Biologia Plantarum

, Volume 59, Issue 2, pp 237–244 | Cite as

Expression of DORMANCY-ASSOCIATED MADS-BOX (DAM)-like genes in apple

Original Papers


Apple (Malus × domestica Borkh.) is a perennial woody plant that undergoes a period of dormancy (in cv. Jonathan between late September and mid-December) to survive freezing temperatures of winter. DORMANCY-ASSOCIATED MADS-BOX (DAM) genes play important roles in the regulation of growth cessation and terminal bud formation in peach. To understand the role of DAM orthologs in apple, we isolated and characterized four DAM-like genes (designated as MdDAMa, MdDAMb, MdDAMc, and MdDAMd) and monitored their expression in apical buds throughout the season by real-time quantitative polymerase chain reaction analyses. The transcription of MdDAMa peaked in October and that of MdDAMc was elevated from August to October, whereas MdDAMb and MdDAMd were practically undetectable. The tandemly arranged genes MdDAMa/MdDAMb and MdDAMc/MdDAMd were localized to chromosomes 16 and 8, respectively. Based on these observations, we infer that MdDAMa and MdDAMc acted in a dominant fashion on each locus and were correlated with the period of endodormancy.

Additional key words

gene expression Malus × domestica RT-qPCR 









genome database for Rosaceae




Malus × domestica


phosphatidyl-ethanolamine binding protein


plant transcription factor database


quantitative trait locus


real time quantitative polymerase chain reaction




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  1. Artlip, T.S., Wisniewski, M.E., Bassett, C.L., Norelli, J.L.: CBF gene expression in peach leaf and bark tissues is gated by a circadian clock. — Tree Physiol. 33: 866–877, 2013.PubMedCrossRefGoogle Scholar
  2. Bielenberg, D.G., Wang, Y., Fan, S., Reighard, G.L., Scorza, R., Abbott, A.G.: A deletion affecting several gene candidates is present in the evergrowing peach mutant. — J. Hered. 95: 436–444, 2004.PubMedCrossRefGoogle Scholar
  3. Bielenberg, D.G., Wang, Y., Li, Z., Zhebentyayeva, T., Fan, S., Reighard, G.L., Scorza, R., Abbott., A.G.: Sequencing and annotation of the evergrowing locus in peach [Prunus persica (L.) Batsch] reveals a cluster of six MADS-box transcription factors as candidate genes for regulation of terminal bud formation. — Tree Genet. Genomes 4: 495–507, 2008.CrossRefGoogle Scholar
  4. Chao, W.S., Dogramaci, M., Foley, M.E., Horvath, D.P., Anderson, J.V.: Selection and validation of endogenous reference genes for qRT-PCR analysis in leafy spurge (Euphorbia esula). — PLoS ONE 7: e42839, 2012.PubMedCentralPubMedCrossRefGoogle Scholar
  5. Falavigna, V.d.S., Porto, D.D., Buffon, V., Margis-Pinheiro, M., Pasquali, G., Revers, L.F.: Differential transcriptional profiles of dormancy-related genes in apple buds. — Plant Mol. Bio. Rep. 32: 796–813, 2014.CrossRefGoogle Scholar
  6. Hawerroth, F.J., Herter, F.G., Petri, J.L., Marafon, A.C., Leonetti J.F.: Evaluation of winter temperatures on apple budbreak using grafted twigs. — Rev. bras. Frutic. 35: 713–721, 2013.CrossRefGoogle Scholar
  7. Horvath, D.P.: Common mechanisms regulate flowering and dormancy. — Plant Sci. 177: 523–531, 2009.CrossRefGoogle Scholar
  8. Horvath, D.P., Chao, W.S., Suttle, J.C., Thimmapuram, J., Anderson. J.V.: Transcriptome analysis identifies novel responses and potential regulatory genes involved in seasonal dormancy transitions of leafy spurge (Euphorbia esula L.). — BMC Genomics 9: 536, 2008.PubMedCentralPubMedCrossRefGoogle Scholar
  9. Horvath, D.P., Sung, S., Kim, D., Chao, W., Anderson, J.: Characterization, expression and function of DORMANCYASSOCIATED MADS-BOX genes from leafy spurge. — Plant mol. Biol. 73: 169–179, 2010.PubMedCrossRefGoogle Scholar
  10. Imai T., Ubi B.E., Saito T., Moriguchi T.: Evaluation of reference genes for accurate normalization of gene expression for real time-quantitative PCR in Pyrus pyrifolia using different tissue samples and seasonal conditions. — PLoS ONE 9: e86492, 2014.PubMedCentralPubMedCrossRefGoogle Scholar
