Effector proteins of extracellular fungal plant pathogens that trigger host resistance

Functional Plant Biology

Volumn 37, Issue 10, 2010, Pages 901-906

  Catanzariti, Ann Maree ^a   Jones, David A ^a  

^a AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

Author keywords

avirulence; effector triggered immunity; hypersensitive response; plant disease resistance; virulence

Indexed keywords

AVIRULENCE; EFFECTOR-TRIGGERED IMMUNITY; HYPERSENSITIVE RESPONSE; PLANT DISEASE; VIRULENCE;

FUNGI; PROTEINS;

PATHOGENS;

BIOACTIVITY; FUNGAL DISEASE; HOST PLANT; HOST-PATHOGEN INTERACTION; IMMUNITY; MOLECULAR ANALYSIS; PLANT DEFENSE; PROTEIN; VIRULENCE;

EID: 77957765220     PISSN: 14454408     EISSN: None     Source Type: Journal    
DOI: 10.1071/FP10077     Document Type: Review

References (45)

1. Balesdent MH, Louvard K, Pinochet X, Rouxel T (2006) Alarge-scale survey of races of Leptosphaeria maculans occurring on oilseed rape in France. European Journal of Plant Pathology 114, 53-65. doi:10.1007/s10658-005-2104-0
2. Bolton MD, van Esse HP, Vossen JH, de Jonge R, Stergiopoulos I, et al.. (2008) The novel Cladosporium fulvum lysin motif effector Ecp6 is a virulence factor with orthologues in other fungal species. Molecular Microbiology 69, 119-136. doi:10.1111/j.1365-2958.2008.06270.x
3. Caplan J, Padmanabhan M, Dinesh-Kumar SP (2008) Plant NB-LRR immune receptors : from recognition to transcriptional reprogramming. Cell Host & Microbe 3, 126-135. doi:10.1016/j.chom.2008.02.010
4. Catanzariti AM, Dodds PN, Ellis JG (2007) Avirulence proteins from haustoria-forming pathogens. FEMS Microbiology Letters 269, 181-188. doi:10.1111/j.1574-6968.2007.00684.x
5. de Kock MJD, Brandwagt BF, Bonnema G, de Wit PJGM, Lindhout P (2005) The tomato Orion locus comprises a unique class of Hcr9 genes. Molecular Breeding 15, 409-422. doi:10.1007/s11032-005-0386-8
6. Fudal I, Ross S, Gout L, Blaise F, Kuhn ML, et al. (2007) Heterochromatinlike regions as ecological niches for avirulencegenes in the Leptosphaeria maculans genome: map-based cloning of AvrLm6. Molecular Plant-Microbe Interactions 20, 459-470. doi:10.1094/MPMI-20-4-0459
7. Gout L, Fudal I, Kuhn ML, Blaise F, Eckert M, et al. (2006) Lost in the middle of nowhere: the AvrLm1 avirulence gene of the Dothideomycete Leptosphaeria maculans. Molecular Microbiology 60, 67-80. doi:10.1111/j.1365- 2958.2006.05076.x
8. Gout L, Kuhn ML, Vincenot L, Bernard-Samain S, Cattolico L, et al. (2007) Genome structure impacts molecular evolution at the AvrLm1 avirulence locus of the plant pathogen Leptosphaeria maculans. Environmental Microbiology 9, 2978-2992. doi:10.1111/j.1462-2920.2007.01408.x
9. Hahn M, Jungling S, Knogge W (1993) Cultivar-specific elicitation of barley defense reactions by the phytotoxic peptide NIP1 from Rhynchosporium secalis. Molecular Plant-Microbe Interactions 6, 745-754.
10. Houterman PM, Cornelissen BJ, Rep M (2008) Suppression of plant resistance gene-based immunity by a fungal effector. PLoS Pathogens 4, e1000061. doi:10.1371/journal.ppat.1000061
11. Houterman PM, Ma L, van Ooijen G, de Vroomen MJ, Cornelissen BJ, et al. (2009) The effector protein Avr2 of the xylem colonizing fungus Fusarium oxysporum activates the tomato resistance protein I-2 intracellularly. The Plant Journal 58, 970-978. doi:10.1111/j.1365-313X.2009.03838.x
12. Huang YJ, Li ZQ, Evans N, Rouxel T, Fitt BDL, et al. (2006) Fitness cost associated with loss of the AvrLm4 avirulence function in Leptosphaeria maculans (phoma stem canker of oilseed rape). European Journal of Plant Pathology 114, 77-89. doi:10.1007/s10658-005-2643-4
13. Huang YJ, Balesdent MH, Li ZQ, Evans N, Rouxel T, et al. (2010) Fitnesscost of virulence differs between the AvrLm1 and AvrLm4 loci in Leptosphaeria maculans (phoma stem canker of oilseed rape). European Journal of Plant Pathology 126, 279-291. doi:10.1007/s10658-009-9539-7
14. Joosten MHAJ, Cozijnsen TJ, de Wit PJGM (1994) Host resistance to a fungal tomato pathogen lost by a single base-pair change in an avirulence gene. Nature 367, 384-386. doi:10.1038/367384a0
