Primary structure and expression of acidic (class II) chitinase in potato

Plant Molecular Biology

Volumn 35, Issue 6, 1997, Pages 749-761

  Büchter, Rainer ^b   Strömberg, Anita ^c   Schmelzer, Elmon ^a   Kombrink, Erich ^a  

^a MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

^b UNIVERSITY OF WUPPERTAL   (Germany)

^c Blomgatan 2E   (Sweden)

Author keywords

Fungal elicitor; Gene expression; Pathogen defense; Pathogenesis related protein; Phytophthora infestans; Salicylic acid; Stress response; Wounding

Indexed keywords

CHITINASE; COMPLEMENTARY DNA; ETHYLENE; ETHYLENE DERIVATIVE; MESSENGER RNA; SALICYLIC ACID; SALICYLIC ACID DERIVATIVE;

AMINO ACID SEQUENCE; ARTICLE; BIOSYNTHESIS; CHEMISTRY; CLASSIFICATION; DNA SEQUENCE; DRUG EFFECT; ENZYME INDUCTION; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PH; POTATO;

AMINO ACID SEQUENCE; BASE SEQUENCE; CHITINASE; DNA, COMPLEMENTARY; ENZYME INDUCTION; ETHYLENES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, PLANT; HYDROGEN-ION CONCENTRATION; MOLECULAR SEQUENCE DATA; RNA, MESSENGER; SALICYLIC ACID; SALICYLIC ACIDS; SEQUENCE ANALYSIS, DNA; SOLANUM TUBEROSUM;

EID: 0031471181     PISSN: 01674412     EISSN: None     Source Type: Journal    
DOI: 10.1023/A:1005830706507     Document Type: Article

References (67)

