Plant Molecular Biology

, Volume 53, Issue 4, pp 493–511 | Cite as

Rootstock effects on gene expression patterns in apple tree scions

  • Philip J. Jensen
  • Jo Rytter
  • Elizabeth A. Detwiler
  • James W. Travis
  • Timothy W. McNellis


Like many fruit trees, apple trees (Malus pumila) do not reproduce true-to-type from seed. Desirable cultivars are clonally propagated by grafting onto rootstocks that can alter the characteristics of the scion. For example, the M.7 EMLA rootstock is semi-dwarfing and reduces the susceptibility of the scion to Erwiniaamylovora, the causal agent of fire blight disease. In contrast, the M.9 T337 rootstock is dwarfing and does not alter fire blight susceptibility of the scion. This study represents a comprehensive comparison of gene expression patterns in scions of the ‘Gala’ apple cultivar grafted to either M.7 EMLA or M.9 T337. Expression was determined by cDNA-AFLP coupled with silver staining of the gels. Scions grafted to the M.9 T337 rootstock showed higher expression of a number of photosynthesis-related, transcription/translation-related, and cell division-related genes, while scions grafted to the M.7 EMLA rootstock showed increased stress-related gene expression. The observed differences in gene expression showed a remarkable correlation with physiological differences between the two graft combinations. The roles that the differentially expressed genes might play in tree stature, stress tolerance, photosynthetic activity, fire blight resistance, and other differences conferred by the two rootstocks are discussed.

