Transcriptomic analysis of Ustilago maydis infecting Arabidopsis reveals important aspects of the fungus pathogenic mechanisms

Plant Signaling and Behavior

Volumn 8, Issue 8, 2013, Pages

  Martínez Soto, Domingo ^a   Robledo Briones, Angélica M ^a   Estrada Luna, Andrés A ^a   Ruiz Herrera, José ^a  

^a DEPARTAMENTO DE FÍSICA   (Mexico)

Author keywords

Arabidopsis thaliana; Experimental pathosystem; Microarrays; Necrotrophic fungus; Plant virulence; Ustilago maydis

Indexed keywords

FUNGAL PROTEIN; POLYSACCHARIDE;

ARABIDOPSIS; ARABIDOPSIS THALIANA; ARTICLE; BIOSYNTHESIS; EXPERIMENTAL PATHOSYSTEM; FUNGAL GENE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GLYCOSYLATION; GROWTH, DEVELOPMENT AND AGING; HOST PATHOGEN INTERACTION; MICROARRAYS; MICROBIOLOGY; NECROTROPHIC FUNGUS; PATHOGENICITY; PLANT DISEASE; PLANT VIRULENCE; SECRETION (PROCESS); USTILAGO; USTILAGO MAYDIS; VIRULENCE;

ARABIDOPSIS THALIANA; EXPERIMENTAL PATHOSYSTEM; MICROARRAYS; NECROTROPHIC FUNGUS; PLANT VIRULENCE; USTILAGO MAYDIS;

ARABIDOPSIS; FUNGAL PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, FUNGAL; GENES, FUNGAL; GLYCOSYLATION; HOST-PATHOGEN INTERACTIONS; PLANT DISEASES; POLYSACCHARIDES; USTILAGO; VIRULENCE;

EID: 84881053814     PISSN: 15592316     EISSN: 15592324     Source Type: Journal    
DOI: 10.4161/psb.25059     Document Type: Article

References (86)

