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The promoter of the nematode resistance gene Hs1pro−1 activates a nematode-responsive and feeding site-specific gene expression in sugar beet (Beta vulgaris L.) and Arabidopsis thaliana

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Abstract

The Hs1pro−1 gene confers resistance to the beet cyst nematode Heterodera schachtii in sugar beet (Beta vulgaris L.) on the basis of a gene-for-gene relationship. RNA-gel blot analysis revealed that the transcript of Hs1pro−1 was present in uninfected roots of resistant beet at low levels but increased by about fourfold one day after nematode infection. Treatments of plants with external stimuli including salicylic acid, jasmonic acid, gibberellic acid and abscisic acid as well as wounding or salt stress did not result in changes in the gene transcription, indicating de novo transcription of Hs1pro−1 upon nematode infection specifically. To study transcriptional regulation of Hs1pro−1 expression at the cellular level, a 3082 bp genomic fragment representing the Hs1pro−1 promoter, isolated from the YAC-DNA housing the Hs1pro−1 gene, was fused to the β-glucuronidase reporter gene (1832prm1::GUS) and transformed into susceptible beet roots and Arabidopsis plants, respectively. Fluorometric and histochemical GUS assays on transgenic beet roots and Arabidopsis plants carrying the 1832prm1::GUS construct demonstrated that the Hs1pro1 promoter is functional in both species and drives a nematode responsive and feeding site-specific GUS-expression. GUS activity was detected as early as at initiation of the nematode feeding sites and GUS staining was restricted to the nematode feeding sites. To delineate the regulatory domains of the Hs1pro−1 promoter, fusion genes with various 5′ deletions of the Hs1pro−1 promoter and the GUS gene were constructed and analysed in transgenic beet roots as well. Cis elements responsible for feeding site-specific gene expression reside between –355 and +247 from the transcriptional initiation site of Hs1pro−1 whereas an enhancer region necessary for higher gene expression is located between −1199 and −705 of the promoter. The Hs1pro−1 promoter drives a nematode feeding site-specific GUS expression in both sugar beet and Arabidopsis suggesting a conserved mechanism of regulation of Hs1pro−1 expression in these two species.

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References

  • Aarts, N., Metz, M., Holub, E., Staskawicz, B.J., Daniels, M.J. and Parker, J.E. 1998. Different requirements for EDS1 and NDR1 by disease resistance genes define at least two R gene-mediated signaling pathways in Arabidopsis. Proc. Natl. Acad. Sci. USA 95: 10306-10311.

    Google Scholar 

  • Abe, H., Yamaguchi-Shinozaki, K., Urao, T., Iwasaki, T., Hosokawa, D. and Shinozaki K. 1997. Role of Arabidopsis MYC andMYB homologs in drought-and abscisic acid-regulated gene expression. Plant Cell 9: 1859-1868.

    Google Scholar 

  • Aravind, L., Dixit, V.M. and Koonin, E.V. 1999. The domains of death: evolution of the apoptosis machinery. Trends Biochem Sci. 24: 47-53.

    Google Scholar 

  • Baker, B., Zambryski, P., Staskawicz, B. and Dinesh-Kumar, S.P. 1997. Signaling in plant-microbe interactions. Science 276: 726-733.

    Google Scholar 

  • Baranowskij, N., Frohberg, C., Prat, S. and Willmitzer, L. 1994. A novel DNA binding protein with homology to Myb oncoproteins containing only one repeat can function as a transcriptional activator. EMBO J 13: 5383-5392.

    Google Scholar 

  • Barthels, N., Lee, F.M., Van der Klap, J., Goddijn, O.J.M., Karimi, M., Puzio, P., Grundler, F.M.W., Ohl, S.A., Lindsey, K., Robertson, L., Robertsen, W.M., Van Montagu, M., Gheysen, G. and Sijmons, P.C. 1997. Regulatory sequences of Arabidopsis drive reporter gene expression in nematode feeding structures. Plant Cell 9: 2119-2134.