apple differential display fire blight gene expression grafting tree stature 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Arthur, J.C. 1885. Proof that bacteria are the direct cause of the disease in trees known as pear blight. Am. Ass. Adv. Sci. Proc. 34: 294–298.Google Scholar
  2. Autio, R.W. and Southwick, F.W. 1986. The effects of rootstock and root-interstem combination on the growth, productivity, and anchorage of a spur and standard strain Delicious apple tree. Fruit Var. J. 40: 128–133.Google Scholar
  3. Bachem, C.W.B., van der Hoeven, R.S., de Bruijn, S.M., Vreugdenhil, D., Zabeau, M. and Visser, R.G.F. 1996.Visualization of differential gene expression using a novel method of RNA fingerprinting based on AFLP: analysis of gene expression during potato tuber development. Plant J. 9: 745–753.CrossRefPubMedGoogle Scholar
  4. Bieleski, R.L. 1969. Accumulation and translocation of sorbitol in apple phloem. Aust. J. Biol. Sci. 22: 611–620.Google Scholar
  5. Blake, P., Webster, T. and Atkinson, C. 1997. Understanding the way rootstocks dwarf fruit trees. Annu. Rep. Hort. Res. Int. 96-97: 32–35.Google Scholar
  6. Braam, J. and Davis, R.W. 1990. Rain-induced, wind-induced, and touch-induced expression of calmodulin and calmodulin-related genes in Arabidopsis. Cell 60: 357–364.CrossRefPubMedGoogle Scholar
  7. Burrill, T.J. 1880. Anthrax of fruit trees; or the so-called fire blight of pear, and twig blight of apple trees. Am. Ass. Adv. Sci. Proc. 29: 583–597.Google Scholar
  8. Carlson, R.F. 1970. Rootstocks in relation to apple cultivars. In: R.F. Carlson. E.S. Degman, A.P. French. R.P. Larsen, V. Maas, J.B. Mowry, H.A. Rollins, W.H. Upshall and E. Wilcox (Eds.) North American Apples: Varieties, Rootstocks, Outlook, Michigan State University Press, East Lansing, MI, pp. 153–180.Google Scholar
  9. Choi, D., Kim, H.M., Yun, H.K., Park, J.A., Kim, W.T. and Bok, S.H. 1996. Molecular cloning of a metallothionein-like gene from Nicotiana glutinosa L. and its induction by wounding and tobacco mosaic virus infection. Plant Physiol. 112: 353–359.CrossRefPubMedPubMedCentralGoogle Scholar
  10. Cline, J.A., Hunter, D.M., Bonn, W.G. and Bijl, M. 2001. Resistance of the Vineland series of apple rootstocks to fire blight caused by Erwinia amylovora. J. Am. Pomol. Soc. 55: 218–221.Google Scholar
  11. Coxe, W. 1817. Pears. In: A View of the Cultivation of Fruit Trees, and the Management of Orchards and Cider, M. Carey and Son, Philadelphia, pp. 175–176.Google Scholar
  12. Denning, W. 1794. On the decay of apple trees. Transactions of the Society for the Promotion of Agriculture, Arts and Manufacturers, Instituted in the State of New York 1: 219–222.Google Scholar
  13. Devaulta, A., Martinez, A.M., Fesquet, D., Labbe, J.C., Morin, N., Tassan, J.P., Nigg, E.A., Cavadire, J.C. and Doree, M. 1995. MAT1 (Menage-A-Trois) A new ring finger protein subunit stabilizing cyclin H-CDK7 complexes in startfish and Xenopus CAK. EMBO J. 14: 5027–5036.Google Scholar
  14. De Veylder, L., Beemster, G.T., Beeckman, T. and Inzé, D. 2001. CKS1At overexpression in Arabidopsis thaliana inhibits growth by reducing meristem size and inhibiting cell-cycle progression. Plant J. 25: 617–626.CrossRefPubMedGoogle Scholar
  15. De Veylder, L., Segers, G., Glab, N., Casteels, P., Van Montagu, M. and Inzé, D. 1997. The Arabidopsis Cks1At protein binds the cyclin-dependent kinases Cdc2aAt and Cdc2bAt. FEBS Lett.412: 446–452.CrossRefPubMedGoogle Scholar
  16. Ding, X.Q., Bill, E., Good, M., Trautwein, A.X. and Vasak, M. 1988. Mossbauer studies on the metal-thiolate cluster formation in Fe(II)-metallothionein. Eur. J. Biochem. 171: 711–714.CrossRefPubMedGoogle Scholar
  17. Doley, D. 1974. Effects of rootstocks and interstocks on cell dimensions in scion stems of apple (Malus pumila Mill.). New Phytol. 73: 173–194.CrossRefGoogle Scholar
