Abstract
Fourteen cDNA clones whose corresponding mRNAs accumulate during the hypersensitive reaction (HR) of tobacco leaves infiltrated with an incompatible strain of the bacterial pathogen Pseudomonas solanacearum have been subdivided by sequence homologies into 6 families. Studies on the accumulation of the mRNAs encoded by these genes in compatible and incompatible plant-bacterial interactions have been carried out and indicate that the 6 cDNA clones can be subdivided into 2 groups. In one group corresponding to 3 cDNA clones, the maximal level of mRNA accumulation is similar in both types of interaction, whereas in the other group, maximal mRNA accumulation in leaves undergoing an HR is 3-to 7-fold higher than in leaves infiltrated with the compatible strain. Within each group, the timing and kinetics of accumulation of the corresponding mRNAs differ for each individual cDNA clone. Run-on experiments indicate that transcriptional activation of these genes plays a major role in the control of their expression. Genomic hybridizations have been performed and indicate that the mRNAs corresponding to the cDNA clones are encoded by multigene families (6 to 20 genes).
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Boller T: Induction of hydrolases as a defense reaction against pathogens. In: Key JL (eds) Cellular and Molecular Biology of Plant Stress, pp. 247–262. A.R. Liss, New York, NY (1985).
Boucher C, Barberis PA, Trigalet AP, Démery DA: Transposon mutagenesis of Pseudomonas solanacearum: isolation of Tn5-induced avirulent mutants. J Gen Microbiol 131: 2449–2457 (1985).
Boucher C, Martinel A, Barberis PA, Alloing G, Zischek C: Virulence genes are carried by a megaplasmid of the plant pathogen Pseudomonas solanacearum. Mol Gen Genet 205: 270–275 (1986).
Buddenhagen I, Kelman A: Biological and physiological aspects of bacterial wilt caused by Pseudomonas solanacearum. Ann Rev Phytopath 2: 203–320 (1964).
Chouikh Y, Volovitch M, Yot P: A simple and fast electrophoretic method for elution of nucleic acid from gels. Mol Biol Rep: 237–239 (1979).
Collinge DB, Milligan DE, Dow JM, Scofield G, Daniels MJ: Gene expression in Brassica campestris showing a hypersensitive response to the incompatible pathogen Xanthomonas campestris pv. Vitians. Plant Mol Biol 8: 405–411 (1987).
Darlix JL, Bromley PA, Spahr PF: Extensive in vitro transcription of Rous Sarcoma Virus RNA by Avian Myeloblastosis Virus DNA polymerase and concurrent activation of the associated RNAse H. J Virol 23: 659–668 (1977).
Dellaporta SL, Wood J, Hicks JB: A plant DNA minipreparation: version II. Plant Mol Biol Rep 1: 19–21 (1983).
Dixon RA, Bolwell GP, Hamdan MAMS, Robbins MP: Molecular biology of disease resistance. In: Day PR, Jellis GJ (eds) Genetics and Pathogenesis, pp. 245–259. Blackwell Scientific Publications, Oxford (1987).
Feinberg AP, Vogelstein B: A technique for radiolabeling DNA restriction endonuclease fragment to high specific activity. Anal Biochem 132: 6–13 (1983).
Feinberg AP, Vogelstein B: A technique for radiolabeling DNA restriction endonuclease fragment to high specific activity. Addendum. Anal Biochem 137: 266–267 (1984).
Godiard L, Ragueh F, Froissard D, Legay JJ, Grosset J, Chartier Y, Meyer Y, Marco Y: Analysis of the synthesis of several PR proteins in tobacco leaves infiltrated with water, compatible and incompatible isolates of Pseudomonas solanacearum. Mol Plant Microbe Interact, in press.
Gubler U, Hoffmann BJ: A simple and very efficient method for generating cDNA libraries. Gene 25: 263–269 (1983).
Hahlbrock K, Cuypers B, Douglas C, Fritzemeier KH, Hoffmann H, Rohwer F, Scheel D, Schutz W: Biochemical interactions of plants with potentially pathogenic fungi. In: Lugtenberg B (ed) Recognition in Microbe-Plant Symbiotic Interactions, pp. 311–323. Springer-Verlag, Berlin (1986).
Heath MC: Hypersensitivity, the cause or the consequence of rust resistance? Phytopathology 66: 935–936 (1976).
Hooftvan Huijsduijnen RAM, Van Loon LC, Bol JF: cDNA cloning of six mRNAs induced by TMV infection of tobacco and a characterization of their translation products. EMBO J 5: 2057–2061 (1986).
Klement Z: Hypersensitivity: In: Mount MS, Lacy GH (eds) Phytopathogenic Prokaryotes, Vol 2, pp. 150–177. Academic Press, New York (1982).
Kombrink E, Schröder M, Hahlbrock K: Several ‘pathogenesis-related’ proteins in potato are 1,3 β-glucanases and chitinases. Proc Natl Acad Sci USA 85: 782–786 (1988).
