Molecular Breeding

, Volume 31, Issue 2, pp 429–440 | Cite as

Genetic and physical characterisation of the locus controlling columnar habit in apple (Malus × domestica Borkh.)

  • Paolo BaldiEmail author
  • Pieter Jacobus Wolters
  • Matteo Komjanc
  • Roberto Viola
  • Riccardo Velasco
  • Silvio Salvi


A better understanding of the genetic control of tree architecture would potentially allow improved tailoring of newly bred apple cultivars in terms of field management aspects, such as planting density, pruning, pest control and disease protection. It would also have an indirect impact on yield and fruit quality. The Columnar (Co) locus strongly suppresses lateral branch elongation and is the most important genetic locus influencing tree architecture in apple. Co has previously been mapped on apple linkage group (LG) 10. In order to obtain fine mapping of Co, both genetically and physically, we have phenotypically analysed and screened three adult segregating experimental populations, with a total of 301 F1 plants, and one substantial 3-year old population of 1,250 F1 plants with newly developed simple sequence repeat (SSR) markers, based on the ‘Golden delicious’ apple genome sequence now available. Co was found to co-segregate with SSR marker Co04R12 and was confined in a region of 0.56 cM between SSR markers Co04R11 and Co04R13, corresponding to 393 kb on the ‘Golden delicious’ genome sequence. In this region, 36 genes were predicted, including at least seven sequences potentially belonging to genes that could be considered candidates for involvement in control of shoot development. Our results provide highly reliable, virtually co-segregating markers that will facilitate apple breeding aimed at modifications of the tree habit and lay the foundations for the cloning of Co.


Tree architecture Fine mapping Co locus Growth habit 



The authors would like to thank Dr. Pierluigi Magnago for his most essential contribution in developing the segregating populations and Luca Pinelli for his technical help.

Supplementary material

11032_2012_9800_MOESM1_ESM.docx (19 kb)
Supplementary material 1 (DOCX 18 kb)