  18. Durrant, W.E., Rowland, O., Piedras, P., Hammond-Kosack, K.E. and Jones, J.D.G. 2000. cDNA-AFLP reveals a striking overlap in race-specific resistance and wound response gene expression profiles. Plant Cell 12: 963–977.CrossRefPubMedPubMedCentralGoogle Scholar
  19. Expert, D. 1999. Withholding and exchanging iron: interactions between Erwinia spp. and their plant hosts. Annu. Rev. Phytopathol. 37: 307–334.CrossRefPubMedGoogle Scholar
  20. Fallahi, E., Colt, W.M., Fallahi, B. and Chun, I.J. 2002. The importance of apple rootstocks on tree growth, yield, fruit quality, leaf nutrition, and photosynthesis with an emphasis on 'Fuji'. Hort. Technol. 12: 38–44.Google Scholar
  21. Ferree, D.C., Hirst, P.M., Schmid, J.C. and Dotson, P.E. 1995. Performance of 3 apple cultivars with 22 dwarfing rootstocks during 8 seasons in Ohio. Fruit Var. J. 49: 171–178.Google Scholar
  22. Ferree, D.C., Schmid, J.C. and Bishop, B.L. 2002. Survival of apple rootstocks to natural infections of fire blight. Hort. Technol. 12: 239–241.Google Scholar
  23. Gao, M., Tao, R., Miura, K., Dandekar, A.M. and Sugiura, A. 2001. Transformation of Japanese persimmon (Diospyros kaki Thunb.) with apple cDNA encoding NADP-dependent sorbitol-6-phosphate dehydrogenase. Plant Sci. 160: 837–845.CrossRefPubMedGoogle Scholar
  24. Garcia-Olmedo, F., Molina, A., Segura, A. and Moreno, M. 1995. The defensive role of nonspecific lipid-transfer proteins in plants. Trends Microbiol. 3: 72–74.CrossRefPubMedGoogle Scholar
  25. Gervais, V., Busso, D., Wasielewski, E., Poterszman, A., Egly, J.M., Thierry, J.C. and Kieffer, B. 2001. Solution structure of the N-terminal domain of the human TFIIH MAT1 subunit: new insights into the RING finger family. J. Biol. Chem. 276: 7457–7464.CrossRefPubMedGoogle Scholar
  26. Hamer, D.H. 1986. Metallothionein. Annu. Rev. Biochem. 55: 913–951.CrossRefPubMedGoogle Scholar
  27. Ito, T., Kim, G.T. and Shinozaki, K. 2000. Disruption of an Arabidopsis cytoplasmic ribosomal protein S13-homologous gene by transposon-mediated mutagenesis causes aberrant growth and development. Plant J. 22: 257–264.CrossRefPubMedGoogle Scholar
  28. Jansson, S. 1999. A guide to the Lhc genes and their relatives in Arabidopsis. Trends Plant Sci. 4: 236–240.CrossRefPubMedGoogle Scholar
  29. Kamboj, J.S., Blake, P.S., Quinlan, J.D. and Webster, A.D. 1997. Recent advances in studies on the dwarfing mechanism of apple rootstocks. Acta Hort. 457: 75–82.CrossRefGoogle Scholar
  30. Kamboj, J.S., Blake, P.S., Quinlan, J.D. and Baker, D.A. 1999a. Identification and quantitation by GC-MS of zeatin and zeatin riboside in xylem sap from rootstock and scion of grafted apple trees. Plant Growth Regul. 28: 199–205.CrossRefGoogle Scholar
  31. Kamboj, J.S., Browning, G., Blake, P.S., Quinlan, J.D. and Baker, D.A. 1999b. GC-MS-SIM analysis of abscisic acid and indole-3-acetic acid in shoot bark of apple rootstocks. Plant Growth Regul. 28: 21–27.CrossRefGoogle Scholar
  32. Ko, K., Norelli, J.L., Reynoird, J.P., Boresjza-Wysocka, E., Brown, S.K. and Aldwinckle, H.S. 2000. Effect of untranslated leader sequence of AMV RNA 4 and signal peptide of pathogenesisrelated protein 1b on attacin gene expression, and resistance to fire blight in transgenic apple. Biotechnol. Lett. 22: 373–381.CrossRefGoogle Scholar
  33. Kristensen, A.K., Brunstedt, J., Nielsen, K.K., Roepstorff, P. and Mikkelsen, J.D. 2000. Characterization of a new antifungal nonspecific lipid transfer protein (nsLTP) from sugar beet leaves. Plant Sci. 155: 31–40.CrossRefPubMedGoogle Scholar
  34. Li, H.Y., Guo, Z.F. and Zhu, Y.X. 1998. Molecular cloning and analysis of a pea cDNA that is expressed in darkness and very rapidly induced by gibberellic acid. Mol. Gen. Genet. 259: 393–397.CrossRefPubMedGoogle Scholar