1. Arlorio M, Ludwig A, Boller T, Bonfante P: Inhibition of fungal growth by plant chitinases and β-1,3-glucanases. A morphological study. Protoplasma 171: 34-43 (1992).
2. Barber MS, Bertram RE, Ride JP: Chitin oligosaccharides elicit lignification in wounded wheat leaves. Physiol Mol Plant Path 34: 3-12 (1989).
3. Bartnicki-Garcia S: Cell wall chemistry, morphogenesis, and taxonomy of fungi. Annu Rev Microbiol 22: 87-108 (1968).
4. Beerhues L, Kombrink E: Primary structure and expression of mRNAs encoding basic chitinase and 1,3-β-glucanase in potato. Plant Mol Biol 24: 353-367 (1994).
5. Boller T: Hydrolytic enzymes in plant disease resistance. In: Kosuge T, Nester EW (eds) Plant-Microbe Interactions, vol 2: Molecular and Genetic Perspectives, pp. 385-413. Macmillan, New York (1987).
6. Brederode FT, Linthorst HJM, Bol JF: Differential induction of acquired resistance and PR gene expression in tobacco by virus infection, ethephon treatment, UV light and wounding. Plant Mol Biol 17: 1117-1125 (1991).
7. Brogue K, Chet I, Holliday M, Cressman R, Biddle P, Knowlton S, Mauvais CJ, Broglie R: Transgenic plants with enhanced resistance to the fungal pathogen Rhizoctonia solani. Science 254: 1194-1197 (1991).
8. Chen EY, Seeburg PH: Supercoil sequencing: a fast and simple method for sequencing plasmid DNA. DNA 4: 165-170 (1985).
9. Chen R-D, Yu L-X, Greer AF, Cheriti H, Tabaeizadeh Z: Isolation of an osmotic stress- and abscisic acid-induced gene encoding an acidic chitinase from Lycopersicon chilense. Mol Gen Genet 245: 195-202 (1994).
10. Cohen Y, Gisi U, Mösinger E: Systemic resistance of potato plants against Phytophthora infestans induced by unsaturated fatty acids. Physiol Mol Plant Path 38: 255-263 (1991).
11. Collinge DB, Kragh KM, Mikkelsen JD, Nielsen KK, Rasmussen U, Vad K: Plant chitinases. Plant J 3: 31-40 (1993).
12. Coquoz J-L, Buchala AJ, Meuwly P, Métraux J-P: Arachidonic acid induces local but not systemic synthesis of salicylic acid and confers systemic resistance in potato plants to Phytophthora infestons and Alternaria solani. Phytopathology 85: 1219-1224 (1995).
13. Cutt JR, Klessig DF: Pathogenesis-related proteins. In: Boller T, Meins F Jr (eds) Genes Involved in Plant Defense, pp. 209-243. Springer-Verlag, Wien (1992).
14. Danhash N, Wagemakers CAM, van Kan JAL, de Wit PJGM: Molecular characterization of four chitinase cDNAs obtained from Cladosporium fulvum-infected tomato. Plant Mol Biol 22: 1017-1029 (1993).
15. Devereux J, Haeberli P, Smithies O: A comprehensive set of sequence analysis programs for the VAX. Nucl Acids Res 12: 387-395 (1984).
16. Doke N, Ramirez AV, Tomiyama K: Systemic induction of resistance in potato plants against Phytophthora infestons by local treatment with hyphal wall components of the fungus. J Phytopath 119: 232-239 (1987).
17. Garcia-Garcia F, Schmelzer E, Hahlbrock K, Roxby R: Differential expression of chitinase and β-1,3-glucanase genes in various tissues of potato plants. Z Naturforsch 49c: 195-203 (1994).
18. Jach G, Görnhardt B, Mundy J, Logemann J, Pinsdorf E, Leah R, Schell J, Maas C: Enhanced quantitative resistance against fungal disease by combinatorial expression of different barley antifungal proteins in transgenic tobacco. Plant J 8: 97-109 (1995).
19. Kawalleck P, Somssich IE, Feldbrügge M, Hahlbrock K, Weisshaar B: Polyubiquitin gene expression and structural properties of the ubi4-2 gene in Petroselinum crispum. Plant Mol Biol 21: 673-684 (1993).
20. Kombrink E, Beerhues L, Garcia-Garcia F, Hahlbrock K, Müller M, Schröder M, Witte B, Schmelzer E: Expression patterns of defense-related genes in infected and uninfected plants. In: Fritig B, Legrand M (eds) Mechanisms of Plant Defense Responses, vol 2, pp. 236-249. Kluwer Academic Publishers, Dordrecht (1993).
21. 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).
22. Kombrink E, Somssich IE: Defense responses of plants to pathogens. In: Andrews JH, Tommerup IC (eds), Advances in Botanical Research (incorporating Advances in Plant Pathology), vol 21, pp. 1-34. Academic Press, London (1995).
23. Kombrink E, Somssich IE: Pathogenesis-related proteins and plant defense. In: Carroll G, Tudzynski P (eds) The Mycota, vol 5, Part A: Plant Relationships, pp. 107-128. Springer-Verlag, Berlin/Heidelberg (1997).