1. Perfect JR, Savani DV, Durack DT. Comparison of itraconazole and fluconazole in treatment of cryptococcal meningitis and candida pyelonephritis in rabbits. Antimicrob Agents Chemother 1986; 29:579-83; PMID:3010846; http://dx.doi.org/10.1128/AAC.29.4.579.
2. Saville SP, Lazzell AL, Monteagudo C, Lopez-Ribot JL. Engineered control of cell morphology in vivo reveals distinct roles for yeast and filamentous forms of Candida albicans during infection. Eukaryot Cell 2003; 2:1053-60; PMID:14555488; http://dx.doi.org/10.1128/EC.2.5.1053-1060.2003.
3. Kontoyiannis DP, Lewis RE. Studying fungal pathogenesis in Drosophila. Microbe 2010; 5:291-5.
4. Chen N, Hsiang T, Goodwin PH. Use of green fluorescent protein to quantify the growth of Colletotrichum during infection of tobacco. J Microbiol Methods 2003; 53:113-22; PMID:12609730; http://dx.doi.org/10.1016/S0167-7012(02)00234-8.
5. Parker D, Beckmann M, Enot DP, Overy DP, Rios ZC, Gilbert M, et al. Rice blast infection of Brachypodium distachyon as a model system to study dynamic host/ pathogen interactions. Nat Protoc 2008; 3:435-45; PMID:18323815; http://dx.doi.org/10.1038/nprot.2007.499.
6. Xue C, Tada Y, Dong X, Heitman J. The human fungal pathogen Cryptococcus can complete its sexual cycle during a pathogenic association with plants. Cell Host Microbe 2007; 1:263-73; PMID:18005707; http://dx.doi.org/10.1016/j.chom.2007.05.005.
7. León-Ramírez C, Cabrera-Ponce JL, Martínez-Espinoza A, Herrera-Estrella L, Méndez-Morán L, Reynaga-Peña G, et al. Infection of alternative host plant species by Ustilago maydis. New Phytol 2004; 164:337-46; http://dx.doi.org/10.1111/j.1469-8137.2004.01171.x
8. Méndez-Morán L, Reynaga-Peña CG, Springer PS, Ruiz-Herrera J. Ustilago maydis infection of the nonnatural host Arabidopsis thaliana. Phytopathology 2005; 95:480-8; PMID:18943312; http://dx.doi.org/10.1094/PHYTO-95-0480.
9. Davis KR, Hammershmidt R. Arabidopsis thaliana as a model for plant-pathogen interactions. In: The American Phytopathological Society, ed. St. Paul, USA, 1993:134.
10. Innes R. Arabidopsis as a model host in molecular plant pathology. In: Singh RP, Singh US, ed(s). Molecular methods in plant pathology. FL, USA: Boca Raton CRC Press, 1995:203-19.
11. Kämper J, Kahmann R, Bölker M, Ma LJ, Brefort T, Saville BJ, et al. Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 2006; 444:97-101; PMID:17080091; http://dx.doi.org/10.1038/nature05248.
12. Ruiz-Herrera J, León-Ramírez CG. Development and dimorphism of the phytopathogenic basidiomycota Ustilago maydis. In: Ruiz-Herrera J, ed. Dimorphic fungi. Their importance as models for differentiation and fungal pathogenesis. Ed. Bentham eBooks elSBN: 978-1-60805-364-3, 2012:105-116.
13. Cabrera-Ponce JL, León-Ramírez CG, Verver-Vargas A, Palma-Tirado L, Ruiz-Herrera J. Metamorphosis of the Basidiomycota Ustilago maydis: transformation of yeast-like cells into basidiocarps. Fungal Genet Biol 2012; 49:765-71; PMID:22921263; http://dx.doi.org/10.1016/j.fgb.2012.07.005.
14. Brefort T, Doehlemann G, Mendoza-Mendoza A, Reissmann S, Djamei A, Kahmann R. Ustilago maydis as a Pathogen. Annu Rev Phytopathol 2009; 47:423-445; PMID:19400641; http://dx.doi.org/10.1146/annurev-phyto-080508-081923.
15. Skibbe DS, Doehlemann G, Fernandes J, Walbot V. Maize tumors caused by Ustilago maydis require organ-specific genes in host and pathogen. Science 2010; 328:89-92; PMID:20360107; http://dx.doi.org/10.1126/science.1185775.
16. Heimel K, Scherer M, Vranes M, Wahl R, Pothiratana C, Schuler D, et al. The transcription factor Rbf1 is the master regulator for b-mating type controlled pathogenic development in Ustilago maydis. PLoS Pathog 2010; 6:e1001035; PMID:20700446; http://dx.doi.org/10.1371/journal.ppat.1001035.