  35. Li, F.S., Cohen, S., Naor, A., Kang, S.Z. and Erez, A. 2002. Studies of canopy structure and water use of apple trees on three rootstocks. Agric. Water Managemt. 55: 1–14.CrossRefGoogle Scholar
  36. Li, J., Wen, J.Q., Lease, K.A., Doke, J.T., Tax, F.E. and Walker, J.C. 2002. BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. Cell 110: 213–222.CrossRefPubMedGoogle Scholar
  37. Mascall, L. 1569a. Howe to set your wylde trees come of pepynes, when they be first plucked up. In: A booke of the art and maner, howe to plante and graffe all sortes of trees, H. Bynneman for J. Wight, London, pp. 6–7.Google Scholar
  38. Mascall, L. 1569b. Foure maner of graffinges. In: A booke of the art and maner, howe to plante and graffe all sortes of trees, H. Bynneman for J. Wight, London, p. 21.Google Scholar
  39. McManus, P.S., Stockwell, V.O., Sundin, G.W. and Jones, A.L. 2002. Antibiotic use in plant agriculture. Annu. Rev. Phytopath. 40: 443–465.CrossRefGoogle Scholar
  40. Michalczuk, L. 2002. Indole-3-acetic acid level in wood, bark and cambial sap of apple rootstocks differing in growth vigour. Acta Physiol. Plant. 24: 131–136.CrossRefGoogle Scholar
  41. Molina, A. and Garcia-Olmedo, F. 1993. Developmental and pathogen-induced expression of three barley genes encoding lipid transfer proteins. Plant J. 4: 983–991.CrossRefPubMedGoogle Scholar
  42. Nassuth, A., Pollari, E., Helmeczy, K., Stewart, S. and Kofalvi, S.A. 2000. Improved RNA extraction and one-tube RT-PCR assay for simultaneous detection of control plant RNA plus several viruses in plant extracts. J. Virol. Meth. 90: 37–49.CrossRefGoogle Scholar
  43. Olien, W.C. and Lasko, A.N. 1984. A comparison of the dwarfing character and water relations of five apple rootstocks. Acta Hort. 146: 151–158.CrossRefGoogle Scholar
  44. Parker, K.G., Leupschen, N.S. and Jones, A.L. 1974. Inoculation trials with Erwinia amylovora to apple rootstocks. Plant Dis. Rep. 58: 243–247.Google Scholar
  45. Pelah, D., Wang, W.X., Altman, A., Shoseyov, O. and Bartels, D. 1997. Differential accumulation of water stress-related proteins, sucrose synthase and soluble sugars in Populus species that differ in their water stress response. Physiol. Plant. 99: 153–159.CrossRefGoogle Scholar
  46. Pla, M., Huguet, G., Verdaguer, D., Puigderrajols, P., Llompart, B., Nadal, A. and Molinas, M. 1998. Stress proteins co-expressed in suberized and lignified cells and in apical meristems. Plant Sci. 139: 49–57.CrossRefGoogle Scholar
  47. Shen, Q.X., Chen, C.N., Brands, A., Pan, S.M. and Ho, T.H.D. 2001. The stress-and abscisic acid-induced barley gene HVA22: developmental regulation and homologues in diverse organisms. Plant Mol. Biol. 45: 327–340.CrossRefPubMedGoogle Scholar
  48. Sheveleva, E.V., Marquez, S., Chmara, W., Zegeer, A., Jensen, R.G. and Bohnert, H.J. 1998. Sorbitol-6-phosphate dehydrogenase expression in transgenic tobacco: high amounts of sorbitol lead to necrotic lesions. Plant Physiol. 117: 831–839.CrossRefPubMedPubMedCentralGoogle Scholar
  49. Singh, N.K., Bracker, C.A., Hasegawa, P.M., Handa, A.K., Buckel, S., Hermodson, M.A., Pfankoch, E., Regnier, F.E. and Bressan, R.A. 1987. Characterization of osmotin – a thaumatin-like protein associated with osmotic adaptation in plant cells. Plant Physiol. 85: 529–536.CrossRefPubMedPubMedCentralGoogle Scholar
  50. Sobiczewski, P., Deckers, T. and Pulawska, J. 1997. Control. In: Fire Blight (Erwinia amylovora) – Some Aspects of Epidemiology and Control, Research Institute of Pomology and Floriculture,Skierniewice, Poland, pp. 26–37.Google Scholar
  51. Soumelidou, K., Morris, D.A., Battey, N.H., Barnett, J.R. and John, P. 1994a. Auxin transport capacity in relation to the dwarfing effect of apple rootstocks. J. Hort. Sci. 69: 719–725.Google Scholar
