Plant Molecular Biology

, Volume 61, Issue 3, pp 383–397 | Cite as

Disease Resistance in Plants that Carry a Feedback-regulated Yeast Poly(A) Binding Protein Gene

  • Balasubrahmanyam Addepalli
  • Ruqiang Xu
  • Tomal Dattaroy
  • Baochun Li
  • W. Troy Bass
  • Qingshun Q. Li
  • Arthur G. Hunt
Article

Abstract

It has been reported that the expression of the yeast poly(A) binding protein gene (PAB1) in plants leads to an induction of disease resistance responses, accompanied by alterations in the growth habit of the plant (Li et al. Plant Mol. Biol. (2000) 42 335). To capitalize on this observation, a feedback-regulated PAB1 gene was assembled and introduced into tobacco and Arabidopsis. The regulation entailed the linking of the expression of the PAB1 gene to control by the lac repressor, and by linking lac repressor expression to the disease resistance state of the plant, such that the induction of systemic defense responses by accumulation of the yeast poly(A) binding protein would turn off the expression of the PAB1 gene. Plants containing this system showed elevated and/or constitutive expression of disease-associated genes and significant resistance to otherwise pathogenic organisms. As well, they displayed a nearly normal growth habit under laboratory and greenhouse settings. These studies indicate that the expression of cytotoxic genes (such as the PAB1 gene) in plants can be controlled so that enhanced disease resistance can be achieved without significantly affecting plant growth and development.

Keywords

constitutive PR gene expression disease resistance feedback regulation lac repressor yeast poly(A) binding protein 

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References

  1. Abad, M.S., Hakimi, S.M., Kaniewski, W.K., Rommens, C.M.T., Shulaev, V.,  et al. 1997Characterization of acquired resistance in lesion mimic transgenic potato expressing bacterio-opsinMol. Plant-Microbe Interact.10635645PubMedGoogle Scholar
  2. Addepalli, B., Meeks, L.R., Forbes, K.P., Hunt, A.G. 2004Novel alternative splicing of mRNAs encoding poly(A) polymerases in ArabidopsisBiochim. Biophys. Acta1679117128PubMedGoogle Scholar
  3. Bowling, S.A., Guo, A., Cao, H., Gordon, A.S., Klessig, D.F., Dong, X. 1994A mutation in Arabidopsis that leads to constitutive expression of systemic acquired resistancePlant Cell618451857PubMedCrossRefGoogle Scholar
  4. Bowling, S.A., Clarke, J.D., Liu, Y., Klessig, D.F., Dong, X. 1997The cpr5 mutant of Arabidopsis expresses both NPR1-dependent and NPR1-independent resistancePlant Cell915731584PubMedCrossRefGoogle Scholar
  5. Brown, M., Figge, J., Hansen, U., Wright, C., Jeang, K.T., Khoury, G., Livingston, D.M., Roberts, T.M. 1987Lac repressor can regulate expression from a hybrid SV40 early promoter containing a lac operator in animal cellsCell49603612PubMedCrossRefGoogle Scholar
  6. Clough, S.J., Bent, A.F. 1998Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thalianaPlant J.16735743PubMedCrossRefGoogle Scholar
  7. Dangl, J.L., Dietrich, R.A., Richberg, M.H. 1996Death don’t have no mercy: cell death programs in plant-microbe interactionsPlant Cell817931807PubMedCrossRefGoogle Scholar
  8. Gallagher, S.R. 1992

