Cladosporium fulvum CfHNNI1 induces hypersensitive necrosis, defence gene expression and disease resistance in both host and nonhost plants

Plant Molecular Biology

Volumn 64, Issue 1-2, 2007, Pages 89-101

  Cai, Xin Zhong ^a   Zhou, Xin ^a   Xu, You Ping ^a   Joosten, Matthieu H A J ^b   De Wit, Pierre J G M ^b  

^a ZHEJIANG UNIVERSITY   (China)

^b WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

CfHNNI1; Cladosporium fulvum; Elicitor; Hypersensitive response (HR); Nonhost resistance; Transgenic tobacco

Indexed keywords

DISEASES; DNA; GENE EXPRESSION; TOBACCO;

CLADOSPORIUM FULVUM; HYPERSENSITIVE RESPONSE (HR); NONHOST RESISTANCE; TRANSGENIC TOBACCO;

PLANTS (BOTANY);

BASIC LEUCINE ZIPPER TRANSCRIPTION FACTOR; FUNGAL PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; CHEMISTRY; CLADOSPORIUM; GENE VECTOR; GENETICS; INNATE IMMUNITY; METABOLISM; MICROBIOLOGY; NECROSIS; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; PHYTOPHTHORA; POTEXVIRUS; TOBACCO; TOMATO; TRANSGENIC PLANT;

AMINO ACID SEQUENCE; BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; CLADOSPORIUM; CONSERVED SEQUENCE; FUNGAL PROTEINS; GENETIC VECTORS; IMMUNITY, NATURAL; LYCOPERSICON ESCULENTUM; NECROSIS; PHYTOPHTHORA; PLANTS, GENETICALLY MODIFIED; POTEXVIRUS; TOBACCO;

DISEASES; GENES; NUCLEIC ACIDS; PLANTS; TOBACCO;

CLADOSPORIUM; CLADOSPORIUM FULVUM; LYCOPERSICON ESCULENTUM; NICOTIANA OBTUSIFOLIA; NICOTIANA TABACUM; OOMYCETES; PHYTOPHTHORA PARASITICA; PSEUDOMONAS SYRINGAE; PSEUDOMONAS SYRINGAE PV. TABACI; SOLANUM TUBEROSUM; TOBACCO MOSAIC VIRUS;

EID: 34247196747     PISSN: 01674412     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11103-007-9136-0     Document Type: Article

References (58)

