Global Genome and Transcriptome Analyses of Magnaporthe oryzae Epidemic Isolate 98-06 Uncover Novel Effectors and Pathogenicity-Related Genes, Revealing Gene Gain and Lose Dynamics in Genome Evolution

PLoS Pathogens

Volumn 11, Issue 4, 2015, Pages

  Dong, Yanhan ^a,b   Li, Ying ^a,b   Zhao, Miaomiao ^a,b   Jing, Maofeng ^a,b   Liu, Xinyu ^a,b   Liu, Muxing ^a,b   Guo, Xianxian ^a,b   Zhang, Xing ^a,b   Chen, Yue ^a,b   Liu, Yongfeng ^c   Liu, Yanhong ^c   Ye, Wenwu ^a,b   Zhang, Haifeng ^a,b   Wang, Yuanchao ^a,b   Zheng, Xiaobo ^a,b   Wang, Ping ^d   Zhang, Zhengguang ^a,b  

^a NANJING AGRICULTURAL UNIVERSITY   (China)

^b BEIJING UNIVERSITY OF POSTS AND TELECOMMUNICATIONS   (China)

^c BGI SHENZHEN   (China)

^d LOUISIANA STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL PROTEIN; IUG18 PROTEIN; IUG6 PROTEIN; IUG9 PROTEIN; PROTEIN BAS1; PROTEIN BAS2; PROTEIN BAS3; PROTEIN BAS4; PROTEIN IUG18; PROTEIN IUG6; PROTEIN IUG9; PROTEIN NUP1; PROTEIN NUP2; PROTEIN NUP3; PROTEIN PWL1; PROTEIN SLP1; SNARE PROTEIN; TRANSCRIPTOME; UNCLASSIFIED DRUG;

AGROBACTERIUM TUMEFACIENS; ARTICLE; CELL DEATH; CONTROLLED STUDY; FUNGAL VIRULENCE; GAIN OF FUNCTION MUTATION; GENE DISRUPTION; GENE EXPRESSION PROFILING; GENE NUMBER; GENE SEQUENCE; GENOME; HOST PATHOGEN INTERACTION; LOSS OF FUNCTION MUTATION; MAGNAPORTHE ORYZAE; MOLECULAR GENETICS; NICOTIANA BENTHAMIANA; NONHUMAN; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RICE; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; TRANSPOSON; EVOLUTION; FUNGAL GENE; FUNGAL GENOME; GENETICS; GENOME-WIDE ASSOCIATION STUDY; MAGNAPORTHE; MICROBIOLOGY; NUCLEOTIDE SEQUENCE; ORYZA; PATHOGENICITY; PLANT DISEASE; POLYMERASE CHAIN REACTION; VIRULENCE;

MAGNAPORTHE ORYZAE; NICOTIANA BENTHAMIANA;

BASE SEQUENCE; BIOLOGICAL EVOLUTION; FUNGAL PROTEINS; GENE EXPRESSION PROFILING; GENES, FUNGAL; GENOME, FUNGAL; GENOME-WIDE ASSOCIATION STUDY; MAGNAPORTHE; MOLECULAR SEQUENCE DATA; ORYZA; PLANT DISEASES; POLYMERASE CHAIN REACTION; VIRULENCE;

EID: 84929493560     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004801     Document Type: Article

References (103)

