Effector-triggered defence against apoplastic fungal pathogens

Trends in Plant Science

Volumn 19, Issue 8, 2014, Pages 491-500

  Stotz, Henrik U ^a   Mitrousia, Georgia K ^a   de Wit, Pierre J G M ^b   Fitt, Bruce D L ^a  

^a UNIVERSITY OF HERTFORDSHIRE   (United Kingdom)

^b WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

Apoplastic fungal pathogens; Cell wall; Extracellular matrix; R gene mediated resistance; Receptor like protein

Indexed keywords

VEGETABLE PROTEIN;

CROP; DISEASE RESISTANCE; FUNGUS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; PLANT DISEASE;

CROPS, AGRICULTURAL; DISEASE RESISTANCE; FUNGI; HOST-PATHOGEN INTERACTIONS; PLANT DISEASES; PLANT PROTEINS;

EID: 84905192195     PISSN: 13601385     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tplants.2014.04.009     Document Type: Review

References (78)

1. Fitt B.D.L., et al. Impacts of changing air composition on severity of arable crop disease epidemics. Plant Pathol. 2011, 60:44-53.
2. Schoch C.L., et al. A multigene phylogeny of the Dothideomycetes using four nuclear loci. Mycologia 2006, 98:1041-1052.
3. Jones J.D.G., Dangl J.L. The plant immune system. Nature 2006, 444:323-329.
4. Dangl J.L., et al. Pivoting the plant immune system from dissection to deployment. Science 2013, 341:746-751.
5. Win J., et al. Effector biology of plant-associated organisms: concepts and perspectives. Cold Spring Harb. Symp. Quant. Biol. 2012, 77:235-247.
6. Medzhitov R. Approaching the asymptote: 20 years later. Immunity 2009, 30:766-775.
7. Thomma B.P., et al. Of PAMPs and effectors: the blurred PTI-ETI dichotomy. Plant Cell 2011, 23:4-15.
8. Boys E.F., et al. Effects of R gene-mediated resistance in Brassica napus (oilseed rape) on asexual and sexual sporulation of Pyrenopeziza brassicae (light leaf spot). Plant Pathol. 2012, 61:543-554.
9. Bozkurt T.O., et al. Oomycetes, effectors, and all that jazz. Curr. Opin. Plant Biol. 2012, 15:483-492.
10. Valent B., Khang C.H. Recent advances in rice blast effector research. Curr. Opin. Plant Biol. 2010, 13:434-441.
11. Thirugnanasambandam A., et al. Infection of Rrs1 barley by an incompatible race of the fungus Rhynchosporium secalis expressing the green fluorescent protein. Plant Pathol. 2011, 60:513-521.
12. Stergiopoulos I., de Wit P.J. Fungal effector proteins. Annu. Rev. Phytopathol. 2009, 47:233-263.
13. Bhattacharjee S., et al. The malarial host-targeting signal is conserved in the Irish potato famine pathogen. PLoS Pathog. 2006, 2:e50.
14. Khang C.H., et al. Translocation of Magnaporthe oryzae effectors into rice cells and their subsequent cell-to-cell movement. Plant Cell 2010, 22:1388-1403.
15. Keon J., et al. Transcriptional adaptation of Mycosphaerella graminicola to programmed cell death (PCD) of its susceptible wheat host. Mol. Plant Microbe Interact. 2007, 20:178-193.
16. Brunner P.C., et al. Coevolution and life cycle specialization of plant cell wall degrading enzymes in a hemibiotrophic pathogen. Mol. Biol. Evol. 2013, 30:1337-1347.
17. Okmen B., et al. Detoxification of tomatine by Cladosporium fulvum is required for full virulence on tomato. New Phytol. 2013, 198:1203-1214.
18. Naumann T.A., et al. Identification of a chitinase-modifying protein from Fusarium verticillioides: truncation of a host resistance protein by a fungalysin metalloprotease. J. Biol. Chem. 2011, 286:35358-35366.
19. van den Burg H.A., et al. Cladosporium fulvum Avr4 protects fungal cell walls against hydrolysis by plant chitinases accumulating during infection. Mol. Plant Microbe Interact. 2006, 19:1420-1430.
20. de Jonge R., et al. Conserved fungal LysM effector Ecp6 prevents chitin-triggered immunity in plants. Science 2010, 329:953-955.
21. Marshall R., et al. 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 Physiol. 2011, 156:756-769.
22. Mentlak T.A., et al. Effector-mediated suppression of chitin-triggered immunity by Magnaporthe oryzae is necessary for rice blast disease. Plant Cell 2012, 24:322-335.
23. Goodwin S.B., et al. Finished genome of the fungal wheat pathogen Mycosphaerella graminicola reveals dispensome structure, chromosome plasticity, and stealth pathogenesis. PLoS Genet. 2011, 7:e1002070.
24. Kema G.H., et al. Large-scale gene discovery in the septoria tritici blotch fungus Mycosphaerella graminicola with a focus on in planta expression. Mol. Plant Microbe Interact. 2008, 21:1249-1260.
25. Liu Z., et al. The cysteine rich necrotrophic effector SnTox1 produced by Stagonospora nodorum triggers susceptibility of wheat lines harboring Snn1. PLoS Pathog. 2012, 8:e1002467.
