Plant Surface Cues Prime for Biotrophic Development
A basic requirement for pathogens to infect their hosts and to cause disease is to detect that they are in contact with the host surface. Plant pathogenic fungi typically respond to leaf surface contact with the development of specialized infection structures enabling the fungus to penetrate the leaf cuticle and to enter the plant tissue. In this study we analyzed the response of the corn smut fungus Ustilago maydis to two plant surface cues, such as hydrophobic surface and cutin monomers. Based on genome-wide gene expression analysis we found that these cues trigger the production of secreted plant cell wall degrading enzymes helping the fungus to penetrate the plant surface. In addition, genes were activated that code for a group of secreted proteins, so-called effectors, that affect virulence after penetration. These results demonstrate that plant surface cues trigger fungal penetration of the plant surface and also prime the fungus for later development inside plant tissue. These specific responses required two cell surface proteins that likely function as plant surface sensors.
Vyšlo v časopise:
Plant Surface Cues Prime for Biotrophic Development. PLoS Pathog 10(7): e32767. doi:10.1371/journal.ppat.1004272
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1004272
Souhrn
A basic requirement for pathogens to infect their hosts and to cause disease is to detect that they are in contact with the host surface. Plant pathogenic fungi typically respond to leaf surface contact with the development of specialized infection structures enabling the fungus to penetrate the leaf cuticle and to enter the plant tissue. In this study we analyzed the response of the corn smut fungus Ustilago maydis to two plant surface cues, such as hydrophobic surface and cutin monomers. Based on genome-wide gene expression analysis we found that these cues trigger the production of secreted plant cell wall degrading enzymes helping the fungus to penetrate the plant surface. In addition, genes were activated that code for a group of secreted proteins, so-called effectors, that affect virulence after penetration. These results demonstrate that plant surface cues trigger fungal penetration of the plant surface and also prime the fungus for later development inside plant tissue. These specific responses required two cell surface proteins that likely function as plant surface sensors.
Zdroje
1. KolattukudyPE, RogersLM, LiD, HwangCS, FlaishmanMA (1995) Surface signaling in pathogenesis. Proc Natl Acad Sci U S A 92: 4080–4087.
2. TuckerSL, TalbotNJ (2001) Surface attachment and pre-penetration stage development by plant pathogenic fungi. Annu Rev Phytopathol 39: 385–417.
3. KumamotoCA (2008) Molecular mechanisms of mechanosensing and their roles in fungal contact sensing. Nat Rev Microbiol 6: 667–673.
4. AbramovitchRB, YangG, KronstadJW (2002) The ukb1 gene encodes a putative protein kinase required for bud site selection and pathogenicity in Ustilago maydis. Fungal Genet Biol 37: 98–108.
5. IshidaN, AkaiS (1968) Electron microscopic observation of cell wall structure during appressorium formation in Colletotrichum lagenarium. Mycopathol Mycol Appl 35: 68–74.
6. SnetselaarKM, MimsCW (1993) Infection of maize stigmas by Ustilago maydis: Light and electron microscopy. Phytopathology 83: 843–850.
7. WesselsJGH (1994) Developmental Regulation of Fungal Cell Wall Formation. Annu Rev Phytopathol 32: 413–437.
8. XuH, MendgenK (1997) Targeted Cell Wall Degradation at the Penetration Site of Cowpea Rust Basidiosporelings. MPMI 10: 87–94.
9. BothM, CsukaiM, StumpfMP, SpanuPD (2005) Gene expression profiles of Blumeria graminis indicate dynamic changes to primary metabolism during development of an obligate biotrophic pathogen. Plant Cell 17: 2107–2122.
10. BothM, EckertSE, CsukaiM, MullerE, DimopoulosG, et al. (2005) Transcript profiles of Blumeria graminis development during infection reveal a cluster of genes that are potential virulence determinants. Mol Plant Microbe Interact 18: 125–133.
11. OhY, DonofrioN, PanH, CoughlanS, BrownDE, et al. (2008) Transcriptome analysis reveals new insight into appressorium formation and function in the rice blast fungus Magnaporthe oryzae. Genome Biol 9: R85.
12. SoanesDM, ChakrabartiA, PaszkiewiczKH, DaweAL, TalbotNJ (2012) Genome-wide transcriptional profiling of appressorium development by the rice blast fungus Magnaporthe oryzae. PLoS Pathog 8: e1002514.
