Plant chitinase/lysozyme isoforms show distinct substrate specificity and cleavage site preference towards lipochitooligosaccharide Nod signals

Plant Journal

Volumn 16, Issue 5, 1998, Pages 571-580

  Schultze, Michael ^a   Staehelin, Christian ^a   Brunner, Frédéric ^a   Gerietet, Isabelle ^a   Legrand, Michel ^a   Fritig, Bernard ^a   Kondorosi, Éva ^a   Kondorosi, Adam ^a,b  

^a CNRS   (France)

^b INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

CHITINASE; CLEAVAGE SITE; ENZYME ACTIVITY; ENZYME SPECIFICITY; GLYCOSYL HYDROLASE; HYDROLYSIS; ISOENZYME; LIPOCHITOOLIGOSACCHARIDE; LYSOZYME; PLANT PRODUCT; RHIZOBIUM; SECONDARY METABOLITE;

EID: 0032437026     PISSN: 09607412     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-313X.1998.00326.x     Document Type: Article

References (56)

1. Armand, S., Tomita, H., Heyraud, A., Gey, C., Watanabe, T. and Henrissat, B. (1994) Stereochemical course of the hydrolysis reaction catalyzed by chitinases A1 and D from Bacillus circulans WL-12. FEBS Lett. 343, 177-180.
2. Beintema, J.J. and Terwisscha van Scheltinga, A.C. (1996). Plant lysozymes. In Lysozymes: Model Enzymes in Biochemistry and Biology (Jollès, P., ed.). Basel: Birkhäuser-Verlag, pp. 75-86.
3. Benhamou, N. and Asselin, A. (1989) Attempted localization of a substrate for chitinases in plant cells reveals abundant N-acetyl-D-glucosamine residues in secondary walls. Biol. Cell, 67, 341-350.
4. Boller, T. (1987). Hydrolytic enzymes in plant disease resistance. In Plant Microbe Interactions, Molecular and Genetic Perspectives, Vol. 2 (Kosuge, T. and Nester, E., eds). New York: Macmillan, pp. 385-413.
5. Boller, T., Gehri, A., Mauch, F. and Vögeli, U. (1983) Chitinase in bean leaves: induction by ethylene, purification, properties, and possible function. Planta, 157, 22-31.
6. Broglie, K., Chet, I., Holliday, M., Cressman, R., Biddle, P., Knowlton, S., Mauvais, C.J. and Broglie, R. (1991) Transgenic plants with enhanced resistance to the fungal pathogen Rhizoctonia solani. Science, 254, 1194-1197.
7. Brunner, F., Stintzi, A., Fritig, B. and Legrand, M. (1998) Substrate specificities of tobacco chitinases. Plant J. 14, 225-234.
8. Collinge, D.B., Kragh, K.M., Mikkelsen, J.D., Nielsen, K.K., Rasmussen, U. and Vad, K. (1993) Plant chitinases. Plant J. 3, 31-40.
9. De Jong, A.J., Cordewener, J., Lo Schiavo, F., Terzi, M., Vandekerckhove, J., Van Kammen, A. and De Vries, S.C. (1992) A carrot somatic embryo mutant is rescued by chitinase. Plant Cell, 4, 425-433.
10. De Jong, A.J., Heidstra, R., Spaink, H.P. et al. (1993) Rhizobium lipooligosaccharides rescue a carrot somatic embryo mutant. Plant Cell, 5, 615-620.
11. Dénarié, J., Debellé, F. and Promé, J.C. (1996) Rhizobium lipochitooligosaccharide nodulation factors: Signaling molecules mediating recognition and morphogenesis. Annu. Rev. Biochem. 65, 503-535.
12. Grison, R., Grezes-Besset, B., Schneider, M., Lucante, N., Olsen, L., Leguay, J.J. and Toppan, A. (1996) Field tolerance to fungal pathogens of Brassica napus constitutively expressing a chimeric chitinase gene. Nature Biotechnol. 14, 643-646.