  52. Soumelidou, K., Battey, N.H., John, P. and Barnett, J.R. 1994b. The anatomy of the developing bud union and its relationship to dwarfing in apple. Ann. Bot. 74: 605–611.CrossRefGoogle Scholar
  53. Suh, M.C., Choi, D. and Liu, J.R. 1998. Cadmium resistance in transgenic tobacco plants expressing the Nicotiana glutinosa L. metallothionein-like gene. Mol. Cells 8: 678–684.PubMedGoogle Scholar
  54. Theissen, G. and Saedler, H. 1999. The golden decade of molecular floral development (1990–1999): a cheerful obituary. Dev. Genet. 25: 181–193.PubMedGoogle Scholar
  55. van der Zwet, T. and Keil, H.L. 1979. Fire blight: a bacterial disease of rosaceous plants. Agriculture Handbook 510, US Department of Agriculture, Washington, DC.Google Scholar
  56. Verlhac, M.H., Chen, R.H., Hanachi, P., Hershey, J.W.B. and Derynck, R. 1997. Identification of partners of TIF34, a component of the yeast eIF3 complex, required for cell proliferation and translation initiation. EMBO J. 16: 6812–6822.CrossRefPubMedPubMedCentralGoogle Scholar
  57. Volarevic, S., Stewart, M.J., Ledermann, B., Zilberman, F., Terracciano, L., Montini, E., Grompe, M., Kozma, S.C. and Thomas, G. 2000. Proliferation, but not growth, blocked by conditional deletion of 40S ribosomal protein S6. Science 288: 2045–2047.CrossRefPubMedGoogle Scholar
  58. von Bargen, S., Salchert, K., Paape, M., Piechulla, B. and Kellmann, J.W. 2001. Interactions between the tomato spotted wilt virus movement protein and plant proteins showing homologies to myosin, kinesin and DnaJ-like chaperones. Plant Physiol. Biochem. 39: 1083–1093.CrossRefGoogle Scholar
  59. Vos, P., Hogers, R., Bleeker, M., Reijans, M., Vandelee, T., Hornes, M., Frijters, A., Pot, J., Peleman, J., Kuiper, M. and Zabeau, M. 1995. AFLP: a new technique For DNA-fingerprinting. Nucl. Acids Res. 23: 4407–4414.CrossRefPubMedPubMedCentralGoogle Scholar
  60. Waite, M.B. 1895. The remedy for pear blight. Science 1: 721.CrossRefGoogle Scholar
  61. Wang, W.X., Pelah, D., Alergand, T., Shoseyov, O. and Altman, A. 2002. Characterization of SP1, a stress-responsive, boilingsoluble, homo-oligomeric protein from aspen. Plant Physiol. 130: 865–875.CrossRefPubMedPubMedCentralGoogle Scholar
  62. Waters, E.R., Lee, G.J. and Vierling, E. 1996. Evolution, structure and function of the small heat shock proteins in plants. J. Exp. Bot. 47: 325–338.CrossRefGoogle Scholar
  63. Weigel, D. 1995. The Apetala2 domain is related to a novel type of DNA-binding domain. Plant Cell 7: 388–389.CrossRefPubMedPubMedCentralGoogle Scholar
  64. Wertheim, S.J. 1998. Rootstock guide: apple, pear, cherry, European plum. Fruit Research Station, Wilhelminadorp, Netherlands.Google Scholar
  65. Wilcox, W.F. 1994. Fire blight fact sheet: Source Title Scholar
  66. Wrobel, R.L., Matvienko, M. and Yoder, J.I. 2002. Heterologous expression and biochemical characterization of an NAD(P)H: quinone oxidoreductase from the hemiparasitic plant Triphysaria versicolor. Plant Physiol. Biochem. 40: 265–272.CrossRefGoogle Scholar
  67. Zheng, C.C., Porat, R., Lu, P.Z. and O'Neill, S.D. 1998. PNZIP is a novel mesophyll-specific cDNA that is regulated by phytochrome and a circadian rhythm and encodes a protein with a leucine zipper motif. Plant Physiol. 116: 27–35.CrossRefPubMedGoogle Scholar

Copyright information

© Kluwer Academic Publishers 2003

Authors and Affiliations

  • Philip J. Jensen
    • 1
  • Jo Rytter
    • 1
  • Elizabeth A. Detwiler
    • 1
  • James W. Travis
    • 2
  • Timothy W. McNellis
    • 1
  1. 1.Department of Plant Pathology, 210 Buckhout LabPennsylvania State UniversityUniversity ParkUSA
  2. 2.Pennsylvania State University Fruit Research and Extension CenterBiglervilleUSA

Personalised recommendations