1. Jantasuriyarat C, Gowda M, Haller K, Hatfield J, Lu G, et al. (2005) Large-scale identification of expressed sequence tags involved in rice and rice blast fungus interaction. Plant Physiol 138: 105–115. 15888683
2. Talbot NJ, (2003) On the trail of a cereal killer: Exploring the biology of Magnaporthe grisea. Annu Rev Microbiol 57: 177–202. 14527276
3. Ebbole DJ, (2007) Magnaporthe as a model for understanding host-pathogen interactions. Annu Rev Phytopathol 45: 437–456. 17489691
4. Mosquera G, Giraldo MC, Khang CH, Coughlan S, Valent B, (2009) Interaction transcriptome analysis identifies Magnaporthe oryzae BAS1-4 as biotrophy-associated secreted proteins in rice blast disease. Plant Cell 21: 1273. doi: 10.1105/tpc.107.055228 19357089
5. Levy M, Correavictoria FJ, Zeigler RS, Xu SZ, Hamer JE, (1993) Genetic Diversity of the Rice Blast Fungus in a Disease Nursery in Colombia. Phytopathology 83: 1427–1433.
6. Kumar J, Nelson RJ, Zeigler RS, (1999) Population structure and dynamics of Magnaporthe grisea in the Indian Himalayas. Genetics 152: 971–984. 10388817
7. Orbach MJ, Farrall L, Sweigard JA, Chumley FG, Valent B, (2000) A telomeric avirulence gene determines efficacy for the rice blast resistance gene Pi-ta. Plant Cell 12: 2019–2032. 11090206
8. 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. Mol Microbiol 60: 67–80. 16556221
9. Valent B, Chumley FG, (1991) Molecular genetic analysis of the rice blast fungus, Magnaporthe grisea. Annu Rev Phytopathol 29: 443–467. 18479196
10. Kim S, Park J, Park SY, Mitchell TK, Lee YH, (2010) Identification and analysis of in planta expressed genes of Magnaporthe oryzae. BMC Genomics 11: 104. doi: 10.1186/1471-2164-11-104 20146797
11. Jantasuriyarat C, Gowda M, Haller K, Hatfield J, Lu G, et al. (2005) Large-scale identification of expressed sequence tags involved in rice and rice blast fungus interaction. Plant physiol 138: 105. 15888683
12. Khang CH, Berruyer R, Giraldo MC, Kankanala P, Park SY, et al. (2010) Translocation of Magnaporthe oryzae effectors into rice cells and their subsequent cell-to-cell movement. Plant Cell 22: 1388–1403. doi: 10.1105/tpc.109.069666 20435900
13. Leung H, Borromeo ES, Bernardo MA, Notteghem JL, (1988) Genetic-analysis of virulence in the rice blast fungus Magnaporthe grisea. Phytopathology 78: 1227–1233.
14. Chao CCT, Ellingboe AH, (1991) Selection for mating competence in Magnaporthe grisea pathogenic to rice. Can J Bot 69: 2130–2134.
15. Dean RA, Talbot NJ, Ebbole DJ, Farman ML, Mitchell TK, et al. (2005) The genome sequence of the rice blast fungus Magnaporthe grisea. Nature 434: 980–986. 15846337
16. Yoshida K, Saitoh H, Fujisawa S, Kanzaki H, Matsumura H, et al. (2009) Association genetics reveals three novel avirulence genes from the rice blast fungal pathogen Magnaporthe oryzae. Plant Cell 21: 1573–1591. doi: 10.1105/tpc.109.066324 19454732
17. Xue M, Yang J, Li Z, Hu S, Yao N, et al. (2012) Comparative analysis of the genomes of two field isolates of the rice blast fungus Magnaporthe oryzae. PLoS Genet 8: e1002869. doi: 10.1371/journal.pgen.1002869 22876203
18. Li R, Li Y, Kristiansen K, Wang J, (2008) SOAP: short oligonucleotide alignment program. Bioinformatics 24: 713–714. doi: 10.1093/bioinformatics/btn025 18227114