    Google Scholar 

  • Bechtholt, N., Ellis, J. and Pelletier, G. 1993. In planta Agrobacterium-mediated gene transfer by infiltration of adult Arabidopsis thaliana plants. Life Sci. 316: 1194-1199.

    Google Scholar 

  • Benfey, P.N., Ren, L. and Chua, N.H. 1989. The CAMV 35S enhancer contains at least two domains which can confer different developmental and tissue-specific expression patterns. EMBO J 8: 2195-2202.

    Google Scholar 

  • Bevan, M. 1984. Binary Agrobacterium vectors for plant transformation. Nucl. Acids Res. 12: 8711-8721.

    Google Scholar 

  • Böckenhoff, A., Prior, D.A.M., Grundler, F.M.W. and Oparka, K.J. 1996. Induction of phloem unloading in Arabidopsis thaliana roots by the parasitic nematode Heterodera schachtii. Plant Physiol. 112: 1421-1427.

    Google Scholar 

  • Bradford, M.M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 72: 248-254.

    Google Scholar 

  • Bucher, P. 1990.Weight matrix descriptions of four eukaryotic RNA polymerase II promoter elements derived from 502 unrelated promoter sequences. J. Mol. Biol. 212: 563-578.

    Google Scholar 

  • Cai, D., Kleine, M., Kifle, S., Harloff, H.J., Sandal, N.N., Marcker, K.A., Klein-Lankhorst, R.M., Salentijn, E.M.J., Lange, W., Grundler, F.M.W., Wyss, U. and Jung, C. 1997. Positional cloning of a gene for nematode resistance in sugar beet. Science 275: 832-834.

    Google Scholar 

  • Cao, H., Li, X. and Dong, X. 1998. Generation of broad-spectrum disease resistance by overexpression of an essential regulatory gene in systemic required resistance. Proc. Natl. Acad. Sci. USA 95: 6531-6536.

    Google Scholar 

  • Century, K.S., Lagman, R.A., Adkisson, M., Morlan, J., Tobias, R., Schwartz, K., Smith, A., Love, J., Ronald, P.C. and Whalen, M.C. 1999. Developmental control of Xa21-mediated disease resistance in rice. Plant J 20: 231-236.

    Google Scholar 

  • Cramer, C.L. 1992. Regulation of defense-related gene expression during plant-pathogen interactions. J. Nematol. 24: 586-587.

    Google Scholar 

  • Dangl, J.L. and Jones, J.D. 2001. Plant pathogens and integrated defence responses to infection. Nature 411: 826-833.

    Google Scholar 

  • Davis, E.L., Hussey, R.S., Baum, T.J., Bakker, J., Schots, A., Rosso, M.N. and Abad, P. 2000. Nematode parasitism genes. Annu. Rev. Phytopath. 38: 365-396.

    Google Scholar 

  • de Boer, J.M., Yan, Y., Wang, X., Smant, G., Davis, E.L. and Baum, T.J. 1999. Developmental expression of secretory Qβ-1,4-endoglucanases in the subventral esophageal glands of Heterodera glycines. Mol. Plant-Microbe Interact. 12: 663-669.

    Google Scholar 

  • Després, C., De Long, C., Glaze, S., Liu, E. and Fobert, P.R. 2000.The Arabidopsis NPR1/NIM protein enhances the DNA binding activity of a subgroup of the TGA family of bZIP transcription factors. Plant Cell 12: 279-290.

    Google Scholar 

  • Elliott, K.A. and Shirsat, A.H. 1998. Promoter regions of the extA extensin gene fromBrassica napus control activation in response to wounding and tensile stress. Plant Mol. Biol. 37: 675-687.

    Google Scholar 

  • Ellis, J., Dodds, P. and Pryor, T. 2000. Structure, function and evolution of plant disease resistance genes. Curr. Opin. Plant Biol. 3: 278-284.