13. Hamel, F., Boivin, R., Tremblay, C. and Bellamare, G. (1997) Structural and evolutionary relationships among chitinases of flowering plants. J. Mol. Evol. 44, 614-624.
14. Hanfrey, C., Fife, M. and Buchanan-Wollaston, V. (1996) Leaf senescence in Brassica napus: expression of genes encoding pathogenesis-related proteins. Plant Mol. Biol. 30, 597-609.
15. Hart, G.W. (1992) Glycosylation. Curr. Op. Cell Biol. 4, 1017-1023.
16. Heidstra, R., Geurts, R., Franssen, H., Spaink, H.P., Van Kammen, A. and Bisseling, T. (1994) Root hair deformation activity of nodulation factors and their fate on Vicia sativa. Plant Physiol. 105, 787-797.
17. Heitz, T., Segond, S., Kauffmann, S., Geoffroy, P., Prasad, V., Brunner, F., Fritig, B. and Legrand, M. (1994) Molecular characterization of a novel tobacco pathogenesis-related (PR) protein: a new plant chitinase/lysozyme. Mol. Gen. Genet. 245, 246-254.
18. Henrissat, B. (1991) A classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem. J. 280, 309-316.
19. Henrissat, B. and Bairoch, A. (1993) New families in the classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem. J. 293, 781-788.
20. Hollis, T., Honda, Y., Fukamizo, T., Marcotte, E., Day, P.J. and Robertus, J.D. (1997) Kinetic analysis of barley chitinase. Arch. Biochem. Biophys. 344, 335-342.
21. Holm, L. and Sander, C. (1994) Structural similarity of plant chitinase and lysozymes from animals and phage. An evolutionary connection. FEBS Lett. 340, 129-132.
22. Iseli, B., Armand, S., Boiler, T., Neuhaus, J.M. and Henrissat, B. (1996) Plant chitinases use two different hydrolytic mechanisms. FEBS Lett. 382, 186-188.
23. Jach, G., Görnhardt, B., Mundy, J., Logemann, J., Pinsdorf, P., Leah, R., Schell, J. and Maas, C. (1995) Enhanced quantitative resistance against fungal disease by combinatorial expression of different barley antifungal proteins in transgenic tobacco. Plant J. 8, 97-109.
24. Jones, J.D.G., Grady, K.L., Suslow, T.V. and Bedbrook, J.R. (1986) Isolation and characterization of genes encoding two chitinase enzymes from Serratia marcescens. EMBO J. 5, 467-473.
25. Kragh, K.M., Hendriks, T., De Jong, A.J., Lo Schiavo, F., Bucherna, N., Højrup, P., Mikkelsen, J.D. and De Vries, S.C. (1996) Characterization of chitinases able to rescue somatic embryos of the temperature-sensitive carrot variant ts11. Plant Mol. Biol. 31, 631-645.
26. Legrand, M., Kauffmann, S., Geoffroy, P. and Fritig, B. (1987) Biological function of pathogenesis-related proteins: Four tobacco pathogenesis-related proteins are chitinases. Proc. Natl Acad. Sci. USA, 84, 6750-6754.
27. Lerouge, P., Roche, P., Faucher, C., Maillet, F., Truchet, G., Promé, J.C. and Dénarié, J. (1990) Symbiotic host-specificity of Rhizobium meliloti is determined by a sulphated and acylated glucosamine oligosaccharide signal. Nature, 344, 781-784.
28. Leung, D.W.M. (1992) Involvement of plant chitinase in sexual reproduction of higher plants. Phytochemistry, 31, 1899-1900.
29. Lin, W., Anuratha, C.S., Datta, K., Potrykus, I., Muthukrishnan, S. and Datta, S.K. (1995) Genetic engineering of rice for resistance to sheath blight. Biotechnology, 13, 686-691.