19. Li R, Zhu H, Ruan J, Qian W, Fang X, et al. (2010) De novo assembly of human genomes with massively parallel short read sequencing. Genome Res 20: 265–272. doi: 10.1101/gr.097261.109 20019144
20. Chen C, Lian B, Hu J, Zhai H, Wang X, et al. (2013) Genome comparison of two Magnaporthe oryzae field isolates reveals genome variations and potential virulence effectors. BMC Genomics 14: 887. doi: 10.1186/1471-2164-14-887 24341723
21. Smith DR, Lee RW, (2008) Nucleotide diversity in the mitochondrial and nuclear compartments of Chlamydomonas reinhardtii: investigating the origins of genome architecture. BMC Evol Biol 8: 156. doi: 10.1186/1471-2148-8-156 18495022
22. Saha S, Bridges S, Magbanua ZV, Peterson DG, (2008) Empirical comparison of ab initio repeat finding programs. Nucleic Acids Res 36: 2284–2294. doi: 10.1093/nar/gkn064 18287116
23. van der Does HC, Rep M, (2007) Virulence genes and the evolution of host specificity in plant-pathogenic fungi. Mol Plant Microbe Interact 20: 1175–1182. 17918619
24. Oliva R, Win J, Raffaele S, Boutemy L, Bozkurt TO, et al. (2010) Recent developments in effector biology of filamentous plant pathogens. Cell Microbiol 12: 705–715. doi: 10.1111/j.1462-5822.2010.01471.x 20374248
25. Rehmany AP, Gordon A, Rose LE, Allen RL, Armstrong MR, et al. (2005) Differential recognition of highly divergent downy mildew avirulence gene alleles by RPP1 resistance genes from two Arabidopsis lines. Plant Cell 17: 1839–1850. 15894715
26. Guo M, Chen Y, Du Y, Dong Y, Guo W, et al. (2011) The bZIP transcription factor MoAP1 mediates the oxidative stress response and is critical for pathogenicity of the rice blast fungus Magnaporthe oryzae. PLoS Pathog 7: e1001302. doi: 10.1371/journal.ppat.1001302 21383978
27. Dou X, Wang Q, Qi Z, Song W, Wang W, et al. (2011) MoVam7, a conserved SNARE involved in vacuole assembly, is required for growth, endocytosis, ROS accumulation, and pathogenesis of Magnaporthe oryzae. PLoS One 6: e16439. doi: 10.1371/journal.pone.0016439 21283626
28. De Vleesschauwer D, Gheysen G, Hofte M, (2013) Hormone defense networking in rice: tales from a different world. Trends Plant Sci 18: 555–565. doi: 10.1016/j.tplants.2013.07.002 23910453
29. Yamada S, Kano A, Tamaoki D, Miyamoto A, Shishido H, et al. (2012) Involvement of OsJAZ8 in jasmonate-induced resistance to bacterial blight in rice. Plant Cell Physiol 53: 2060–2072. doi: 10.1093/pcp/pcs145 23104764
30. Takai R, Isogai A, Takayama S, Che FS, (2008) Analysis of flagellin perception mediated by flg22 receptor OsFLS2 in rice. Mol Plant Microbe Interact 21: 1635–1642. doi: 10.1094/MPMI-21-12-1635 18986259
31. Saeed AI, Sharov V, White J, Li J, Liang W, et al. (2003) TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34: 374–378. 12613259
32. Wang P, Shen G, (2011) The endocytic adaptor proteins of pathogenic fungi: charting new and familiar pathways. Med Mycol 49: 449–457. doi: 10.3109/13693786.2011.553246 21254965
33. Giraldo MC, Dagdas YF, Gupta YK, Mentlak TA, Yi M, et al. (2013) Two distinct secretion systems facilitate tissue invasion by the rice blast fungus Magnaporthe oryzae. Nat Commun 4: 1996. doi: 10.1038/ncomms2996 23774898
34. Hogenhout SA, Van der Hoorn RAL, Terauchi R, Kamoun S, (2009) Emerging concepts in effector biology of plant-associated organisms. Mol Plant Microbe Interact 22: 115–122. doi: 10.1094/MPMI-22-2-0115 19132864