    Google Scholar 

  • Elmayan, T. and Tepfer, M. 1995. Evaluation in tobacco of the organ specificity and strength of the rolD promoter, domain A of the 35S promoter and the 35S2 promoter. Transgenic Res. 4: 388-396.

    Google Scholar 

  • Ernst, K., Kumar, A., Kriseleit, D., Kloos, D.-U., Phillips, M.S. and Ganal, M.W. 2002. The broad-spectrum potato cyst nematode resistance gene (Hero) from tomato is the only member of a large gene family of NBS-LRR genes with an unusual amino acid repeat in the LRR region. Plant J. 31: 1-12.

    Google Scholar 

  • Escobar, C., De Meutter, J., Aristizábal, A., Sanz-Alférez, S., Del Campo, F.F., Barthels, N., Van der Eycken, W., Seurinck, J., Van Montagu, M., Gheysen, G. and Fenoll, C. 1999 Isolation of the LEMMI9 gene and promoter analysis during compatible lantnematode interaction. Mol. Plant-Microbe Interact. 12: 440-449.

    Google Scholar 

  • Eulgem, T., Rushton, P.J., Schmelzer, E., Hahlbrock, K. and Somssich, I.E. 1999. Early nuclear events in plant defence signalling: rapid gene activation by WRKY transcription factors. EMBO J. 18: 4689-4699.

    Google Scholar 

  • Eulgem, T., Rushton, P.J., Robatzek, S. and Somssich, I.E. 2000. The WRKY superfamily of plant transcription factors. Trends Plant Sci. 5: 199-206.

    Google Scholar 

  • Favery, B., Lecomte, P., Gil, N., Bechtold, N., Bouchez, D., Dalmasso, A. and Abad, P. 1998. RPE, a plant gene involved in early developmental steps of nematode feeding cells. EMBO J. 17: 6799-6811.

    Google Scholar 

  • Feinberg, A. and Vogelstein, B. 1983 A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Ann. Biochem. 132: 6-13.

    Google Scholar 

  • Fenoll, C., Aristizabal, F.A., Sanz-Alferez, S. and Del Campo, F.F. 1997. Regulation of gene expression in feeding sites. In: C. Fencoll, F.M.W. Grundler and S.A. Ohl (Eds.) Cellular and Molecular Aspects of Plant-Nematode Interactions, Kluwer Academic Publishers, Dordrecht, Netherlands, pp. 250-261.

    Google Scholar 

  • Feys, B.J. and Parker, J.E. 2000. Interplay of signaling pathways in plant disease resistance. Trends Genet. 16: 449-455.

    Google Scholar 

  • Flor, H.H. 1971. Current status for the gene-for-gene concept. Annu. Rev. Phytopath. 9: 275-296.

    Google Scholar 

  • Foster, R., Izawa, T. and Chua, N.H. 1994. Plant bZIP Proteins gather at ACGT elements. FASEB J. 8: 192-200.

    Google Scholar 

  • Frith, M.C., Hansen, U. and Weng, Z. 2001 Detection of cis-element clusters in higher eukaryotic DNA. Bioinformatics 17: 878-889.

    Google Scholar 

  • Gamborg, O.L., Miller, R.A. and Ojima, K. 1968. Nutrient requirements of suspension cultures of soybean root cells. Exp. Cell Res. 50: 151-158.

    Google Scholar 

  • Gheysen, G., Van der Eycken, W., Barthels, N. and Karimi, M. 1996. The exploitation of nematode-responsive plant genes in novel nematode control methods. Pesticide Sci. 47: 95-101.

    Google Scholar 

  • Goddijn, O.J.M., Lindsey, K., Van der Lee, F.M., Klap, J.C. and Sijmons, P.C. 1993. Differential gene expression in nematodeinduced feeding structures of transgenic plants harbouring promoter-gusA fusion constructs. Plant J. 4: 863-873.