Lamb CJ, Corbin DR, Lawton MA, Sauer N, Wingate VPM: Recognition and response in plants: pathogen interaction: In: Lugtenberg B (ed) Recognition in Microbe-Plant Symbiotic Interactions, pp. 333–344. Springer-Verlag, Berlin (1986).
Legrand M, Kauffmann S, Geoffroy P, Fritig B: Biological functions of pathogenesis-related proteins are chitinases. Proc Natl Acad Sci USA 84: 6750–6754 (1987).
Maniatis T, Frisch E, Sambrook J: Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York (1982).
Mazau D, Esquerré-Tugayé MT: Hydroxyrich-glycoprotein accumulation in the cell walls of plants infected by various pathogens. Physiol Mol Plant Pathol 29: 147–157 (1986).
Message B, Boistard P, Pitrat M, Schmit J, Boucher C: A new class of fluidal avirulent mutants of Pseudomonas solanacearum unable to induce a hypersensitive reaction. Proc 4th International Conference of Plant Pathogenic Bacteria, Station de Pathologie végétale INRA, Beaucouze, pp. 823–833 (1978).
Okayama H, Berg P: High efficiency cloning of full-length cDNA. Mol Cell Biol 2: 161–171 (1982).
Panopoulos NJ, Walton JD, Willis DK: Plant gene research—Genes involved in microbe-plant interactions: In: Berma DPS, Hohn T (eds) Genetic and Biochemical Basis of Virulence in Plant Pathogens, pp. 339–374. Springer-Verlag, Vienna, New York (1984).
Ragueh F, Lescure N, Roby D, Marco Y: Gene expression in Nicotiana tabacum in response to compatible and incompatible isolates of Pseudomonas solanacearum. Physiol Mol Plant Pathol 35: 23–33 (1989).
Roby D, Toppan A, Esquerré-Tugayé MT: Cell surfaces in plant-microorganism interactions. VI. Elicitors of ethylene from Colletotrichum lagenarium trigger chitinase activity in melon plants. Plant Physiol 81: 228–233 (1986).
Rochaix JD, Malnoe PM: Use of DNA-RNA hybridization for locating chloroplast genes and for estimating the size and abundance of chloroplast DNA transcripts. In: Edelman et al. (eds) Methods in Chloroplast Molecular Biology, pp. 477–490. Elsevier Biomedical Press (1982).
Showalter AM, Bell NJ, Cramer CL, Bailey JA, Varner JE, Lamb CJ: Accumulation of hydroxyproline-rich glycoprotein mRNAs in response to fungal elicitor and infection. Proc Natl Acad Sci USA 82: 6551–6555 (1985).
Slusarenko AJ, Longland A, Friend J: Changes in gene activity during expression of the hypersensitive response in Phaseolus vulgaris cv. ‘Red Mexican’ to an avirulent race 1 isolate of Pseudomonas syringae pv. phaseolicola. Physiol Mol Plant Pathol 29: 79–94 (1986).
Stahl RE, Cook RA: Evidence that bacterial contact with plant cells is necessary for the hypersensitive reaction. Physiol Plant Pathol 14: 77–89 (1979).
Stout JT, Katovich, Hurley C: Chromatin and chromosomal protein research I: In: Stein G, Stein J, Kleinsmith LJ (eds) Methods in Cell Biology, Vol XVI, pp. 87–96. Academic Press, Inc, London (1977).
Van Loon LC: The induction of pathogenesis-related proteins by pathogens and specific chemicals. Neth J Plant Pathol 89: 265–273 (1983).
Van Loon LC: Pathogenesis-related proteins. Plant Mol Biol 4: 111–116 (1985).
Wahl GM, Stern M, Stark GR: Efficient transfer of large DNA fragments from agarose gels to diazobenzyloxymethyl-paper and rapid hybridization by using dextran sulfate. Proc Natl Acad Sci USA 76: 3683–3687 (1979).
Wiborg O, Pedersen MS, Wind A, Berglund LE, Marcker KA, Vuust J: The human ubiquitin family: some genes contain multiple directly repeated ubiquitin coding sequences. EMBO J 4: 755–759 (1985).
Willmitzer L, De Beuckeleer M, Lemmers M, Van Montagu M, Schell J: DNA from Ti plasmid present in nucleus and absent from plastids of crown gall plant cells. Nature 287: 359–361 (1980).
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Marco, Y.J., Ragueh, F., Godiard, L. et al. Transcriptional activation of 2 classes of genes during the hypersensitive reaction of tobacco leaves infiltrated with an incompatible isolate of the phytopathogenic bacterium Pseudomonas solanacearum . Plant Mol Biol 15, 145–154 (1990). https://doi.org/10.1007/BF00017732
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DOI: https://doi.org/10.1007/BF00017732