30. Lotan, T., Ori, N. and Fluhr, R. (1989) Pathogenesis-related proteins are developmentally regulated in tobacco flowers. Plant Cell, 1, 881-887.
31. Mauch, F., Mauch-Mani, B. and Boller, T. (1988) Antifungal hydrolases in pea tissue II. Inhibition of fungal growth by combinations of chitinase and b-1,3-glucanase. Plant Physiol. 88, 936-942.
32. Meins, F., Fritig, B., Linthorst, H.J.M., Mikkelsen, J.D., Neuhaus, J.-M. and Ryals, J. (1994) Plant chitinases genes. Plant Mol. Biol. Rep. 12, S22-S28.
33. Melchers, L.S., Apotheker-de Groot, M., Van der Knaap, J., Ponstein, A.S., Sela-Buurlage, M.B., Bol, J.F., Cornelissen, B.J.C., Van den Elzen, P.J.M. and Linthorst, H.J.M. (1994) A new class of tobacco chitinases homologous to bacterial exo-chitinases displays antifungal activity. Plant J. 5, 469-480.
34. Mikkelsen, J.D., Berglund, L., Nielsen, K.K., Christiansen, H. and Bojsen, K. (1992). Structure of endochitinase genes from sugar beets. In Advances in Chitin and Chitosan (Brine, C.J., Sandford, P.A. and Zikakis, J.P., eds). Amsterdam: Elsevier, pp. 344-353.
35. Minic, Z., Brown, S., De Kouchkovsky, Y., Schultze, M. and Staehelin, C. (1998) Purification and characterization of a novel chitinase-lysozyme, of another chitinase, both hydrolysing Rhizobium meliloti Nod factors, and of a pathogenesis-related protein from Medicago sativa roots. Biochem. J. 332, 329-335.
36. Monzingo, A.F., Marcotte, E.M., Hart, P.J. and Robertus, J.D. (1996) Chitinases, chitosanases, and lysozymes can be divided into procaryotic and eucaryotic families sharing a conserved core. Nature Struct. Biology, 3, 133-140.
37. Neale, A.D., Wahleithner, J.A., Lund, M., Bonnett, H.T., Kelly, A., Meeks-Wagner, D.R., Peacock, W.J. and Dennis, E.S. (1990) Chitinase, B-1,3-glucanase, osmotin, and extension are expressed in tobacco explants during flower formation. Plant Cell, 2, 673-684.
38. Neuhaus, J.M., Ahl-Goy, P., Hinz, U., Flores, S. and Meins, F. (1991) High-level expression of a tobacco chitinase gene in Nicotiana sylvestris. Susceptibility of transgenic plants to Cercospora nicotianae infection. Plant Mol. Biol. 16, 141-151.
39. Neuhaus, J.M., Fritig, B., Linthorst, H.J.M., Meins, F., Mikkelsen, J.D. and Ryals, J. (1996) A revised nomenclature for chitinase genes. Plant Mol. Biol. Rep. 14, 102-104.
40. Nielsen, K.K., Bojsen, K., Roepstorff, P. and Mikkelsen, J.D. (1994) A hydroxyproline-containing class IV chitinase of sugar beet is glycosylated with xylose. Plant Mol. Biol. 25, 241-257.
41. Nielsen, K.K., Mikkelsen, J.D., Kragh, K.M. and Bojsen, K. (1993) An acidic class III chitinase in sugar beet: Induction by Cercospora beticola, characterization, and expression in transgenic tobacco plants. Mol. Plant Microbe Interact. 6, 495-506.
42. Ponstein, A.S., Bres-Vloemans, S.A., Sela-Buurlage, M.B., Van den Elzen, P.J.M., Melchers, L.S. and Cornelissen, B.J.C. (1994) A novel pathogen- and wound-inducible tobacco (Nicotiana tabacum) protein with antifungal activity. Plant Physiol. 104, 109-118.
43. Samac, D.A. and Shah, D.M. (1994) Effect of chitinase antisense RNA expression on disease susceptibility of Arabidopsis plants. Plant Mol. Biol. 25, 587-596.
