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Two pathogen-responsive genes in parsley encode a tyrosine-rich hydroxyproline-rich glycoprotein (hrgp) and an anionic peroxidase

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Abstract

Two recently isolated cDNAs representing genes that are transcriptionally activated in fungus-infected parsley leaves or elicitor-treated, cultured parsley cells are shown to encode a hydroxyproline-rich glycoprotein (HRGP) and an anionic peroxidase. The deduced HRGP protein is rich in tyrosine residues, a feature also found in other pathogen- and wound-induced plant HRGPs. Expression of the peroxidase gene(s) is induced rapidly upon elicitation and precedes that of the HRGP gene. In situ hybridization experiments demonstrate the presence of HRGP and peroxidase mRNAs in parsley tissue around fungal infection sites. Peroxidase mRNA accumulation is particularly sharply restricted to plant cells directly adjacent to fungal hyphae. These results provide further evidence for an important role of specific cell wall modifications in plant defense.

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References

  • Ayers AR, Ebel J, Valente B, Albersheim P (1976) Host-pathogen interactions. X. Fractionation and biological activity of an elicitor isolated from the mycelial walls of Phytophthora megasperma var. sojae. Plant Physiol 57:760–765

    Google Scholar 

  • Bowles DJ (1990) Defense-related proteins in higher plants. Annu Rev Biochem 59:873–907

    Google Scholar 

  • Bradley DJ, Kjellbom P, Lamb CJ (1992) Elicitor- and wound-induced oxidative cross-linking of a proline-rich plant cell wall protein: a novel, rapid defense response. Cell 70:21–30

    Google Scholar 

  • Chen EY, Seeburg PH (1985) Supercoil sequencing: a fast and simple method for sequencing plasmid DNA. DNA 4:165–170

    Google Scholar 

  • Chen J, Varner JE (1985a) An extracellular matrix protein in plants: characterization of a genomic clone for carrot extensin. EMBO J 4:2145–2151

    Google Scholar 

  • Chen J, Varner JE (1985b) Isolation and characterization of cDNA clones for carrot extensin and prolin-rich 33 kDa protein. Proc Natl Acad Sci USA 82:4399–4403

    Google Scholar 

  • Collinge DB, Gregersen PL, Thordal-Christensen H (1994) The induction of gene expression in response to pathogenic microbes. In: Basra AS (ed) Mechanisms of plant growth and improved productivity: modern approaches and perspectives. Marcel Dekker, New York, pp 391–433

    Google Scholar 

  • Corbin DR, Sauer N, Lamb CJ (1987) Differential regulation of a hydroxyproline-rich glycoprotein gene family in wounded and infected plants. Mol Cell Biol 7:4337–4344

    Google Scholar 

  • Devereux J, Haeberli P, Smithies O (1984) A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res 12:387–395

    Google Scholar 

  • Dixon RA, Harrison MJ (1990) Activation, structure, and organization of genes involved in microbial defense in plants. Adv Genet. 28:165–234

    Google Scholar 

  • Dixon RA, Lamb CJ (1990) Molecular communication in interactions between plants and microbial pathogens. Annu Rev Plant Physiol Plant Mol Biol 41:339–367

    Google Scholar 

  • Epstein L, Lamport DTA (1984) An intramolecular linkage involving isodityrosine in extensin. Phytochemistry 23:1241–1246

    Google Scholar 

  • Everdeen DS, Kiefer S, Willard JJ, Muldoon EP, Dey PM, Li X-B, Lamport DTA (1988) Enzymic cross-linkage of monomeric extensin precursors in vitro. Plant Physiol 87:616–621

    Google Scholar 

  • Feinberg AP, Vogelstein B (1983) A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem 132:6–13

    Google Scholar 

  • Fry SC (1986) Cross-linking of matrix polymers in the growing cell walls of angiosperms. Annu Rev Plant Physiol 37:165–186

    Google Scholar 

  • Hahlbrock K, Scheel D (1989) Physiology and molecular biology of phenylpropanoid metabolism. Annu Rev Plant Physiol Plant Mol Biol 40:347–369

