Skip to main content
Log in

The columnar mutation (“Co gene”) of apple (Malus × domestica) is associated with an integration of a Gypsy-like retrotransposon

  • Published:
Molecular Breeding Aims and scope Submit manuscript

Abstract

The columnar growth habit of apple trees (Malus × domestica Borkh.) is a unique plant architecture phenotype that arose as a bud sport mutation of a McIntosh tree in the 1960s. The mutation (“Co gene”) led to trees (McIntosh Wijcik) with thick, upright main stems and short internodes that generate short fruit spurs instead of long lateral branches. Although Co has been localized to chromosome 10, in a region approximately between 18.5 and 19 Mb, its molecular nature is unknown. In a classical positional cloning approach in combination with the analysis of NGS data, we cloned and analyzed the Co region. Our results show that the insertion of a Ty3/Gypsy retrotransposon into a non-coding region at position 18.8 Mb is the only detectable genomic difference between McIntosh and McIntosh Wijcik and is found in all columnar cultivars. The genetic effect of the insertion is unclear; however, Illumina® RNA-seq data of McIntosh and McIntosh Wijcik suggest that the columnar growth habit is associated with differential expression of the retrotransposon transcript, causing changes in the expression levels of many protein coding genes. The mechanism by which the Gypsy retrotransposon is involved in generating the columnar habit is not yet clear; our findings form the basis for tackling this question.

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

Access this article

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

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(3):403–410. doi:10.1006/jmbi.1990.9999S0022-2836(05)80360-2

    CAS  PubMed  Google Scholar 

  • Asíns MJ, Monforte AJ, Mestre PF, Carbonell EA (1999) Citrus and Prunuscopia-like retrotransposons. Theor Appl Genet 99(3–4):503–510. doi:10.1007/s001220051263

    Article  PubMed  Google Scholar 

  • 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(5):437–450. doi:10.1007/s00438-012-0689-5

    Article  CAS  PubMed  Google Scholar 

  • Baldi P, Wolters P, Komjanc M, Viola R, Velasco R, Salvi S (2013) Genetic and physical characterisation of the locus controlling columnar habit in apple (Malus × domestica Borkh.). Mol Breed 31(2):429–440. doi:10.1007/s11032-012-9800-1

    Article  CAS  Google Scholar 

  • Bennetzen JL, Schrick K, Springer PS, Brown WE, SanMiguel P (1994) Active maize genes are unmodified and flanked by diverse classes of modified, highly repetitive DNA. Genome 37(4):565–576. doi:10.1139/g94-081

    Article  CAS  PubMed  Google Scholar 

  • Buhariwalla C, Greaves S, Magrath R, Mithen R (1995) Development of specific PCR primers for the amplification of polymorphic DNA from the obligate root pathogen Plasmodiophora brassicae. Physiol Mol Plant Pathol 47(2):83–94

    Article  CAS  Google Scholar 

  • Burge C, Karlin S (1997) Prediction of complete gene structures in human genomic DNA. J Mol Biol 268(1):78–94. doi:10.1006/jmbi.1997.0951

    Article  CAS  PubMed  Google Scholar 

  • Burgoyne LA, Wagar MA, Atkinson MR (1970) Calcium-dependent priming of DNA synthesis in isolated rat liver nuclei. Biochem Biophys Res Commun 39(2):254–259

    Article  CAS  PubMed  Google Scholar 

  • 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(3):350–359

    CAS  Google Scholar 

  • Du C, Fefelova N, Caronna J, He L, Dooner HK (2009) The polychromatic Helitron landscape of the maize genome. Proc Natl Acad Sci USA 106(47):19916–19921

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eimert K, Reutter G, Strolka B (2003) Fast and reliable detection of doubled-haploids in Asparagus officinalis by stringent RAPD-PCR. J Agric Sci 141(01):73–78