26. Joosten M.H., et al. The biotrophic fungus Cladosporium fulvum circumvents Cf-4-mediated resistance by producing unstable AVR4 elicitors. Plant Cell 1997, 9:367-379.
27. van Kan J.A., et al. Cloning and characterization of cDNA of avirulence gene avr9 of the fungal pathogen Cladosporium fulvum, causal agent of tomato leaf mold. Mol. Plant Microbe Interact. 1991, 4:52-59.
28. Kooman-Gersmann M., et al. Correlation between binding affinity and necrosis-inducing activity of mutant AVR9 peptide elicitors. Plant Physiol. 1998, 117:609-618.
29. Balesdent M.H., et al. The dispensable chromosome of Leptosphaeria maculans shelters an effector gene conferring avirulence towards Brassica rapa. New Phytol. 2013, 198:887-898.
30. Fudal I., et al. Heterochromatin-like regions as ecological niches for avirulence genes in the Leptosphaeria maculans genome: map-based cloning of AvrLm6. Mol. Plant Microbe Interact. 2007, 20:459-470.
31. Parlange F., et al. 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. Mol. Microb. 2009, 71:851-863.
32. Huang Y.J., et al. Temperature and leaf wetness duration affect phenotypic expression of Rlm6-mediated resistance to Leptosphaeria maculans in Brassica napus. New Phytol. 2006, 170:129-141.
33. Sasek V., et al. Recognition of avirulence gene AvrLm1 from hemibiotrophic ascomycete Leptosphaeria maculans triggers salicylic acid and ethylene signaling in Brassica napus. Mol. Plant Microbe Interact. 2012, 25:1238-1250.
34. Duncan K.E., Howard R.J. Cytological analysis of wheat infection by the leaf blotch pathogen Mycosphaerella graminicola. Mycol. Res. 2000, 104:1074-1082.
35. Yang F., et al. Battle through signaling between wheat and the fungal pathogen Septoria tritici revealed by proteomics and phosphoproteomics. Mol. Cell. Proteomics 2013, 12:2497-2508.
36. Kirsten S., et al. Necrosis-inducing proteins of Rhynchosporium commune, effectors in quantitative disease resistance. Mol. Plant Microbe Interact. 2012, 25:1314-1325.
37. Steiner-Lange S., et al. Differential defense reactions in leaf tissues of barley in response to infection by Rhynchosporium secalis and to treatment with a fungal avirulence gene product. Mol. Plant Microbe Interact. 2003, 16:893-902.
38. Vleeshouwers V.G., et al. Understanding and exploiting late blight resistance in the age of effectors. Annu. Rev. Phytopathol. 2011, 49:507-531.
39. Lorang J.M., et al. Plant disease susceptibility conferred by a 'resistance' gene. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:14861-14866.
40. Tada Y., et al. Victorin triggers programmed cell death and the defense response via interaction with a cell surface mediator. Plant Cell Physiol. 2005, 46:1787-1798.
41. van Doorn W.G., et al. Morphological classification of plant cell deaths. Cell Death Differ. 2011, 18:1241-1246.
42. Belfanti E., et al. The HcrVf2 gene from a wild apple confers scab resistance to a transgenic cultivated variety. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:886-890.
43. Larkan N.J., et al. The Brassica napus blackleg resistance gene LepR3 encodes a receptor-like protein triggered by the Leptosphaeria maculans effector AVRLM1. New Phytol. 2013, 197:595-605.
44. Rouxel T., Balesdent M.H. From model to crop plant-pathogen interactions: cloning of the first resistance gene to Leptosphaeria maculans in Brassica napus. New Phytol. 2013, 197:356-358.
45. Rooney H.C., et al. Cladosporium Avr2 inhibits tomato Rcr3 protease required for Cf-2-dependent disease resistance. Science 2005, 308:1783-1786.
46. Kruger J., et al. A tomato cysteine protease required for Cf-2-dependent disease resistance and suppression of autonecrosis. Science 2002, 296:744-747.
47. Van't Klooster J.W., et al. Affinity of Avr2 for tomato cysteine protease Rcr3 correlates with the Avr2-triggered Cf-2-mediated hypersensitive response. Mol. Plant Pathol. 2011, 12:21-30.
48. Liebrand T.W., et al. Receptor-like kinase SOBIR1/EVR interacts with receptor-like proteins in plant immunity against fungal infection. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:10010-10015.
49. Liebrand T.W., et al. Two for all: receptor-associated kinases SOBIR1 and BAK1. Trends Plant Sci. 2014, 19:123-132.
50. Vinatzer B.A., et al. Apple contains receptor-like genes homologous to the Cladosporium fulvum resistance gene family of tomato with a cluster of genes cosegregating with Vf apple scab resistance. Mol. Plant Microbe Interact. 2001, 14:508-515.
51. Xu M., Korban S.S. A cluster of four receptor-like genes resides in the Vf locus that confers resistance to apple scab disease. Genetics 2002, 162:1995-2006.
