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Systematic Analysis of ZnCys Transcription Factors Required for Development and Pathogenicity by High-Throughput Gene Knockout in the Rice Blast Fungus


Magnaporthe oryzae is not only the fungus causing the rice blast disease, which leads to 20–30% losses in rice production, but also a primary model pathosystem for understanding host-pathogen interactions. However, there is no high-throughput gene knockout system constructed, and little is known about most of the genes in this fungus. We developed a high-throughput gene knockout system, and using this system, we obtained null mutants of 104 fungal-specific Zn2Cys6 transcription factor (TF) genes by screening 8741 primary transformants in M. oryzae. We analyzed the functions of these TF genes in development, pathogenesis, and stress responses under 9 conditions. We found that 61 Zn2Cys6 TF genes play indispensable and diversified roles in fungal development and pathogenicity. CNF1 is the first reported TF gene that strongly and negatively regulates asexual development in the rice blast fungus, and CCA1, CNF1, CNF2, CONx1, GPF1, GTA1, MoCOD1 and PCF1 are required for pathogenicity. We further found via RNA-seq that GPF1 and CNF2 have similar mechanisms in gene expression regulation related to pathogenicity. The resulting data provide new insights into how Zn2Cys6 TF genes regulate important traits during the infection cycle of this rice blast pathogen.


Vyšlo v časopise: Systematic Analysis of ZnCys Transcription Factors Required for Development and Pathogenicity by High-Throughput Gene Knockout in the Rice Blast Fungus. PLoS Pathog 10(10): e32767. doi:10.1371/journal.ppat.1004432
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004432

Souhrn

Magnaporthe oryzae is not only the fungus causing the rice blast disease, which leads to 20–30% losses in rice production, but also a primary model pathosystem for understanding host-pathogen interactions. However, there is no high-throughput gene knockout system constructed, and little is known about most of the genes in this fungus. We developed a high-throughput gene knockout system, and using this system, we obtained null mutants of 104 fungal-specific Zn2Cys6 transcription factor (TF) genes by screening 8741 primary transformants in M. oryzae. We analyzed the functions of these TF genes in development, pathogenesis, and stress responses under 9 conditions. We found that 61 Zn2Cys6 TF genes play indispensable and diversified roles in fungal development and pathogenicity. CNF1 is the first reported TF gene that strongly and negatively regulates asexual development in the rice blast fungus, and CCA1, CNF1, CNF2, CONx1, GPF1, GTA1, MoCOD1 and PCF1 are required for pathogenicity. We further found via RNA-seq that GPF1 and CNF2 have similar mechanisms in gene expression regulation related to pathogenicity. The resulting data provide new insights into how Zn2Cys6 TF genes regulate important traits during the infection cycle of this rice blast pathogen.


Zdroje

1. DeanR, Van KanJA, PretoriusZA, Hammond-KosackKE, Di PietroA, et al. (2012) The Top 10 fungal pathogens in molecular plant pathology. Mol Plant Pathol 13: 414–430.

2. OuSH (1980) Pathogen variability and host resistance in rice blast disease. Annu Rev Phytopathol 18: 167–187.

3. DeanRA, TalbotNJ, EbboleDJ, FarmanML, MitchellTK, et al. (2005) The genome sequence of the rice blast fungus Magnaporthe grisea. Nature 434: 980–986.

4. ValentB, ChumleyFG (1991) Molecular genetic analysis of the rice blast fungus, Magnaporthe grisea. Annu Rev Phytopathol 29: 443–467.

5. TalbotNJ (2003) On the trail of a cereal killer: Exploring the biology of Magnaporthe grisea. Annu Rev Microbiol 57: 177–202.

6. JeonJ, ParkSY, ChiMH, ChoiJ, ParkJ, et al. (2007) Genome-wide functional analysis of pathogenicity genes in the rice blast fungus. Nat Genet 39: 561–565.

7. LuJP, FengXX, LiuXH, LuQ, WangHK, et al. (2007) Mnh6, a nonhistone protein, is required for fungal development and pathogenicity of Magnaporthe grisea. Fungal Genet Biol 44: 819–829.

