Structure Analysis Uncovers a Highly Diverse but Structurally Conserved Effector Family in Phytopathogenic Fungi

PLoS Pathogens

Volumn 11, Issue 10, 2015, Pages

  de Guillen, Karine ^a,b   Ortiz Vallejo, Diana ^c,d   Gracy, Jérome ^a,b   Fournier, Elisabeth ^c,d   Kroj, Thomas ^c,d   Padilla, André ^a,b  

^a CENTRE DE BIOCHIMIE STRUCTURALE   (France)

^b UNIV MONTPELLIER   (France)

^c CEMAGREF   (France)

^d CIRAD   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AVR PIA; AVR1 CO39; FUNGAL PROTEIN; MYCOTOXIN; PROTEIN TOXB; UNCLASSIFIED DRUG;

ARTICLE; FUNGUS; GENE EXPRESSION PROFILING; MAGNAPORTHE GRISEA; MAGNAPORTHE ORYZAE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN EXPRESSION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; PYRENOPHORA; PYRENOPHORA TRITICI REPENTIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; SEQUENCE ANALYSIS; STRUCTURE ANALYSIS; AMINO ACID SEQUENCE; ASCOMYCETES; CHEMISTRY; MOLECULAR GENETICS; PATHOGENICITY; PROTEIN SECONDARY STRUCTURE;

AMINO ACID SEQUENCE; ASCOMYCOTA; FUNGAL PROTEINS; MAGNETIC RESONANCE SPECTROSCOPY; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, SECONDARY;

EID: 84946053171     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1005228     Document Type: Article

References (93)