44. Schlumbaum, A., Mauch, F., Vögeli, U. and Boller, T. (1986) Plant chitinases are potent inhibitors of fungal growth. Nature, 324, 365-367.
45. Schmidt, J., Röhrig, H., John, M., Wieneke, U., Stacey, G., Koncz, C. and Schell, J. (1993) Alteration of plant growth and development by Rhizobium nodA and nodB genes involved in the synthesis of oligosaccharide signal molecules. Plant J. 4, 651-658.
46. Schultze, M. and Kondorosi, A. (1998) Regulation of symbiotic root nodule development. Annu. Rev. Genet. 32, 33-57.
47. Schultze, M., Quiclet-Sire, B., Kondorosi, É., Virelizier, H., Glushka, J.N., Endre, G., Géro, S.D. and Kondorosi, Á. (1992) Rhizobium meliloti produces a family of sulfated lipooligosaccharides exhibiting different degrees of plant host specificity. Proc. Natl Acad. Sci. USA, 89, 192-196.
48. Spaink, H.P., Wijfjes, A.H.M., Van Vliet, T.B., Kijne, J.W. and Lugtenberg, B.J.J. (1993) Rhizobial lipo-oligosaccharide signals and their role in plant morphogenesis; are analogous lipophilic chitin derivatives produced by the plant? Austr. J. Plant Physiol. 20, 381-392.
49. Staehelin, C., Foucher, F., Kondorosi, É., Kondorosi, A. and Schultze, M. (1996). Substrate specificity of six lipochitooligosaccharide cleaving enzymes from Medicago. In Chitin Enzymology Volume 2 (Muzzarelli, R.A.A., ed.). Grottammare, Italy: Atec Edizioni, pp. 371-378.
50. Staehelin, C., Granado, J., Müller, J., Wiemken, A., Mellor, R.B., Felix, G., Regenass, M., Broughton, W.J. and Boiler, T. (1994b) Perception of Rhizobium nodulation factors by tomato cells and inactivation by root chitinases. Proc. Natl Acad. Sci. USA, 91, 2196-2200.
51. Staehelin, C., Schultze, M., Kondorosi, É. and Kondorosi, A. (1995) Lipo-chitooligosaccharide nodulation signals from Rhizobium meliloti induce their rapid degradation by the host plant alfalfa. Plant Physiol. 108, 1607-1614.
52. Staehelin, C., Schultze, M., Kondorosi, É., Mellor, R.B., Boller, T. and Kondorosi, Á. (1994a) Structural modifications in Rhizobium meliloti Nod factors influence their stability against hydrolysis by root chitinases. Plant J. 5, 319-330.
53. Stintzi, A., Heitz, T., Prasad, V., Wiedemann-Merdinoglu, S., Kauffmann, S., Geoffroy, P., Legrand, M. and Fritig, B. (1993) Plant 'pathogenesis-related' proteins and their role in defense against pathogens. Biochimie, 75, 687-706.
54. Vierheilig, H., Alt, M., Neuhaus, J.M., Boller, T. and Wiemken, A. (1993) Colonization of transgenic Nicotiana sylvestris plants, expressing different forms of Nicotiana tabacum chitinase, by the root pathogen Rhizoctonia solani and by the mycorrhizal symbiont Glomus mosseae. Mol. Plant-Microbe Interact. 6, 261-264.
55. Vogelsang, R. and Barz, W. (1993) Purification, characterization and differential hormonal regulation of a b-1,3-glucanase and two chitinases from chickpea (Cicer arietinum L). Planta, 189, 60-69.
56. Zhu, Q., Maher, E.A., Masoud, S., Dixon, R.A. and Lamb, C.J. (1994) Enhanced protection against fungal attack by constitutive co-expression of chitinase and glucanase genes in transgenic tobacco. Biotechnology, 12, 807-812.