    Google Scholar 

  • Goellner, M., Smant, G., De Boer, J.M., Baum, T.J. and Davis, E.L. 2000. Expression of Qβ-1,4-endoglucanase genes by Globodera tabacum during parasitism of tobacco roots. J. Nematol. 32: 154-165.

    Google Scholar 

  • Goellner, M., Wang, X. and Davis, E.L. 2001. Endo-1,4-glucanase expression in compatible plant-nematode interactions. Plant Cell 13: 2241-2255.

    Google Scholar 

  • Golinowski, W., Sobczak, M., Kurek, W. and Grymaszewska, G. 1997. The structure of syncytia. In: C. Fenoll, F.M.W. Grundler and S.A. Ohl (Eds.) Cellular and Molecular Aspects of Plant-Nematode Interactions, Kluwer Academic Publishers, Dordrecht, Netherlands, pp. 80-97.

    Google Scholar 

  • Grundler, F.M.W., Sobczak, M. and Lange, S. 1997. Defence responses of Arabidopsis thaliana during invasion and feeding site induction by the plant-parasitic nematode Heterodera glycines. Physiol. Mol. Plant Path. 50: 419-429.

    Google Scholar 

  • Guan, L., Zhao, J. and Scandalios, J. 2000. Cis-elements and transfactors that regulate expression of the maize Cat1 antioxidant gene in response to ABA and osmotic stress: H2O2 is the likely intermediary signaling molecule for the response. Plant J. 22: 87-95.

    Google Scholar 

  • Hatton, D., Sablowski, R., Yung, M.H., Smith, C., Schuch, W. and Bevan, M. 1995. Two classes of cis sequences contribute to tissue-specific expression of a PAL2 promoter in transgenic tobacco. Plant J. 7: 859-876.

    Google Scholar 

  • Higo, K., Ugawa, Y., Iwamoto, M. and Korenaga, T. 1999. Plant cis-acting regulatory DNA-elements (PLACE). Nucl. Acids Res. 27: 297-300.

    Google Scholar 

  • Holtmann, B., Kleine, M. and Grundler, F.M.W. 2000. Ultrastructure and anatomy of nematode induced syncytia in roots of susceptible and resistant sugar beet. Protoplasma 211: 39-50.

    Google Scholar 

  • Hussey, R.S. and Grundler, F.M.W. 1998. Nematode parasitism of plants. In: R.N. Perry and D. Wright (Eds.) Physiology and Biochemistry of Free-Living and Plant-Parasitic Nematodes, vol. 9, CAB International Press, UK, pp. 213-243.

    Google Scholar 

  • Ishige, F., Takaichi, M., Foster, R., Chua, N.H. and Oeda, K. 1999. A G-box motif (GCCACGTGCC) tetramer confers high-level constitutive expression in dicot and monocot plants. Plant J. 18: 443-448.

    Google Scholar 

  • Jefferson, R.A.A., Kavanagh, T.A. and Bevan, M.W. 1987. GUSfusion: Qβ-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6: 3901-3907.

    Google Scholar 

  • Jung, C. and Löptien, H. 1986. Breeding nematode-resistant sugar beet. In: W. Horn, C.J. Jensen, W. Odenbach and O. Schieder (Eds.) Genetic Manipulation in Plant Breeding, Walter de Gruyter, Berlin/New York, pp. 167-169.

    Google Scholar 

  • Jung, C., Cai, D. and Kleine, M. 1998. Engeneering nematode resistance in crop species. Trends Plant Sci. 3: 266-271.

    Google Scholar 

  • Keller, B. and Heierli, D. 1994. Vascular expression of the grp1.8 promoter is controlled by three specific regulatory elements and one unspecific activating sequence. Plant Mol. Biol. 26: 747-756.

    Google Scholar 

  • Kifle, S., Shao, M., Jung, C. and Cai, D. 1999. An improved transformation protocol for studying gene expression in 'hairy roots'of sugar beet (Beta vulgaris L.). Plant Cell Rep. 18: 514-19.