    Article  CAS  Google Scholar 

  • Fernández-Fernández F, Evans K, Clarke J, Govan C, James C, Marič S, Tobutt K (2008) Development of an STS map of an interspecific progeny of Malus. Tree Genet Genomes 4(3):469–479. doi:10.1007/s11295-007-0124-y

    Article  Google Scholar 

  • Fisher DV (1969) Spur-type strains of McIntosh for high density plantings. British Columbia Fruit Grow Assoc Q Rep 14(2):3–10

    Google Scholar 

  • Fisher DV (1995) The ‘Wijick Spur McIntosh’. Fruit Var J 49:212–213

    Google Scholar 

  • Fujimoto R, Kinoshita Y, Kawabe A, Kinoshita T, Takashima K, Nordborg M, Nasrallah ME, Shimizu KK, Kudoh H, Kakutani T (2008) Evolution and control of imprinted FWA genes in the genus Arabidopsis. PLoS Genet 4(4):e1000048. doi:10.1371/journal.pgen.1000048

    Article  PubMed  PubMed Central  Google Scholar 

  • Gelvonauskienė D, Gelvonauskis B, Sasnauskas A (2006) Impact of rootstocks on columnar apple tree growth in a nursery. Sodininkystė ir daržininkystė 25(3):51–56

    Google Scholar 

  • Góngora-Castillo E, Ibarra-Laclette E, Trejo-Saavedra DL, Rivera-Bustamante RF (2012) Transcriptome analysis of symptomatic and recovered leaves of geminivirus-infected pepper (Capsicum annuum). Virol J 9(1):1–16

    Article  Google Scholar 

  • Grandbastien M-A, Spielmann A, Caboche M (1989) Tnt1, a mobile retroviral-like transposable element of tobacco isolated by plant cell genetics. Nature 337(6205):376–380

    Article  CAS  PubMed  Google Scholar 

  • Grunstein M, Hogness DS (1975) Colony hybridization: a method for the isolation of cloned DNAs that contain a specific gene. Proc Natl Acad Sci USA 72(10):3961–3965

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hemmat M, Weeden NF, Manganaris AG, Lawson DM (1994) Molecular marker linkage map for apple. J Hered 85(1):4–11

    CAS  PubMed  Google Scholar 

  • 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(3):347–349

    CAS  Google Scholar 

  • Jiang N, Bao Z, Temnykh S, Cheng Z, Jiang J, Wing RA, McCouch SR, Wessler SR (2002a) Dasheng: a recently amplified nonautonomous long terminal repeat element that is a major component of pericentromeric regions in rice. Genetics 161(3):1293–1305

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang N, Jordan IK, Wessler SR (2002b) Dasheng and RIRE2. A nonautonomous long terminal repeat element and its putative autonomous partner in the rice genome. Plant Physiol 130(4):1697–1705

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang N, Bao Z, Zhang X, Eddy SR, Wessler SR (2004) Pack-MULE transposable elements mediate gene evolution in plants. Nature 431(7008):569–573. doi:10.1038/nature02953

    Article  CAS  PubMed  Google Scholar 

  • Kalendar R, Grob T, Regina M, Suoniemi A, Schulman A (1999) IRAP and REMAP: two new retrotransposon-based DNA fingerprinting techniques. Theor Appl Genet 98(5):704–711. doi:10.1007/s001220051124

    Article  CAS  Google Scholar 

  • Kesley DF, Brown SK (1992) “McIntosh Wijcik”: a columnar mutation of “McIntosh” apple proving useful in physiology and breeding research. Fruit Var J 46:83–87

    Google Scholar 

  • Kim MY, Song KJ, Hwang J-H, Shin Y-U, 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(4):512–517

    CAS  Google Scholar 

  • Kinoshita Y, Saze H, Kinoshita T, Miura A, Soppe WJJ, Koornneef M, Kakutani T (2007) Control of FWA gene silencing in Arabidopsis thaliana by SINE-related direct repeats. Plant J 49(1):38–45. doi:10.1111/j.1365-313X.2006.02936.x