13. O'ConnellRJ, ThonMR, HacquardS, AmyotteSG, KleemannJ, et al. (2012) Lifestyle transitions in plant pathogenic Colletotrichum fungi deciphered by genome and transcriptome analyses. Nat Genet 44: 1060–1065.
14. LerochM, KleberA, SilvaE, CoenenT, KoppenhoferD, et al. (2013) Transcriptome profiling of Botrytis cinerea conidial germination reveals upregulation of infection-related genes during the prepenetration stage. Eukaryot Cell 12: 614–626.
15. KwonYH, HochHC, StaplesRC (1991) Cytoskeletal organization in Uromyces urediospore germling apices during appressorium formation. Protoplasma 165: 37–50.
16. MendgenK, HahnM, DeisingH (1996) Morphogenesis and mechanisms of penetration by plant pathogenic fungi. Annu Rev Phytopathol 34: 367–386.
17. DagdasYF, YoshinoK, DagdasG, RyderLS, BielskaE, et al. (2012) Septin-mediated plant cell invasion by the rice blast fungus, Magnaporthe oryzae. Science 336: 1590–1595.
18. RyderLS, DagdasYF, MentlakTA, KershawMJ, ThorntonCR, et al. (2013) NADPH oxidases regulate septin-mediated cytoskeletal remodeling during plant infection by the rice blast fungus. Proc Natl Acad Sci U S A 110: 3179–3184.
19. BrefortT, DoehlemannG, Mendoza-MendozaA, ReissmannS, DjameiA, et al. (2009) Ustilago maydis as a Pathogen. Annu Rev Phytopathol 47: 423–445.
20. DjameiA, KahmannR (2012) Ustilago maydis: dissecting the molecular interface between pathogen and plant. PLoS Pathog 8: e1002955.
21. KamperJ, KahmannR, BolkerM, MaLJ, BrefortT, et al. (2006) Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 444: 97–101.
22. DoehlemannG, WahlR, HorstRJ, VollLM, UsadelB, et al. (2008) Reprogramming a maize plant: transcriptional and metabolic changes induced by the fungal biotroph Ustilago maydis. Plant J 56: 181–195.
23. SnetselaarKM, MimsCW (1992) Sporidial fusion and infection of maize seedlings by the smut fungus Ustilago maydis. Mycologia 84: 192–203.
24. BechingerC, GiebelKF, SchnellM, LeidererP, DeisingHB, et al. (1999) Optical measurements of invasive forces exerted by appressoria of a plant pathogenic fungus. Science 285: 1896–1899.
25. HowardRJ, FerrariMA, RoachDH, MoneyNP (1991) Penetration of hard substrates by a fungus employing enormous turgor pressures. Proc Natl Acad Sci U S A 88: 11281–11284.
26. SchirawskiJ, BohnertHU, SteinbergG, SnetselaarK, AdamikowaL, et al. (2005) Endoplasmic reticulum glucosidase II is required for pathogenicity of Ustilago maydis. Plant Cell 17: 3532–3543.
27. TonukariNJ, Scott-CraigJS, WaltonJD (2000) The Cochliobolus carbonum SNF1 gene is required for cell wall-degrading enzyme expression and virulence on maize. Plant Cell 12: 237–248.
28. NadalM, Garcia-PedrajasMD, GoldSE (2010) The snf1 gene of Ustilago maydis acts as a dual regulator of cell wall degrading enzymes. Phytopathology 100: 1364–1372.
29. ZhaoX, MehrabiR, XuJR (2007) Mitogen-activated protein kinase pathways and fungal pathogenesis. Eukaryot Cell 6: 1701–1714.
30. MullerP, WeinzierlG, BrachmannA, FeldbruggeM, KahmannR (2003) Mating and pathogenic development of the Smut fungus Ustilago maydis are regulated by one mitogen-activated protein kinase cascade. Eukaryot Cell 2: 1187–1199.
31. HeimelK, SchererM, VranesM, WahlR, PothiratanaC, et al. (2010) The transcription factor Rbf1 is the master regulator for b-mating type controlled pathogenic development in Ustilago maydis. PLoS Pathog 6: e1001035.
32. Flor-ParraI, VranesM, KamperJ, Perez-MartinJ (2006) Biz1, a zinc finger protein required for plant invasion by Ustilago maydis, regulates the levels of a mitotic cyclin. Plant Cell 18: 2369–2387.
33. Pothiratana C (2007) Functional characterization of the homeodomain transcription factor Hdp1 in Ustilago maydis. Dissertation of the Faculty of Biology, Philipps-University Marburg, Germany.
