Skip to main content
Log in

Acidic and basic class III chitinase mRNA accumulation in response to TMV infection of tobacco

  • Research Articles
  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Complementary DNA clones encoding acidic and basic isoforms of the class III chitinase were isolated from Nicotiana tabacum. The clones share ca. 65% identity, are equally homologous to the class III chitinases from cucumber and Arabidopsis, and are members of small gene families in tobacco. An acidic class III chitinase was purified from the intercellular fluid of tobacco leaves infected with tobacco mosaic virus (TMV). Partial amino acid sequencing of the protein confirmed that it was encoded by one of the cDNA clones. The mRNAs of the class III chitinases are coordinately expressed in response to TMV infection, both in infected and uninfected tissue. The acidic and basic class III chitinases constitute previously undescribed pathogenesis-related proteins in tobacco.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Abeles FB, Bosshart RP, Forrence LE, Habig WH: Preparation and purification of glucanase and chitinase from bean leaves. Plant Physiol 47: 129–134 (1971).

    Google Scholar 

  2. Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K: Current Protocols in Molecular Biology. John Wiley, New York (1987).

    Google Scholar 

  3. Awade A, De Tapia M, Didierjean L, Burkhard G: Biological function of bean pathogenesis related (PR-3 and PR-4) proteins. Plant Sci 63: 121–130 (1989).

    Google Scholar 

  4. Bednarek SY, Raikhel NV: The barley lectin carboxyl-terminal propeptide is a vacuolar protein sorting determinant in plants. Plant Cell 33, in press (1991).

  5. Bernasconi P, Jolles P, Pilet PE: Increase of lysozyme and chitinase in Rubus calli caused by infection and some polymers. Plant Sci 44: 79–83 (1986).

    Google Scholar 

  6. Bernasconi P, Locher R, Pilet PE, Jolles J, Jolles P: Purification and N-terminal amino-acid sequence of a basic lysozyme from Parthenocissus quinquifolia culture in vitro. Biochim Biophys Acta 915: 254–260 (1987).

    Google Scholar 

  7. Boller T: Induction of hydrolases as a defense reaction against pathogens. UCLA Symp Mol Cell Mol Biol NS 22: 247–262 (1985).

    Google Scholar 

  8. Boller T, Gehri A, Mauch F, Vögeli U: Chitinase in bean leaves: induction by ethylene, purification, properties, and possible function. Planta 157: 22–31 (1983).

    Google Scholar 

  9. Boller T, Kende H: Regulation of wound ethylene synthesis in plants. Nature 286: 259–260 (1980).

    Google Scholar 

  10. Boller T, Métraux J-P: Extracellular localization of chitinase in cucumber. Physiol Mol Plant Path 33: 11–16 (1988).

    Google Scholar 

  11. Broglie KE, Gaynor JJ, Broglie RM: Ethylene-regulated gene expression: Molecular cloning of the genes encoding an endochitinase from Phaseolus vulgaris. Proc Natl Acad Sci USA 83: 6820–6824 (1986).

    PubMed  Google Scholar 

  12. Church GM, Gilbert W: Genomic sequencing. Proc Natl Acad Sci USA 81: 1991–1995 (1984).

    PubMed  Google Scholar 

  13. Durand-Tarif M: Etude de l'induction, par l'éthéphon, de l'expression du gène codant pour la chitinase chez la tomate et analyse de la structure de ce gène. Doctoral dissertation, Université de Paris Sud, Paris (1986).

  14. Friedrich L, Moyer M, Ward E, Ryals J: Pathogenesis-related protein 4 is structurally homologous to the carboxy-terminal domains of hevein, Win-1 and Wind-2. Mol Gen Genet 239: 113–119 (1991).

    Article  Google Scholar 

  15. Gaynor JJ: Primary structure of an endochitinase mRNA from solanum tuberosum. Nucl Acids Res 16: 5210 (1988).

    PubMed  Google Scholar 

  16. Gerstel DU: Segregation in new allopolyploids of Nicotiana. I. Comparison of 6 × (N. tabacum × tomentosiformis and 6 × (N. tabacum × sylvestris). Genetics 45: 1723–1734 (1960).

