An epidermis/papilla-specific oxalate oxidase-like protein in the defence response of barley attacked by the powdery mildew fungus

Plant Molecular Biology

Volumn 36, Issue 1, 1998, Pages 101-112

  Wei, Yangdou ^a,c   Zhang, Ziguo ^a,d   Andersen, Claus H ^a,e   Schmelzer, Elmon ^b   Gregersen, Per L ^a   Collinge, David B ^a   Smedegaard Petersen, Viggo ^a   Thordal Christensen, Hans ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

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

^c UNIVERSITY OF GUELPH   (Canada)

^d UNIVERSITY OF OXFORD   (United Kingdom)

^e Danish Plant Breeding Ltd   (Denmark)

Author keywords

Epidermis; Germin; H2O2; Oxalate oxidase; Papilla; Resistance

Indexed keywords

CELL WALL; CROSS LINKING; DNA ISOLATION; FUNGUS RESISTANCE; INOCULATION; OLIGOMER; OXALATE OXIDASE; WESTERN BLOTTING;

AMINO ACID SEQUENCE; ASCOMYCOTA; BASE SEQUENCE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, PLANT; GENE LIBRARY; HORDEUM; MOLECULAR SEQUENCE DATA; OXIDOREDUCTASES; PLANT EPIDERMIS; PLANT LEAVES; POLYMERASE CHAIN REACTION; PROTEIN SORTING SIGNALS; RECOMBINANT PROTEINS; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; SEQUENCE HOMOLOGY, NUCLEIC ACID; TIME FACTORS; TRANSCRIPTION, GENETIC;

BLUMERIA; BLUMERIA GRAMINIS; EMBRYOPHYTA; ERYSIPHALES; ERYSIPHE; FUNGI; HORDEUM; HORDEUM VULGARE SUBSP. VULGARE;

EID: 0031905755     PISSN: 01674412     EISSN: None     Source Type: Journal    
DOI: 10.1023/A:1005955119326     Document Type: Article

References (55)