34. Mendoza-MendozaA, BerndtP, DjameiA, WeiseC, LinneU, et al. (2009) Physical-chemical plant-derived signals induce differentiation in Ustilago maydis. Mol Microbiol 71: 895–911.
35. BrachmannA, SchirawskiJ, MullerP, KahmannR (2003) An unusual MAP kinase is required for efficient penetration of the plant surface by Ustilago maydis. EMBO J 22: 2199–2210.
36. LanverD, Mendoza-MendozaA, BrachmannA, KahmannR (2010) Sho1 and Msb2-related proteins regulate appressorium development in the smut fungus Ustilago maydis. Plant Cell 22: 2085–2101.
37. Fernandez-AlvarezA, Marin-MenguianoM, LanverD, Jimenez-MartinA, Elias-VillalobosA, et al. (2012) Identification of O-mannosylated virulence factors in Ustilago maydis. PLoS Pathog 8: e1002563.
38. Perez-NadalesE, Di PietroA (2011) The membrane mucin Msb2 regulates invasive growth and plant infection in Fusarium oxysporum. Plant Cell 23: 1171–1185.
39. 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.
40. JonesJD, DanglJL (2006) The plant immune system. Nature 444: 323–329.
41. MullerO, SchreierPH, UhrigJF (2008) Identification and characterization of secreted and pathogenesis-related proteins in Ustilago maydis. Mol Genet Genomics 279: 27–39.
42. EisenMB, SpellmanPT, BrownPO, BotsteinD (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci U S A 95: 14863–14868.
43. DjameiA, SchipperK, RabeF, GhoshA, VinconV, et al. (2011) Metabolic priming by a secreted fungal effector. Nature 478: 395–398.
44. DoehlemannG, ReissmannS, AssmannD, FleckensteinM, KahmannR (2011) Two linked genes encoding a secreted effector and a membrane protein are essential for Ustilago maydis-induced tumour formation. Mol Microbiol 81: 751–766.
45. MuellerAN, ZiemannS, TreitschkeS, AssmannD, DoehlemannG (2013) Compatibility in the Ustilago maydis-maize interaction requires inhibition of host cysteine proteases by the fungal effector Pit2. PLoS Pathog 9: e1003177.
46. Schipper K (2009) Charakterisierung eines Ustilago maydis Genclusters, das für drei neuartige sekretierte Effektoren kodiert. Dissertation of the Faculty of Biology, Philipps-University Marburg, Germany.
47. SchirawskiJ, MannhauptG, MunchK, BrefortT, SchipperK, et al. (2010) Pathogenicity determinants in smut fungi revealed by genome comparison. Science 330: 1546–1548.
48. FarfsingJW, AuffarthK, BasseCW (2005) Identification of cis-active elements in Ustilago maydis mig2 promoters conferring high-level activity during pathogenic growth in maize. Mol Plant Microbe Interact 18: 75–87.
49. HemetsbergerC, HerrbergerC, ZechmannB, HillmerM, DoehlemannG (2012) The Ustilago maydis effector Pep1 suppresses plant immunity by inhibition of host peroxidase activity. PLoS Pathog 8: e1002684.
50. DoehlemannG, van der LindeK, AssmannD, SchwammbachD, HofA, et al. (2009) Pep1, a secreted effector protein of Ustilago maydis, is required for successful invasion of plant cells. PLoS Pathog 5: e1000290.
51. BoltonMD, ThommaBP (2008) The complexity of nitrogen metabolism and nitrogen-regulated gene expression in plant pathogenic fungi. PMPP 72: 104–110.
52. FriasM, GonzalezC, BritoN (2011) BcSpl1, a cerato-platanin family protein, contributes to Botrytis cinerea virulence and elicits the hypersensitive response in the host. New Phytol 192: 483–495.
53. CantarelBL, CoutinhoPM, RancurelC, BernardT, LombardV, et al. (2009) The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics. Nucleic Acids Res 37: D233–238.
54. DoehlemannG, WahlR, VranesM, de VriesRP, KamperJ, et al. (2008) Establishment of compatibility in the Ustilago maydis/maize pathosystem. J Plant Physiol 165: 29–40.
55. Stone BA, Clarke AE (1992) Chemistry and Biology of (1–3) β-Glucans. La Trobe University Press, Bundoora, Australia: 808 pp.