  1. Aida M, Ishida T, Fukaki H, Fujisawa H, Tasaka M (1997) Genes involved in organ separation in Arabidopsis: an analysis of the cup-shaped cotyledon Mutant. Plant Cell 9:841–857PubMedCrossRefGoogle Scholar
  2. Bai T, Zhu Y, Fernández-Fernández F, Keulemans J, Brown S, Xu K (2012) Fine genetic mapping of the Co locus controlling columnar growth habit in apple. Mol Genet Genomics 287:437–450PubMedCrossRefGoogle Scholar
  3. Burge C, Karlin S (1997) Prediction of complete gene structures in human genomic DNA. J Mol Biol 268:78–94PubMedCrossRefGoogle Scholar
  4. Busov VB, Johannes E, Whetten RW, Sederoff RR, Spiker SL, Lanz-Garcia C, Goldfarb B (2004) An auxin-inducible gene from loblolly pine (Pinus taeda L.) is differentially expressed in mature and juvenile-phase shoots and encodes a putative transmembrane protein. Planta 218:916–927PubMedCrossRefGoogle Scholar
  5. Chagné D, Carlisle CM, Blond C, Volz RK, Whitworth CJ, Oraguzie NC, Crowhurst RN, Allan AC, Espley RV, Hellens RP, Gardiner SE (2007) Mapping a candidate gene (MdMYB10) for red flesh and foliage colour in apple. BMC Genomics 8:212PubMedCrossRefGoogle Scholar
  6. Conner PJ, Brown SK, Weeden NF (1997) Randomly amplified polymorphic DNA-based genetic linkage maps of three apple cultivars. J Am Soc Hortic Sci 122:350–359Google Scholar
  7. Cook DR, Varshney RK (2010) From genome studies to agricultural biotechnology: closing the gap between basic plant science and applied agriculture. Curr Opin Plant Biol 13:115–118PubMedCrossRefGoogle Scholar
  8. Czemmel S, Stracke R, Weisshaar B, Cordon N, Harris NN, Walker AR, Robinson SP, Bogs J (2009) The grapevine R2R3-MYB transcription factor VvMYBF1 regulates flavonol synthesis in developing grape berries. Plant Physiol 151:1513–1530PubMedCrossRefGoogle Scholar
  9. De Wit I, Cook NC, Keulemans J (2004) Characterization of tree architecture in two-year-old apple seedling populations of different rogenies with a common columnar gene parent. Acta Hortic 663:363–368Google Scholar
  10. Doligez A, Adam-Blondon AF, Cipriani G, Di Gaspero G, Laucou V, Merdinoglu D, Meredith CP, Riaz S, Roux C, This P (2006) An integrated SSR map of grapevine based on five mapping populations. Theor Appl Genet 113:369–382PubMedCrossRefGoogle Scholar
  11. Feller A, Machemer K, Braun EL, Grotewold E (2011) Evolutionary and comparative analysis of MYB and bHLH plant transcription factors. Plant J 66:94–116PubMedCrossRefGoogle Scholar
  12. Fisher DV (1970) Spur strains of McIntosh discovered in British Columbia. Can Fruit Var Hortic Digest 24:27–32Google Scholar
  13. Flachowsky H, Hättasch C, Höfer M, Peil A, Hanke MV (2010) Overexpression of LEAFY in apple leads to a columnar phenotype with shorter internodes. Planta 231:251–263PubMedCrossRefGoogle Scholar
  14. Galli P, Broggini GAL, Gessler C, Patocchi A (2010) High-resolution genetic map of the Rvi15 (Vr2) apple scab resistance locus. Mol Breed 26:561–572CrossRefGoogle Scholar
  15. Guo M, Thomas J, Collins G, Timmermans MCP (2008) Direct repression of KNOX loci by the ASYMMETRIC LEAVES1 complex of Arabidopsis. Plant Cell 20:48–58PubMedCrossRefGoogle Scholar
  16. Hemmat M, Weeden NF, Conner PJ, Brown SK (1997) A DNA marker for columnar growth habit in apple contains a simple sequence repeat. J Am Soc Hortic Sci 122:347–349Google Scholar
  17. Janick J, Cummins JN, Brown SK, Hemmat M (1996) Apples. In: Janick J, Moore JN (eds) Fruit breeding: tree and tropical fruits. Wiley, London, pp 1–77Google Scholar
  18. Kelsey DF, Brown SK (1992) ‘McIntosh Wijick’: a columnar mutation of ‘McIntosh’ apple proving useful in physiology and breeding research. Fruit Var 46:83–87Google Scholar
  19. Kenis K, Keulemans J (2004) QTL analysis of growth characteristics in apple. Acta Hortic 663:369–374Google Scholar
  20. Kenis K, Keulemans J (2007) Study of tree architecture of apple (Malus × domestica Borkh.) by QTL analysis of growth traits. Mol Breed 19:193–208CrossRefGoogle Scholar