1. Aist JR, Bushnell WR: Invasion of plants by powdery mildew fungi, and cellular mechanisms of resistance. In: Cole GT, Hoch HC (eds) The Fungal Spore and Disease Initiation in Plants and Animals, pp. 321-345. Plenum Press, New York (1991).
2. Anderson MLM, Young BD: Quantitative filter hybridisation. In: Hames BD, Higgins SJ (eds) Nucleic Acid Hybridisation: A Practical Approach, pp. 73-111. IRL Press, Oxford (1985).
3. Ausubel FM, Brent R, Kingston RE, Moore DD, Smith JA, Seidman JG, Struhl K: Current Protocols in Molecular Biology 1987-1988. John Wiley, New York (1987).
4. Baker CJ, Orlandi EW: Active oxygen in plant pathogenesis. Annu Rev Phytopath 33: 299-321 (1995).
5. Berna A, Bernier F: Regulated expression of a wheat germin gene in tobacco: oxalate oxidase activity and apoplastic localization of the heterologous protein. Plant Mol Biol 33: 417-429 (1997).
6. Bernier F, Limieux G, Pallotta D: Gene families encode the major encystment-specific proteins of Physarum polycephalum plasmodia. Gene 59: 265-277 (1987).
7. Boyd LA, Smith PH, Foster EM Brown JKM: The effects of allelic variation at the Mla resistance locus in barley on the early development of Erysiphe graminis f.sp. hordei and host responses. Plant J 7: 959-968 (1995).
8. Brandt J, Thordal-Christensen H, Vad K, Gregersen PL, Collinge DB: A pathogen-induced gene of barley encodes a protein showing high similarity to a protein kinase regulator. Plant J. 2: 815-820 (1992).
9. Bryngelsson T, Sommer-Knudsen J, Gregersen PL, Collinge DB, Ek B, Thordal-Christensen H: Purification, characterization and molecular cloning of basic PR-1-type pathogenesis-related proteins from barley. Mol Plant-Microbe Interact 7: 267-275 (1994).
10. Clark AM, Verbeke JA, Bohnert HJ: Epidermis-specific gene expression in Pachyphytum. Plant Cell 4: 1189-1198 (1992).
11. Clark TA, Zeyen RJ, Carver TLW, Smith AG, Bushnell WR: Epidermal cell cytoplasmic events and response gene transcript accumulation during Erysiphe graminis attack in isogenic barley lines differing at the Ml-o locus. Physiol Mol Plant Path 46: 1-16 (1995).
12. Collinge DB, Bryngelsson T. Gregersen PL, Smedegaard-Petersen V, Thordal-Christensen H: Resistance against fungal pathogens: its nature and regulation. In: Basra AS, Basra R (eds) Mechanisms of Environmental Stress Resistance in Plants, pp. 335-372. Harwood Academic Publishers, Chur, Switzerland (1997).
13. Collinge DB, Gregersen PL, Thordal-Christensen H: The induction of gene expression in response to pathogenic microbes. In: Basra AS (ed) Mechanisms of Plant Growth and Improved Productivity: Modern Approaches, pp. 391-433. Marcel Dekker, New York (1984).
14. 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: 405-414 (1987).
15. Davidson AD, Manners JM, Simpson RS, Scott KJ: Altered host gene expression in near-isogenic barley conditioned by different genes for resistance during infection by Erysiphe graminis f.sp. hordei. Physiol Mol Plant Path 32: 127-139 (1988).
16. Devereux J, Haeberli P, Smithies O: A comprehensive set of sequence analysis programs for the VAX. Nucl Acids Res 12: 387-395 (1984).
17. Dixon RA, Harrison MJ: Activation, structure, and organization of genes involved in microbial defense in plants. Adv Gen 28: 165-234 (1990).
18. Domon J-M, Dumas B, Lainé E, Meyer Y, David A, David H: Three glycosylated polypeptides secreted by several embryogenic cell cultures of pine show highly specific serological affinity to antibodies directed against the wheat germin apoprotein monomer. Plant Physiol 108: 141-148 (1995).
19. Dumas B, Freyssinet G, Pallett KE. Tissue-specific expression of germin-like oxlate oxidase during development and fungal infection of barley seedlings. Plant Physiol 107: 1091-1096 (1995).
20. Dumas B, Sailland A, Cheviet J-P, Freyssinet g, Pallett K. Identification of barley oxalate oxidase as a germin-like protein. CR Acad Sci Paris 316: 793-798 (1993).
21. 12-specificed race-specific resistance to powdery mildew in barley. Plant Cell 6: 983-994 (1994).
22. Gregersen PL, Collinge DB, Smedegaard-Petersen V: Early induction of new mRNAs accompanies the resistance reaction of barley to the wheat pathogen, Erysiphe graminis f.sp. tritici. Physiol Mol Plant Path 36: 471-481 (1990).
23. Gregersen PL, Thordal-Christensen H, Förster H, Collinge DB: Differential gene transcript accumulation in barley leaf epidermis and mesophyll in response to attack by Blumeria graminis f.sp. hordei. Physiol Mol Plant Path (in press)
24. Harlow E, Lane D: Antibodies: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY (1988).
25. Heintzen C, Fischer R, Melzer S, Kappeler S, Apel K, Staiger D. Circardian oscillations of a transcript encoding a germin-like protein that is associated with cell walls in young leaves of the long-day plant Sinapis alba L. Plant Physiol 106: 905-915 (1994).
26. Hurkman WJ, Lane BG, Tanaka CK: Nucleotide sequence of a transcript encoding a germin-like protein that is present in salt-stressed barley (Hordeum vulgare L.) roots. Plant Physiol 104: 803-804 (1994).
27. Hurkman WJ, Tanaka CK: Germin gene expression is induced in wheat leaves by powdery mildew infection. Plant Physiol 111: 735-739 (1996).