1. Hogenhout S a, Van der Hoorn R a L, Terauchi R, Kamoun S, Emerging concepts in effector biology of plant-associated organisms. Mol Plant Microbe Interact. 2009;22: 115–122. doi: 10.1094/MPMI-22-2-0115 19132864
2. Jones JDG, Dangl JL, The plant immune system. Nature. 2006;444: 323–9. 17108957
3. Doehlemann G, Requena N, Schaefer P, Brunner F, Connell RO, Parker JE. Reprogramming of plant cells by filamentous plant-colonizing microbes. 2014; 803–814.
4. Stergiopoulos I, de Wit PJGM, Fungal effector proteins. Annu Rev Phytopathol. 2009;47: 233–63. doi: 10.1146/annurev.phyto.112408.132637 19400631
5. Presti L Lo, Lanver D, Schweizer G, Tanaka S, Liang L, Tollot M, et al. Fungal Effectors and Plant Susceptibility. Annu Rev Plant Biol. 2015;66: 513–545. doi: 10.1146/annurev-arplant-043014-114623 25923844
6. Giraldo MC, Valent B, Filamentous plant pathogen effectors in action. Nat Rev Microbiol. Nature Publishing Group; 2013;11: 800–14. doi: 10.1038/nrmicro3119 24129511
7. Bozkurt TO, Schornack S, Banfield MJ, Kamoun S, Oomycetes, effectors, and all that jazz. Curr Opin Plant Biol. Elsevier Ltd; 2012; 1–10.
8. Haas BJ, Kamoun S, Zody MC, Jiang RHY, Handsaker RE, Cano LM, et al. Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature. 2009;461: 393–8. doi: 10.1038/nature08358 19741609
9. Jiang RHY, Tripathy S, Govers F, Tyler BM, RXLR effector reservoir in two Phytophthora species is dominated by a single rapidly evolving superfamily with more than 700 members. Proc Natl Acad Sci U S A. 2008;105: 4874–4879. doi: 10.1073/pnas.0709303105 18344324
10. Duplessis S, Cuomo C a, Lin Y-C, Aerts A, Tisserant E, Veneault-Fourrey C, et al. Obligate biotrophy features unraveled by the genomic analysis of rust fungi. Proc Natl Acad Sci U S A. 2011;108: 9166–71. doi: 10.1073/pnas.1019315108 21536894
11. Pedersen C, Themaat EVL van, McGuffin LJ, Abbott JC, Burgis TA, Barton G, et al. Structure and evolution of barley powdery mildew effector candidates. BMC Genomics. 2012;13: 694. doi: 10.1186/1471-2164-13-694 23231440
12. Spanu PD, Abbott JC, Amselem J, Burgis T a, Soanes DM, Stüber K, et al. Genome expansion and gene loss in powdery mildew fungi reveal tradeoffs in extreme parasitism. Science. 2010;330: 1543–6. doi: 10.1126/science.1194573 21148392
13. Hacquard S, Joly DL, Lin Y-C, Tisserant E, Feau N, Delaruelle C, et al. A comprehensive analysis of genes encoding small secreted proteins identifies candidate effectors in Melampsora larici-populina (poplar leaf rust). Mol Plant Microbe Interact. 2012;25: 279–93. doi: 10.1094/MPMI-09-11-0238 22046958
14. Dean R, Kan JANALVAN, Pretorius ZA, Hammond-kosack KIME, Pietro ADI, Spanu PD, et al. The Top 10 fungal pathogens in molecular plant pathology. 2012;13: 414–430.
15. Gurr S, Samalova M, Fisher M, The rise and rise of emerging infectious fungi challenges food security and ecosystem health. Fungal Biol Rev. 2011;25: 181–188.
16. Skamnioti P, Gurr SJ, Against the grain: safeguarding rice from rice blast disease. Trends Biotechnol. 2009;27: 141–50. doi: 10.1016/j.tibtech.2008.12.002 19187990
17. Galhano R, Talbot NJ, The biology of blast: Understanding how Magnaporthe oryzae invades rice plants. Fungal Biol Rev. Elsevier Ltd; 2011;25: 61–67.
18. Liu J, Wang X, Mitchell T, Hu Y, Liu X, Dai L, et al. Recent progress and understanding of the molecular mechanisms of the rice-Magnaporthe oryzae interaction. Mol Plant Pathol. 2010;11: 419–427. doi: 10.1111/j.1364-3703.2009.00607.x 20447289
19. Mentlak TA, Talbot NJ, Kroj T, Francisrtin Kamoun S, Effector Translocation and Delivery by the Rice Blast Fungus Magnaporthe oryzae. In: Effectors in Plant–Microbe Interactions. Wiley-Blackwell; 2011. pp. 219–241.
20. Valent B, Khang CH, Recent advances in rice blast effector research. Curr Opin Plant Biol. Elsevier Ltd; 2010;13: 434–41. doi: 10.1016/j.pbi.2010.04.012 20627803