35. de Jonge R, Bolton MD, Kombrink A, van den Berg GC, Yadeta KA, et al. (2013) Extensive chromosomal reshuffling drives evolution of virulence in an asexual pathogen. Genome Res 23: 1271–1282. doi: 10.1101/gr.152660.112 23685541
36. Dou D, Kale SD, Wang X, Chen Y, Wang Q, et al. (2008) Conserved C-terminal motifs required for avirulence and suppression of cell death by Phytophthora sojae effector Avr1b. Plant Cell 20: 1118–1133. doi: 10.1105/tpc.107.057067 18390593
37. Block A, Li GY, Fu ZQ, Alfano JR, (2008) Phytopathogen type III effector weaponry and their plant targets. Curr Opin Plant Biol 11: 396–403. doi: 10.1016/j.pbi.2008.06.007 18657470
38. Li W, Wang B, Wu J, Lu G, Hu Y, et al. (2009) 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 22: 411–420. doi: 10.1094/MPMI-22-4-0411 19271956
39. Liu W, Liu J, Ning Y, Ding B, Wang X, et al. (2013) Recent progress in understanding PAMP- and effector-triggered immunity against the rice blast fungus Magnaporthe oryzae. Mol Plant 6: 605–620. doi: 10.1093/mp/sst015 23340743
40. Raffaele S, Kamoun S, (2012) Genome evolution in filamentous plant pathogens: why bigger can be better. Nat Rev Microbiol 10: 417–430. doi: 10.1038/nrmicro2790 22565130
41. Kim S, Park SY, Kim KS, Rho HS, Chi MH, et al. (2009) Homeobox transcription factors are required for conidiation and appressorium development in the rice blast fungus Magnaporthe oryzae. PLoS Genet 5: e1000757. doi: 10.1371/journal.pgen.1000757 19997500
42. Yang J, Zhao XY, Sun J, Kang ZS, Ding SL, et al. (2010) A novel protein Com1 is required for normal conidium morphology and full virulence in Magnaporthe oryzae. Mol Plant Microbe Interact 23: 112–123. doi: 10.1094/MPMI-23-1-0112 19958144
43. Shi ZX, Leung H, (1995) Genetic analysis of sporulation in Magnaporthe grisea by chemical and insertional mutagenesis. Mol Plant Microbe Interact 8: 949–959.
44. Zhou Z, Li G, Lin C, He C, (2009) Conidiophore stalk-less1 encodes a putative zinc-finger protein involved in the early stage of conidiation and mycelial infection in Magnaporthe oryzae. Mol Plant Microbe Interact 22: 402–410. doi: 10.1094/MPMI-22-4-0402 19271955
45. Nishimura M, Fukada J, Moriwaki A, Fujikawa T, Ohashi M, et al. (2009) Mstu1, an APSES transcription factor, is required for appressorium-mediated infection in Magnaporthe grisea. Biosci Biotechnol Biochem 73: 1779–1786. 19661696
46. Chen Y, Zhai S, Zhang H, Zuo R, Wang J, et al. (2014) Shared and distinct functions of two Gti1/Pac2 family proteins in growth, morphogenesis and pathogenicity of Magnaporthe oryzae. Environ Microbiol 16: 788–801. doi: 10.1111/1462-2920.12204 23895552
47. Jiang CJ, Shimono M, Sugano S, Kojima M, Yazawa K, et al. (2010) Abscisic acid interacts antagonistically with salicylic acid signaling pathway in rice-Magnaporthe grisea interaction. Mol Plant Microbe Interact 23: 791–798. doi: 10.1094/MPMI-23-6-0791 20459318
48. Park CH, Chen S, Shirsekar G, Zhou B, Khang CH, et al. (2012) 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 24: 4748–4762. doi: 10.1105/tpc.112.105429 23204406
49. Oh SK, Young C, Lee M, Oliva R, Bozkurt TO, et al. (2009) In planta expression screens of Phytophthora infestans RXLR effectors reveal diverse phenotypes, including activation of the Solanum bulbocastanum disease resistance protein Rpi-blb2. Plant Cell 21: 2928–2947. doi: 10.1105/tpc.109.068247 19794118
