Analysis of two in planta expressed LysM effector homologs from the fungus mycosphaerella graminicola reveals novel functional properties and varying contributions to virulence on wheat

Plant Physiology

Volumn 156, Issue 2, 2011, Pages 756-769

  Marshall, Rosalind ^a   Kombrink, Anja ^a,b   Motteram, Juliet ^a   Loza Reyes, Elisa ^a   Lucas, John ^a   Hammond Kosack, Kim E ^a   Thomma, Bart P H J ^b   Rudd, Jason J ^a  

^a ROTHAMSTED RESEARCH   (United Kingdom)

^b WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CLADOSPORIUM FULVUM; FUNGI; LYCOPERSICON ESCULENTUM; MYCOSPHAERELLA GRAMINICOLA; TRITICUM AESTIVUM;

EID: 79958055482     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.111.176347     Document Type: Article

References (61)

1. Adhikari TB, Balaji B, Breeden J, Goodwin SB (2007) Resistance of wheat to Mycosphaerella graminicola involves early and late peaks of gene expression. Physiol Mol Plant Pathol 71: 55-68
2. An G, Evert PR, Mitra A, Ha SB (1988) Binary vectors. In SB Gelvin, RA Schilperroort, eds, Plant Molecular Biology Manual A3. Kluwer Academic Press, Dordrecht, The Netherlands, pp 1-19
3. Barber MS, Bertram RE, Ride JP (1989) Chitin oligosaccharides elicit lignification in wounded wheat leaves. Physiol Mol Plant Pathol 34: 3-12
4. Bielawski JP, Yang Z (2005) Maximum likelihood methods for detecting adaptive protein evolution. In R Nielsen, ed, Statistical Methods in Molecular Evolution. Springer, New York, pp 103-124
5. Boller T, He SY (2009) Innate immunity in plants: an arms race between pattern recognition receptors in plants and effectors in microbial pathogens. Science 324: 742-744
6. Bolton MD, van Esse HP, Vossen JH, de Jonge R, Stergiopoulos I, Stulemeijer IJE, van den Berg GCM, Borrás-Hidalgo O, Dekker HL, de Koster CG, et al (2008) The novel Cladosporium fulvum lysin motif effector Ecp6 is a virulence factor with orthologues in other fungal species. Mol Microbiol 69: 119-136
7. Bowler J, Scott E, Tailor R, Scalliet G, Ray J, Csukai M (2010) New capabilities for Mycosphaerella graminicola research. Mol Plant Pathol 11: 691-704
8. Brading PA, Verstappen ECP, Kema GHJ, Brown JKM (2002) A geneforgene relationship between wheat and Mycosphaerella graminicola, the Septoria tritici blotch pathogen. Phytopathology 92: 439-445
9. Cohen L, Eyal Z (1993) The histology of processes associated with the infection of resistant and susceptible wheat cultivars with S. tritici. Plant Pathol 42: 737-743
10. de Jonge R, Bolton MD, Thomma BP (March 30, 2011) How filamentous pathogens co-opt plants: the ins and outs of fungal effectors. Curr Opin Plant Biol http://dx.doi.org/10.1016/j.pbi.2011.03.005
11. de Jonge R, Thomma BP (2009) Fungal LysM effectors: extinguishers of host immunity? Trends Microbiol 17: 151-157
12. de Jonge R, van Esse HP, Kombrink A, Shinya T, Desaki Y, Bours R, van der Krol S, Shibuya N, Joosten MH, Thomma BP (2010) Conserved fungal LysMeffector Ecp6 prevents chitin-triggered immunity in plants. Science 329: 953-955
13. Deller S, Hammond-Kosack KE, Rudd JJ (2011) The complex interactions between host immunity and non-biotrophic fungal pathogens of wheat leaves. J Plant Physiol 168: 63-71
14. De Wit PJ, Mehrabi R, Van den Burg HA, Stergiopoulos I (2009) Fungal effector proteins: past, present and future. Mol Plant Pathol 10: 735-747
15. Doehlemann G, van der Linde K, Amann D, Schwammbach D, Hof A, Mohanty A, Jackson D, Kahmann R (2009) Pep1, a secreted effector protein of Ustilago maydis, is required for successful invasion of plant cells. PLoS Pathog 5: e1000290
16. Eyal Z (1999) The Septoria tritici and Stagonospora nodorum blotch diseases of wheat. Eur J Plant Pathol 105: 629-641
17. Flor HH (1971) Current status of gene-for-gene concept. Annu Rev Phytopathol 9: 275-296
18. Fraaije BA, Cools HJ, Fountaine J, Lovell DJ, Motteram J, West JS, Lucas JA (2005) Role of ascospores in further spread of QoI-resistant cytochrome b alleles (G143A) in field populations of Mycosphaerella graminicola. Phytopathology 95: 933-941
19. Friesen TL, Faris JD, Solomon PS, Oliver RP (2008) Host-specific toxins: effectors of necrotrophic pathogenicity. Cell Microbiol 10: 1421-1428