8. NishimuraM, FukadaJ, MoriwakiA, FujikawaT, OhashiM, et al. (2009) Mstu1, an APSES transcription factor, is required for appressorium-mediated infection in Magnaporthe grisea. Biosci Biotechnol Biochem 73: 1779–1786.

9. ChoiJ, KimY, KimS, ParkJ, LeeYH (2009) MoCRZ1, a gene encoding a calcineurin-responsive transcription factor, regulates fungal growth and pathogenicity of Magnaporthe oryzae. Fungal Genet Biol 46: 243–254.

10. QiZ, WangQ, DouX, WangW, ZhaoQ, et al. (2012) MoSwi6, an APSES family transcription factor, interacts with MoMps1 and is required for hyphal and conidial morphogenesis, appressorial function and pathogenicity of Magnaporthe oryzae. Mol Plant Pathol 13: 677–689.

11. YangJ, ZhaoX, SunJ, KangZ, DingS, 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.

12. OdenbachD, BrethB, ThinesE, WeberRW, AnkeH, et al. (2007) The transcription factor Con7p is a central regulator of infection-related morphogenesis in the rice blast fungus Magnaporthe grisea. Mol Microbiol 64: 293–307.

13. ZhouZ, LiG, LinC, HeC (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.

14. KramerB, ThinesE, FosterAJ (2009) MAP kinase signalling pathway components and targets conserved between the distantly related plant pathogenic fungi Mycosphaerella graminicola and Magnaporthe grisea. Fungal Genet Biol 46: 667–681.

15. LiuW, XieS, ZhaoX, ChenX, ZhengW, et al. (2010) A homeobox gene is essential for conidiogenesis of the rice blast fungus Magnaporthe oryzae. Mol Plant Microbe Interact 23: 366–375.

16. KimS, ParkSY, KimKS, RhoHS, ChiMH, et al. (2009) Homeobox transcription factors are required for conidiation and appressorium development in the rice blast fungus Magnaporthe oryzae. PLoS Genet 5: e1000757.

17. BattagliaE, KlaubaufS, ValletJ, RibotC, LebrunMH, et al. (2013) Xlr1 is involved in the transcriptional control of the pentose catabolic pathway, but not hemi-cellulolytic enzymes in Magnaporthe oryzae. Fungal Genet Biol 57: 76–84.

18. LiY, LiangS, YanX, WangH, LiD, et al. (2010) Characterization of MoLDB1 required for vegetative growth, infection-related morphogenesis, and pathogenicity in the rice blast fungus Magnaporthe oryzae. Mol Plant Microbe Interact 23: 1260–1274.

19. YanX, LiY, YueX, WangC, QueY, et al. (2011) Two novel transcriptional regulators are essential for infection-related morphogenesis and pathogenicity of the rice blast fungus Magnaporthe oryzae. PLoS Pathog 7: e1002385.

20. MehrabiR, DingS, XuJR (2008) MADS-box transcription factor mig1 is required for infectious growth in Magnaporthe grisea. Eukaryot Cell 7: 791–799.

21. ParkG, XueC, ZhengL, LamS, XuJR (2002) MST12 regulates infectious growth but not appressorium formation in the rice blast fungus Magnaporthe grisea. Mol Plant Microbe Interact 15: 183–192.

22. LiG, ZhouX, KongL, WangY, ZhangH, et al. (2011) MoSfl1 is important for virulence and heat tolerance in Magnaporthe oryzae. PLoS One 6: e19951.

23. GuoM, ChenY, DuY, DongY, GuoW, 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 pathogens 7: e1001302.

24. GuoM, GuoW, ChenY, DongS, ZhangX, 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. Molecular plant-microbe interactions 23: 1053–1068.

25. LeeK, SinghP, ChungWC, AshJ, KimTS, et al. (2006) Light regulation of asexual development in the rice blast fungus, Magnaporthe oryzae. Fungal Genet Biol 43: 694–706.

26. NguyenQB, KadotaniN, KasaharaS, TosaY, MayamaS, et al. (2008) Systematic functional analysis of calcium-signalling proteins in the genome of the rice-blast fungus, Magnaporthe oryzae, using a high-throughput RNA-silencing system. Mol Microbiol 68: 1348–1365.

27. SonH, SeoYS, MinK, ParkAR, LeeJ, et al. (2011) A phenome-based functional analysis of transcription factors in the cereal head blight fungus, Fusarium graminearum. PLoS Pathog 7: e1002310.