    Google Scholar 

  • Kinkema, M., Fan, W. and Dong, X. 2000. Nuclear localisation of NPR1 is required for activation of PR gene expression. Plant Cell 12: 2339-2350.

    Google Scholar 

  • Kleine, M., Cai, D., Eibl, C., Herrmann, R.G. and Jung, C. 1995. Physical mapping and cloning of a translocation in sugar beet (Beta vulgaris L.) carrying a gene for nematode (Heterodera schachtii) resistance from B. procumbens. Theor. Appl. Genet. 90: 399-406.

    Google Scholar 

  • Koncz, C. and Schell, J. 1986. The promoter of TL-DNA gene 5 controls the tissue-specific expression of chimeric genes carried by a novel type of Agrobacterium binary vector. Mol. Gen. Genet. 204: 383-396.

    Google Scholar 

  • Lescot, M., Déhais, P., Thijs, G., Marchal, K., Moreau, Y., Van de Peer, Y., Rouzé, P. and Rombauts, S. 2002. PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucl. Acids Res. 30: 325-327.

    Google Scholar 

  • Li, P., Nijhawan, D., Budihardjo, I., Srinivasula, S.M., Ahmad, M., Alnemri, E.S. and Wang, X. 1997. Cytochrome c and dATPdependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 91: 479-489.

    Google Scholar 

  • Liu, Z., Taub, C.C. and McClung, C.R. 1996. Identification of an Arabidopsis thaliana ribulose-1,5-bisphosphate carboxy lase/oxygenase activase (RCA) minimal promoter regulated by light and circadian clock. Plant Physiol. 112: 43-51.

    Google Scholar 

  • Logemann, E., Parniske, M. and Hahlbrock, K. 1995. Modes of expression and common structural features of the complete phenylalanine ammonia-lyase gene family in parsley. Proc. Natl. Acad. Sci. USA 92: 5905-5909.

    Google Scholar 

  • Lois, R., Dietrich, A., Hahlbrock, K. and Schulz, W. 1989. A phenylalanine ammonia-lyase gene from parsley: structure, regulation and identification of elicitor and light responsive cis-acting elements. EMBO J. 8: 1641-1648.

    Google Scholar 

  • Mariani, C., Gossele, V., De Beuckeleer, M., De Block, M., Goldberg, R.B., De Greef, W. and Leemans, J. 1992. A chimaeric ribonuclease-inhibitor gene restores fertility to male sterile plants. Nature 357: 384-387.

    Google Scholar 

  • Martin, G.B., Brommonschenkel, S., Chunwongse, J., Frary, A., Ganal, M.W., Spivey, R., Wu, T., Earle, E.D. and Tanksley, S.D. 1993. Map-based cloning of a protein kinase gene conferring disease resistance in tomato. Science 262: 1432-1436.

    Google Scholar 

  • Michelmore, R.W. and Meyers, B.C. 1998. Clusters of resistance genes in plants evolve by divergent selection and birth-and-death process. Genome Res. 8: 1113-1130.

    Google Scholar 

  • Milligan, S.B., Bodeau, J., Yaghoobi, J., Kaloshian, I., Zabel, P. and Williamson, V.M. 1998. The root knot nematode resistance gene Mi from tomato is a member of the leucine zipper, nucleotide binding, leucine-rich repeat family of plant genes. Plant Cell 10: 1307-131.

    Google Scholar 

  • Niebel, A., Heungens, K., Barthels, N., Inzé, D., Van Montagu, M. and Gheysen, G. 1995. Characterization of a pathogen-induced potato catalase and its systemic expression upon nematode and bacterial infection. Mol. Plant-Microbe Interact. 8: 371-378.

    Google Scholar 

  • Niebel, A., De Almeida-Engler, J., Hemerly, A., Ferreira, P., Inzé, D., Van Montagu, M. and Gheysen, G. 1996. Induction of cdc2a and cyc1At expression in Arabidopsis thaliana during early phases of nematode-induced feeding cell formation. Plant J. 10: 1037-1043.