24. Kössel H, Edwards K, Koch W, Langridge P, Schiefermayr E, Schwarz Z, Strittmatter G, Zenke G: Structural and functional analysis of an rRNA operon and its flanking tRNA genes from Zea mays chloroplasts. Nucl Acids Res Symp Ser 11: 117-120 (1982).
25. Kurosaki F, Tashiro N, Nishi A: Role of chitinase and chitin oligosaccharides in lignification response of cultured carrot cells treated with mycelial walls. Plant Cell Physiol 29: 527-531 (1988).
26. Lawton K, Ward E, Payne G, Moyer M, Ryals J: Acidic and basic class in chitinase mRNA accumulation in response to TMV infection of tobacco. Plant Mol Biol 19: 735-743 (1992).
27. Lawton KA, Beck J, Potter S, Ward E, Ryals J: Regulation of cucumber class in chitinase gene expression. Mol Plant-Microbe Interact 7: 48-57 (1994).
28. Linthorst HJM: Pathogenesis-related proteins of plants. Crit Rev Plant Sci 10: 123-150 (1991).
29. Linthorst HJM, van Loon LC, van Rossum CMA, Mayer A, Bol JF, van Roekel JSC, Meulenhoff EJS, Cornelissen BJC: Analysis of acidic and basic chitinases from tobacco and petunia an their constitutive expression in transgenic tobacco. Mol Plant-Microbe Interact 3: 252-258 (1990).
30. Logemann J, Jach G, Logemann S, Leah R, Wolf G, Mundy J, Oppenheim A, Chet I, Schell J: Expression of a ribosome inhibiting protein (RIP) or a bacterial chitinase leads to fungal resistance in transgenic plants. In: Fritig B, Legrand M (eds) Mechanisms of Plant Defense Responses, pp. 446-448. Kluwer Academic Publishers, Dordrecht (1993).
31. Lois R, Dietrich A, Hahlbrock K, Schulz W: A phenylalanine ammonia-lyase gene from parsley: structure, regulation and identification of elicitor and light responsive cis-acting elements. EMBO J 8: 1641-1648 (1989).
32. Malamy J, Carr JP, Klessig DF, Raskin I: Salicylic acid: a likely endogenous signal in the resistance response of tobacco to viral infection. Science 250: 1002-1004 (1990).
33. Margis-Pinheiro M, Metz-Boutigue MH, Awade A, de Tapia M, le Ret M, Burkard 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).
34. Mauch F, Mauch-Mani B, Boller T: Antifungal hydrolases in pea tissue. II. Inhibition of fungal growth by combinations of chitinase and 1,3-β-glucanase. Plant Physiol 88: 936-942 (1988).
35. Melchers LS, Apotheker-de Groot M, van der Knaap JA, Ponstein AS, Sela-Buurlage MB, Bol JF, Cornelissen BJC, van den Elzen PJM, Linthorst HJM: A new class of tobacco chitinase homologous to bacterial exo-chitinases displays antifungal activity. Plant J 5: 469-480 (1994).
36. Metraux JP, 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).
37. Métraux JP, Signer H, Ryals J, Ward E, Wyss-Benz M, Gaudin J, Raschdorf K, Schmid E, Blum W, Inverardi B: Increase in salicylic acid at the onset of systemic acquired resistance in cucumber. Science 250: 1004-1006 (1990).
38. Neuhaus J-M, Ahl-Goy P, Hinz U, Flores S, Meins F Jr: 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 (1991).
39. Neuhaus J-M, Sticher L, Meins F Jr, 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).
40. Niebel A, Heungens K, Barthels N, Inzé D, Van Montagu M, Gheysen G: Characterization of a pathogen-induced potato catalase and its systemic expression upon nematode and bacterial infection. Mol Plant-Microbe Interact 8: 371-378 (1995).
41. Nielsen KK, Mikkelsen JD, Kragh KM, Bojsen K: 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 (1993).
42. Ori N, Sessa G, Lotan T, Himmelhoch S, Fluhr R: A major stylar matrix polypeptide (sp41) is a member of the pathogenesis-related proteins superclass. EMBO J 9: 3429-3436 (1990).
43. Payne G, Ahl P, Moyer M, Harper A, Beck J, Meins F Jr, 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).
44. Rasmussen JB, Hammerschmidt R, Zook MN: Systemic induction of salicylic acid accumulation in cucumber after inoculation with Pseudomonas syringae pv syringae. Plant Physiol 97: 1342-1347 (1991).
45. Ren Y-Y, West CA: Elicitation of diterpene biosynthesis in rice (Oryza saliva L.) by chitin. Plant Physiol 99: 1169-1178 (1992).
46. Roby D, Gadelle A, Toppan A: Chitin oligosaccharides as elicitors of chitinase activity in melon plants. Biochem Biophys Res Commun 143: 885-892 (1987).