21. Park C-H, Chen S, Shirsekar G, Zhou B, Khang CH, Songkumarn P, et al. The Magnaporthe oryzae Effector AvrPiz-t Targets the RING E3 Ubiquitin Ligase APIP6 to Suppress Pathogen-Associated Molecular Pattern-Triggered Immunity in Rice. Plant Cell. 2012.
22. Mentlak TA, Kombrink A, Shinya T, Ryder LS, Otomo I, Saitoh H, et al. Effector-mediated suppression of chitin-triggered immunity by magnaporthe oryzae is necessary for rice blast disease. Plant Cell. 2012;24: 322–35. doi: 10.1105/tpc.111.092957 22267486
23. Mosquera G, Giraldo MC, Khang CH, Coughlan S, Valent B, Interaction transcriptome analysis identifies Magnaporthe oryzae BAS1-4 as Biotrophy-associated secreted proteins in rice blast disease. Plant Cell. 2009;21: 1273–90. doi: 10.1105/tpc.107.055228 19357089
24. Saitoh H, Fujisawa S, Mitsuoka C, Ito A, Hirabuchi A, Ikeda K, et al. Large-scale gene disruption in Magnaporthe oryzae identifies MC69, a secreted protein required for infection by monocot and dicot fungal pathogens. PLoS Pathog. 2012;8: e1002711. doi: 10.1371/journal.ppat.1002711 22589729
25. Soanes DM, Alam I, Cornell M, Wong HM, Hedeler C, Paton NW, et al. Comparative genome analysis of filamentous fungi reveals gene family expansions associated with fungal pathogenesis. PLoS One. 2008;3: e2300. doi: 10.1371/journal.pone.0002300 18523684
26. Yoshida KK, Saitoh H, Fujisawa S, Kanzaki H, Matsumura H, Tosa Y, et al. Association genetics reveals three novel avirulence genes from the rice blast fungal pathogen Magnaporthe oryzae. Plant Cell. 2009;21: 1573–91. doi: 10.1105/tpc.109.066324 19454732
27. Chen X, Coram T, Huang X, Wang M, Dolezal A, Understanding Molecular Mechanisms of Durable and Non-durable Resistance to Stripe Rust in Wheat Using a Transcriptomics Approach. Curr Genomics. 2013;14: 111–126. doi: 10.2174/1389202911314020004 24082821
28. Kim S, Hu J, Oh Y, Park J, Choi J, Lee Y-H, et al. Combining ChIP-chip and expression profiling to model the MoCRZ1 mediated circuit for Ca/calcineurin signaling in the rice blast fungus. PLoS Pathog. 2010;6: e1000909. doi: 10.1371/journal.ppat.1000909 20502632
29. Dodds PN, Rathjen JP, Plant immunity: towards an integrated view of plant-pathogen interactions. Nat Rev Genet. Nature Publishing Group; 2010;11: 539–48. doi: 10.1038/nrg2812 20585331
30. Miki H, Matsui K, Kito H, Otsuka K, Ashizawa T, Yasuda N, et al. Molecular cloning and characterization of the AVR-Pia locus from a Japanese field isolate of Magnaporthe oryzae. 2009;10: 361–374.
31. Orbach MJ, Farrall L, Sweigard J a, Chumley FG, Valent B, A telomeric avirulence gene determines efficacy for the rice blast resistance gene Pi-ta. Plant Cell. 2000;12: 2019–32. 11090206
32. Ribot C, Césari S, Abidi I, Chalvon V, Bournaud C, Vallet J, et al. The Magnaporthe oryzae effector AVR1-CO39 is translocated into rice cells independently of a fungal-derived machinery. Plant J. 2012;74: 1–12.
33. Sweigard J a, Carroll a M, Kang S, Farrall L, Chumley FG, Valent B, Identification, cloning, and characterization of PWL2, a gene for host species specificity in the rice blast fungus. Plant Cell. 1995;7: 1221–33. 7549480
34. Wu J, Kou Y, Bao J, Li Y, Tang M, Zhu X, et al. Comparative genomics identifies the Magnaporthe oryzae avirulence effector AvrPi9 that triggers Pi9 -mediated blast resistance in rice. 2015;
35. Li W, Wang B, Wu J, Lu G, Hu Y, Zhang X, et al. The Magnaporthe oryzae avirulence gene AvrPiz-t encodes a predicted secreted protein that triggers the immunity in rice mediated by the blast resistance gene Piz-t. Mol Plant Microbe Interact. 2009;22: 411–20. doi: 10.1094/MPMI-22-4-0411 19271956
36. Ashikawa I, Hayashi N, Yamane H, Kanamori H, Wu J, Matsumoto T, et al. Two adjacent nucleotide-binding site-leucine-rich repeat class genes are required to confer Pikm-specific rice blast resistance. Genetics. 2008;180: 2267–76. doi: 10.1534/genetics.108.095034 18940787
37. Cesari S, Thilliez G, Ribot C, Chalvon V, Michel C, Jauneau A, et al. The rice resistance protein pair RGA4/RGA5 recognizes the Magnaporthe oryzae effectors AVR-Pia and AVR1-CO39 by direct binding. Plant Cell. 2013;25: 1463–81. doi: 10.1105/tpc.112.107201 23548743