56. CarpitaNC, DefernezM, FindlayK, WellsB, ShoueDA, et al. (2001) Cell wall architecture of the elongating maize coleoptile. Plant Physiol 127: 551–565.
57. SchauweckerF, WannerG, KahmannR (1995) Filament-specific expression of a cellulase gene in the dimorphic fungus Ustilago maydis. Biol Chem Hoppe Seyler 376: 617–625.
58. GibsonDM, KingBC, HayesML, BergstromGC (2011) Plant pathogens as a source of diverse enzymes for lignocellulose digestion. Curr Opin Microbiol 14: 264–270.
59. SpanuPD, AbbottJC, AmselemJ, BurgisTA, SoanesDM, et al. (2010) Genome expansion and gene loss in powdery mildew fungi reveal tradeoffs in extreme parasitism. Science 330: 1543–1546.
60. Van VuB, ItohK, NguyenQB, TosaY, NakayashikiH (2012) Cellulases belonging to glycoside hydrolase families 6 and 7 contribute to the virulence of Magnaporthe oryzae. Mol Plant Microbe Interact 25: 1135–1141.
61. de VriesRP, KesterHC, PoulsenCH, BenenJA, VisserJ (2000) Synergy between enzymes from Aspergillus involved in the degradation of plant cell wall polysaccharides. Carbohydr Res 327: 401–410.
62. BeylotMH, McKieVA, VoragenAG, Doeswijk-VoragenCH, GilbertHJ (2001) The Pseudomonas cellulosa glycoside hydrolase family 51 arabinofuranosidase exhibits wide substrate specificity. Biochem J 358: 607–614.
63. YajimaW, LiangY, KavNN (2009) Gene disruption of an arabinofuranosidase/beta-xylosidase precursor decreases Sclerotinia sclerotiorum virulence on canola tissue. Mol Plant Microbe Interact 22: 783–789.
64. AlbertM (2013) Peptides as triggers of plant defence. J Exp Bot 64: 5269–5279.
65. WernerS, SuguiJA, SteinbergG, DeisingHB (2007) A chitin synthase with a myosin-like motor domain is essential for hyphal growth, appressorium differentiation, and pathogenicity of the maize anthracnose fungus Colletotrichum graminicola. Mol Plant Microbe Interact 20: 1555–1567.
66. OdenbachD, ThinesE, AnkeH, FosterAJ (2009) The Magnaporthe grisea class VII chitin synthase is required for normal appressorial development and function. Mol Plant Pathol 10: 81–94.
67. Garcera-TeruelA, Xoconostle-CazaresB, Rosas-QuijanoR, OrtizL, Leon-RamirezC, et al. (2004) Loss of virulence in Ustilago maydis by Umchs6 gene disruption. Res Microbiol 155: 87–97.
68. TreitschkeS, DoehlemannG, SchusterM, SteinbergG (2010) The myosin motor domain of fungal chitin synthase V is dispensable for vesicle motility but required for virulence of the maize pathogen Ustilago maydis. Plant Cell 22: 2476–2494.
69. WeberI, AssmannD, ThinesE, SteinbergG (2006) Polar localizing class V myosin chitin synthases are essential during early plant infection in the plant pathogenic fungus Ustilago maydis. Plant Cell 18: 225–242.
70. DeMariniDJ, AdamsAE, FaresH, De VirgilioC, ValleG, et al. (1997) A septin-based hierarchy of proteins required for localized deposition of chitin in the Saccharomyces cerevisiae cell wall. J Cell Biol 139: 75–93.
71. BenhamouN (1995) Immunocytochemistry of plant defense mechanisms induced upon microbial attack. Microsc Res Tech 31: 63–78.
72. KawanoY, ShimamotoK (2013) Early signaling network in rice PRR-mediated and R-mediated immunity. Curr Opin Plant Biol 16: 496–504.
73. TanakaK, NguyenCT, LiangY, CaoY, StaceyG (2012) Role of LysM receptors in chitin-triggered plant innate immunity. Plant Signal Behav 8: e22598.
74. RideJP, BarberMS (1990) Purification and Characterization of Multiple Forms of Endochitinase from Wheat Leaves. Plant Sci 71: 185–197.
75. El GueddariNE, RauchhausU, MoerschbacherBM, DeisingHB (2002) Developmentally regulated conversion of surface-exposed chitin to chitosan in cell walls of plant pathogenic fungi. New Phytologist 156: 103–112.