47. Ryals JA, Neuenschwander UH, Willits MG, Molina A, Steiner H-Y, Hunt MD: Systemic acquired resistance. Plant Cell 8: 1809-1819 (1996).
48. Samac DA, Shah DM: Developmental and pathogen-induced activation of the Arabidopsis acidic chitinase promoter. Plant Cell 3: 1063-1072 (1991).
49. Schmelzer E, Krüger-Lebus S, Hahlbrock K: Temporal and spatial patterns of gene expression around sites of attempted fungal infection in parsley leaves. Plant Cell 1: 993-1001 (1989).
50. Schröder M, Hahlbrock K, Kombrink E: Temporal and spatial patterns of 1,3-β-glucanase and chitinase induction in potato leaves infected by Phytophthora infestans. Plant J 2: 161-172 (1992).
51. Sela-Buurlage MB, Ponstein AS, Bres-Vloemans SA, Melchers LS, van den Elzen PJM, Cornelissen BJC: Only specific tobacco (Nicotiana tabacum) chitinases and β-1,3-glucanases exhibit antifungal activity. Plant Physiol 101: 857-863 (1993).
52. Shinshi H, Mohnen D, Meins F Jr: 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 84: 89-93 (1987).
53. Somssich IE, Bollmann J, Hahlbrock K, Kombrink E, Schulz W: Differential early activation of defense-related genes in elicitor-treated parsley cells. Plant Mol Biol 12: 227-234 (1989).
54. Stintzi A, Heitz T, Prasad V, Wiedemann-Merdinoglu S, Kauffmann S, Geoffroy P, Legrand M, Fritig B: Plant 'pathogenesis-related' proteins and their role in defense against pathogens. Biochimie 75: 687-706 (1993).
55. Strömberg A, Brishammar S: Induction of systemic resistance in potato (Solanum tuberosum L.) plants to late blight by local treatment with Phytophthora infestans (Mont.) de Bary, Phytophthora cryptogea Pethyb. & Laff., or dipotassium phosphate. Potato Res 34: 219-225 (1991).
56. Uknes S, Winter AM, Delaney T, Vernooij B, Morse A, Friedrich L, Nye G, Potter S, Ward E, Ryals J: Biological induction of systemic acquired resistance in Arabidopsis. Mol Plant-Microbe Interact 6: 692-698 (1993).
57. van den Elzen PJM, Jongedijk E, Melchers LS, Cornelissen BJC: Virus and fungal resistance: from laboratory to field. Phil Trans R Soc Lond B 342: 271-278 (1993).
58. van Loon LC, Pierpoint WS, Boller T, Conejero V: Recommendations for naming plant pathogenesis-related proteins. Plant Mol Biol Rep 12: 245-264 (1994).
59. Verburg JG, Smith CE, Lisek CA, Huynh QK: Identification of an essential tyrosine residue in the catalytic site of a chitinase isolated from Zea mays that is selectively modified during inactivation with 1-ethyl-3(3-dimethylaminopropyl)-carbodiimide. J Biol Chem 267: 3886-3893 (1992).
60. Vernooij B, Friedrich L, Morse A, Reist R, Kolditz-Jawhar R, Ward E, Uknes S, Kessmann H, Ryals J: Salicylic acid is not the translocated signal responsible for inducing systemic acquired resistance but is required in signal transduction. Plant Cell 6: 959-965 (1994).
61. von Heijne G: Patterns of amino acids near signal-sequence cleavage sites. Eur J Biochem 133: 17-21 (1983).
62. Ward ER, Uknes SJ, Williams SC, Dincher SS, Wiederhold DL, Alexander DC, Ahl-Goy P, Métraux J-P, Ryals JA: Coordinate gene activity in response to agents that induce systemic acquired resistance. Plant Cell 3: 1085-1094 (1991).
63. Wemmer T, Kaufmann H, Kirch H-H, Schneider K, Lottspeich F, Thompson RD: The most abundant soluble basic protein of the stylar transmitting tract in potato (Solanum tuberosum L.) is an endochitinase. Planta 194: 264-273 (1994).
64. Witte B, Hahlbrock K, Kombrink E: Purification, characterization and cloning of inducible and constitutively expressed chitinases from potato leaves. (In preparation.)
65. Wubben JP, Lawrence CB, de Wit PJGM: Differential induction of chitinase and 1,3-β-glucanase gene expression in tomato by Cladosporium fulvum and its race-specific elicitors. Physiol Mol Plant Path 48: 105-116 (1996).
66. Zhu B, Chen THH, Li PH: Expression of three osmotin-like protein genes in response to osmotic stress and fungal infection in potato. Plant Mol Biol 28: 17-26 (1995).
67. Zhu Y, Maher EA, Masoud S, Dixon RA, Lamb CJ: Enhanced protection against fungal attack by constitutive co-expression of chitinase and glucanase genes in transgenic tobacco. Bio/technology 12: 807-812 (1994).