15. Laugé R, Joosten MHAJ, van den Ackerveken GFJM, van den Broek HWJ, de Wit PJGM (1997) The in planta-produced extracellular proteins ECP1 and ECP2 of Cladosporium fulvum are virulence factors. Molecular Plant-Microbe Interactions 10, 725-734. doi:10.1094/MPMI. 1997.10.6.725
16. 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 non-host plants. The Plant Journal 23, 735-745. doi:10.1046/j.1365-313x.2000.00843.x
17. Luderer R, Takken FL, de Wit PJGM, Joosten MHAJ (2002) Cladosporium fulvum overcomes Cf-2-mediated resistance by producing truncated AVR2 elicitor proteins. Molecular Microbiology 45, 875-884. doi:10.1046/j.1365-2958.2002. 03060.x
18. Ma LJ, van der Does HC, Borkovich KA, Coleman JJ, Daboussi MJ, et al. (2010) Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 464, 367-373. doi:10.1038/nature 08850
19. Marmeisse R, van den Ackerveken GFJM, Goosen T, de Wit PJGM, van den Broek HWJ (1993) Disruption of the avirulence gene avr9 in 2 races of the tomato pathogen Cladosporium fulvum causes virulence on tomato genotypes with the complementary resistance gene Cf9. Molecular Plant-Microbe Interactions 6, 412-417.
20. Panstruga R, Dodds PN (2009) Terrific protein traffic: the mystery of effector protein delivery by filamentous plant pathogens. Science 324, 748-750. doi:10.1126/science.1171652
21. Parlange F, Daverdin G, Fudal I, Kuhn ML, Balesdent MH, et al. (2009) Leptosphaeria maculans avirulence gene AvrLm4-7 confers a dual recognition specificity by the Rlm4 and Rlm7 resistance genes of oilseed rape, and circumvents Rlm4-mediated recognition through a single amino acid change. Molecular Microbiology 71, 851-863. doi:10.1111/j.1365-2958.2008.06547.x
22. Pérez-García A, Snoeijers SS, Joosten MHAJ, Goosen T, de Wit PJGM (2001) Expression of the avirulence gene Avr9 of the fungal tomato pathogen Cladosporium fulvum is regulated by the global nitrogen response factor NRF1. Molecular Plant-Microbe Interactions 14, 316-325. doi:10.1094/MPMI.2001. 14.3.316
23. Rep M, van der Does HC, Meijer M, van Wijk R, Houterman PM, et al. (2004) A small, cysteine-rich protein secreted by Fusarium oxysporum during colonization of xylem vessels is required for I-3-mediated resistance in tomato. Molecular Microbiology 53, 1373-1383. doi:10.1111/j.1365-2958.2004.04177.x
24. Rep M, Meijer M, Houterman PM, van der Does HC, Cornelissen BJ (2005) Fusarium oxysporum evades I-3-mediated resistance without altering the matching avirulence gene. Molecular Plant-Microbe Interactions 18, 15-23. doi:10.1094/MPMI-18-0015
25. Rohe M, Gierlich A, Hermann H, Hahn M, Schmidt B, et al. (1995) The racespecific elicitor, NIP1, from the barley pathogen, Rhynchosporium secalis, determines avirulence on host plants of the Rrs1 resistance genotype. The EMBO Journal 14, 4168-4177.
26. Rooney HCE, van't Klooster JW, van der Hoorn RAL, Joosten MHAJ, Jones JDG, et al. (2005) Cladosporium Avr2 inhibits tomato Rcr3 protease required for Cf-2-dependent disease resistance. Science 308, 1783-1786. doi:10.1126/science. 1111404
27. Schürch S, Linde CC, Knogge W, Jackson LF, McDonald BA (2004) Molecular population genetic analysis differentiates two virulence mechanisms of the fungal avirulence gene NIP1. Molecular Plant-Microbe Interactions 17, 1114-1125. doi:10.1094/MPMI.2004.17. 10.1114
28. Shabab M, Shindo T, Gu C, Kaschani F, Pansuriya T, et al. (2008) Fungal effector protein AVR2 targets diversifying defense-related Cys proteases of tomato. The Plant Cell 20, 1169-1183. doi:10.1105/tpc.107.056325
29. Simons G, Groenendijk J, Wijbrandi J, Reijans M, Groenen J, et al. (1998) Dissection of the Fusarium I2gene clusterintomato reveals six homologs and one active gene copy. The Plant Cell 10, 1055-1068.
30. Stergiopoulos I, de Kock MJD, Lindhout P, de Wit PJGM (2007) Allelic variation in the effector genes of the tomato pathogen Cladosporium fulvum reveals different modes of adaptive evolution. Molecular Plant-Microbe Interactions 20, 1271-1283. doi:10.1094/MPMI-20-10-1271