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi S, Goto-Yamamoto N, Hirochika H (2004) Retrotransposon-induced mutations in grape skin color. Science 304(5673):982

    Article  PubMed  Google Scholar 

  • Kohany O, Gentles A, Hankus L, Jurka J (2006) Annotation, submission and screening of repetitive elements in Repbase: repbasesubmitter and Censor. BMC Bioinformatics 7(1):474

    Article  PubMed  PubMed Central  Google Scholar 

  • Krost C, Petersen R, Schmidt ER (2012) The transcriptomes of columnar and standard type apple trees (Malus × domestica)—a comparative study. Gene 498:223–230. doi:10.1016/j.gene.2012.01.078

    Article  CAS  PubMed  Google Scholar 

  • Krost C, Petersen R, Lokan S, Brauksiepe B, Braun P, Schmidt E (2013) Evaluation of the hormonal state of columnar apple trees (Malus × domestica) based on high throughput gene expression studies. Plant Mol Biol 81(3):211–220. doi:10.1007/s11103-012-9992-0

    Article  CAS  PubMed  Google Scholar 

  • Lamesch P, Berardini TZ, Li D, Swarbreck D, Wilks C, Sasidharan R, Muller R, Dreher K, Alexander DL, Garcia-Hernandez M, Karthikeyan AS, Lee CH, Nelson WD, Ploetz L, Singh S, Wensel A, Huala E (2012) The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools. Nucleic Acids Res 40(D1):D1202–D1210

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lapins KO (1969) Segregation of compact growth types in certain apple seedling progenies. Can J Plant Sci 49:765–768

    Article  Google Scholar 

  • Lapins KO (1976) Inheritance of compact growth type in apple. J Am Soc Hortic Sci 101:133–135

    Google Scholar 

  • Lapins KO, Fisher DV (1974) Four natural spur-type mutants of McIntosh apple. Can J Plant Sci 54(2):359–362

    Article  Google Scholar 

  • Lapins KO, Watkins R (1973) Genetics of compact growth habit. Report of East Malling Research Station for 1972, p 136

  • Laten HM, Majumdar A, Gaucher EA (1998) SIRE-1, a copia/Ty1-like retroelement from soybean, encodes a retroviral envelope-like protein. Proc Natl Acad Sci USA 95(12):6897–6902

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lauri PE, Lespinnasse JM (1993) The relationship between cultivar fruiting-type and fruiting branch characteristics in apple trees. Acta Hortic 349:259–263

    Google Scholar 

  • Liebhard R, Gianfranceschi L, Koller B, Ryder CD, Tarchini R, Van de Weg E, Gessler C (2002) Development and characterisation of 140 new microsatellites in apple (Malus × domestica Borkh.). Mol Breed 10:217–241

    Article  CAS  Google Scholar 

  • Lisch D (2009) Epigenetic regulation of transposable elements in plants. Annu Rev Plant Biol 60:43–66

    Article  CAS  PubMed  Google Scholar 

  • Lisch D (2013) How important are transposons for plant evolution? Nat Rev Genet 14(1):49–61

    Article  CAS  PubMed  Google Scholar 

  • Llorens C, Futami R, Covelli L, Domínguez-Escribá L, Viu JM, Tamarit D, Aguilar-Rodríguez J, Vicente-Ripolles M, Fuster G, Bernet GP, Maumus F, Munoz-Pomer A, Sempere JM, Latorre A, Moya A (2011) The Gypsy database (GyDB) of mobile genetic elements: release 2.0. Nucleic Acids Res 39(Suppl 1):D70–D74

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marco A, Marín I (2005) Retrovirus-like elements in plants. Recent Res Dev Plant Sci 3:15–24

    CAS  Google Scholar 

  • Meulenbroek B, Verhaegh J, Janse J (1998) Inheritance studies with columnar type trees. Acta Hortic 484:255–260

    Google Scholar 

  • Moriya S, Iwanami H, Kotoda N, Takahashi S, Yamamoto T, Kazuyuki A (2009) Development of a marker-assisted selection system for columnar growth habit in apple breeding. J Jpn Soc Hortic Sci 78(3):279–287