    Google Scholar 

  17. Gerstel DU: Segregation in new allopolyploids of Nicotiana. II. Discordant ratios from individual loci in 6 × (N. tabacum × N. sylvestris). Genetics 48: 677–689 (1963).

    Google Scholar 

  18. Gerstel DU: Evolutionary problems in some polyploid crop plants. Hereditas Suppl 2: 481604 (1966).

    Google Scholar 

  19. Gerstel DU: Tobacco. In: Simmonds NW (eds) Evolution of Crop Plants, pp. 273–277. Longman, London (1976).

    Google Scholar 

  20. Hattoni M, Sakaki Y: Dideoxy sequencing method using denatured plasmid templates. Anal Biochem 162: 232–238 (1986).

    Google Scholar 

  21. Howard JB, Glazer AN: Papaya-D N-terminal lysozyme sequences and enzymatic properties. J Biol Chem 244: 1399–1409 (1969).

    PubMed  Google Scholar 

  22. Jekel PA, Hartmann BH, Beintema JJ: The primary structure of hevamine, an enzyme with lysozyme/chitinase activity from Hevea brasiliensis latex. Eur J Biochem 200: 123–130 (1991).

    PubMed  Google Scholar 

  23. Keefe D, Hinz U, Meins FJr: The effect of ethylene on the cell-type-specific and intracellular localization of β-1,3-glucanase and chitinase in tobacco leaves. Planta 182: 43–51 (1990).

    Article  Google Scholar 

  24. Lagrimini M, Burkhart W, Moyer M, Rohstein S: 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 (1987).

    Google Scholar 

  25. Leah R, Mikkelsen J, Mundy J, Svendsen IB: Identification of a 28000 dalton endochitinase in barley endosperm. Carlsberg Res Comm 52: 31–37 (1987).

    Google Scholar 

  26. Linthorst HJM, van Loon LC, van Rossum CMA, Mayer A, Bol JF, van Roekel JSC, Meulenhoff JS, Cornelissen BJC: Analysis of acidic and basic chitinases from tobacco and petunia and their constitutive expression in transgenic tobacco. Mol Plant-Microbe Inter 3: 252–258 (1990).

    Google Scholar 

  27. Lotan T, Ori N, Fluhr R: Pathogenesis-related proteins are developmentally regulated in tobacco flowers. Plant Cell 1: 881–887 (1989).

    PubMed  Google Scholar 

  28. Margis-Pinheiro M, Metz-Boutigue MH, Awade A, de Tapia M, le Ret M, Burkhard G: Isolation of a complementary DNA encoding the bean PR4 chitinase: an acidic enzyme with an amino-terminus cysteine-rich domain. Plant Mol Biol 17: 243–253 (1991).

    PubMed  Google Scholar 

  29. Mauch F, Hadwiger LA, Boller T: Ethylene: symptom, not signal for the induction of chitinase and β-1,3-glucanase in pea pods by pathogens and elicitors. Plant Physiol 76: 607–611 (1984).

    Google Scholar 

  30. Mauch F, Hadwiger LA, Boller T: Antifungal hydrolases in pea tissue I. Purification and characterization of two chitinases and two β-1,3-glucanases differentially regulated during development and in response to fungal infection. Plant Physiol 87: 325–333 (1988).

    Google Scholar 

  31. Mauch F, Mauch-Mani B, Boller T: Antifungal hydrolases in pea tissue II. Inhibition of fungal growth by combinations of chitinase and β-1,3-glucanase. Plant Physiol 88: 936–942 (1988).

    Google Scholar 

  32. Meins FJr, Ahl P: Induction of chitinase and β-1,3-glucanase in tobacco leaves infected with Pseudomonas tabaci and Phytophthora parasitica var. nicotiana. Plant Sci 61: 155–161 (1989).

    Article  Google Scholar 

  33. Meins F Jr, Neuhaus J-M, Sperisen C, Ryals J: The primary structure of plant pathogenesis-related glucanohydrolases and their genes. In: Boller T, Meins F Jr (eds) Genes Involved in Plant Defense. Springer-Verlag, Wien/New York, in press.

  34. Métraux J-P, Burkhart W, Moyer M, Dincher S, Middlesteadt W, Williams S, Payne G, Carnes M, Ryals J: Isolation of a complementary DNA encoding a chitinase with structural homology to a bifunctional lysozyme/chitinase. Proc Natl Acad Sci USA 86: 896–900 (1989).