28. YuJH, HamariZ, HanKH, SeoJA, Reyes-DominguezY, et al. (2004) Double-joint PCR: a PCR-based molecular tool for gene manipulations in filamentous fungi. Fungal Genet Biol 41: 973–981.

29. ColotHV, ParkG, TurnerGE, RingelbergC, CrewCM, et al. (2006) A high-throughput gene knockout procedure for Neurospora reveals functions for multiple transcription factors. Proc Natl Acad Sci U S A 103: 10352–10357.

30. TalbotNJ, FosterAJ (2001) Genetics and genomics of the rice blast fungus Magnaporthe grisea: developing an experimental model for understanding fungal diseases of cereals. Advances in Botanical Research 34: 263–287.

31. VillalbaF, CollemareJ, LandraudP, LambouK, BrozekV, et al. (2008) Improved gene targeting in Magnaporthe grisea by inactivation of MgKU80 required for non-homologous end joining. Fungal Genetics and Biology 45: 68–75.

32. TakahashiT, MasudaT, KoyamaY (2006) Enhanced gene targeting frequency in ku70 and ku80 disruption mutants of Aspergillus sojae and Aspergillus oryzae. Molecular Genetics and Genomics 275: 460–470.

33. NayakT, SzewczykE, OakleyCE, OsmaniA, et al. (2006) A Versatile and Efficient Gene-Targeting System for Aspergillus nidulans. Genetics 172: 1557–1566.

34. da Silva FerreiraME, KressMR, SavoldiM, GoldmanMH, HartlA, et al. (2006) The akuB(KU80) mutant deficient for nonhomologous end joining is a powerful tool for analyzing pathogenicity in Aspergillus fumigatus. Eukaryot Cell 5: 207–211.

35. LiHJ, LuJP, LiuXH, ZhangLL, LinFC (2012) Vectors building and usage for gene knockout, protein expression and fluorescent fusion protein in the rice blast fungus. Journal of Agricultural Biotechnology 20: 94–104.

36. ParkJ, JangS, KimS, KongS, ChoiJ, et al. (2008) FTFD: an informatics pipeline supporting phylogenomic analysis of fungal transcription factors. Bioinformatics 24: 1024–1025.

37. Marchler-BauerA, LuS, AndersonJB, ChitsazF, DerbyshireMK, et al. (2010) CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res 39: D225–229.

38. YuanGF, FuYH, MarzlufGA (1991) nit-4, a pathway-specific regulatory gene of Neurospora crassa, encodes a protein with a putative binuclear zinc DNA-binding domain. Mol Cell Biol 11: 5735–5745.

39. ChungH, ChoiJ, ParkS-Y, JeonJ, LeeYH (2013) Two conidiation-related Zn(II)2Cys6 transcription factor genes in the rice blast fungus. Fungal Genetics and Biology 61: 133–141.

40. TaniS, KatsuyamaY, HayashiT, SuzukiH, KatoM, et al. (2001) Characterization of the amyR gene encoding a transcriptional activator for the amylase genes in Aspergillus nidulans. Curr Genet 39: 10–15.

41. ParkSY, ChoiJ, LimSE, LeeGW, ParkJ, et al. (2013) Global expression profiling of transcription factor genes provides new insights into pathogenicity and stress responses in the rice blast fungus. PLoS Pathog 9: e1003350.

42. DonofrioNM, OhY, LundyR, PanH, BrownDE, et al. (2006) Global gene expression during nitrogen starvation in the rice blast fungus, Magnaporthe grisea. Fungal Genet Biol 43: 605–617.

43. TalbotNJ, McCaffertyHRK, MaM, MooreK, HamerJE (1997) Nitrogen starvation of the rice blast fungus Magnaporthe grisea may act as an environmental cue for disease symptom expression. Physiological and Molecular Plant Pathology 50: 179–195.

44. EbboleDJ, JinY, ThonM, PanH, BhattaraiE, et al. (2004) Gene discovery and gene expression in the rice blast fungus, Magnaporthe grisea: analysis of expressed sequence tags. Mol Plant Microbe Interact 17: 1337–1347.