31. Stergiopoulos I, van den Burg HA, Ökmen B, Beenen HG, van Liere S, et al. (2010) Tomato Cf resistance proteins mediate recognition of cognate homologous effectors from fungi pathogenic on dicots and monocots. Proceedings of the National Academy of Sciences of the United States of America 107, 7610-7615. doi:10.1073/pnas.1002910107
32. Thomma BPHJ, Bolton MD, Clergeot PH, de Wit PJGM (2006) Nitrogen controls in planta expression of Cladosporium fulvum Avr9 but no other effector genes. Molecular Plant Pathology 7, 125-130. doi:10.1111/j.1364-3703.2006.00320.x
33. van den Ackerveken GFJM, van Kan JA, de Wit PJGM (1992) Molecular analysis of the avirulence gene avr9 of the fungal tomato pathogen Cladosporium fulvum fully supports the gene-for-gene hypothesis. The Plant Journal 2, 359-366. doi:10.1046/j.1365-313X.1992.t01-34-00999.x
34. van den Burg HA, Westerink N, Francoijs KJ, Roth R, Woestenenk E, et al. (2003) Natural disulfide bond-disrupted mutants of AVR4 of the tomato pathogen Cladosporium fulvum are sensitive to proteolysis, circumvent Cf-4-mediated resistance, but retain their chitin binding ability. Journal of Biological Chemistry 278, 27340-27346. doi:10.1074/jbc. M212196200
35. van den Burg HA, Harrison SJ, Joosten MHAJ, Vervoort J, de Wit PJGM (2006) Cladosporium fulvum Avr4 protects fungal cell walls against hydrolysis by plant chitinases accumulating during infection. Molecular Plant-Microbe Interactions 19, 1420-1430. doi:10.1094/MPMI-19-1420
36. van der Does HC, Duyvesteijn RGE, Goltstein PM, van Schie CCN, Manders EMM, et al. (2008) Expression of effector gene SIX1 of Fusarium oxysporum requires living plant cells. Fungal Genetics and Biology 45, 1257-1264. doi:10.1016/j.fgb.2008.06.002
37. van den Hooven HW, van den Burg HA, Vossen P, Boeren S, de Wit PJGM, et al. (2001) Disulfide bond structure of the AVR9 elicitor of the fungal tomato pathogen Cladosporium fulvum: evidence for a cystine knot. Biochemistry 40, 3458-3466. doi:10.1021/bi0023089
38. van Esse HP, Bolton MD, Stergiopoulos I, de Wit PJGM, Thomma BPHJ (2007) The chitin-binding Cladosporium fulvum effector protein Avr4 is a virulence factor. Molecular Plant-Microbe Interactions 20, 1092-1101. doi:10.1094/MPMI-20- 9-1092
39. van Esse HP, Van't Klooster JW, Bolton MD, Yadeta KA, van Baarlen P, et al. (2008) The Cladosporium fulvum virulence protein Avr2 inhibits host proteases required for basal defense. The Plant Cell 20, 1948-1963. doi:10.1105/tpc.108.059394
40. van't Slot KAE, van den Burg HA, Kloks C, Hilbers CW, Knogge W, et al. (2003) Solution structure of the plant disease resistance-triggering protein NIP1 from the fungus Rhynchosporium secalis shows a novel betasheet fold. The Journal of Biological Chemistry 278, 4530-45736. doi:10.1074/jbc. M308304200
41. van't Slot KAE, Gierlich A, Knogge W (2007) A single binding site mediates resistance-and disease-associated activities of the effector protein NIP1 from the barley pathogen Rhynchosporium secalis. Plant Physiology 144, 1654-1666. doi:10.1104/pp. 106.094912
42. Vervoort J, van den Hooven HW, Berg A, Vossen P, Vogelsang R, et al. (1997) The race-specific elicitor AVR9 of the tomato pathogen Cladosporium fulvum: a cystine knot protein. Sequence-specific 1H NMR assignments, secondary structure and global fold of the protein. FEBS Letters 404, 153-158. doi:10.1016/S0014-5793 (97) 00117-8
43. Westerink N, Brandwagt BF, de Wit PJGM, Joosten MHAJ (2004) Cladosporium fulvum circumvents the second functional resistance gene homologue at the Cf-4 locus (Hcr9-4E) by secretion of a stable avr4E isoform. Molecular Microbiology 54, 533-545. doi:10.1111/j.1365-2958.2004.04288.x
44. Wevelsiep L, Kogel KH, Knogge W (1991) Purification and characterization of peptides from Rhynchosporium secalis inducing necrosis in barley. Physiological and Mo1ecular Plant Pathology 39, 417-482.
45. +-ATPase by phytotoxic peptides from the fungal pathogen Rhynchosporium secalis. Plant Physiology 101, 297-301.