38. Qu S, Liu G, Zhou B, Bellizzi M, Zeng L, Dai L, et al. The broad-spectrum blast resistance gene Pi9 encodes a nucleotide-binding site-leucine-rich repeat protein and is a member of a multigene family in rice. Genetics. 2006;172: 1901–14. 16387888
39. Okuyama Y, Kanzaki H, Abe A, Yoshida K, Tamiru M, Saitoh H, et al. A multifaceted genomics approach allows the isolation of the rice Pia-blast resistance gene consisting of two adjacent NBS-LRR protein genes. Plant J. 2011;66: 467–79. doi: 10.1111/j.1365-313X.2011.04502.x 21251109
40. Bryan GT, Wu KS, Farrall L, Jia Y, Hershey HP, McAdams S a, et al. tA single amino acid difference distinguishes resistant and susceptible alleles of the rice blast resistance gene Pi-ta. Plant Cell. 2000;12: 2033–46. 11090207
41. Zhou B, Qu S, Liu G, Dolan M, Sakai H, Lu G, et al. The eight amino-acid differences within three leucine-rich repeats between Pi2 and Piz-t resistance proteins determine the resistance specificity to Magnaporthe grisea. Mol Plant Microbe Interact. 2006;19: 1216–28. 17073304
42. Zhang Z-M, Zhang X, Zhou Z-R, Hu H-Y, Liu M, Zhou B, et al. Solution structure of the Magnaporthe oryzae avirulence protein AvrPiz-t. J Biomol NMR. 2013;55: 219–23. doi: 10.1007/s10858-012-9695-5 23334361
43. Nyarko A, Singarapu KK, Figueroa M, Manning V a, Pandelova I, Wolpert TJ, et al. Solution NMR Structures of Pyrenophora tritici-repentis ToxB and Its Inactive Homolog Reveal Potential Determinants of Toxin Activity. J Biol Chem. 2014;289: 25946–25956. doi: 10.1074/jbc.M114.569103 25063993
44. Barthe P, Ropars V, Roumestand C, DYNAMOF: a program for the dynamics analysis of relaxation data obtained at multiple magnetic fields. Comptes Rendus Chim. 2006;9: 503–513.
45. Holm L, Rosenström P, Dali server: Conservation mapping in 3D. Nucleic Acids Res. 2010;38: 545–549.
46. Ciuffetti LM, Manning V a, Pandelova I, Betts MF, Martinez JP, Host-selective toxins, Ptr ToxA and Ptr ToxB, as necrotrophic effectors in the Pyrenophora tritici-repentis-wheat interaction. New Phytol. 2010;187: 911–919. doi: 10.1111/j.1469-8137.2010.03362.x 20646221
47. Chiapello H, Mallet L, Guérin C, Aguileta G, Amselem J, Kroj T, et al. Deciphering genome content and evolutionary realtionships of isolates from the fungus Magnaporthe oryzae attacking different hosts. Genome Biol Evol. 2015;in press.
48. Klaubauf S, Tharreau D, Fournier E, Groenewald JZ, Crous PW, de Vries RP, et al. Resolving the polyphyletic nature of Pyricularia (Pyriculariaceae). Stud Mycol. ELSEVIER B.V; 2014;79: 85–120. doi: 10.1016/j.simyco.2014.09.004 25492987
49. Césari S, Kanzaki H, Fujiwara T, Bernoux M, Chalvon V, Kawano Y, et al. The NB-LRR proteins RGA4 and RGA5 interact functionally and physically to confer disease resistance. EMBO J. 2014;33: 1941–1959. doi: 10.15252/embj.201487923 25024433
50. Césari S, Bernoux M, Moncuquet P, Kroj T, Dodds PN, A novel conserved mechanism for plant NLR protein pairs: the “integrated decoy” hypothesis. Front Plant Sci. 2014;5: 606. doi: 10.3389/fpls.2014.00606 25506347
51. Pedersen C, Themaat V, Ver E, McGuffin L, Abbott JC, Burgis TA, et al. Structure and evolution of barley powdery mildew effector candidates. BMC Genomics. 2012
52. Chuma I, Isobe C, Hotta Y, Ibaragi K, Futamata N, Kusaba M, et al. Multiple translocation of the AVR-Pita effector gene among chromosomes of the rice blast fungus Magnaporthe oryzae and related species. PLoS Pathog. 2011;7: e1002147. doi: 10.1371/journal.ppat.1002147 21829350
53. Rouxel T, Grandaubert J, Hane JK, Hoede C, van de Wouw AP, Couloux A, et al. Effector diversification within compartments of the Leptosphaeria maculans genome affected by Repeat-Induced Point mutations. Nat Commun. 2011;2: 202. doi: 10.1038/ncomms1189 21326234