52. Gout L., et al. Lost in the middle of nowhere: the AvrLm1 avirulence gene of the Dothideomycete Leptosphaeria maculans. Mol. Microbiol. 2006, 60:67-80.
53. Szankowski I., et al. Highly scab-resistant transgenic apple lines achieved by introgression of HcrVf2 controlled by different native promoter lengths. Tree Genet. Genomes 2009, 5:349-358.
54. van't Slot K.A., et al. A single binding site mediates resistance- and disease-associated activities of the effector protein NIP1 from the barley pathogen Rhynchosporium secalis. Plant Physiol. 2007, 144:1654-1666.
55. Rohe M., et al. The race-specific elicitor, NIP1, from the barley pathogen, Rhynchosporium secalis, determines avirulence on host plants of the Rrs1 resistance genotype. EMBO J. 1995, 14:4168-4177.
56. de Jonge R., et al. Tomato immune receptor Ve1 recognizes effector of multiple fungal pathogens uncovered by genome and RNA sequencing. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:5110-5115.
57. Bonardi V., et al. A new eye on NLR proteins: focused on clarity or diffused by complexity?. Curr. Opin. Immunol. 2012, 24:41-50.
58. Maekawa T., et al. NLR functions in plant and animal immune systems: so far and yet so close. Nat. Immunol. 2011, 12:817-826.
59. Faris J.D., et al. Candidate gene analysis of quantitative disease resistance in wheat. Theor. Appl. Genet. 1999, 98:219-225.
60. Nagy E.D., Bennetzen J.L. Pathogen corruption and site-directed recombination at a plant disease resistance gene cluster. Genome Res. 2008, 18:1918-1923.
61. Bai S., et al. Structure-function analysis of barley NLR immune receptor MLA10 reveals its cell compartment specific activity in cell death and disease resistance. PLoS Pathog. 2012, 8:e1002752.
62. Bozkurt T.O., et al. Cellular and transcriptional responses of wheat during compatible and incompatible race-specific interactions with Puccinia striiformis f. sp. tritici. Mol. Plant Pathol. 2010, 11:625-640.
63. Shen K.A., et al. Dm3 is one member of a large constitutively expressed family of nucleotide binding site-leucine-rich repeat encoding genes. Mol. Plant Microbe Interact. 2002, 15:251-261.
64. Berruyer R., et al. Quantitative and qualitative influence of inoculation methods on in planta growth of rice blast fungus. Phytopathology 2006, 96:346-355.
65. Si-Ammour A., et al. Quantification of induced resistance against Phytophthora species expressing GFP as a vital marker: beta-aminobutyric acid but not BTH protects potato and Arabidopsis from infection. Mol. Plant Pathol. 2003, 4:237-248.
66. Coll N.S., et al. Programmed cell death in the plant immune system. Cell Death Differ. 2011, 18:1247-1256.
67. Jupe F., et al. Resistance gene enrichment sequencing (RenSeq) enables reannotation of the NB-LRR gene family from sequenced plant genomes and rapid mapping of resistance loci in segregating populations. Plant J. 2013, 76:530-544.
68. Stukenbrock E.H., McDonald B.A. The origins of plant pathogens in agro-ecosystems. Annu. Rev. Phytopathol. 2008, 46:75-100.
69. Marcroft S.J., et al. Effect of rotation of canola (Brassica napus) cultivars with different complements of blackleg resistance genes on disease severity. Plant Pathol. 2012, 61:934-944.
70. Bowen J.K., et al. Venturia inaequalis: the causal agent of apple scab. Mol. Plant Pathol. 2011, 12:105-122.
71. Avrova A., Knogge W. Rhynchosporium commune: a persistent threat to barley cultivation. Mol. Plant Pathol. 2012, 13:986-997.
72. de Wit P.J.G.M., et al. The genomes of the fungal plant pathogens Cladosporium fulvum and Dothistroma septosporum reveal adaptation to different hosts and lifestyles but also signatures of common ancestry. PLoS Genet. 2012, 8:e1003088.
73. Stergiopoulos I., et al. Mating-type genes and the genetic structure of a world-wide collection of the tomato pathogen Cladosporium fulvum. Fungal Genet. Biol. 2007, 44:415-429.
74. Kema G.H.J., et al. Histology of the pathogenesis of Mycosphaerella graminicola in wheat. Phytopathology 1996, 86:777-786.
75. Higgins V.J. Response of tomato to leaf injection with conidia of virulent and avirulent races of Cladosporium fulvum. Physiol. Plant Pathol. 1982, 20:145-155.
76. Huang Y.J., et al. Effects of temperature on ascospore germination and penetration of oilseed rape (Brassica napus) leaves by A- or B-group Leptosphaeria maculans (phoma stem canker). Plant Pathol. 2003, 52:245-255.
77. Tan K-C., et al. Quantitative variation in effector activity of ToxA isoforms from Stagonospora nodorum and Pyrenophora tritici-repentis. Mol. Plant Microbe Interact. 2012, 25:515-522.
78. Monaghan J., Zipfel C. Plant pattern recognition receptor complexes at the plasma membrane. Curr. Opin. Plant Biol. 2012, 15:349-357.