Skip to main content
SpringerLink
Log in

Rootstock effects on gene expression patterns in apple tree scions

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

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 Erwinia amylovora, 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.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • 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 

  • 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 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Bieleski, R.L. 1969. Accumulation and translocation of sorbitol in apple phloem. Aust. J. Biol. Sci. 22: 611–620.

    CAS  Google Scholar 

  • 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 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • 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 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Doley, D. 1974. Effects of rootstocks and interstocks on cell dimensions in scion stems of apple (Malus pumila Mill.). New Phytol. 73: 173–194.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Expert, D. 1999. Withholding and exchanging iron: interactions between Erwinia spp. and their plant hosts. Annu. Rev. Phytopathol. 37: 307–334.

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • 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 

  • 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 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Hamer, D.H. 1986. Metallothionein. Annu. Rev. Biochem. 55: 913–951.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Jansson, S. 1999. A guide to the Lhc genes and their relatives in Arabidopsis. Trends Plant Sci. 4: 236–240.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • 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 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • Theissen, G. and Saedler, H. 1999. The golden decade of molecular floral development (1990–1999): a cheerful obituary. Dev. Genet. 25: 181–193.

    CAS  PubMed  Google Scholar 

  • 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 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Waite, M.B. 1895. The remedy for pear blight. Science 1: 721.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Weigel, D. 1995. The Apetala2 domain is related to a novel type of DNA-binding domain. Plant Cell 7: 388–389.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wertheim, S.J. 1998. Rootstock guide: apple, pear, cherry, European plum. Fruit Research Station, Wilhelminadorp, Netherlands.

    Google Scholar 

  • Wilcox, W.F. 1994. Fire blight fact sheet: Source Title http://www.nysipm.cornell.edu/factsheets/treefruit/diseases/fb/fb.html).

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Plant Pathology, 210 Buckhout Lab, Pennsylvania State University, University Park, PA, 16802, USA

    Philip J. Jensen, Jo Rytter, Elizabeth A. Detwiler & Timothy W. McNellis

  2. Pennsylvania State University Fruit Research and Extension Center, P.O. Box 330, 290 University Drive, Biglerville, PA, 17307, USA

    James W. Travis

Authors
  1. Philip J. Jensen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jo Rytter
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Elizabeth A. Detwiler
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. James W. Travis
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Timothy W. McNellis
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Timothy W. McNellis.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jensen, P.J., Rytter, J., Detwiler, E.A. et al. Rootstock effects on gene expression patterns in apple tree scions. Plant Mol Biol 53, 493–511 (2003). https://doi.org/10.1023/B:PLAN.0000019122.90956.3b

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1023/B:PLAN.0000019122.90956.3b

Search

Navigation