76. DeisingH, SiegristJ (1995) Chitin Deacetylase Activity of the Rust Uromyces-Viciae-Fabae Is Controlled by Fungal Morphogenesis. Fems Microbiology Letters 127: 207–211.
77. MaerzS, SeilerS (2010) Tales of RAM and MOR: NDR kinase signaling in fungal morphogenesis. Curr Opin Microbiol 13: 663–671.
78. DurrenbergerF, KronstadJ (1999) The ukc1 gene encodes a protein kinase involved in morphogenesis, pathogenicity and pigment formation in Ustilago maydis. Mol Gen Genet 261: 281–289.
79. SartorelE, Perez-MartinJ (2012) The distinct interaction between cell cycle regulation and the widely conserved morphogenesis-related (MOR) pathway in the fungus Ustilago maydis determines morphology. J Cell Sci 125: 4597–4608.
80. TeertstraWR, DeelstraHJ, VranesM, BohlmannR, KahmannR, et al. (2006) Repellents have functionally replaced hydrophobins in mediating attachment to a hydrophobic surface and in formation of hydrophobic aerial hyphae in Ustilago maydis. Microbiology 152: 3607–3612.
81. TeertstraWR, van der VeldenGJ, de JongJF, KruijtzerJA, LiskampRM, et al. (2009) The filament-specific Rep1-1 repellent of the phytopathogen Ustilago maydis forms functional surface-active amyloid-like fibrils. J Biol Chem 284: 9153–9159.
82. WostenHA, BohlmannR, EckerskornC, LottspeichF, BolkerM, et al. (1996) A novel class of small amphipathic peptides affect aerial hyphal growth and surface hydrophobicity in Ustilago maydis. EMBO J 15: 4274–4281.
83. RueppA, ZollnerA, MaierD, AlbermannK, HaniJ, et al. (2004) The FunCat, a functional annotation scheme for systematic classification of proteins from whole genomes. Nucleic Acids Res 32: 5539–5545.
84. ColemanST, FangTK, RovinskySA, TuranoFJ, Moye-RowleyWS (2001) Expression of a glutamate decarboxylase homologue is required for normal oxidative stress tolerance in Saccharomyces cerevisiae. J Biol Chem 276: 244–250.
85. MolinaL, KahmannR (2007) An Ustilago maydis gene involved in H2O2 detoxification is required for virulence. Plant Cell 19: 2293–2309.
86. HewaldS, LinneU, SchererM, MarahielMA, KamperJ, et al. (2006) Identification of a gene cluster for biosynthesis of mannosylerythritol lipids in the basidiomycetous fungus Ustilago maydis. Appl Environ Microbiol 72: 5469–5477.
87. TeichmannB, LinneU, HewaldS, MarahielMA, BolkerM (2007) A biosynthetic gene cluster for a secreted cellobiose lipid with antifungal activity from Ustilago maydis. Mol Microbiol 66: 525–533.
88. RonEZ, RosenbergE (2001) Natural roles of biosurfactants. Environ Microbiol 3: 229–236.
89. LubkowitzM (2011) The oligopeptide transporters: a small gene family with a diverse group of substrates and functions? Mol Plant 4: 407–415.
90. HahnM, NeefU, StruckC, GottfertM, MendgenK (1997) A putative amino acid transporter is specifically expressed in haustoria of the rust fungus Uromyces fabae. Mol Plant Microbe Interact 10: 438–445.
91. StruckC, MuellerE, MartinH, LohausG (2004) The Uromyces fabae UfAAT3 gene encodes a general amino acid permease that prefers uptake of in planta scarce amino acids. Mol Plant Pathol 5: 183–189.
92. DivonHH, Rothan-DenoyesB, DavydovO, ADIP, FluhrR (2005) Nitrogen-responsive genes are differentially regulated in planta during Fusarium oxyspsorum f. sp. lycopersici infection. Mol Plant Pathol 6: 459–470.
93. WahlR, WippelK, GoosS, KamperJ, SauerN (2010) A novel high-affinity sucrose transporter is required for virulence of the plant pathogen Ustilago maydis. PLoS Biol 8: e1000303.
94. BenitoB, GarciadeblasB, SchreierP, Rodriguez-NavarroA (2004) Novel p-type ATPases mediate high-affinity potassium or sodium uptake in fungi. Eukaryot Cell 3: 359–368.
95. ZhouXL, StumpfMA, HochHC, KungC (1991) A mechanosensitive channel in whole cells and in membrane patches of the fungus Uromyces. Science 253: 1415–1417.