45. WangY, WuJ, ParkZY, KimSG, RakwalR, et al. (2011) Comparative secretome investigation of Magnaporthe oryzae proteins responsive to nitrogen starvation. J Proteome Res 10: 3136–3148.

46. ChenGQ, LiuXH, ZhangLL, CaoHJ, LuJP, et al. (2013) Involvement of MoVMA11, a putative vacuolar atpase c′ subunit, in vacuolar acidification and infection-related morphogenesis of Magnaporthe oryzae. PLoS ONE 8: e67804.

47. SweigardJA, CarrollAM, FarrallL, ChumleyFG, ValentB (1998) Magnaporthe grisea pathogenicity genes obtained through insertional mutagenesis. Mol Plant Microbe Interact 11: 404–412.

48. LiuS, DeanRA (1997) G protein alpha subunit genes control growth, development, and pathogenicity of Magnaporthe grisea. Mol Plant Microbe Interact 10: 1075–1086.

49. ZhangH, TangW, LiuK, HuangQ, ZhangX, et al. (2011) Eight RGS and RGS-like proteins orchestrate growth, differentiation, and pathogenicity of Magnaporthe oryzae. PLoS Pathog 7: e1002450.

50. RamanujamR, YishiX, LiuH, NaqviNI (2012) Structure-function analysis of Rgs1 in Magnaporthe oryzae: role of DEP domains in subcellular targeting. PLoS One 7: e41084.

51. NishimuraM, ParkG, XuJR (2003) The G-beta subunit MGB1 is involved in regulating multiple steps of infection-related morphogenesis in Magnaporthe grisea. Mol Microbiol 50: 231–243.

52. ZhaoX, KimY, ParkG, XuJR (2005) A mitogen-activated protein kinase cascade regulating infection-related morphogenesis in Magnaporthe grisea. Plant Cell 17: 1317–1329.

53. JeonJ, GohJ, YooS, ChiMH, ChoiJ, et al. (2008) A putative MAP kinase kinase kinase, MCK1, is required for cell wall integrity and pathogenicity of the rice blast fungus, Magnaporthe oryzae. Mol Plant Microbe Interact 21: 525–534.

54. XuJR, StaigerCJ, HamerJE (1998) Inactivation of the mitogen-activated protein kinase Mps1 from the rice blast fungus prevents penetration of host cells but allows activation of plant defense responses. Proc Natl Acad Sci U S A 95: 12713–12718.

55. LiuXH, LuJP, ZhangL, DongB, MinH, et al. (2007) Involvement of a Magnaporthe grisea serine/threonine kinase gene, MgATG1, in appressorium turgor and pathogenesis. Eukaryotic Cell 6: 997–1005.

56. LuJP, LiuXH, FengXX, MinH, LinFC (2009) An autophagy gene, MgATG5, is required for cell differentiation and pathogenesis in Magnaporthe oryzae. Curr Genet 55: 461–473.

57. DongB, LiuXH, LuJP, ZhangFS, GaoHM, et al. (2009) MgAtg9 trafficking in Magnaporthe oryzae. Autophagy 5: 946–953.

58. DengYZ, QuZ, HeY, NaqviNI (2012) Sorting nexin Snx41 is essential for conidiation and mediates glutathione-based antioxidant defense during invasive growth in Magnaporthe oryzae. Autophagy 8: 1058.

59. HuangK, CzymmekKJ, CaplanJL, SweigardJA, DonofrioNM (2011) HYR1-mediated detoxification of reactive oxygen species is required for full virulence in the rice blast fungus. PLoS Pathog 7: e1001335.

60. FernandezJ, WilsonRA (2014) Characterizing roles for the glutathione reductase, thioredoxin reductase and thioredoxin peroxidase-encoding genes of Magnaporthe oryzae during rice blast disease. PLoS One 9: e87300.

61. DuY, ZhangH, HongL, WangJ, ZhengX, et al. (2013) Acetolactate synthases MoIlv2 and MoIlv6 are required for infection-related morphogenesis in Magnaporthe oryzae. Mol Plant Pathol 14: 870–884.

62. YiM, ParkJH, AhnJH, LeeYH (2008) MoSNF1 regulates sporulation and pathogenicity in the rice blast fungus Magnaporthe oryzae. Fungal Genet Biol 45: 1172–1181.