    Google Scholar 

  • Okubara, P.A., Pawlowski, K., Murphy, T.M. and Berry, A.M. 1999. Symbiotic root nodules of the actinorhizal plant Datisca glomerata express Rubisco activase mRNA. Plant Physiol. 120: 411-420.

    Google Scholar 

  • Opperman, C.H., Taylor, C.G. and Conkling, M.A. 1994. Rootknot nematode-directed expression of a plant root-specific gene. Science 263: 221-223.

    Google Scholar 

  • Paulson, R.E. and Webster, J.M. 1972. Ultrastructure of the hypersensitive reaction in roots of tomato, Lycopersicon esculentum L., to infection by the root-knot nematode, Meloidogyne incognita. Physiol. Plant Path. 2: 227-234.

    Google Scholar 

  • Pla, M., Vilardell, J., Guiltinan, M., Marcotte, W.R., Niogret, M.F., Quatrano, R.S. and Pagès, M. 1993. The cis-regulatory element CCACGTGG is involved in ABA and water-stress responses of the maize gene rab28. Plant Mol. Biol. 21: 259-266.

    Google Scholar 

  • Popeijus, H., Overmars, H., Jones, J., Blok, V. and Goverse, A. 2000. Degradation of plant cell walls by a nematode. Nature 406: 36-37.

    Google Scholar 

  • Puzio, P.S., Cai, D., Ohl, S.A., Wyss, U. and Grundler, F.M.W. 1998. Isolation of regulatory DNA regions related to differentiation of nematode feeding structures in Arabidopsis thaliana. Physiol. Mol. Plant Path. 53: 177-193.

    Google Scholar 

  • Puzio, P.S., Lausen, J., De Almeida-Engler, J., Cai, D., Gheysen, G. and Grundler, F.M.W. 1999. Isolation of a gene from Arabidopsis thaliana related to nematode feeding structures. Gene 239: 163-172.

    Google Scholar 

  • Rice, S.L., Stone, A.R. and Leadbeater, B.S.C. 1987. Changes in cell structure in roots of resistant potatoes parasitized by potato cyst nematodes. 2. Potatoes with resistance from Solanum vernei. Physiol. Mol. Plant. Path. 31: 1-14.

    Google Scholar 

  • Rogers, S.O. and Bendich, A.J. 1985. Extraction of DNA from milligram amounts of fresh, herbarium and mummified plant tissues. Plant Mol. Biol. 5: 69-76.

    Google Scholar 

  • Romero, I., Fuertes, A., Benito, M.J., Malpica, J.M., Leyva, A. and Paz-Ares, J. 1998. More than 80 R2R3-MYB regulatory genes in the genome of Arabidopsis thaliana. Plant J. 14: 273-284.

    Google Scholar 

  • Rosso, M.N., Favery, B., Piotte, C., Arthaud, L., de Boer, J.M., Hussey, R.S., Bakker, J., Baum, T.J. and Abad, P. 1999. Isolation of a cDNA encoding a Qβ-1,4-endoglucanase in the root-knot nematode Meloidogyne incognita and expression analysis during plant parasitism. Mol. Plant-Microbe Interact. 12: 585-591.

    Google Scholar 

  • Rushton, P.J., Torres, J.T., Parniske, M., Wernert, P., Hahlbrock, K. and Somssich, I.E. 1996. Interaction of elicitor-induced DNAbinding proteins with elicitor response elements in the promoters of parsley PR1 genes. EMBO J. 15: 5690-5700.

    Google Scholar 

  • Rushton, P.J. and Somssich, I.E. 1998. Transcriptional control of plant genes responsive to pathogens. Curr. Opin. Plant Biol. 1: 311-315.

    Google Scholar 

  • Sanger, F., Nicklen, S. and Coulsen, A.R. 1977. DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA 74: 5463-5467.