  11. Jeanmougin, F., Thompson, J.D., Gouy, M., Higgins D.G., Gibson, T.J.: Multiple sequence alignment with Clustal X. — Trends Biochem. Sci. 23: 403–405, 1998.PubMedCrossRefGoogle Scholar
  12. Jiménez, S., Lawton-Rauh, A.L., Reighard, G.L., Abbott, A.G., Bielenberg, D.G.: Phylogenetic analysis and molecular evolution of the dormancy associated MADS-box genes from peach. — BMC Plant Biol. 9: 81–93, 2009.PubMedCentralPubMedCrossRefGoogle Scholar
  13. Kotoda, N., Hayashi, H., Suzuki, M., Igarashi, M., Hatsuyama, Y., Kidou, S., Igasaki, T., Nishiguchi, M., Yano, K., Shimizu, T., Takahashi, S., Iwanami, H., Moriya, S., Abe, K.: Molecular characterization of FLOWERING LOCUS Tlike genes of apple (Malus×domestica Borkh.). — Plant Cell Physiol. 51: 561–577, 2010.PubMedCrossRefGoogle Scholar
  14. Kuroda, H., Sagisaka, S.: Ultrastructural changes in apical meristem cells of apple flower buds associated with dormancy and cold tolerance. — J. jap. Soc. hort. Sci. 70: 553–560, 2001.CrossRefGoogle Scholar
  15. Lang, G.A., Early, J.D., Arryave, N.J., Darnell, R.L., Martin, G.C., Stutte, G.W.: Toward reduced universal terminology. — Hort. Sci. 29: 809–811, 1985.Google Scholar
  16. Lee, J.H., Yoo, S.J., Park, S.H., Hwang, I., Lee, J.S., Ahn, J.H.: Role of SVP in the control of flowering time by ambient temperature in Arabidopsis. — Genes Dev. 21: 397–402, 2007.PubMedCentralPubMedCrossRefGoogle Scholar
  17. Leida, C., Conesa, A., Llácer, G., Badenes, M.L., Rios, G.: Histone modifications and expression of DAM6 gene in peach are modulated during bud dormancy release in a cultivar-dependent manner. — New Phytol. 193: 67–80, 2012.PubMedCrossRefGoogle Scholar
  18. Li, D., Liu, C., Shen, L., Wu, Y., Chen, H., Robertson, M., Helliwell, C.A., Ito, T., Meyerowitz, E., Yu, H.: A repressor complex governs the integration of flowering signals in Arabidopsis. — Dev. Cell 15: 110–120, 2008.PubMedCrossRefGoogle Scholar
  19. Li, Z., Reighard, G.L., Abbott, A.G., Bielenberg, D.G.: Dormancy-associated MADS genes from the EVG locus of peach [Prunus persica (L.) Batsch] have distinct seasonal and photoperiodic expression patterns. — J. exp. Bot. 60: 3521–3530, 2009.PubMedCentralPubMedCrossRefGoogle Scholar
  20. Li, Z.M., Zhang, J.Z., Mei, L., Deng, X.X., Hu, C.G., Yao, J.L.: PtSVP, an SVP homolog from trifoliate orange (Poncirus trifoliata L. Raf.), shows seasonal periodicity of meristem determination and affects flower development in transgenic Arabidopsis and tobacco plants. — Plant mol. Biol. 74: 129–142, 2010.PubMedCrossRefGoogle Scholar
  21. Mazzitelli, L., Hancock, R.D., Haupt, S., Walker, P.G., Pont, S.D.A., McNicol, J., Cardle, L., Morris, J., Viola, R., Brennan, R., Hedley, P.E., Taylor, M.A.: Coordinated gene expression during phases of dormancy release in raspberry (Rubus idaeus L.) buds. — J. exp. Bot. 58: 1035–1045, 2007.PubMedCrossRefGoogle Scholar
  22. Nicholas, K.B., Nicholas, H.B., Jr., Deerfield, D.W.II: GeneDoc: analysis and visualization of genetic variation. — EMB 4: 1–4, 1997.Google Scholar
  23. Perrière, G., Gouy, M.: www-Query: an on-line retrieval system for biological sequence banks. — Biochimie. 78: 364–369, 1996.PubMedCrossRefGoogle Scholar
  24. Saito, T., Bai, S., Ito, A., Sakamoto, D., Saito, T., Ubi, B.E., Imai, T., Moriguchi, T.: Expression and genomic structure of the dormancy-associated MADS box genes MADS13 in Japanese pears (Pyrus pyrifolia Nakai) that differ in their chilling requirement for endodormancy release. — Tree Physiol. 33: 654–667, 2013.PubMedCrossRefGoogle Scholar
  25. Sasaki, R., Yamane, H., Ooka, T., Jotatsu, H., Kitamura, Y., Akagi, T., Tao, R.: Functional and expressional analyses of PmDAM genes associated with endodormancy in Japanese apricot (Prunus mume). — Plant Physiol. 157: 485–497, 2011.PubMedCentralPubMedCrossRefGoogle Scholar