17. Torto TA, Li S, Styer A, Huitema E, Testa A, Gow NA, et al. EST mining and functional expression assays identify extracellular effector proteins from the plant pathogen Phytophthora. Genome Res 2003; 13:1675-1685; PMID:12840044; http://dx.doi.org/10.1101/gr.910003.
18. Hemetsberger C, Herrberger C, Zechmann B, Hillmer M, Doehlemann G. The Ustilago maydis effector Pep1 suppresses plant immunity by inhibition of host peroxidase activity. PLoS Pathog 2012; 8:e1002684; PMID:22589719; http://dx.doi.org/10.1371/journal.ppat.1002684.
19. Zahiri A, Heimel K, Wahl R, Rath M, Kämper J. The Ustilago maydis forkhead transcription factor Fox1 is involved in the regulation of genes required for the attenuation of plant defenses during pathogenic development. Mol Plant Microbe Interact 2010; 23:1118-1129; PMID:20687802; http://dx.doi.org/10.1094/MPMI-23-9-1118.
20. Doehlemann G, van der Linde K, Assmann D, Schwammbach D, Hof A, Mohanty A, et al. Pep1, a secreted effector protein of Ustilago maydis, is required for successful invasion of plant cells. PLoS Pathog 2009; 5:e1000290; PMID:19197359; http://dx.doi.org/10.1371/journal.ppat.1000290.
21. Doehlemann G, Reissmann S, Assmann D, Fleckenstein M, Kahmann R. Two linked genes encoding a secreted effector and a membrane protein are essential for Ustilago maydis-induced tumour formation. Mol Microbiol 2011; 81:751-66; PMID:21692877; http://dx.doi.org/10.1111/j.1365-2958.2011.07728.x
22. Khrunyk Y, Münch K, Schipper K, Lupas AN, Kahmann R. The use of FLP-mediated recombination for the functional analysis of an effector gene family in the biotrophic smut fungus Ustilago maydis. New Phytol 2010; 187:957-68; PMID:20673282; http://dx.doi.org/10.1111/j.1469-8137.2010.03413.x
23. Teertstra WR, Deelstra HJ, Vranes M, Bohlmann R, Kahmann R, Kämper J, et al. Repellents have functionally replaced hydrophobins in mediating attachment to a hydrophobic surface and in formation of hydrophobic aerial hyphae in Ustilago maydis. Microbiology 2006; 152:3607-12; PMID:17159213; http://dx.doi.org/10.1099/mic.0.29034-0.
24. Müller O, Schreier PH, Uhrig JF. Identification and characterization of secreted and pathogenesis-related proteins in Ustilago maydis. Mol Genet Genomics 2008; 279:27-39; PMID:17917743; http://dx.doi.org/10.1007/s00438-007-0291-4.
25. Vollmeister E, Schipper K, Baumann S, Haag C, Pohlmann T, Stock J, et al. Fungal development of the plant pathogen Ustilago maydis. FEMS Microbiol Rev 2012; 36:59-77; PMID:21729109; http://dx.doi.org/10.1111/j.1574-6976.2011.00296.x
26. Govrin EM, Levine A. The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Curr Biol 2000; 10:751-7; PMID:10898976; http://dx.doi.org/10.1016/S0960-9822(00)00560-1.
27. Mayer AM, Staples RC, Gil-ad NL. Mechanisms of survival of necrotrophic fungal plant pathogens in hosts expressing the hypersensitive response. Phytochemistry 2001; 58:33-41; PMID:11524110; http://dx.doi.org/10.1016/S0031-9422(01)00187-X
28. Elías-Villalobos A, Fernández-Álvarez A, Ibeas JI. The general transcriptional repressor Tup1 is required for dimorphism and virulence in a fungal plant pathogen. PLoS Pathog 2011; 7:e1002235; PMID:21909277; http://dx.doi.org/10.1371/journal.ppat.1002235.
29. Horst RJ, Zeh C, Saur A, Sonnewald S, Sonnewald U, Voll LM. The Ustilago maydis Nit2 homolog regulates nitrogen utilization and is required for efficient induction of filamentous growth. Eukaryot Cell 2012; 11:368-80; PMID:22247264; http://dx.doi.org/10.1128/EC.05191-11.