    Google Scholar 

  • Saraste, M., Sibbald, P.R. and Wittinghofer, A. 1990. The P-loop: a common motif in ATP-and GTP-binding proteins. Trends Biochem. Sci. 15: 430-434.

    Google Scholar 

  • Sasser, J.N. 1987. A world perspective of nematology: the role of the society. In: D.W. Freckman (Ed.) Vistas on Nematology, Society for Nematology, Hyattsville, MD, pp. 7-14.

    Google Scholar 

  • Sijmons, P.C., Grundler, F.M.W., Von Mende, N., Burrows, P.R. and Wyss, U. 1991. Arabidopsis thaliana as a new model host for plant-parasitic nematodes. Plant J. 1: 245-254.

    Google Scholar 

  • Sijmons, P.C., Atkinson, H.J. and Wyss, U. 1994. Parasitic strategies of root nematodes and associated host cell responses. Annu. Rev. Phytopath. 32: 235-259.

    Google Scholar 

  • Smant, G., Stokkermans, J.P.W.G., Yitang, Y., De Boer, J.M., Baum, T.J., Wang, X., Hussey, R.S., Henrissat, B., Davis, E.L., Helder, J., Schoots, A. and Bakker, J. 1998. Endogenous cellulases in animals: isolation of Qβ-1,4-endonuclease genes from two species of plant-parasitic cyst nematodes. Proc. Natl. Acad. Sci. USA 95: 4906-4911.

    Google Scholar 

  • Sobczak, M., Golinowski, W. and Grundler, F.M.W. 1997. Changes in the structure of Arabidopsis thaliana roots induced during development of males of the plant parasitic nematode Heterodera schachtii. Eur. J. Plant Path. 103: 113-124.

    Google Scholar 

  • Tang, X., Xie, M., Kim, Y.J., Zhou, J. and Klessig, F. 1999. Overexpression of Pto activates defense responses and confers broad resistance. Plant Cell 11: 15-29.

    Google Scholar 

  • Toxopeus, H. and Lubberts, J.H. 1979. Breeding for resistance to the sugar beet nematode (Heterodera schachtii Schm.) in cruciferous crops. In: Cruciferae Conference, Wageningen, Netherlands, pp. 151.

    Google Scholar 

  • Traut, T.W. 1994. The functions and consensus motifs of nine types of peptide segments that form different types of nucleotidebinding sites. Eur. J. Biochem. 222: 9-19.

    Google Scholar 

  • Urao, T., Yamaguchi-Shinozaki, K., Urao, S. and Shinozaki, K. 1993. An Arabidopsis myb homolog is induced by dehydration stress and its gene product binds to the conserved MYB recognition sequence. Plant Cell 5: 1529-1539.

    Google Scholar 

  • van der Biezen, E.A. and Jones, J.D. 1998. The NB-ARC domain: a novel signalling motif shared by plant resistance gene products and regulators of cell death in animals. Curr. Biol. 8: 226-227.

    Google Scholar 

  • van der Biezen, E.A., Sun, J., Coleman, M.J., Bibb, M.J. and Jones, J.D. 2000. Arabidopsis RelA/SpoT homologs implicate (p)ppGpp in plant signaling. Proc. Natl. Acad. Sci. USA 97: 3747-3752.

    Google Scholar 

  • Van der Eycken, W., De Almeida-Engler, J., Inzé, D., Van Montagu, M. and Gheysen, G. 1996. A molecular study of root-knot nematode-induced feeding sites. Plant J. 9: 45-54.

    Google Scholar 

  • van der Vossen, E.A.G., Rouppe van der Voort, J.N.A.M., Kanyuka, K., Bendahmane, A., Sandbrink, H., Baulcombe, D.C., Bakker, J., Stiekema, W.J. and Klein-Lankhorst, R.M. 2000. Homologues of a single resistance-gene cluster in potato confer resistance to distinct pathogens: a virus and a nematode. Plant J. 23: 567-576.