  21. Khan MA, Durel CE, 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 50:568–577PubMedCrossRefGoogle Scholar
  22. Kim MY, Song KJ, Hwang J-H, Shin YU, Lee HJ (2003) Development of RAPD and SCAR markers linked to the Co gene conferring columnar growth habit in apple (Malus pumila Mill.). J Hortic Sci Biotechnol 78:512–517Google Scholar
  23. Kitomi Y, Ito H, Hobo T, Aya K, Kitano H, Inukai Y (2011) The auxin responsive AP2/ERF transcription factor CROWN ROOTLESS5 is involved in crown root initiation in rice through the induction of OsRR1, a type-A response regulator of cytokinin signaling. Plant J 67:472–484PubMedCrossRefGoogle Scholar
  24. Lapins KO (1974) Spur type growth habit in 60 apple progenies. J Am Soc Hortic Sci 99:568–572Google Scholar
  25. Lapins KO (1976) Inheritance of compact growth type in apple. J Am Soc Hortic Sci 101:33–135Google Scholar
  26. Lauri PE, Lespinasse JM (1993) The relationship between cultivar fruiting type and fruiting branch characteristics in apple trees. Acta Hortic 349:259–263Google Scholar
  27. Lee S, Lee S, Yang KY, Kim YM, Park SY, Kim SY, Soh MS (2006) Overexpression of PRE1 and its homologous genes activates Gibberellin-dependent responses in Arabidopsis thaliana. Plant Cell Physiol 47:591–600PubMedCrossRefGoogle Scholar
  28. Lespinasse Y (1992) Le pommier. In: Gallais A, Bannerot H (eds) Amélioration des espèces végétales cultivées, objectifs et critères de sélection. INRA Editions, Paris, pp 579–594Google Scholar
  29. Lespinasse JM, Delort JF (1986) Apple tree management in vertical axis: appraisal after ten years of experiments. Acta Hortic 160:139–155Google Scholar
  30. Liebhard R, Koller B, Gianfranceschi L, Gessler C (2003) Creating a saturated reference map for the apple (Malus x domestica Borkh.) genome. Theor Appl Genet 106:1497–1508PubMedGoogle Scholar
  31. Moriya S, Iwanami H, Kotoda N, Takahashi S, Yamamoto T, Abe K (2009) Development of a marker-assisted selection system for columnar growth habit in apple breeding. J Jpn Soc Hortic Sci 78:279–287CrossRefGoogle Scholar
  32. Moriya S, Okada K, Haji T, Yamamoto T, Abe K (2012) Fine mapping of Co, a gene controlling columnar growth habit located on apple (Malus x domestica Borkh.) linkage group 10. Plant Breed 131:641–646CrossRefGoogle Scholar
  33. Patocchi A, Vinatzer BA, Gianfranceschi L, Tartarini S, Zhang HB, Sansavini S, Gessler C (1999) Construction of a 550 kb BAC contig spanning the genomic region containing the apple scab resistance gene Vf. Mol Gen Genet 262:884–891PubMedCrossRefGoogle Scholar
  34. Sablowski RW, Meyerowitz EM (1998) A homolog of NO APICAL MERISTEM is an immediate target of the floral homeotic genes APETALA3/PISTILLATA. Cell 92:93–103PubMedCrossRefGoogle Scholar
  35. Schuelke M (2000) An economic method for the fluorescent labelling of PCR fragments. Nat Biotechnol 18:233–234PubMedCrossRefGoogle Scholar
  36. Silfverberg-Dilworth E, Matasci CL, Van de Weg WE, Van Kaauwen MPW, Walser M, Kodde LP, Soglio V, Gianfranceschi L, Durel CE, Costa F, Yamamoto T, Koller B, Gessler C, Patocchi A (2006) Microsatellite markers spanning the apple (Malus x domestica Borkh.) genome. Tree Genet Genomics 2:202–224CrossRefGoogle Scholar
  37. Souer E, van Houwelingen A, Kloos D, Mol J, Koes R (1996) The no apical meristem gene of Petunia is required for pattern formation in embryos and flowers and is expressed at meristem and primordia boundaries. Cell 85:159–170PubMedCrossRefGoogle Scholar
  38. Stanke M, Steinkamp R, Waack S, Morgenstern B (2004) AUGUSTUS: a web server for gene finding in eukaryotes. Nucleic Acids Res 32:309–312CrossRefGoogle Scholar
  39. Suresh BM, Hampapathalu AN (2007) IMEx: imperfect microsatellite extractor. Bioinformatics 23:1181–1187CrossRefGoogle Scholar