50. Durrant WE, Dong X, (2004) Systemic acquired resistance. Annu Rev Phytopathol 42: 185–209. 15283665
51. Vlot AC, Dempsey DA, Klessig DF, (2009) Salicylic Acid, a multifaceted hormone to combat disease. Annu Rev Phytopathol 47: 177–206. doi: 10.1146/annurev.phyto.050908.135202 19400653
52. Yang Y, Qi M, Mei C, (2004) Endogenous salicylic acid protects rice plants from oxidative damage caused by aging as well as biotic and abiotic stress. Plant J 40: 909–919. 15584956
53. Wu J, Kou Y, Bao J, Li Y, Tang M, et al. (2015) Comparative genomics identifies the Magnaporthe oryzae avirulence effector AvrPi9 that triggers Pi9-mediated blast resistance in rice. New Phytol.
54. Chuma I, Isobe C, Hotta Y, Ibaragi K, Futamata N, et al. (2011) Multiple translocation of the AVR-Pita effector gene among chromosomes of the rice blast fungus Magnaporthe oryzae and related species. PLoS Pathog 7: e1002147. doi: 10.1371/journal.ppat.1002147 21829350
55. Burt A, (2000) Perspective: sex, recombination, and the efficacy of selection—was Weismann right? Evolution 54: 337–351. 10937212
56. McDonald BA, Linde C, (2002) Pathogen population genetics, evolutionary potential, and durable resistance. Annu Rev Phytopathol 40: 349–379. 12147764
57. Raffaele S, Kamoun S, (2012) Genome evolution in filamentous plant pathogens: why bigger can be better. Nat Rev Microbiol 10: 417–430. doi: 10.1038/nrmicro2790 22565130
58. Kamoun S, (2007) Groovy times: filamentous pathogen effectors revealed. Curr Opin Plant Biol 10: 358–365. 17611143
59. Kang S, Sweigard JA, Valent B, (1995) The PWL host specificity gene family in the blast fungus Magnaporthe grisea. Mol Plant Microbe Interact 8: 939–948. 8664503
60. Sweigard JA, Carroll AM, Kang S, Farrall L, Chumley FG, et al. (1995) Identification, cloning, and characterization of PWL2, a gene for host species specificity in the rice blast fungus. Plant Cell 7: 1221–1233. 7549480
61. Ahn N, Kim S, Choi W, Im KH, Lee YH, (2004) Extracellular matrix protein gene, EMP1, is required for appressorium formation and pathogenicity of the rice blast fungus, Magnaporthe grisea. Molecules and Cells 17: 166–173. 15055545
62. Kim S, Ahn IP, Rho HS, Lee YH, (2005) MHP1, a Magnaporthe grisea hydrophobin gene, is required for fungal development and plant colonization. Mol Microbiol 57: 1224–1237. 16101997
63. Ellis JG, Rafiqi M, Gan P, Chakrabarti A, Dodds PN, (2009) Recent progress in discovery and functional analysis of effector proteins of fungal and oomycete plant pathogens. Curr Opin Plant Biol 12: 399–405. doi: 10.1016/j.pbi.2009.05.004 19540152
64. Stergiopoulos I, de Wit PJ, (2009) Fungal effector proteins. Annu Rev Phytopathol 47: 233–263. doi: 10.1146/annurev.phyto.112408.132637 19400631
65. Valent B, Khang CH, (2010) Recent advances in rice blast effector research. Curr Opin Plant Biol 13: 434–441. doi: 10.1016/j.pbi.2010.04.012 20627803
66. Bozkurt TO, Schornack S, Banfield MJ, Kamoun S, (2012) Oomycetes, effectors, and all that jazz. Curr Opin Plant Biol 15: 483–492. doi: 10.1016/j.pbi.2012.03.008 22483402
67. Huang J, Si W, Deng Q, Li P, Yang S, (2014) Rapid evolution of avirulence genes in rice blast fungus Magnaporthe oryzae. BMC Genet 15: 45. doi: 10.1186/1471-2156-15-45 24725999