  26. Takos, A.M., Ubi, B.E., Robinson, S.P., Walker, A.R.: Condensed tannin biosynthesis genes are regulated separately from other flavonoid biosynthesis genes in apple fruit skin. — Plant Sci. 170: 487–499, 2006.CrossRefGoogle Scholar
  27. Tanaka, N., Ureshino, A., Shigeta, N., Mimida, N., Komori, S., Takahashi, S., Tanaka-Moriya, Y., Wada. M.: Overexpression of Arabidopsis FT gene in apple leads to perpetual flowering — Plant Biotechnol. 31: 11–20, 2014.CrossRefGoogle Scholar
  28. Ubi, B.E., Sakamoto, D., Ban, Y., Shimada, T., Ito, A., Nakajima, I., Takemura, Y., Tamura, F., Saito, T., Moriguchi, T.: Molecular cloning of dormancy-associated MADS-box gene homologs and their characterization during seasonal endodormancy transitional phases of Japanese pear. — J. amer. Soc. hort. Sci. 135: 174–182, 2010.Google Scholar
  29. Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A. Speleman, F.: Accurate normalization of realtime quantitative RT-PCR data by geometric averaging of multiple internal control genes — Genome Biol. 3: research0034.1-0034.11, 2002Google Scholar
  30. Velasco, R., Zharkikh, A., Affourtit, J., Dhingra, A., Cestaro, A., Kalyanaraman, A., Fontana, P., Bhatnagar, S.K., 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, L.M., Gutin, N., Lanchbury, J., Macalma, T., Mitchell, J.T., 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, V.T., King, S.T., Vick, J., Tao, Q., Mraz, A., Stormo, A., Stormo, K., Bogden, R., Ederle, D., Stella, A., Vecchietti, A., Kater, M.M., Masiero, S., Lasserre, P., Lespinasse, Y., Allan, A.C., Bus, V., Chagné, D., Crowhurst, R.N., Gleave, A.P., Lavezzo, E., Fawcett, J.A., Proost, S., Rouzé, P., Sterck, L., Toppo, S., Lazzari, B., Hellens, R.P., Durel, C.E., Gutin, A., Bumgarner, R.E., Gardiner, S.E., Skolnick, M., Egholm, M., Van de Peer, Y., Salamini, F., Viola, R.: The genome of the domesticated apple (Malus × domestica Borkh.). — Nat. Genet. 42: 833–839, 2010.PubMedCrossRefGoogle Scholar
  31. Wang, Y., Georgi, L.L., Reighard, G.L., Scorza, R., Abbott, A.G.: Genetic mapping of the evergrowing gene in peach [Prunus persica (L.) Batsch]. — Genetics 93: 352–358, 2002.Google Scholar
  32. Welling, A., Palva, E.T.: Molecular control of cold acclimation in trees. — Physiol. Plant. 127: 167–181, 2006.CrossRefGoogle Scholar
  33. Wu, R.M., Walton, E.F., Richardson, A.C., Wood, M., Hellens, R.P., Varkonyi-Gasic, E.: Conservation and divergence of four kiwifruit SVP-like MADS-box genes suggest distinct roles in kiwifruit bud dormancy and flowering. — J. exp. Bot. 63: 797–807, 2012.Google Scholar
  34. Wisniewski, M., Norelli, J., Bassett, C., Artlip, T., Macarisin, D.: Ectopic expression of a novel peach (Prunus persica) CBF transcription factor in apple (Malus × domestica) results in short-day induced dormancy and increased cold hardiness. — Planta 233: 971–983, 2011.PubMedCrossRefGoogle Scholar
  35. Yamane, H., Kashiwa, Y., Ooka, T., Tao, R., Yonemori, K.: Suppression subtractive hybridization and differential screening reveals endodormancy-associated expression of an SVP/AGL24-type MADS-box gene in lateral vegetative buds of Japanese apricot. — J. amer. Soc. hort. Sci. 133: 708–716, 2008.Google Scholar
  36. Zhang, H., Jin, J.P., Tang, L., Zhao, Y., Gu, X.C., Gao, G., Luo, J.C.: PlantTFDB 2.0: update and improvement of the comprehensive plant transcription factor database. — Nucl. Acids Res. 39: D1114–D1117, 2011.PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  1. 1.Faculty of AgricultureIwate UniversityMorioka, IwateJapan
  2. 2.Graduate School of Life and Environmental SciencesUniversity of TsukubaTsukuba, IbarakiJapan
  3. 3.Department of Plant, Cell and EnvironmentNARO Institute of Fruit Tree ScienceTsukuba, IbarakiJapan
  4. 4.Apple Research DivisionNARO Institute of Fruit Tree ScienceMorioka, IwateJapan

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