    Google Scholar 

  • van Huystee RB (1987) Some molecular aspects of plant peroxidase biosynthetic studies. Annu Rev Plant Physiol 38:205–217

    Google Scholar 

  • Ishige F, Mori H, Yamazaki K, Imaseki H (1933) Identification of a basic glycoprotein induced by ethylene in primary leaves of azuki bean as a cationic peroxidase. Plant Physiol 101:193–199

    Google Scholar 

  • Jahnen W, Hahlbrock K (1988) Cellular localization of non-host resistance reactions of parsley (Petroselinum crispum) to fungal infection. Planta 173:197–204

    Google Scholar 

  • Johansson A, Rasmussen SK, Harthill JE, Welinder KG (1992) cDNA, amino acid and carbohydrate sequence of barley seedspecific peroxidase BP1. Plant Mol Biol 18:1151–1161

    Google Scholar 

  • Kawalleck P, Plesch G, Hahlbrock K, Somssich IE (1992) Induction by fungal elicitor of S-adenosyl-l-methionine synthetase and S-adenosyl-l-homocysteine hydrolase mRNAs in cultured cells and leaves of Petroselinum crispum. Proc Natl Acad Sci USA 89:4713–4717

    Google Scholar 

  • Kawalleck P, Keller H, Hahlbrock K, Scheel D, Somssich IE (1993) A pathogen-responsive gene of parsley encodes tyrosine decarboxylase. J Biol Chem 268:2189–2194

    Google Scholar 

  • Kiedrowski S, Kawalleck P, Hahlbrock K, Somssich I, Dangl JL (1992) Rapid activation of a novel plant defense gene strictly dependent on the Arabidopsis RPM1 disease resistance locus. EMBO J 11:4677–4684

    Google Scholar 

  • Kolattukudy PE (1987) Lipid-derived defense polymers and waxes and their role in plant-microbe interaction. In: Stumpf PK, Conn EE (ed) The Biochemistry of Plants. Academic Press, New York, pp 291–314

    Google Scholar 

  • Lagrimini ML (1991) Wound-induced deposition of polyphenols in transgenic plants overexpressing peroxidase. Plant Physiol 96:577–583

    Google Scholar 

  • Lagrimini LM, Rothstein S (1987) Tissue specificity of tobacco peroxidase isozymes and their induction by wounding and tobacco mosaic virus infection. Plant Physiol 84:438–442

    Google Scholar 

  • Lagrimini ML, Burkhart W, Moyer M, Rothstein S (1987) Molecular cloning of complementary DNA encoding the lignin-forming peroxidase from tobacco: molecular analysis and tissue-specific expression. Proc Natl Acad Sci USA 84:7542–7546

    Google Scholar 

  • Lawton MA, Lamb CJ (1987) Transcriptional activation of plant defense genes by fungal elicitor, wounding, and infection. Mol Cell Biol 7:335–341

    Google Scholar 

  • Lois R, Dietrich A, Hahlbrock K, 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 

  • Mohan R, Kolattukudy PE (1990) Differential activation of expression of a suberization-associated anionic peroxidase gene in near-isogenic resistant and susceptible tomato lines by elicitors of Verticillium albo-atratrum. Plant Physiol 92:276–280

    Google Scholar 

  • Mohan R, Bajar AM, Kolattukudy PE (1993) Induction of a plant peroxidase gene (tap I) by wounding in transgenic tobacco and activation of tap1/GUS and tap2/GUS chimeric gene fusions in transgenic tobacco by wounding and pathogen attack. Plant Mol Biol 21:341–354

    Google Scholar 

  • Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:6323–6327

    Google Scholar 

  • Nürnberger T, Nennstiel D, Jabs T, Sacks W, Hahlbrock K, Scheel D (1994) High affinity binding of a fungal oligopeptide elicitor to parsley plasma membranes triggers multiple defense responses. Cell 78:449–460

    Google Scholar 

  • Roberts E, Kolattukudy PE (1989) Molecular cloning, nucleotide sequence, and abscisic acid induction of a suberization-associated highly anionic peroxidase. Mol Gen Genet 217:223–232