    PubMed  Google Scholar 

  35. Neuhaus J-M, Sticher L, Meins FJr, Boller T: A short C-terminal sequence is necessary and sufficient for the targeting of chitinases to the plant vacuole. Proc Natl Acad Sci USA 88: 10362–10366 (1991).

    PubMed  Google Scholar 

  36. Payne G, Ahl P, Moyer M, Harper A, Beck J, Meins FJr, Ryals J: Isolation of complementary DNA clones encoding pathogenesis-related proteins P and Q, two acidic chitinases from tobacco. Proc Natl Acad Sci USA 87: 98–102 (1990).

    PubMed  Google Scholar 

  37. Payne G, Ward E, Gaffney T, Ahl-Goy P, Moyer M, Harper A, Meins FJr, Ryals J: Evidence for a third structural class of β-1,3-glucanase in tobacco. Plant Mol Biol 16: 797–808 (1990).

    Google Scholar 

  38. Pegg GF: Glucanohydrolases of higher plants: a possible defense mechanism against parasitic fungi. In: Solheim B, Raa J (eds) Cell Wall Biochemistry Related to specificity in Host-Pathogen Relationships, pp. 305–345. Universitetsforlaget, Tromsø (1977).

    Google Scholar 

  39. Reed KC, Mann DA: Rapid transfer of DNA from agarose gels to nylon membranes. Nucl Acids Res 13: 7207–7221 (1985).

    PubMed  Google Scholar 

  40. Robert WK, Selitrennikoff CP: Plant and bacterial chitinase differ in antifungal activity. J Gen Microbiol 134: 169–176 (1988).

    Google Scholar 

  41. Roby D, Toppan A, Esquerri-Tugaye 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).

    Google Scholar 

  42. Samac DA, Hironaka CM, Yallay PE, Shah DM: Isolation and characterization of the genes encoding basic and acidic chitinase in Arabidopsis thaliana. Plant Physiol 93: 907–914 (1990).

    Google Scholar 

  43. Schlumbaum A, Mauch F, Vögeli U, Boller T: Plant chitinases are potent inhibitors of fungal growth. Nature 324: 365–367 (1986).

    Google Scholar 

  44. Shinshi H, Mohnen D, Meins FJr: Regulation of a plant pathogenesis-related enzyme: Inhibition of chitinase and chitinase mRNA accumulation in cultured tobacco tissues by auxin and cytokinin. Proc Natl Acad Sci USA 64: 89–93 (1987).

    Google Scholar 

  45. Shinshi H, Neuhaus J-M, Ryals J, Meins FJr: Structure of a tobacco endochitinase gene: evidence that different chitinase genes can arise by transposition of sequences encoding a cysteine-rich domain. Plant Mol Biol 14: 357–368 (1990).

    PubMed  Google Scholar 

  46. Vögeli-Lange R, Hansen-Gehri A, Boller T, Meins FJr: Induction of the defense-related glucanohydrolases, β-1,3-glucanase and chitinase, by tobacco mosaic virus infection of tobacco leaves. Plant Sci 54: 171–176 (1988).

    Article  Google Scholar 

  47. Ward E, Payne G, Moyer M, Williams S, Dincher S, Sharkey K, Beck J, Taylor H, Ahl-Goy P, Meins FJr, Ryals J: Differential regulation of β-1,3-glucanase messenger RNA in response to pathogen infection. Plant Physiol 96: 390–397 (1991).

    Google Scholar 

  48. Ward E, Uknes S, Williams S, Dincher S, Wiederhold D, Alexander D, Ahl-Goy P, Métraux J-P, Ryals J: Coordinate gene activity in response to agents that induce systemic acquired resistance. Plant Cell 3: 1085–1094 (1991).

    Article  PubMed  Google Scholar 

  49. Yang SF, Hoffmann NE: Ethylene biosynthesis and its regulation in higher plants. Annu Rev Plant Physiol 35: 165–189 (1984).

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lawton, K., Ward, E., Payne, G. et al. Acidic and basic class III chitinase mRNA accumulation in response to TMV infection of tobacco. Plant Mol Biol 19, 735–743 (1992). https://doi.org/10.1007/BF00027070

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00027070

Key words

Navigation