54. Ma L-J, van der Does HC, Borkovich K a, Coleman JJ, Daboussi M-J, Di Pietro A, et al. Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature. 2010;464: 367–73. doi: 10.1038/nature08850 20237561
55. Jonge R De, Bolton MD, Kombrink A, De Jonge R, Bolton MD, Kombrink A, et al. Extensive chromosomal reshuffling drives evolution of virulence in an asexual pathogen. Genome Res. 2013;23: 1271–1282. doi: 10.1101/gr.152660.112 23685541
56. Win J, Krasileva K V, Kamoun S, Shirasu K, Staskawicz BJ, Banfield MJ, Heitman J, Sequence Divergent RXLR Effectors Share a Structural Fold Conserved across Plant Pathogenic Oomycete Species. PLoS Pathog. 2012;8: e1002400. doi: 10.1371/journal.ppat.1002400 22253591
57. Baxter L, Tripathy S, Ishaque N, Boot N, Cabral A, Kemen E, et al. Signatures of adaptation to obligate biotrophy in the Hyaloperonospora arabidopsidis genome. Science. 2010;330: 1549–1551. doi: 10.1126/science.1195203 21148394
58. Raffaele S, Farrer R a, Cano LM, Studholme DJ, MacLean D, Thines M, et al. Genome evolution following host jumps in the Irish potato famine pathogen lineage. Science. 2010;330: 1540–3. doi: 10.1126/science.1193070 21148391
59. Dou D, Kale SD, Wang X, Chen Y, Wang Q, Wang X, et al. Conserved C-terminal motifs required for avirulence and suppression of cell death by Phytophthora sojae effector Avr1b. Plant Cell. 2008;20: 1118–33. doi: 10.1105/tpc.107.057067 18390593
60. Boutemy LS, King SRF, Win J, Hughes RK, Clarke T a, Blumenschein TM a, et al. Structures of Phytophthora RXLR effector proteins: a conserved but adaptable fold underpins functional diversity. J Biol Chem. 2011;286: 35834–42. doi: 10.1074/jbc.M111.262303 21813644
61. Chou S, Krasileva K V, Holton JM, Steinbrenner AD, Alber T, Staskawicz BJ, Hyaloperonospora arabidopsidis ATR1 effector is a repeat protein with distributed recognition surfaces. Proc Natl Acad Sci U S A. 2011;108: 13323–8. doi: 10.1073/pnas.1109791108 21788488
62. Yaeno T, Li H, Chaparro-Garcia A, Schornack S, Koshiba S, Watanabe S, et al. Phosphatidylinositol monophosphate-binding interface in the oomycete RXLR effector AVR3a is required for its stability in host cells to modulate plant immunity. Proc Natl Acad Sci U S A. 2011;108: 14682–7. doi: 10.1073/pnas.1106002108 21821794
63. Bayry J, Aimanianda V, Guijarro JI, Sunde M, Latgé JP, Hydrophobins-unique fungal proteins. PLoS Pathog. 2012;8: 6–9.
64. Kubicek CP, Baker S, Gamauf C, Kenerley CM, Druzhinina IS, Purifying selection and birth-and-death evolution in the class II hydrophobin gene families of the ascomycete Trichoderma/Hypocrea. BMC Evol Biol. 2008;8: 4. doi: 10.1186/1471-2148-8-4 18186925
65. Wosten H a, H YDROPHOBINS: Multipurpose Proteins. Annu Rev Microbiol. 2001;55: 625–46. 11544369
66. Kwan a HY, Winefield RD, Sunde M, Matthews JM, Haverkamp RG, Templeton MD, et al. Structural basis for rodlet assembly in fungal hydrophobins. Proc Natl Acad Sci U S A. 2006;103: 3621–3626. 16537446
67. Stergiopoulos I, Kourmpetis Y a I, Slot JC, Bakker FT, De Wit PJGM, Rokas A, In silico characterization and molecular evolutionary analysis of a novel superfamily of fungal effector proteins. Mol Biol Evol. 2012;29: 3371–84. doi: 10.1093/molbev/mss143 22628532
68. Ve T, Williams SJ, Catanzariti A-M, Rafiqi M, Rahman M, Ellis JG, et al. Structures of the flax-rust effector AvrM reveal insights into the molecular basis of plant-cell entry and effector-triggered immunity. Proc Natl Acad Sci U S A. 2013
69. Wang C-IAC-I a, Guncar G, Forwood JK, Teh T, Catanzariti A-MA-M, Lawrence GJ, et al. Crystal structures of flax rust avirulence proteins AvrL567-A and -D reveal details of the structural basis for flax disease resistance specificity. Plant Cell. 2007;19: 2898–912. 17873095
70. Sarma GN, Manning VA, Ciuffetti LM, Karplus PA. Structure of Ptr ToxA: An RGD-Containing Host-Selective Toxin from Pyrenophora tritici-repentis. 2005;17: 3190–3202.
71. Studier FW, Protein production by auto-induction in high density shaking cultures. Protein Expr Purif. 2005;41: 207–234. 15915565