    Article  CAS  Google Scholar 

  • 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 × domestica Borkh.) linkage group 10. Plant Breed 131:641–647. doi:10.1111/j.1439-0523.2012.01985.x

    Article  CAS  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15(3):473–497. doi:10.1111/j.1399-3054.1962.tb08052.x

    Article  CAS  Google Scholar 

  • Otto D, Petersen R, Krost C, Brandl R, Brauksiepe B, Braun P, Schmidt ER (2013) Molecular characterization of the Co gene region in Malus × domestica. Acta Hortic (in press)

  • Petersen R, Krost C (2013) Tracing a key player in the regulation of plant architecture: the columnar growth habit of apple trees (Malus × domestica). Planta 1–22. doi:10.1007/s00425-013-1898-9

  • Peterson-Burch BD, Wright DA, Laten HM, Voytas DF (2000) Retroviruses in plants? Trends Genet 16(4):151–152

    Article  CAS  PubMed  Google Scholar 

  • Ramsay L, Macaulay M, Cardle L, Morgante M, Ivanissevich SD, Maestri E, Powell W, Waugh R (1999) Intimate association of microsatellite repeats with retrotransposons and other dispersed repetitive elements in barley. Plant J 17(4):415–425. doi:10.1046/j.1365-313X.1999.00392.x

    Article  CAS  PubMed  Google Scholar 

  • Salvi S, Sponza G, Morgante M, Tomes D, Niu X, Fengler KA, Meeley R, Ananiev EV, Svitashev S, Bruggemann E, Li B, Hainey CF, Radovic S, Zaina G, Rafalski JA, Tingey SV, Miao G-H, Phillips RL, Tuberosa R (2007) Conserved noncoding genomic sequences associated with a flowering-time quantitative trait locus in maize. Proc Natl Acad Sci USA 104(27):11376–11381

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • SanMiguel P, Tikhonov A, Jin Y-K, Motchoulskaia N, Zakharov D, Melake-Berhan A, Springer PS, Edwards KJ, Lee M, Avramova Z, Bennetzen JL (1996) Nested retrotransposons in the intergenic regions of the maize genome. Science 274(5288):765–768

    Article  CAS  PubMed  Google Scholar 

  • Sheng Y, Mancino V, Birren B (1995) Transformation of Escherichia coli with large DNA molecules by electroporation. Nucleic Acids Res 23(11):1990–1996

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shizuya H, Birren B, Kim UJ, Mancino V, Slepak T, Tachiiri Y, Simon M (1992) Cloning and stable maintenance of 300-kilobase-pair fragments of human DNA in Escherichia coli using an F-factor-based vector. Proc Natl Acad Sci USA 89(18):8794–8797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith CM, Rodriguez-Buey M, Karlsson J, Campbell MM (2004) The response of the poplar transcriptome to wounding and subsequent infection by a viral pathogen. New Phytol 164(1):123–136. doi:10.1111/j.1469-8137.2004.01151.x

    Article  CAS  Google Scholar 

  • Southern EM (1975) Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol 98(3):503–517

    Article  CAS  PubMed  Google Scholar 

  • Stekel DJ, Git Y, Falciani F (2000) The comparison of gene expression from multiple cDNA libraries. Genome Res 10(12):2055–2061

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Studer A, Zhao Q, Ross-Ibarra J, Doebley J (2011) Identification of a functional transposon insertion in the maize domestication gene tb1. Nat Genet 43(11):1160–1163. doi:10.1038/ng.942

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun H-Y, Dai H-Y, Zhao G-L, Ma Y, Ou C-Q, Li H, Li L-G, Zhang Z-H (2008) Genome-wide characterization of long terminal repeat retrotransposons in apple reveals the differences in heterogeneity and copy number between Ty1-copia and Ty3-gypsy retrotransposons. J Integr Plant Biol 50(9):1130–1139. doi:10.1111/j.1744-7909.2008.00717.x