96. ImazakiI, KurahashiM, IidaY, TsugeT (2007) Fow2, a Zn(II)2Cys6-type transcription regulator, controls plant infection of the vascular wilt fungus Fusarium oxysporum. Mol Microbiol 63: 737–753.
97. ZhaoC, WaalwijkC, de WitPJ, van der LeeT, TangD (2011) EBR1, a novel Zn(2)Cys(6) transcription factor, affects virulence and apical dominance of the hyphal tip in Fusarium graminearum. Mol Plant Microbe Interact 24: 1407–1418.
98. BanuettF, HerskowitzI (1989) Different a alleles of Ustilago maydis are necessary for maintenance of filamentous growth but not for meiosis. Proc Natl Acad Sci USA 86: 5878–5882.
99. KaffarnikF, MullerP, LeibundgutM, KahmannR, FeldbruggeM (2003) PKA and MAPK phosphorylation of Prf1 allows promoter discrimination in Ustilago maydis. EMBO J 22: 5817–5826.
100. UrbanM, KahmannR, BolkerM (1996) Identification of the pheromone response element in Ustilago maydis. Mol Gen Genet 251: 31–37.
101. HofA, ZechmannB, SchwammbachD, HuckelhovenR, DoehlemannG (2014) Alternative cell death mechanisms determine epidermal resistance in incompatible barley-ustilago interactions. Mol Plant Microbe Interact 27: 403–414.
102. Holliday R (1974) Ustilago maydis. In: King RC, editor. Handbook of Genetics. New York, USA: Plenum Press. pp. 575–595.
103. Rodriguez-NavarroA, RamosJ (1984) Dual system for potassium transport in Saccharomyces cerevisiae. J Bacteriol 159: 940–945.
104. BrachmannA, KonigJ, JuliusC, FeldbruggeM (2004) A reverse genetic approach for generating gene replacement mutants in Ustilago maydis. Mol Genet Genomics 272: 216–226.
105. KamperJ (2004) A PCR-based system for highly efficient generation of gene replacement mutants in Ustilago maydis. Mol Genet Genomics 271: 103–110.
106. BaumannS, PohlmannT, JungbluthM, BrachmannA, FeldbruggeM (2012) Kinesin-3 and dynein mediate microtubule-dependent co-transport of mRNPs and endosomes. J Cell Sci 125: 2740–2752.
107. AichingerC, HanssonK, EichhornH, LessingF, MannhauptG, et al. (2003) Identification of plant-regulated genes in Ustilago maydis by enhancer-trapping mutagenesis. Mol Genet Genomics 270: 303–314.
108. FreitagJ, LanverD, BohmerC, SchinkKO, BolkerM, et al. (2011) Septation of infectious hyphae is critical for appressoria formation and virulence in the smut fungus Ustilago maydis. PLoS Pathog 7: e1002044.
109. EichhornH, LessingF, WinterbergB, SchirawskiJ, KamperJ, et al. (2006) A ferroxidation/permeation iron uptake system is required for virulence in Ustilago maydis. Plant Cell 18: 3332–3345.
110. IrizarryRA, BolstadBM, CollinF, CopeLM, HobbsB, et al. (2003) Summaries of affymetrix GeneChip probe level data. Nucleic Acids Res 31: e15.
111. EisenhartC (1947) The assumptions underlying the analysis of variance. Biometrics 3: 1–21.
112. BenjaminiY, HochbergY (1995) Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society, Series B 57: 289–300.
113. LivakKJ, SchmittgenTD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) Method. Methods 25: 402–408.
Štítky
Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
PLOS Pathogens
2014 Číslo 7
- Parazitičtí červi v terapii Crohnovy choroby a dalších zánětlivých autoimunitních onemocnění
- Očkování proti virové hemoragické horečce Ebola experimentální vakcínou rVSVDG-ZEBOV-GP
- Koronavirus hýbe světem: Víte jak se chránit a jak postupovat v případě podezření?
Najčítanejšie v tomto čísle
- Molecular and Cellular Mechanisms of KSHV Oncogenesis of Kaposi's Sarcoma Associated with HIV/AIDS
- Holobiont–Holobiont Interactions: Redefining Host–Parasite Interactions
- Helminth Infections, Type-2 Immune Response, and Metabolic Syndrome
- BCKDH: The Missing Link in Apicomplexan Mitochondrial Metabolism Is Required for Full Virulence of and