1. Arnold DL, Gibbon MJ, Jackson RW, Wood JR, Brown J, Mansfield JW, Taylor JD, Vivian A (2001) Molecular characterization of avrPphD, a widely distributed gene from Pseudomonas syringae pv. phaseolicola involved in non-host recognition by pea (Pisum sativum). Physiol Mol Plant Pathol 58:55-62
2. Asai T, Tena G, Plotnikova J, Willmann MR, Chiu WL, Gomez-Gomez L, Boller T, Ausubel FM, Sheen J (2002) MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415:977-983
3. Belbahri L, Boucher C, Candresse T, Nicole M, Ricci P, Keller H (2001) A local accumulation of the Ralstonia solanacearum PopA protein in transgenic tobacco renders a compatible plant-pathogen interaction incompatible. Plant J 28:419-430
4. Birch PRJ, Rehmany AP, Pritchard L, Kamoun S, Beynon JL (2006) Trafficking arms: oomycete effectors enter host plant cells. Trend Microbiol 14:8-11
5. Boudart G, Charpentier M, Lafitte C, Martinez Y, Jauneau A, Gaulin E, Esquerre-Tugaye M-T, Dumas B (2003) Elicitor activity of a fungal endopolygalacturonase in tobacco required a functional catalytic site and cell wall localization. Plant Physiol 131:93-101
6. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254
7. Cai X (2004) Identification of amino acids of Cladosporium fulvum CfHNNI1 required for function of necrosis induction in plants. Acta Bot Sin 46:738-743
8. Cai X, Takken FLW, Joosten MHAJ, De Wit PJGM (2001) Specific recognition of AVR4 and AVR9 results in distinct patterns of hypersensitive cell death in tomato, but similar patterns of defence-related gene expression. Mol Plant Pathol 2:77-86
9. Cai X, Xu Q, Wang C, Zheng Z (2006) Development of a virus-induced gene-silencing system for functional analysis of the RPS2-dependent resistance signalling pathways in Arabidopsis. Plant Mol Biol 62:223-232
10. Cai X, Zheng Z (1999) Induction of systemic resistance in tomato by an incompatible race of Cladosporium fulvum and the accumulation dynamics of salicylic acid in tomato plants. Acta Phytopathol Sin 29:261-264
11. Christopher-Kozjan R, Heath MC (2003) Cytological and pharmacological evidence that biotrophic fungi trigger different cell death execution processes in host and nonhost cells during the hypersensitive response. Physiol Mol Plant Pathol 62:265-275
12. Collins NC, Thordal-Christensen H, Lipka V, Bau S, Kombrink E, Qiu J-L, Hückelhoven R, Stein M, Freialdenhoven A, Somerville SC, Schulze-Lefert P (2003) SNARE-proteinmediated disease resistance at the plant cell wall. Nature 425:973-977
13. Danhash N, Wagemakers CAM, Van Kan JAL, De Wit PJGM (1993) Molecular characterization of four cDNAs obtained from Cladosporium fulvum-infected tomato. Plant Mol Biol 22:1017-1029
14. De Wit PJGM (1992) Molecular characterisation of gene-for-gene systems in plant-fungus interactions and the application of avirulence genes in control of plant pathogens. Annu Rev Phytopathol 30:391-418
15. De Wit PJGM, Flach W (1979) Differential accumulation of phytoalexins in tomato leaves, but not in fruits after inoculation with virulent and avirulent races of Cladosporium fulvum. Physiol Plant Pathol 15:257-267
16. De Wit PJGM, Flach W (1982) Evidence for the occurrence of race and cultivar-specific elicitors of necrosis in intercellular fluids of compatible interactions of Cladosporium fulvum and tomato. Physiol Plant Pathol 21:1-11
17. Ebel J, Cosio EG (1994) Elicitors of plant defence responses. Int Rev Cytol 148:1-36
18. Ellis J, Catanzariti AM, Dodds P (2006) The problem of how fungal and oomycete avirulence proteins enter plant cells. Trend Plant Sci 11:61-63
19. Gurr SJ, Rushton PJ (2005) Engineering plants with increased disease resistance: how are we going to express it? Trend Biotech 23:283-290
20. Hammond-Kosack KE, Parker JE (2003) Deciphering plantpathogen communication: fresh perspectives for molecular resistance breeding. Curr Opin Biotech 14:177-193
21. Heath MC (2000) Nonhost resistance and nonspecific plant responses. Curr Opin Plant Biol 3:15-319
22. Holub EB, Cooper A (2004) Matrix, reinvention in plants: how genetics is unveiling secrets of non-host disease resistance. Trends Plant Sci 9:211-214
23. Jones DA, Takemoto D (2004) Plant innate immunity - direct and indirect recognition of general and specific pathogenassociated molecules. Curr Opin Immunol 16:48-62
24. Joosten MHAJ, De Wit PJGM (1999) The tomato-Cladosporium fulvum interaction: a versatile experimental system to study plant-pathogen interactions. Annu Rev Phytopathol 37:335-367
25. Kamoun S (2001) Nonhost resistance to Phytophthora: novel prospects for a classical problem. Curr Opin Plant Biol 4:295-300
26. Kamoun S, Huitema E, Vleeshouwers V (1999) Resistance to oomycetes: a general role for the hypersensitive response? Trends Plant Sci 4:196-200
27. Kang L, Li J, Zhao T, Xiao F, Tang X, Thilmony R, He SY, Zhou J-M (2003) Interplay of the Arabidopsis nonhost resistance gene NHO1 with bacterial virulence. Proc Natl Acad Sci USA 100:3519-3524
28. Keller H, Pamboukdjian N, Ponchet M, Poupet A, Delon R, Verrier J-L, Roby D, Ricci P (1999) Pathogen-induced elicitin production in transgenic tobacco generates a hypersensitive response and non-specific disease resistance. Plant Cell 11:223-235
29. Kobayashi Y, Yamada M, Kobayashi I, Kunoh H (1997) Actin microfilaments are required for the expression of nonhost resistance in higher plants. Plant Cell Physiol 38:725-733
30. Lauge R, Goodwin PH, De Wit PJGM, Joosten MHAJ (2000) Specific HR-associated recognition of secreted proteins from Cladosporium fulvum occurs in both host and nonhost plants. Plant J 23:735-745