63. WangZY, ThorntonCR, KershawMJ, DebaoL, TalbotNJ (2003) The glyoxylate cycle is required for temporal regulation of virulence by the plant pathogenic fungus Magnaporthe grisea. Mol Microbiol 47: 1601–1612.

64. LiuXH, ZhuangFL, LuJP, LinFC (2011) Identification and molecular cloning Moplaa gene, a homologue of Homo sapiens PLAA, in Magnaporthe oryzae. Microbiological research 167: 8–13.

65. TongAH, EvangelistaM, ParsonsAB, XuH, BaderGD, et al. (2001) Systematic genetic analysis with ordered arrays of yeast deletion mutants. Science 294: 2364–2368.

66. KimDU, HaylesJ, KimD, WoodV, ParkHO, et al. (2010) Analysis of a genome-wide set of gene deletions in the fission yeast Schizosaccharomyces pombe. Nat Biotechnol 28: 617–623.

67. RhoHS, KangS, LeeYH (2001) Agrobacterium tumefaciens-mediated transformation of the plant pathogenic fungus, Magnaporthe grisea. Mol Cells 12: 407–411.

68. GinzingerDG (2002) Gene quantification using real-time quantitative PCR: an emerging technology hits the mainstream. Exp Hematol 30: 503–512.

69. InghamDJ, BeerS, MoneyS, HansenG (2001) Quantitative real-time PCR assay for determining transgene copy number in transformed plants. Biotechniques 31: 132–134, 136–140.

70. RogersSO, BendichAJ (1985) Extraction of DNA from milligram amounts of fresh, herbarium and mummified plant tissues. Plant Molecular Biology 5: 69–76.

71. KhangCH, ParkSY, LeeYH, KangS (2005) A dual selection based, targeted gene replacement tool for Magnaporthe grisea and Fusarium oxysporum. Fungal Genet Biol 42: 483–492.

72. BrethB, OdenbachD, YemelinA, SchlinckN, SchroderM, et al. (2013) The role of the Tra1p transcription factor of Magnaporthe oryzae in spore adhesion and pathogenic development. Fungal Genet Biol 57: 11–22.

73. TsujiG, KenmochiY, TakanoY, SweigardJ, FarrallL, et al. (2000) Novel fungal transcriptional activators, Cmr1p of Colletotrichum lagenarium and pig1p of Magnaporthe grisea, contain Cys2His2 zinc finger and Zn(II)2Cys6 binuclear cluster DNA-binding motifs and regulate transcription of melanin biosynthesis genes in a developmentally specific manner. Mol Microbiol 38: 940–954.

74. ZhengW, ZhaoZ, ChenJ, LiuW, KeH, et al. (2009) A Cdc42 ortholog is required for penetration and virulence of Magnaporthe grisea. Fungal Genet Biol 46: 450–460.

75. TalbotNJ, EbboleDJ, HamerJE (1993) Identification and characterization of MPG1, a gene involved in pathogenicity from the rice blast fungus Magnaporthe grisea. Plant Cell 5: 1575–1590.

76. YouFM, HuoN, GuYQ, LuoMC, MaY, et al. (2008) BatchPrimer3: a high throughput web application for PCR and sequencing primer design. BMC Bioinformatics 9: 253.

77. Sambrook J, Russell DW (2001) Molecular cloning, a labortary manual (3nd ed). Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, USA.

78. CarrollAM, SweigardJA, ValentB (1994) Improved vectors for selecting resistance to hygromycin. Fungal Genet Newsl 41.

79. MotoyamaT, OchiaiN, MoritaM, IidaY, UsamiR, et al. (2008) Involvement of putative response regulator genes of the rice blast fungus Magnaporthe oryzae in osmotic stress response, fungicide action, and pathogenicity. Curr Genet 54: 185–195.

80. ZhangLL, CaoHJ, LiXD, LinFC, FengXX, et al. (2013) MoTCTP, a homolog of translationally controlled tumor protein, is required for fungal growth and conidiation in Magnaporthe oryzae. Chinese J Cell Biol 35: 1141–1154.

81. Trapnell, PachterL, SalzbergSL (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25: 1105–1111.

82. TrapnellC, WilliamsBA, PerteaG, MortazaviA, KwanG, et al. (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28: 511–515.