  40. Tani E, Tsaballa A, Stedel C, Kalloniati C, Papaefthimiou D, Polidoros A, Darzentas N, Ganopoulos I, Flemetakis E, Katinakis P, Tsaftaris A (2011) The study of a SPATULA-like bHLH transcription factor expressed during peach (Prunus persica) fruit development. Plant Physiol Biochem 49:654–663PubMedCrossRefGoogle Scholar
  41. Tao Q, Wang A, Zhang HB (2002) One large-insert plant-transformation-competent BIBAC library and three BAC libraries of Japonica rice for genome research in rice and other grasses. Theor Appl Genet 105:1058–1066PubMedCrossRefGoogle Scholar
  42. Tian YK, Wang CH, Zhang JS, James C, Dai HY (2005) Mapping Co, a gene controlling the columnar phenotype of apple, with molecular markers. Euphytica 145:181–188CrossRefGoogle Scholar
  43. Tobutt KR (1985) Breeding columnar apples at East Malling. Acta Hortic 159:63–68Google Scholar
  44. Troggio M, Gleave A, Salvi S, Chagné D, Cestaro A, Kumar S, Crowhurst RN, Gardiner SE (2012) Apple, from genome to breeding. Tree Genet Genomics 8(3):509–529CrossRefGoogle Scholar
  45. Van Ooijen JW, Voorrips RE (2001) JoinMap 3.0. Software for the calculation of genetic linkage maps. Plant Research International, WageningenGoogle Scholar
  46. 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, Chagné D, Crowhurst RN, Gleave AP, Lavezzo E, Fawcett JA, Proost S, Rouzé P, Sterck L, Toppo S, Lazzari B, Hellens RP, Durel CE, 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 x domestica Borkh.). Nat Genet 42:833–839PubMedCrossRefGoogle Scholar
  47. Vezzulli S, Troggio M, Coppola G, Jermakow A, Cartwright D, Zharkikh A, Stefanini M, Grando MS, Viola R, Adam-Blondon AF, Thomas M, This P, Velasco R (2008) A reference integrated map for cultivated grapevine (Vitis vinifera L.) from three crosses, based on 283 SSR and 501 SNP-based markers. Theor Appl Genet 117:499–511PubMedCrossRefGoogle Scholar
  48. Xie Q, Frugis G, Colgan D, Chua NH (2000) Arabidopsis NAC1 transduces auxin signal downstream of TIR1 to promote lateral root development. Genes Dev 14:3024–3036PubMedCrossRefGoogle Scholar
  49. Yamagishi K, Tatematsu K, Yano R, Preston J, Kitamura S, Takahashi H, McCourt P, Kamiya Y, Nambara E (2009) CHOTTO1, a double AP2 domain protein of Arabidopsis thaliana, regulates germination and seedling growth under excess supply of glucose and nitrate. Plant Cell Physiol 50:330–340PubMedCrossRefGoogle Scholar
  50. Yano R, Kanno Y, Jikumaru Y, Nakabayashi K, Kamiya Y, Nambara E (2009) CHOTTO1, a putative double APETALA2 repeat transcription factor, is involved in abscisic acid-mediated repression of gibberellin biosynthesis during seed germination in Arabidopsis. Plant Physiol 151:641–654PubMedCrossRefGoogle Scholar
  51. Zhang YG, Dai HY (2011) Comparison of photosynthetic and morphological characteristics, and microstructure of roots and shoots, between columnar apple and standard apple trees of hybrid seedlings. PHYTON 80:119–125Google Scholar
  52. Zhang W, Sun Y, Timofejeva L, Chen C, Grossniklaus U, Ma H (2006) Regulation of Arabidopsis tapetum development and function by DYSFUNCTIONAL TAPETUM1 (DYT1) encoding a putative bHLH transcription factor. Development 133:3085–3095PubMedCrossRefGoogle Scholar
  53. Zhang Y, Cao G, Qu LJ, Gu H (2009) Characterization of Arabidopsis MYB transcription factor gene AtMYB17 and its possible regulation by LEAFY and AGL15. J Genet Genomics 36:99–107PubMedCrossRefGoogle Scholar
  54. Zhu YD, Zhang W, Li GC, Wang T (2007) Evaluation of inter-simple sequence repeat analysis for mapping the Co gene in apple (Malus pumila Mill.). J Hortic Sci Biotechnol 82:371–376Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2012

Authors and Affiliations

  • Paolo Baldi
    • 1
    Email author
  • Pieter Jacobus Wolters
    • 1
  • Matteo Komjanc
    • 1
  • Roberto Viola
    • 1
  • Riccardo Velasco
    • 1
  • Silvio Salvi
    • 1
    • 2
  1. 1.IASMA Research and Innovation Center, Fondazione Edmund MachSan Michele all’AdigeItaly
  2. 2.Faculty of AgricultureUniversity of BolognaBolognaItaly

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