31. Lauge R, Joosten MHAJ, Haanstra JPW, Goodwin PH, Lindhout P, De Wit PJGM (1998) Successful search for a resistance gene in tomato targeted against a virulence factor of a fungal pathogen. Proc Natl Acad Sci USA 95:9014-9018
32. Lipka V, Dittgen J, Bednarek P, Bhat R, Wiermer M, Stein M, Landtag J, Brandt W, Rosahl S, Scheel D, Llorente F, Molina A, Parker J, Somerville S, Schulze-Lefert P (2005) Pre- and postinvasion defenses both contribute to nonhost resistance in Arabidopsis. Science 310:1180-1183
33. Liu YL, Schiff M, Dinesh-Kumar SP (2002) Virus-induced gene silencing in tomato. Plant J 31:777-786
34. Mayda E, Tornero P, Conejero V, Vera P (1999) A tomato homeobox gene (HD-zip) is involved in limiting the spread of programmed cell death. Plant J 20:591-600
35. 2 plays different roles in determining penetration failure in three diverse plant-fungal interactions. Plant J 29:257-268
36. Mellersh DG, Heath MC (2003) An investigation into the involvement of defence signaling pathways in components of the nonhost resistance of Arabidopsis thaliana to rust fungi also reveals a model system for studying rust fungal compatibility. Mol Plant-Microbe Interact 16:398-404
37. Mysore KS, Ryu C-M (2004) Nonhost resistance: how much do we know? Trends Plant Sci 9:97-104
38. Nurnberger T, Brunner F (2002) Innate immunity in plants and animals: emerging parallels between the recognition of general elicitors and pathogen-associated molecular patterns. Curr Opin Plant Biol 5:1-7
39. Nurnberger T, Lipka V (2005) Non-host resistance in plants: new insights into an old phenomenon. Mol Plant Pathol 6:335-345
40. O'Connell RJ, Panstruga R (2006) Tête à tête inside a plant cell: establishing compatibility between plants and biotrophic fungi and oomycetes. New Phytol 171:699-718
41. Osbourn AE (1996) Preformed antimicrobial compounds and plant defence against fungal attack. Plant Cell 8:1821-1831
42. Poinssot B, Vandelle E, Bentejac M, Adrian M, Levis C, Brygoo Y, Garin J, Sicilia F, Coutos-Thevenot P, Pugin A (2003) The endopolygalacturonase 1 from Botrytis cinerea activates grapevine defence reactions unrelated to its enzymatic activity. Mol Plant-Microbe Interact 16:553-564
43. Pontier D, Godiard L, Marco Y, Roby D (1994) Hsr203J, a tobacco gene whose activation is rapid, highly localized and specific for incompatible plant/pathogen interactions. Plant J 5:507-521
44. Pontier D, Tronchet M, Rogowsky P, Lam E, Roby D (1998) Activation of hsr203, a plant gene expressed during incompatible plant-pathogen interactions, is correlated with programmed cell death. Mol Plant-Microbe Interact 11:544-554
45. Rotblat B, Enshell-Seijffers D, Gershoni JM, Schuster S, Avni A (2002) Identification of an essential component of the elicitation active site of the EIX protein elicitor. Plant J 32:1049-1055
46. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, vol 2, 2nd edn. Cold Spring Harbour Laboratory Press, New York
47. Shimizu R, Taguchi F, Marutani M, Mukaihara T, Inagaki Y, Toyoda K, Shiraishi T, Ichinose Y (2003) The ΔfliD mutant of Pseudomonas syringae pv. tabaci, which secretes flagellin monomers, induces a strong hypersensitive reaction (HR) in non-host tomato cells. Mol Genet Genomics 269:21-30
48. Stein M, Dittgen J, Sanchez-Rodriguez C, Hou BH, Molina A, Schulze-Lefert P, Lipka V, Somerville S (2006) Arabidopsis PEN3/PDR8, an ATP binding cassette transporter, contributes to nonhost resistance to inappropriate pathogens that enter by direct penetration. Plant Cell 18:731-746
49. Takken FLW, Luderer R, Gabriels SHEJ, Westerink N, Lu R, De Wit PJGM, Joosten MHAJ (2000) A functional cloning strategy, based on a binary PVX-expression vector, to isolate HR-inducing cDNAs of plant pathogens. Plant J 24:275-283
50. Thordal-Christensen H (2003) Fresh insights into processes of nonhost resistance. Curr Opin Plant Biol 6:351-357
51. Van Kan JAL, Joosten MHAJ, Wagemakers CAM, Van den Berg-Velthuis GCM, De Wit PJGM (1992) Differential accumulation of mRNAs encoding extracellular and intracellular PR proteins in tomato induced by virulent and avirulent races of Cladosporium fulvum. Plant Mol Biol 20:513-527
52. Wang C, Cai X, Lin J, Zheng Z (2003) The role of salicylic acid and ethylene in resistance of tobacco to black shank. Acta Phytophyl Sin 30:295-299
53. Wang C, Cai X, Wang X, Zheng Z (2006a) Optimisation of tobacco rattle virus-induced gene silencing in Arabidopsis. Func Plant Biol 33:347-355
54. Wang C, Cai X, Xu Y (2006b) Molecular mechanism of interaction between tomato and leaf mold pathogen Cladosporium fulvum. Acta Phytopathol Sin 36:385-391
55. Wang C, Cai X, Zheng Z (2005) High humidity represses Cf-4/Avr4-and Cf-9/Avr9-dependent hypersensitive cell death and defense gene expression. Planta 222:947-956
56. Yun BW, Atkinson HA, Gaborit C, Greenland A, Read ND, Pallas JA, Loake GJ (2003) Loss of actin cytoskeletal function and EDS1 activity, in combination, severely compromises non-host resistance in Arabidopsis against wheat powdery mildew. Plant J 34:768-777
57. Zhao BY, Ardales EY, Raymundo A, Bai JF, Trick HN, Leach JE, Hulbert SH (2004) The avrRxo1 gene from the rice pathogen Xanthomonas oryzae pv. oryzicola confers a nonhost defense reaction on maize with resistance gene Rxo1. Mol Plant-Microbe Interact 17:771-779
58. Zhao BY, Lin XH, Poland J, Trick H, Leach J, Hulbert S (2005) A maize resistance gene functions against bacterial streak disease in rice. Proc Natl Acad Sci USA 102:15383-15388