    Quantitation of GUS activity by fluorometry

    Gallagher, SR eds. GUS Protocols: Using the GUS Gene as a Reporter of Gene ExpressionAcademic PressNew York4759
    Google Scholar
  9. Gan, S., Amasino, R.M. 1995Inhibition of leaf senescence by autoregulated production of cytokininScience27019861988PubMedGoogle Scholar
  10. Gorlach, J., Volrath, S., Knauf-Beiter, G., Hengy, G., Beckhove, U., Kogel, K.H., Oostendorp, M., Staub, T., Ward, E., Kessmann, H., Ryals, J. 1996Benzothiadiazole, a novel class of inducers of systemic acquired resistance, activates gene expression and disease resistance in wheatPlant Cell8629643PubMedCrossRefGoogle Scholar
  11. Hammond-Kosack, K.E., Harrison, K., Jones, J.D. 1994Developmentally regulated cell death on expression of the fungal avirulence gene Avr9 in tomato seedlings carrying the disease-resistance gene Cf-9Proc. Natl. Acad. Sci. USA911044510449PubMedCrossRefGoogle Scholar
  12. Hammond-Kosack, K.E., Tang, S., Harrison, K., Jones, J.D. 1998The tomato Cf-9 disease resistance gene functions in tobacco and potato to confer responsiveness to the fungal avirulence gene product avr 9Plant Cell1012511266PubMedCrossRefGoogle Scholar
  13. Heil, M., Baldwin, I.T. 2002Fitness costs of induced resistance: experimental support for a slippery conceptTrends Plant Sci.76167PubMedCrossRefGoogle Scholar
  14. Keller, H., Pamboukdjian, N., Ponchet, M., Poupet, A., Delon, R. J., Roby, D., Verrier, R. J., Ricci, P. 1999Pathogen-induced elicitin expression in transgenic tobacco generates a hypersensitive response and nonspecific disease resistancePlant Cell11223235PubMedCrossRefGoogle Scholar
  15. Li, Q.Q., Lanken, C., Yang, J., Lawrence, C.B., Hunt, A.G. 2000The yeast polyadenylate binding protein, (PAB1) gene acts as a disease lesion mimic gene when expressed in plantsPlant Mol. Biol.42335344PubMedCrossRefGoogle Scholar
  16. Li, Q.Q., Lawrence, C.B., Xing, H.-Y., Babbitt, R.A., Bass, W.T., Maiti, I.B., Everett, N.P. 2001Enhanced disease resistance conferred by expression of an antimicrobial magainin analog in transgenic tobaccoPlanta212635639PubMedCrossRefGoogle Scholar
  17. MacDonald, M.H., Mogen, B.D., Hunt, A.G. 1991Characterization of the polyadenylation signal of the T-DNA-encoded octopine synthase geneNucl. Acids Res.1955755581PubMedGoogle Scholar
  18. Maiti, I.B., Murphy, J.F., Shaw, J.G., Hunt, A.G. 1993Plants that express a potyvirus proteinase gene are resistant to virus infectionProc. Natl. Acad. Sci. USA9061106114PubMedCrossRefGoogle Scholar
  19. McNellis, T.W., Mudgett, M.B., Li, K., Aoyama, T., Horvath, D., Chua, N., Staskawicz, B.J. 1998Glucocorticoid-inducible expression of a bacterial avirulence gene in transgenic Arabidopsis induces hypersensitive cell deathPlant J.14247257PubMedCrossRefGoogle Scholar
  20. Mittler, R., Shulaev, V., Lam, E. 1995Coordinated activation of programmed cell death and defense mechanisms in transgenic tobacco plants expressing a bacterial proton pumpPlant Cell72942PubMedCrossRefGoogle Scholar
  21. Morris, S.W., Vernooij, B., Titatarn, S., Starrett, M., Thomas, S., Wiltse, C.C., Frederiksen, R.A., Bhandhufalck, A., Hulbert, S., Uknes, S. 1998Induced resistance responses in maizeMol. Plant Microb. Interact.11643658Google Scholar
  22. Oh, J.-W., Kong, Q., Song, C., Carpenter, C.D., Simon, A.E. 1995Open reading frames of turnip crinkle virus involved in satellite symptom expression and incompatibility with Arabidopsis thaliana ecotype DijonMol. Plant Microb. Interact.8979987Google Scholar
  23. Ohshima, M., Harada, N., Matsuoka, M., Ohashi, Y. 1990Nucleotide sequence of the PR-1 gene of Nicotiana tabacumNucl. Acids Res.18181PubMedGoogle Scholar
  24. Oldroyd, G.E.D., Staskawicz, B.J. 1998Genetically engineered broad-spectrum disease resistance in tomatoProc. Natl. Acad. Sci. USA951030010305PubMedCrossRefGoogle Scholar