20. Friesen TL, Stukenbrock EH, Liu ZH, Meinhardt S, Ling H, Faris JD, Rasmussen JB, Solomon PS, McDonald BA, Oliver RP (2006) Emergence of a new disease as a result of interspecific virulence gene transfer. Nat Genet 38: 953-956
21. Goldman N, Yang ZH (1994) A codon-based model of nucleotide substitution for protein-coding DNA sequences. Mol Biol Evol 11: 725-736
22. Houterman PM, Cornelissen BJ, Rep M (2008) Suppression of plant resistance gene-based immunity by a fungal effector. PLoS Pathog 4: e1000061
23. Jing HC, Lovell D, Gutteridge R, Jenk D, Kornyukhin D, Mitrofanova OP, Kema GHJ, Hammond-Kosack KE (2008) Phenotypic and genetic analysis of the Triticum monococcum-Mycosphaerella graminicola interaction. New Phytol 179: 1121-1132
24. Jones JDG, Dangl JL (2006) The plant immune system. Nature 444: 323-329
25. 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
26. Kema GHJ, van der Lee TAJ, Mendes O, Verstappen ECP, Lankhorst RK, Sandbrink H, van der Burgt A, Zwiers LH, Csukai M, Waalwijk C (2008) Large-scale gene discovery in the Septoria tritici blotch fungus Mycosphaerella graminicola with a focus on in planta expression. Mol Plant Microbe Interact 21: 1249-1260
27. Kema GHJ, Yu DZ, Rijkenberg FHJ, Shaw MW, Baayen RP (1996) Histology of the pathogenesis of Mycosphaerella graminicola in wheat. Phytopathology 86: 777-786
28. Keon J, Antoniw J, Carzaniga R, Deller S, Ward JL, Baker JM, Beale MH, Hammond-Kosack KE, Rudd JJ (2007) Transcriptional adaptation of Mycosphaerella graminicola to programmed cell death (PCD) of its susceptible wheat host. Mol Plant Microbe Interact 20: 178-193
29. Keon J, Bailey A, Hargreaves J (2000) A group of expressed cDNA sequences from the wheat fungal leaf blotch pathogen, Mycosphaerella graminicola (Septoria tritici). Fungal Genet Biol 29: 118-133
30. Keon J, Rudd JJ, Antoniw J, Skinner W, Hargreaves J, Hammond-Kosack KE (2005) Metabolic and stress adaptation by Mycosphaerella graminicola during sporulation in its host revealed throughmicroarray transcription profiling. Mol Plant Pathol 6: 527-540
31. Liu ZH, Faris JD, Oliver RP, Tan KC, Solomon PS, McDonald MC, McDonald BA, Nunez A, Lu SW, Rasmussen JB, et al (2009) SnTox3 acts in effector triggered susceptibility to induce disease on wheat carrying the Snn3 gene. PLoS Pathog 5: e1000581
32. Luttrell ES (1974) Parasitism of fungi on vascular plants. Mycologia 66: 1-15
33. Milne I, Lindner D, Bayer M, Husmeier D, McGuire G, Marshall DF, Wright F (2009) TOPALi v2: a rich graphical interface for evolutionary analyses of multiple alignments on HPC clusters and multi-core desktops. Bioinformatics 25: 126-127
34. Miya A, Albert P, Shinya T, Desaki Y, Ichimura K, Shirasu K, Narusaka Y, Kawakami N, Kaku H, Shibuya N (2007) CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc Natl Acad Sci USA 104: 19613-19618
35. Motteram J, Küfner I, Deller S, Brunner F, Hammond-Kosack KE, Nürnberger T, Rudd JJ (2009) Molecular characterization and functional analysis of MgNLP, the sole NPP1 domain-containing protein, from the fungal wheat leaf pathogen Mycosphaerella graminicola. Mol Plant Microbe Interact 22: 790-799
36. Nürnberger T, Kemmerling B (2009) PAMP-triggered basal immunity in plants. Plant Innate Immunity 51: 1-38
37. Nürnberger 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: 318-324
38. Petutschnig EK, Jones AME, Serazetdinova L, Lipka U, Lipka V (2010) The lysin motif receptor-like kinase (LysM-RLK) CERK1 is a major chitin-binding protein in Arabidopsis thaliana and subject to chitininduced phosphorylation. J Biol Chem 285: 28902-28911
39. Pnini-Cohen S, Zilberstein A, Schuster S, Sharon A, Eyal Z (2000) Elucidation of Septoria tritici X wheat interactions using GUS-expressing isolates. Phytopathology 90: 297-304
40. Ridout CJ, Skamnioti P, Porritt O, Sacristan S, Jones JDG, Brown JKM (2006) Multiple avirulence paralogues in cereal powdery mildew fungi may contribute to parasite fitness and defeat of plant resistance. Plant Cell 18: 2402-2414
41. Rivas S, Thomas CM (2005) Molecular interactions between tomato and the leaf mold pathogen Cladosporium fulvum. Annu Rev Phytopathol 43: 395-436