83. ZhangH, ZhaoQ, GuoX, GuoM, QiZ, et al. (2014) Pleiotropic Function of the Putative Zinc-Finger Protein MoMsn2 in Magnaporthe oryzae. Mol Plant Microbe Interact 27: 446–460.

84. OhY, FranckWL, HanS-O, ShowsA, GokceE, et al. (2012) Polyubiquitin Is Required for Growth, Development and Pathogenicity in the Rice Blast Fungus Magnaporthe oryzae. PloS one 7: e42868.

85. DingSL, LiuW, IliukA, RibotC, ValletJ, et al. (2010) The tig1 histone deacetylase complex regulates infectious growth in the rice blast fungus Magnaporthe oryzae. Plant Cell 22: 2495–2508.

86. ChenJ, ZhengW, ZhengS, ZhangD, SangW, et al. (2008) Rac1 is required for pathogenicity and Chm1-dependent conidiogenesis in rice fungal pathogen Magnaporthe grisea. PLoS Pathog 4: e1000202.

87. SaitohH, FujisawaS, MitsuokaC, ItoA, HirabuchiA, 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.

88. KershawMJ, TalbotNJ (2009) Genome-wide functional analysis reveals that infection-associated fungal autophagy is necessary for rice blast disease. Proceedings of the National Academy of Sciences 106: 15967–15972.

89. SongW, DouX, QiZ, WangQ, ZhangX, et al. (2010) R-SNARE homolog MoSec22 is required for conidiogenesis, cell wall integrity, and pathogenesis of Magnaporthe oryzae. PLoS One 5: e13193.

90. ZhangH, ZhaoQ, LiuK, ZhangZ, WangY, 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.

91. DouX, WangQ, QiZ, SongW, WangW, 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.

92. RamanujamR, NaqviNI (2010) PdeH, a high-affinity cAMP phosphodiesterase, is a key regulator of asexual and pathogenic differentiation in Magnaporthe oryzae. PLoS pathogens 6: e1000897.

93. GaoHM, LiuXG, ShiHB, LuJP, YangJ, et al. (2013) MoMon1 is required for vacuolar assembly, conidiogenesis and pathogenicity in the rice blast fungus Magnaporthe oryzae. Res Microbiol 164: 300–309.

94. LiuW, ZhouX, LiG, LiL, KongL, et al. (2011) Multiple plant surface signals are sensed by different mechanisms in the rice blast fungus for appressorium formation. PLoS Pathog 7: e1001261.

95. PatkarRN, SureshA, NaqviNI (2010) MoTea4-mediated polarized growth is essential for proper asexual development and pathogenesis in Magnaporthe oryzae. Eukaryotic cell 9: 1029–1038.

96. ChenY, ZhaiS, ZhangH, ZuoR, WangJ, et al. (2013) Shared and distinct functions of two Gti1/Pac2 family proteins in growth, morphogenesis and pathogenicity of Magnaporthe oryzae. Environ Microbiol 16: 788–801.

97. LiuXH, LuJP, DongB, GuY, LinFC (2010) Disruption of MoCMK1, encoding a putative calcium/calmodulin-dependent kinase, in Magnaporthe oryzae. Microbiological research 165: 402–410.

98. ZhengW, ChenJ, LiuW, ZhengS, ZhouJ, et al. (2007) A Rho3 homolog is essential for appressorium development and pathogenicity of Magnaporthe grisea. Eukaryotic cell 6: 2240–2250.

99. PatkarRN, Ramos-PamplonaM, GuptaAP, FanY, NaqviNI (2012) Mitochondrial beta-oxidation regulates organellar integrity and is necessary for conidial germination and invasive growth in Magnaporthe oryzae. Mol Microbiol 86: 1345–1363.

100. UrbanM, BhargavaT, HamerJE (1999) An ATP-driven efflux pump is a novel pathogenicity factor in rice blast disease. EMBO J 18: 512–521.

101. LiuH, SureshA, WillardFS, SiderovskiDP, LuS, et al. (2007) Rgs1 regulates multiple Gα subunits in Magnaporthe pathogenesis, asexual growth and thigmotropism. The EMBO journal 26: 690–700.

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Hygiena a epidemiológia Infekčné lekárstvo Laboratórium

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