    Google Scholar 

  • Roberts E, Kutchan T, Kolattukudy PE (1988) Cloning and sequencing of cDNA for a highly anionic peroxidase from potato and the induction of its mRNA in suberizing potato tubers and tomato fruits. Plant Mol Biol. 11:15–26

    Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York

    Google Scholar 

  • Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74:5463–5467

    Google Scholar 

  • Schmelzer E, Krüger-Lebus S, Hahlbrock K (1989) Temporal and spatial patterns of gene expression around sites of attempted fungal infection in parsley leaves. Plant Cell 1:993–1001

    Google Scholar 

  • Sheng J, Jeong J, Mehdy MC (1993) Developmental regulation and phytochrome-mediated induction of mRNAs encoding a proline-rich protein, glycine-rich proteins, and hydroxyprolinerich glycoproteins in Phaseolus vulgaris L. Proc Natl Acad Sci USA 90:828–832

    Google Scholar 

  • Showalter AM (1993) Structure and function of plant cell wall proteins. Plant Cell 5:9–23

    Google Scholar 

  • Showalter AM, Bell JN, Cramer CL, Bailey JA, Varner JE, Lamb CJ (1985) Accumulation of hydroxyproline-rich glycoprotein mRNAs in response to fungal elicitor and infection. Proc Natl Acad Sci USA 82:6551–6555

    Google Scholar 

  • Showalter AM, Zhou J, Rumeau D, Worst SG, Varner JE (1991) Tomato extensin and extensin-like cDNAs: structure and expression in response to wounding. Plant Mol Biol. 16:547–565

    Google Scholar 

  • Somssich IE (1994) Regulatory elements governing pathogenesisrelated (pr) gene expression. In: Nover L (ed) Plant Promoters and Transcription Factors. Springer-Verlag, Berlin Heidelberg, pp 163–179

    Google Scholar 

  • Somssich IE, Schmelzer E, Bollmann J, Hahlbrock K (1986) Rapid activation by fungal elicitor of genes encoding “pathogenesis related” proteins in cultured parsley cells. Proc Natl Acad Sci USA 83:2427–2430

    Google Scholar 

  • Somssich IE, Schmelzer E, Kawalleck P, Hahlbrock K (1988) Gene structure and in situ transcript localization of pathogenesis-related protein 1 in parsley. Mol Gen Genet 213:93–98

    Google Scholar 

  • Somssich IF, Bollmann J, Hahlbrock K, Kombrink E, Schulz W (1989) Differential early activation of defense-related genes in elicitor-treated parsley cells. Plant Mol Biol. 12:227–234

    Google Scholar 

  • Stintzi A, Heitz T, Prasad V, Wiedemann-Merdinoglu S, Kauffmann S, Geoffroy P, Legrand M, Fritig B (1993) Plant ‘pathogenesis-related’ proteins and their role in defense against pathogens. Biochimie 75:687–706

    Google Scholar 

  • Tyson H (1992a) Relationships among amino acid sequences of animal, microbial and plant peroxidases. Theor Appl Genet 84:643–655

    Google Scholar 

  • Tyson H (1992b) Relationships, derived from optimum alignments, among amino acid sequences of plant peroxidases. Can J Bot 70:543–556

    Google Scholar 

  • Varner JE, Lin L-S (1989) Plant cell wall architecture. Cell 56:231–239

    Google Scholar 

  • Vera P, Tornero P, Conejero V (1993) Cloning and expression analysis of a viroid-induced peroxidase from tomato plants. Mol Plant-Microbe Interact 6:790–794

    Google Scholar 

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Communicated by H. Saedler

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Kawalleck, P., Schmelzer, E., Hahlbrock, K. et al. Two pathogen-responsive genes in parsley encode a tyrosine-rich hydroxyproline-rich glycoprotein (hrgp) and an anionic peroxidase. Molec. Gen. Genet. 247, 444–452 (1995). https://doi.org/10.1007/BF00293146

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  • DOI: https://doi.org/10.1007/BF00293146

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