  25. Petersen, M., Brodersen, P., Naested, H., Andreasson, E., Lindhart, U., Johansen, B., Nielsen, H.B., Lacy, M., Austin, M.J., Parker, J.E., Sharma, S.B., Klessig, D.F., Martienssen, R., Mattsson, O., Jensen, A.B., Mundy, J. 2000Arabidopsis MAP kinase 4 negatively regulates systemic acquired resistanceCell10311111120PubMedCrossRefGoogle Scholar
  26. Rao, M.V., Davis, K.R. 1999Ozone-induced cell death occurs via two distinct mechanisms in Arabidopsis: the role of salicylic acidPlant J.17603614PubMedCrossRefGoogle Scholar
  27. Reuveni, M., Siegel, M.R., Nesmith, W.C. 1985Bioassays using detached tobacco leaves to determine the sensitivity of Peronospora tabacina to fungicidesPesticide Sci.16244249Google Scholar
  28. Rizhsky, L., Mittler, R. 2001Inducible expression of bacterio-opsin in transgenic tobacco and tomato plantsPlant Mol. Biol.46313323PubMedCrossRefGoogle Scholar
  29. Rogers, E.E., Ausubel, F.M. 1997Arabidopsis enhanced disease susceptibility mutants exhibit enhanced susceptibility to several bacterial pathogens and alterations in PR-1 gene expressionPlant Cell9305316PubMedCrossRefGoogle Scholar
  30. Rufty, R.C., Main, C.E. 1989Components of partial resistance to blue mold in six tobacco genotypes under controlled environmental conditionsPhytopathol79606609Google Scholar
  31. Ryals, J.A., Neuenschwander, U.H., Willits, M.G., Molina, A., Steiner, H.-Y., Hunt, M. 1996Systemic acquired resistancePlant Cell818091819PubMedCrossRefGoogle Scholar
  32. Schardl, C., Byrd, A.D., Benzion, G.B., Altschuler, M.A., Hildebrand, D.F., Hunt, A.G. 1987Design and construction of a versatile system for the expression of foreign genes in plantsGene61111PubMedCrossRefGoogle Scholar
  33. Sticher, L., Mauch-Mani, B., Metrauz, J.P. 1997Systemic acquired resistanceAnnu. Rev. Phytopathol.35235270PubMedCrossRefGoogle Scholar
  34. Thomma, B., Eggermont, K., Penninckx, I., Mauch-Mani, B., Vogelsang, R., Cammue, B.P.A, Broekaert, W.F. 1998Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogensProc. Natl. Acad. Sci. USA951510715111CrossRefGoogle Scholar
  35. Loon, L.C., Bakker, P.A.H.M., Pieterse, C.M.J. 1998Systemic resistance induced by rhizosphere bacteriaAnnu. Rev. Phytopathol.36453483PubMedCrossRefGoogle Scholar
  36. Wilde, R.J., Shufflebottom, D., Cooke, S., Jasinska, I., Merryweather, A., Berl, R., Brammer, W.J., Bevan, M., Schuch, W. 1992Control of gene expression in tobacco cells using a bacterial operator–repressor systemEMBO J.1112511259PubMedGoogle Scholar
  37. Wu, S., Schoenbeck, M.A., Greenhagen, B.T., Takahashi, S., Lee, S., Coates, R.M., Chappell, J. 2005Surrogate splicing for functional analysis of sequiterpene synthase genesPlant Physiol.13813221333PubMedCrossRefGoogle Scholar
  38. Xing, H., Lawrence, C.B., Chambers, O., Davies, H.M., Everett, N.P., and Li, Q.Q. 2006. Increased pathogen resistance and yield in transgenic plants expressing combinations of the modified antimicrobial peptides based on indolicidin and magainin. Planta, in press (advanced publication online; DOI 10.1007/s00425–005–0143–6)Google Scholar
  39. Yang, J., Hunt, A.G. 1994Immunological characterization of plant polyadenylate-binding proteinsPlant Sci.99161170CrossRefGoogle Scholar
  40. Yu, I.C., Parker, J., Bent, A.F. 1998Gene-for-gene disease resistance without the hypersensitive response in Arabidopsis dnd1 mutantProc. Natl. Acad. Sci. USA9578197824PubMedCrossRefGoogle Scholar

Copyright information

© Springer 2006

Authors and Affiliations

  • Balasubrahmanyam Addepalli
    • 1
  • Ruqiang Xu
    • 2
  • Tomal Dattaroy
    • 1
    • 4
  • Baochun Li
    • 3
  • W. Troy Bass
    • 3
  • Qingshun Q. Li
    • 2
  • Arthur G. Hunt
    • 1
  1. 1.Department of Plant and Soil SciencesUniversity of KentuckyLexingtonUSA
  2. 2.Department of BotanyMiami UniversityOxfordUSA
  3. 3.Kentucky Tobacco Research and Development CenterUniversity of KentuckyLexingtonUSA
  4. 4.Metahelix Life Sciences Pvt. LtdBangaloreIndia

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