    Google Scholar 

  • Wang, Z.X., Yano, M., Yamanouchi, U., Iwamoto, M., Monna, L., Hayasaka, H., Katayose, Y. and Sasaki, T. 1999. The Pib gene for rice blast resistance belongs to the nucleotide binding and leucine-rich repeat class of plant disease resistance genes. Plant J. 19: 55-64.

    Google Scholar 

  • Wang, Z.X., Yamanouchi, U., Katayose, Y., Iwamoto, M., Sasaki, T. and Yano, M. 2001. Expression of the Pibrice-blast-resistance gene family is up-regulated by environmental conditions favouring infection and by chemical signals that trigger secondary plant defences. Plant Mol. Biol. 47: 653-661.

    Google Scholar 

  • Werneke, J.N., Chatfield, J.M. and Ogren, W.L. 1989. Alternative mRNA splicing generates the two ribulose-bisphosphate carboxylase/oxygenase activase polypeptides in spinach and Arabidopsis. Plant Cell 1: 815-825.

    Google Scholar 

  • White, S.E., Habera, L.F. and Wessler, S.R. 1994. Retrotransposons in flanking regions of normal plant genes: a role for copia-like elements in the evolution of gene structure and repression. Proc. Natl. Acad. Sci. USA 91: 11792-11796.

    Google Scholar 

  • Williamson, V.M. and Hussey, R.S. 1996. Nematode pathogenesis and resistance in plants. Plant Cell 8: 1735-1745.

    Google Scholar 

  • Wyss, U. 2002. Feeding behaviour of plant-parasitic nematodes. In: D. Lee (Ed.) Biology of Nematodes, Taylor & Francis, London, pp. 233-259.

    Google Scholar 

  • Yamaguchi-Shinozaki, K. and Shinozaki, K. 1994. A Novel cisacting element in an arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress. Plant Cell 6: 251-264.

    Google Scholar 

  • Yang, S., Sweetman, J.P., Amirsadeghi, S., Barghchi, M., Huttly, A.K., Chung, W.-I. and Twell, D. 2001. Novel anther-specific myb genes from tobacco as putative regulators of phenylalanine ammonia-lyase expression. Plant Physiol. 126: 1738-1753.

    Google Scholar 

  • Yoshimura, S., Yamanouchi, U., Katayose, Y., Toki, S., Wang, Z.X., Kono, I., Kurata, N., Yano, M., Iwata, N. and Sasaki, T. 1998. Expression of Xa1, a bacterial blight-resistance gene in rice, is induced by bacterial inoculation. Proc. Natl. Acad. Sci. USA 95: 1663-1669.

    Google Scholar 

  • Yu, D., Chen, C. and Chen, Z. 2001. Evidence for an important role of WRKY binding proteins in the regulation of NPR1 gene expression. Plant Cell 13: 1527-1539.

    Google Scholar 

  • Zhang, Y., Fan, W., Kinkema, M., Li, X. and Dong, X. 1999. Interaction of NPR1 with basic leucine zipper protein transcription factors that bind sequences required for salicylic acid induction of the Pr-1 gene. Proc. Natl. Acad. Sci. USA 96: 6523-6528.

    Google Scholar 

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Authors and Affiliations

  1. Institute of Crop Science and Plant Breeding, Christian Albrechts University of Kiel, Olshausenstrasse 40, 24098, Kiel, Germany

    Tim Thurau, Sirak Kifle, Christian Jung & Daguang Cai

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  1. Tim Thurau
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  2. Sirak Kifle
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  3. Christian Jung
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  4. Daguang Cai
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Correspondence to Daguang Cai.

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Thurau, T., Kifle, S., Jung, C. et al. The promoter of the nematode resistance gene Hs1pro−1 activates a nematode-responsive and feeding site-specific gene expression in sugar beet (Beta vulgaris L.) and Arabidopsis thaliana . Plant Mol Biol 52, 643–660 (2003). https://doi.org/10.1023/A:1024887516581

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