (1997) Sensibilite varietale au feu bacterien (1re partie). L’Arboriculture Fruitiere 503:57–62

    Google Scholar 

  • Le Roux P-M, Khan M, Broggini B, Duffy C, Gessler C, Patocchi A (2010) Mapping of quantitative trait loci for fire blight resistance in the apple cultivars 'Florina' and 'Nova Easygro'. Genome 53:710–722

    Article  PubMed  Google Scholar 

  • Milčevičová R, Gosch C, Halbwirth H, Stich K, Hanke M-V, Peil A, Flachowsky H, Rozhon W, Jonak C, Oufir M, Hausman JF, Matušíková I, Fluch S, Wilhelm E (2010) Erwinia amylovora-induced defense mechanisms of two apple species that differ in susceptibility to fire blight. Plant Sci 179:60–67

    Article  Google Scholar 

  • Parravicini G, Gessler C, Denancé C, Lasserre-Zuber P, Vergne E, Brisset M-N, Patocchi A, Durel C-E, Broggini GAL (2011) Identification of serine/threonine kinase and nucleotide-binding site–leucine-rich repeat (NBS-LRR) genes in the fire blight resistance quantitative trait locus of apple cultivar ‘Evereste’. Mol Plant Pathol 12(5):493–505

    Article  CAS  PubMed  Google Scholar 

  • Peil A, Garcia-Libreros T, Richter K, Trognitz F, Trognitz B, Hanke M-V, Flachowsky H (2007) Strong evidence for a fire blight resistance gene of Malus robusta located on linkage group 3 detected by rapid genome scanning. Plant Breed 126:470–476

    Article  CAS  Google Scholar 

  • Peil A, Richter K, Garcia-Libreros T, Hanke V, Flachowsky H, Celton J-M, Horner M, Gardiner S, Bus V (2008) Confirmation of the fire blight QTL of Malus × robusta 5 on linkage group 3. Acta Horticult 793:297–303

    Article  CAS  Google Scholar 

  • Peil A, Hanke M-V FH, Richter K, Rode J (2011) Inoculation of Malus × robusta 5 progeny with a strain breaking the resistance to fire blight reveals a minor QTL on LG5. Acta Horticult 896:357–362

    Article  Google Scholar 

  • SAS (2010) Administering SAS® EnterpriseGuide® 4.3.SAS Institute Inc. Cary, NC

  • Velasco R, Zharkikh A, Affourtit J, Dhingra A, Cestaro A, Kalyanaraman A, Fontana P, Bhatnagar SK, Troggio M, Pruss D et al (2010) The genome of the domesticated apple (Malus x domestica Borkh.). Nat Genet 42:833–839

    Article  CAS  PubMed  Google Scholar 

  • Vogt I, Wohner T, Richter K, Flachowsky H, Sundin GW, Wensing A, Savory EA, Geider K, Day B, Hanke MV, Peil A (2013) Gene-for-gene relationship in the host-pathogen system Malus × robusta 5-Erwinia amylovora. New Phytol 197:1262–1275

    Article  CAS  PubMed  Google Scholar 

  • Watkins R (1971) Apple rootstocks. Ann Rep East Malling Res Stat for 1970(93):97–98

    Google Scholar 

  • Wöhner T, Eldin AM, Peil A (2014a) Malus × robusta, JKI Data Sheets-Fruit Varieties 1. doi:10.5073/jkidfv.2014.001

  • Wöhner TW, Flachowsky H, Richter K, Garcia-Libreros T, Trognitz F, Hanke MV, Peil A (2014b) QTL mapping of fire blight resistance in Malus × robusta 5 after inoculation with different strains of Erwinia amylovora. Mol Breed 34:217–230

    Article  Google Scholar 

Download references

Acknowledgments

We gratefully acknowledge Gennaro Fazio from the National Germplasm Repository Geneva, New York (USA), and Edward Zurawicz from the Institute of Pomology and Floriculture, Skierniewice (Poland), for sharing bud wood of different accessions of Malus ×robusta. We are also grateful to S. Bartsch, K. Neumann, and N. Richelhof for technical assistance. This work was supported by the Deutsche Forschungsgemeinschaft (DFG), project numbers AOBJ 574457 and AOBJ 611951.

Data archiving statement

Ten homolog nucleotide sequences of the fire blight resistance gene FB_MR5 of Malus ×robusta 5 from different Malus wild species were submitted. The accession numbers and a description of the submitted data are listed in Table S2. All sequence data were deposited with the DNA Data Bank of Japan (DDBJ), European Molecular Biology Laboratory (EMBL/EBI) Nucleotide Sequence Database and GenBank (National Center for Biotechnology Information).

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Authors and Affiliations

  1. Julius Kühn-Institut, Institute for Breeding Research on Fruit Crops, Pillnitzer Platz 3a, D-01326, Dresden, Germany

    Thomas Wöhner, Andreas Peil, Magda-Viola Hanke & Henryk Flachowsky

  2. Medical Theoretical Center (MTZ), Experimental Center, Faculty of Medicine Carl Gustav Carus, Technical University Dresden, Fiedlerstr. 42, 01307, Dresden, Germany

    Erik Szentgyörgyi

  3. Julius Kühn-Institut, Institute for Resistance Research and Stress Tolerance, Erwin-Baur-Str. 27, D-06484, Quedlinburg, Germany

    Klaus Richter

Authors
  1. Thomas Wöhner
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  2. Erik Szentgyörgyi
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  3. Andreas Peil
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  4. Klaus Richter
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  5. Magda-Viola Hanke
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  6. Henryk Flachowsky
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Corresponding author

Correspondence to Henryk Flachowsky.

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Communicated by D. Chagné

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Table S1

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Table S2

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Wöhner, T., Szentgyörgyi, E., Peil, A. et al. Homologs of the FB_MR5 fire blight resistance gene of Malus ×robusta 5 are present in other Malus wild species accessions. Tree Genetics & Genomes 12, 2 (2016). https://doi.org/10.1007/s11295-015-0962-y

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  • DOI: https://doi.org/10.1007/s11295-015-0962-y

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