68. Saitoh H, Fujisawa S, Mitsuoka C, Ito A, Hirabuchi A, et al. (2012) Large-scale gene disruption in Magnaporthe oryzae identifies MC69, a secreted protein required for infection by monocot and dicot fungal pathogens. PLoS Pathog 8: e1002711. doi: 10.1371/journal.ppat.1002711 22589729
69. Talbot NJ, Ebbole DJ, Hamer JE, (1993) Identification and characterization of MPG1, a gene involved in pathogenicity from the rice blast fungus Magnaporthe grisea. Plant Cell 5: 1575–1590. 8312740
70. Jeong JS, Mitchell TK, Dean RA, (2007) The Magnaporthe grisea snodprot1 homolog, MSP1, is required for virulence. FEMS Microbiol Lett 273: 157–165. 17590228
71. Mentlak TA, Kombrink A, Shinya T, Ryder LS, Otomo I, et al. (2012) Effector-mediated suppression of chitin-triggered immunity by Magnaporthe oryzae is necessary for rice blast disease. Plant Cell 24: 322–335. doi: 10.1105/tpc.111.092957 22267486
72. Friesen TL, Stukenbrock EH, Liu Z, Meinhardt S, Ling H, et al. (2006) Emergence of a new disease as a result of interspecific virulence gene transfer. Nat Genet 38: 953–956. 16832356
73. de Jonge R, van Esse HP, Kombrink A, Shinya T, Desaki Y, et al. (2010) Conserved fungal LysM effector Ecp6 prevents chitin-triggered immunity in plants. Science 329: 953–955. doi: 10.1126/science.1190859 20724636
74. Li L, Stoeckert CJ, Jr.Roos DS, (2003) OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 13: 2178–2189. 12952885
75. Korf I, (2004) Gene finding in novel genomes. BMC Bioinformatics 5: 59. 15144565
76. Besemer J, Borodovsky M, (2005) GeneMark: web software for gene finding in prokaryotes, eukaryotes and viruses. Nucleic Acids Res 33: W451–454. 15980510
77. Birney E, Clamp M, Durbin R, (2004) GeneWise and Genomewise. Genome Res 14: 988–995. 15123596
78. Kanehisa M, Goto S, Kawashima S, Okuno Y, Hattori M, (2004) The KEGG resource for deciphering the genome. Nucleic Acids Res 32: D277–280. 14681412
79. Tatusov RL, Fedorova ND, Jackson JD, Jacobs AR, Kiryutin B, et al. (2003) The COG database: an updated version includes eukaryotes. BMC Bioinformatics 4: 41. 12969510
80. Magrane M, Consortium U, (2011) UniProt Knowledgebase: a hub of integrated protein data. Database (Oxford) 2011: bar009.
81. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, et al. (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 25: 25–29. 10802651
82. Sonnhammer EL, von Heijne G, Krogh A, (1998) A hidden Markov model for predicting transmembrane helices in protein sequences. Proc Int Conf Intell Syst Mol Biol 6: 175–182. 9783223
83. Petersen TN, Brunak S, von Heijne G, Nielsen H, (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8: 785–786. doi: 10.1038/nmeth.1701 21959131
84. Nguyen Ba AN, Pogoutse A, Provart N, Moses AM, (2009) NLStradamus: a simple Hidden Markov Model for nuclear localization signal prediction. BMC Bioinformatics 10: 202. doi: 10.1186/1471-2105-10-202 19563654
85. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389–3402. 9254694
86. Benson G, (1999) Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 27: 573–580. 9862982
87. Kurtz S, Phillippy A, Delcher AL, Smoot M, Shumway M, et al. (2004) Versatile and open software for comparing large genomes. Genome Biol 5: R12. 14759262