42. Rooney HCE, Van't Klooster JW, van der Hoorn RAL, Joosten MH, Jones JDG, deWit PJ (2005) Cladosporium Avr2 inhibits tomato Rcr3 protease required for Cf-2-dependent disease resistance. Science 308: 1783-1786
43. Rudd JJ, Antoniw J, Marshall R, Motteram J, Fraaije B, Hammond-Kosack K (2010) Identification and characterisation of Mycosphaerella graminicola secreted or surface-associated proteins with variable intragenic coding repeats. Fungal Genet Biol 47: 19-32
44. Rudd JJ, Keon J, Hammond-Kosack KE (2008) The wheat mitogen-activated protein kinases TaMPK3 and TaMPK6 are differentially regulated at multiple levels during compatible disease interactions with Mycosphaerella graminicola. Plant Physiol 147: 802-815
45. Shimizu T, Nakano T, Takamizawa D, Desaki Y, Ishii-Minami N, Nishizawa Y, Minami E, Okada K, Yamane H, Kaku H, et al (2010) Two LysM receptor molecules, CEBiP and OsCERK1, cooperatively regulate chitin elicitor signaling in rice. Plant J 64: 204-214
46. Solomon PS, Rathjen JP (2010) Pathogen effectors shed light on plant diseases. Funct Plant Biol 37: III-IV
47. Solomon PS, Tan K-C, Oliver RP (2003) The nutrient supply of pathogenic fungi: a fertile field for study. Mol Plant Pathol 4: 203-210
48. Stergiopoulos I, de Wit PJ (2009) Fungal effector proteins. Annu Rev Phytopathol 47: 233-263
49. Stergiopoulos I, van den Burg HA, Okmen B, Beenen HG, van Liere S, Kema GHJ, de Wit PJ (2010) Tomato Cf resistance proteins mediate recognition of cognate homologous effectors from fungi pathogenic on dicots and monocots. Proc Natl Acad Sci USA 107: 7610-7615
50. Tanaka S, Ichikawa A, Yamada K, Tsuji G, Nishiuchi T, Mori M, Koga H, Nishizawa Y, O'Connell R, Kubo Y (2010) HvCEBiP, a gene homologous to rice chitin receptor CEBiP, contributes to basal resistance of barley to Magnaporthe oryzae. BMC Plant Biol 10: 288
51. Thomma BP, Bolton MD, Clergeot PH, de Wit PJ (2006) Nitrogen controls in planta expression of Cladosporium fulvum Avr9 but no other effector genes. Mol Plant Pathol 7: 125-130
52. Thomma BPHJ, van Esse HP, Crous PW, de Wit PJGM (2005) Cladosporium fulvum (syn. Passalora fulva), a highly specialized plant pathogen as a model for functional studies on plant pathogenic Mycosphaerellaceae. Mol Plant Pathol 6: 379-393
53. van den Burg HA, Harrison SJ, Joosten MH, Vervoort J, de Wit PJ (2006) Cladosporium fulvum Avr4 protects fungal cell walls against hydrolysis by plant chitinases accumulating during infection. Mol Plant Microbe Interact 19: 1420-1430
54. van den Burg HA, Spronk CA, Boeren S, Kennedy MA, Vissers JPC, Vuister GW, de Wit PJ, Vervoort J (2004) Binding of the AVR4 elicitor of Cladosporium fulvum to chitotriose units is facilitated by positive allosteric protein-protein interactions: the chitin-binding site of AVR4 represents a novel binding site on the folding scaffold shared between the invertebrate and the plant chitin-binding domain. J Biol Chem 279: 16786-16796
55. Vander P, Varum KM, Domard A, El Gueddari NE, Moerschbacher BM (1998) Comparison of the ability of partially N-acetylated chitosans and chitooligosaccharides to elicit resistance reactions in wheat leaves. Plant Physiol 118: 1353-1359
56. van der Does HC, Duyvesteijn RGE, Goltstein PM, van Schie CCN, Manders EMM, Cornelissen BJC, Rep M (2008) Expression of effector gene SIX1 of Fusarium oxysporum requires living plant cells. Fungal Genet Biol 45: 1257-1264
57. van Esse HP, Bolton MD, Stergiopoulos I, de Wit PJ, Thomma BP (2007) The chitin-binding Cladosporium fulvum effector protein Avr4 is a virulence factor. Mol Plant Microbe Interact 20: 1092-1101
58. van Esse HP, Van't Klooster JW, Bolton MD, Yadeta KA, van Baarlen P, Boeren S, Vervoort J, de Wit PJ, Thomma BP (2008) The Cladosporium fulvum virulence protein Avr2 inhibits host proteases required for basal defense. Plant Cell 20: 1948-1963
59. Wolpert TJ, Dunkle LD, Ciuffetti LM (2002) Host-selective toxins and avirulence determinants: what's in a name? Annu Rev Phytopathol 40: 251-285
60. Yang ZH (1997) PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13: 555-556
61. Zwiers LH, De Waard MA (2001) Efficient Agrobacterium tumefaciensmediated gene disruption in the phytopathogen Mycosphaerella graminicola. Curr Genet 39: 388-393