72. Habeeb AFSA, Hirs C. H. W., SNT [37] Reaction of protein sulfhydryl groups with Ellman’s reagent. In: Methods in Enzymology. Academic Press; 1972. pp. 457–464. doi: 10.1016/S0076-6879(72)25041-8
73. Wishart DS, Bigam CG, Yao J, Abildgaard F, Dyson HJ, Oldfield E, et al. 1H, 13C and 15N chemical shift referencing in biomolecular NMR. J Biomol NMR. 1995;6: 135–140. 8589602
74. Vranken WF, Boucher W, Stevens TJ, Fogh RH, Pajon A, Llinas M, et al. The CCPN data model for NMR spectroscopy: Development of a software pipeline. Proteins Struct Funct Bioinforma. 2005;59: 687–696.
75. Carr HY, Purcell EM, Effects of Diffusion on Free Precession in Nuclear Magnetic Resonance Experiments. Phys Rev. 1954;94: 630–632.
76. Meiboom S, Gill D, Modified Spin-Echo Method for Measuring Nuclear Relaxation Times. Rev Sci Instrum. 1958;29: 688.
77. Kay LE, Torchia DA, Bax A, Backbone dynamics of proteins as studied by nitrogen-15 inverse detected heteronuclear NMR spectroscopy: application to staphylococcal nuclease. Biochemistry. 1989;28: 8972–8979. 2690953
78. Güntert P, Automated NMR structure calculation with CYANA. Methods Mol Biol. 2004;278: 353–378. 15318003
79. Brunger AT, Version 1.2 of the Crystallography and NMR system. Nat Protoc. 2007;2: 2728–2733. 18007608
80. Shen Y, Delaglio F, Cornilescu G, Bax A, TALOS+: a hybrid method for predicting protein backbone torsion angles from NMR chemical shifts. J Biomol NMR. 2009;44: 213–223. doi: 10.1007/s10858-009-9333-z 19548092
81. Nederveen AJ, Doreleijers JF, Vranken W, Miller Z, Spronk CAEM, Nabuurs SB, et al. RECOORD: A recalculated coordinate database of 500+ proteins from the PDB using restraints from the BioMagResBank. Proteins Struct Funct Bioinforma. 2005;59: 662–672.
82. Laskowski RA, Moss DS, Thornton JM, Main-chain bond lengths and bond angles in protein structures. J Mol Biol. 1993;231: 1049–1067. 8515464
83. Suzek BE, Huang H, McGarvey P, Mazumder R, Wu CH, UniRef: comprehensive and non-redundant UniProt reference clusters. Bioinformatics. 2007;23: 1282–1288. 17379688
84. Petersen TN, Brunak S, von Heijne G, Nielsen H, SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods. 2011;8: 785–786. doi: 10.1038/nmeth.1701 21959131
85. Zhang Y, Skolnick J, TM-align: a protein structure alignment algorithm based on the TM-score. Nucleic Acids Res. 2005;33: 2302–2309. 15849316
86. Finn RD, Clements J, Eddy SR, HMMER web server: interactive sequence similarity searching. Nucleic Acids Res. 2011;39: W29–W37. doi: 10.1093/nar/gkr367 21593126
87. Edgar RC, MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32: 1792–1797. 15034147
88. Crooks GE, Hon G, Chandonia J-M, Brenner SE, WebLogo: a sequence logo generator. Genome Res. 2004;14: 1188–1190. 15173120
89. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S, MEGA6: Molecular evolutionary genetics analysis version 6.0. Mol Biol Evol. 2013;30: 2725–2729. doi: 10.1093/molbev/mst197 24132122
90. Berruyer R, Adreit H, Milazzo J, Gaillard S, Berger a, Dioh W, et al. Identification and fine mapping of Pi33, the rice resistance gene corresponding to the Magnaporthe grisea avirulence gene ACE1. Theor Appl Genet. 2003;107: 1139–1147. 12838393
91. Faivre-Rampant O, Thomas J, Allègre M, Morel J-B, Tharreau D, Nottéghem J-L, et al. Characterization of the model system rice-Magnaporthe for the study of nonhost resistance in cereals. New Phytol. 2008;180: 899–910. doi: 10.1111/j.1469-8137.2008.02621.x 19138233
92. Delteil A, Blein M, Faivre-rampant O, Guellim A, Estevan J, Hirsch J, et al. Building a mutant resource for the study of disease resistance in rice reveals the pivotal role of several genes involved in defence. 2012;13: 72–82.
93. Magnan CN, Baldi P, SSpro/ACCpro 5: almost perfect prediction of protein secondary structure and relative solvent accessibility using profiles, machine learning and structural similarity. Bioinformatics. 2014;30: 2592–2597. doi: 10.1093/bioinformatics/btu352 24860169