88. Guo M, Guo W, Chen Y, Dong S, Zhang X, et al. (2010) The basic leucine zipper transcription factor Moatf1 mediates oxidative stress responses and is necessary for full virulence of the rice blast fungus Magnaporthe oryzae. Mol Plant Microbe Interact 23: 1053–1068. doi: 10.1094/MPMI-23-8-1053 20615116
89. Zhang C, Wang G, Wang J, Ji Z, Liu Z, et al. (2013) Characterization and comparative analyses of muscle transcriptomes in Dorper and small-tailed Han sheep using RNA-Seq technique. PLoS One 8: e72686. doi: 10.1371/journal.pone.0072686 24023632
90. Li R, Yu C, Li Y, Lam TW, Yiu SM, et al. (2009) SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 25: 1966–1967. doi: 10.1093/bioinformatics/btp336 19497933
91. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B, (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5: 621–628. doi: 10.1038/nmeth.1226 18516045
92. Feng J, Meyer CA, Wang Q, Liu JS, Shirley Liu X, et al. (2012) GFOLD: a generalized fold change for ranking differentially expressed genes from RNA-seq data. Bioinformatics 28: 2782–2788. doi: 10.1093/bioinformatics/bts515 22923299
93. Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, et al. (2008) KEGG for linking genomes to life and the environment. Nucleic Acids Res 36: D480–484. 18077471
94. Sweigard JA, Chumley FG, Valent B, (1992) Disruption of a Magnaporthe grisea cutinase gene. Mol Gen Genet 232: 183–190. 1557024
95. Zhang H, Zhao Q, Liu K, Zhang Z, Wang Y, et al. (2009) MgCRZ1, a transcription factor of Magnaporthe grisea, controls growth, development and is involved in full virulence. FEMS Microbiol Lett 293: 160–169. doi: 10.1111/j.1574-6968.2009.01524.x 19260966
96. Zhang H, Xue C, Kong L, Li G, Xu JR, (2011) A Pmk1-interacting gene is involved in appressorium differentiation and plant infection in Magnaporthe oryzae. Eukaryot Cell 10: 1062–1070. doi: 10.1128/EC.00007-11 21642506
97. Chen Y, Zuo R, Zhu Q, Sun Y, Li M, et al. (2014) MoLys2 is necessary for growth, conidiogenesis, lysine biosynthesis, and pathogenicity in Magnaporthe oryzae. Fungal Genet Biol 67: 51–57. doi: 10.1016/j.fgb.2014.04.001 24731804
98. Jacobs KA, Collins-Racie LA, Colbert M, Duckett M, Golden-Fleet M, et al. (1997) A genetic selection for isolating cDNAs encoding secreted proteins. Gene 198: 289–296. 9370294
99. Robert H, Schidst I, Andrew R, (1995) Studies on the transformation of intact yeast cells by the LiAc/SSDNA/PEG procedure. Yeast 11: 355–360. 7785336
100. Lu R, Malcuit I, Moffett P, Ruiz MT, Peart J, et al. (2003) High throughput virus-induced gene silencing implicates heat shock protein 90 in plant disease resistance. EMBO J 22: 5690–5699. 14592968
101. Wang QQ, Han CZ, Ferreira AO, Yu XL, Ye WW, et al. (2011) Transcriptional programming and functional interactions within the Phytophthora sojae RXLR effector repertoire. Plant Cell 23: 2064–2086. doi: 10.1105/tpc.111.086082 21653195
102. Hellens RP, Edwards EA, Leyland NR, Bean S, Mullineaux PM, (2000) pGreen: a versatile and flexible binary Ti vector for Agrobacterium-mediated plant transformation. Plant Mol Biol 42: 819–832. 10890530
103. Yu X, Tang J, Wang Q, Ye W, Tao K, et al. (2012) The RxLR effector Avh241 from Phytophthora sojae requires plasma membrane localization to induce plant cell death. New Phytol 196: 247–260. doi: 10.1111/j.1469-8137.2012.04241.x 22816601