    Article  CAS  PubMed  Google Scholar 

  • Thimm O, Bläsing O, Gibon Y, Nagel A, Meyer S, Krüger P, Selbig J, Müller LA, Rhee SY, Stitt M (2004) Mapman: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J 37(6):914–939. doi:10.1111/j.1365-313X.2004.02016.x

    Article  CAS  PubMed  Google Scholar 

  • Tian Y-K, Wang C-H, Zhang J-S, James C, Dai H-Y (2005) Mapping Co, a gene controlling the columnar phenotype of apple, with molecular markers. Euphytica 145(1):181–188

    Article  CAS  Google Scholar 

  • Tobutt KR (1985) Breeding columnar apples at east malling. Acta Hortic 159:63–68

    Google Scholar 

  • Tobutt KR (1994) Combining apetalous parthenocarpy with columnar growth habit in apple. Euphytica 77(1–2):51–54. doi:10.1007/bf02551460

    Article  Google Scholar 

  • Vali U, Brandstrom M, Johansson M, Ellegren H (2008) Insertion–deletion polymorphisms (indels) as genetic markers in natural populations. BMC Genet 9(1):8

    Article  PubMed  PubMed Central  Google Scholar 

  • Van Damme M, Andel A, Huibers RP, Panstruga R, Weisbeek PJ, Van den Ackerveken G (2005) Identification of Arabidopsis loci required for susceptibility to the downy mildew pathogen Hyaloperonospora parasitica. Mol Plant Microbe Interact 18(6):583–592. doi:10.1094/mpmi-18-0583

    Article  PubMed  Google Scholar 

  • Van Damme M, Huibers RP, Elberse J, Van den Ackerveken G (2008) Arabidopsis DMR6 encodes a putative 2OG-Fe(II) oxygenase that is defense-associated but required for susceptibility to downy mildew. Plant J 54(5):785–793. doi:10.1111/j.1365-313X.2008.03427.x

    Article  PubMed  Google Scholar 

  • 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 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 × domestica Borkh.). Nat Genet 42(10):833–839. doi:10.1038/ng.654

    Google Scholar 

  • Venturi S, Dondini L, Donini P, Sansavini S (2006) Retrotransposon characterisation and fingerprinting of apple clones by S-SAP markers. Theor Appl Genet 112(3):440–444. doi:10.1007/s00122-005-0143-8

    Article  CAS  PubMed  Google Scholar 

  • Vicient C (2010) Transcriptional activity of transposable elements in maize. BMC Genom 11(1):601

    Article  Google Scholar 

  • Vignols F, Rigau J, Torres MA, Capellades M, Puigdomènech P (1995) The brown midrib3 (bm3) mutation in maize occurs in the gene encoding caffeic acid O-methyltransferase. Plant Cell Online 7(4):407–416

    CAS  Google Scholar 

  • Wessler SR (1996) Plant retrotransposons: turned on by stress. Curr Biol 6(8):959–961. doi:10.1016/S0960-9822(02)00638-3

    Article  CAS  PubMed  Google Scholar 

  • Wright DA, Voytas DF (1998) Potential retroviruses in plants: Tat1 is related to a group of Arabidopsis thaliana Ty3/gypsy retrotransposons that encode envelope-like proteins. Genetics 149(2):703–715

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yao J-L, Dong Y-H, Morris BAM (2001) Parthenocarpic apple fruit production conferred by transposon insertion mutations in a MADS-box transcription factor. Proc Natl Acad Sci USA 98(3):1306–1311

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu C, Zhang J, Peterson T (2011) Genome rearrangements in maize induced by alternative transposition of reversed Ac/Ds termini. Genetics 188(1):59–67

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 Revista Int Bot Exp 68:119–126

    Google Scholar 

  • Zohary D, Hopf M (2000) Domestication of plants in the Old World, 3rd edn. Oxford University Press, Oxford

    Google Scholar 

Download references

Acknowledgments

This work was supported by grants of the Federal Ministry of Agriculture and Nutrition (No. 511-06.01-28-1-43.042-07 and No. 313-06.01-28-1-43.042-07). We thank Benjamin Rieger and Dr. Steffen Rapp for the bioinformatics support.