28. Hurkman WJ, Tao HP, Tanaka CK: Germin-like polypeptides increase in barley roots during salt stress. Plant Physiol 97: 366-374 (1991).
29. Jakobsen KS, Breivold E, Hornes E: Purification of mRNA directly from crude plant tissues in 15 minutes using magnetic oligo dT microspheres. Nucl Acids Res 18: 3669 (1990).
30. Joshi CP: An inspection of the domain between putative TATA box and translation start site in 79 plant genes. Nucl Acids Res 15: 6643-6653 (1987).
31. Kita N, Toyota H, Shishiyama J: Histochemical reactions of papillae and cytoplasmic aggregate in epidermal cells of barley leaves infected by Erysiphe graminis hordei. Ann Phytopath Soc Japan 46: 263-265 (1980).
32. Kølster P, Munk L, Stølen O, Løhde J: Near-isogenic barley lines with genes for resistance to powdery mildew. Crop Sci 26: 903-907 (1986).
33. Lane BG: Oxalate, germin, and the extracellular matrix of higher plants. FASEB J 8: 294-301 (1994).
34. Lane BG, Bernier F, Dratewka-Kos E, Shafai R, Kennedy TD, Pyne C, Munro JR, Vaughan T, Walters D, Altomare F: Homologies between members of the germin gene family in hexaploid wheat and similarities between these wheat germins and certain Physarum spherulins. J Biol Chem 16: 10461-10469 (1991).
35. Lane BG, Dunwell JM, Ray JA, Schmitt MR, Cuming AC: Germin, a protein marker of early plant development, is an oxalate oxidase. J Biol Chem 268: 12239-12242 (1993).
36. Michalowski CB, Bohnert HJ: Nucleotide sequence of a root-specific transcript encoding a germin-like protein from the halophyte Mesembryanthemum crystallinum. Plant Physiol 100: 537-538 (1992).
37. Ono M, Sage-Ono K, Inoue M, Kamada H, Harada H: Transient increase in the level of mRNA for a germin-like protein in leaves of the short-day plant Pharbatis nil during the photoperiodic induction of flowering. Plant Cell Physiol 37: 855-861 (1996).
38. Pundir CS: Purification and properties of oxalate oxidase from Sorghum leaves. Phytochemistry 30: 1065-1067 (1991).
39. Russo VM, Bushnell WR: Responses of barley cells to puncture by microneedles and to attempted penetration by Erysiphe graminis f.sp. hordei. Can J Bot 67: 2912-2921 (1989).
40. Sambrook J, Fritsch EF, Maniatis T: Molecular Cloning: A Laboratory Manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY (1989).
41. Satyapal, Pundir CS: Purification and properties of an oxalate oxidase from leaves of grain sorghum hybrid CSH-5. Biochim Biophys Acta 1161: 1-5 (1993).
42. Schmelzer E, Jahnen W, Hahlbrock K: In situ localization of light-induced chalcone synthase mRNA, chalcone synthase, and flavonoid end priducts in epidermal cells of parsley leaves. Proc Natl Acad Sci USA 85: 2989-2993 (1988).
43. 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).
44. Scott KJ: The molecular analysis of barley resistance to powdery mildew. In: Shewry PR (ed) Barley: Genetics, Biochemistry, Molecular Biology and Biotechnology, pp. 481-495. CAB International, Wallingford, UK (1992).
45. Smart MG, Aist JR, Israel HW: Structure and function of wall appositions. 1. General histochemistry of papillae in barley coleoptiles attacked by Erysiphe graminis f. sp. hordei. Can J Bot 64: 793-801 (1986).
46. Swart S, Logman TJJ, Smit G, Lugtenberg BJJ, Kijne JW: Purification and partial characterization of a glycoprotein from pea (Pisum sativum) with receptor activity for rhicadhesin, an attachment protein of Rhizobiaceae. Plant Mol Biol 24: 171-183 (1994).
47. Thordal-Christensen H, Brandt J, Cho BH, Rasmussen SK, Gregersen PL, Smedegaard-Petersen V, Collinge DB: cDNA cloning and characterization of two barley peroxidase transcripts induced differentially by the powdery mildew fungus Erysiphe graminis. Physiol Mol Plant Path 40: 395-409 (1992).
48. Thordal-Christensen H, Smedegaard-Petersen V: Comparison of resistance-inducing abilities of virulent and avirulent races of Erysiphe graminis f.sp. hordei and a race of Erysiphe graminis f.sp. tritici in barley. Plant Path 37: 20-27 (1988).
49. Thordal-Christensen H, Smedegaard-Petersen V: Correlation between induced resistance and host fluorescence in barley inoculated with Erysiphe graminis. J Phytopath 123: 34-46 (1988).
50. 2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J 11: 1187-1194 (1997).
51. von Heijne G: Signals for protein import into organelles. In: Herrmann RG, Larkins B (eds), Plant Molecular Biology 2, pp. 583-593. Plenum, New York (1991).
52. Wei YD, de Neergaard E, Thordal-Christensen H, Collinge DB, Smedegaard-Petersen V: Accumulation of a putative guanidine compound in relation to other early defence reactions in epidermal cells of barley and wheat exhibiting resistance to Erysiphe graminis f.sp. hordei. Physiol Mol Plant Path 45: 469-484 (1994).
53. Zeyen RJ, Carver TLW, Ahlstrand GG: Relating cytoplasmic detail of powdery mildew infection to presence of insoluble silicon by sequential use of light microscopy, SEM, and X-ray microanalysis. Physiol Plant Path 22: 101-108 (1983).
54. 2-producing enzyme, accumulates in barley attacked by the powdery mildew fungus. Plant J 8: 139-145 (1995).
55. Zhang Z, Yang J, Collinge DB, Thordal-Christensen H: Ethanol increases sensitivity of oxalate oxidase assays and facilitates direct activity staining in SDS gels. Plant Mol Biol Rep 14: 266-272 (1996).