Conflict of interest

The authors declare no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Erwin R. Schmidt.

Additional information

Dominik Otto and Romina Petersen in alphabetical order and have contributed equally to this work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

11032_2013_1_MOESM1_ESM.tif

Supplementary Fig. 1 Screenshots of mappings of genomic paired end reads against the 8.2 kb insertion. Mappings were conducted in CLC Genomics Workbench (CLC bio) against the BAC metacontig sequence anchored around position 18.8 Mb on chromosome 10. (A) Mapping of genomic paired end reads of McIntosh. (B) Mapping of genomic paired end reads of McIntosh Wijcik. The left and right borders of the insertion are highlighted in red; the insertion sequence is marked in purple. Paired reads with matching partners are blue, forward reads are green, reverse reads are red and reads matching to more than one position are shown in yellow. (TIFF 2705 kb)

11032_2013_1_MOESM2_ESM.tif

Supplementary Fig. 2 Verification of the transposon presence on different columnar and non-columnar varieties In addition to the results shown in Fig. 2, PCRs with the primer pair spanning the right border of Gy-44 were conducted on template DNA of an additional four non-columnar and 11 columnar (underlined) cultivars. The expected fragment of 633 bp was only obtained from columnar cultivars. M: GeneRulerTM 50 bp DNA Ladder (Fermentas) (TIFF 7839 kb)

11032_2013_1_MOESM3_ESM.tif

Supplementary Fig. 3 Marker analysis of the non-columnar cultivar Topaz PCRs were carried out with the particular published pair of primers. Genomic DNAs of the non-columnar cultivar A14, the non-columnar cultivar Topaz and the columnar cultivar P28 (underlined) were used as templates for the PCRs. C18470-25831, C1753-3520, C7629-2209 and C6835.384-2 were designed by Bai et al. (2012). Mdo.chr10.11 - Mdo.chr10.14 and Mdo.chr10.15-like are derived from Moriya et al. (2012) and Hi01a03 from Moriya et al. (2009). Primers Mdo.chr10.15-like are more specific than the published primers for Mdo.chr10.15. SCAR682 and SCAR216 originate from Tian et al. (2005), EMPc105 and Ch03d11 from Fernández-Fernández et al. (2008) and I2_3_M1, K25_M1, H1_M1 and 1C3_M2 are our own indel-based primers (Otto et al. (2013)). M: GeneRulerTM 50 bp DNA Ladder (Fermentas) (TIFF 9627 kb)

11032_2013_1_MOESM4_ESM.xlsx

Supplementary Table 1. Phenotypes and pedigrees of apple cultivars used for marker analyses. The upper part lists the phenotype and parents of all apple varieties used in this study (where known) and the lower part lists the phenotype and parentage of the parent cultivars with McIntosh Wijcik origin. (XLSX 10 kb)

11032_2013_1_MOESM5_ESM.xlsx

Supplementary Table 2. Analysis of differential gene expression. Reads of the leaf transcriptomes of McIntosh and McIntosh Wijcik were mapped to the apple genome (Velasco et al. 2010) and the number of total gene reads were extracted for each MDP. All annotated genes (MDPs) were assigned to UniProtKB/SwissProt hits and differential expression of unigenes was evaluated based on Rj values (Stekel et al. 2000). Unigenes are ranked according to their significance of differential expression. (XLSX 675 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Otto, D., Petersen, R., Brauksiepe, B. et al. The columnar mutation (“Co gene”) of apple (Malus × domestica) is associated with an integration of a Gypsy-like retrotransposon. Mol Breeding 33, 863–880 (2014). https://doi.org/10.1007/s11032-013-0001-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11032-013-0001-3

Keywords

Navigation