30. Nicholls S, MacCallum DM, Kaffarnik FAR, Selway L, Peck SC, Brown AJP. Activation of the heat shock transcription factor Hsf1 is essential for the full virulence of the fungal pathogen Candida albicans. Fungal Genet Biol 2011; 48:297-305; PMID:20817114; http://dx.doi.org/10.1016/j.fgb.2010.08.010.
31. Du H, Guan G, Xie J, Sun Y, Tong Y, Zhang L, et al. Roles of Candida albicans Gat2, a GATA-type zinc finger transcription factor, in biofilm formation, filamentous growth and virulence. PLoS ONE 2012; 7:e29707; PMID:22276126; http://dx.doi.org/10.1371/journal.pone.0029707.
32. Singh P, Chauhan N, Ghosh A, Dixon F, Calderone RS. SKN7 of Candida albicans: mutant construction and phenotype analysis. Infect Immun 2004; 72:2390-2394; PMID:15039366; http://dx.doi.org/10.1128/IAI.72.4.2390-2394.2004.
33. Wormley FL Jr., Heinrich G, Miller JL, Perfect JR, Cox GM. Identification and characterization of an SKN7 homolog in Cryptococcus neoformans. Infect Immun 2005; 73:5022-30; PMID:16041017; http://dx.doi.org/10.1128/IAI.73.8.5022-5030.2005.
34. Brachmann A, Weinzierl G, Kämper J, Kahmann R. Identification of genes in the bW/bE regulatory cascade in Ustilago maydis. Mol Microbiol 2001; 42:1047-63; PMID:11737646; http://dx.doi.org/10.1046/j.1365-2958.2001.02699.x
35. Smith SE, Smith FA. Structure and function of the interfaces in biotrophic symbioses as they relate to nutrient transport. New Phytol 1990; 114:1-38; http://dx.doi.org/10.1111/j.1469-8137.1990.tb00370.x
36. Ruiz-Herrera J, León-Ramirez C, Guevara-Olvera L, Cárabez-Trejo A. Yeast-mycelial dimorphism of haploid and diploid strains of Ustilago maydis. Microbiology 1995; 141:695-703; http://dx.doi.org/10.1099/13500872-141-3-695.
37. El Gueddari NE, Rauchhaus U, Moerschbacher BM, Deising HB. Developmentally regulated conversion of surface-exposed chitin to chitosan in cell walls of plant pathogenic fungi. New Phytol 2002; 156:103-12; http://dx.doi.org/10.1046/j.1469-8137.2002.00487.x
38. Robledo-Briones M, Ruiz-Herrera J. Transcriptional regulation of the genes encoding chitin and β-1,3- glucan synthases from Ustilago maydis. Curr Microbiol 2012; 65:85-90; PMID:22538468; http://dx.doi.org/10.1007/s00284-012-0129-0.
39. Gilbert NM, Donlin MJ, Gerik KJ, Specht CA, Djordjevic JT, Wilson CF, et al. KRE genes are required for β-1,6-glucan synthesis, maintenance of capsule architecture and cell wall protein anchoring in Cryptococcus neoformans. Mol Microbiol 2010; 76:517-534; PMID:20384682; http://dx.doi.org/10.1111/j.1365-2958.2010.07119.x
40. Bates S, Hughes HB, Munro CA, Thomas WP, MacCallum DM, Bertram G, et al. Outer chain N-glycans are required for cell wall integrity and virulence of Candida albicans. J Biol Chem 2005; 281:90-98; PMID:16263704; http://dx.doi.org/10.1074/jbc.M510360200.
41. Nishikawa A, Poster JB, Jigami Y, Dean N. Molecular and phenotypic analysis of CaVRG4, encoding an essential Golgi apparatus GDP-mannose transporter. J Bacteriol 2002; 184:29-42; PMID:11741841; http://dx.doi.org/10.1128/JB.184.1.29-42.2002.
42. Rouabhia M, Schaller M, Corbucci C, Vecchiarelli A, Prill SK, Giasson L, et al. Virulence of the fungal pathogen Candida albicans requires the five isoforms of protein mannosyltransferases. Infect Immun 2005; 73:4571-80; PMID:16040968; http://dx.doi.org/10.1128/IAI.73.8.4571-4580.2005.
43. Olson GM, Fox DS, Wang P, Alspaugh JA, Buchanan KL. Role of protein O-mannosyltransferase Pmt4 in the morphogenesis and virulence of Cryptococcus neoformans. Eukaryot Cell 2007; 6:222-34; PMID:17142566; http://dx.doi.org/10.1128/EC.00182-06.
44. Fernández-Alvarez A, Elías-Villalobos A, Ibeas JI. The O-mannosyltransferase PMT4 is essential for normal appressorium formation and penetration in Ustilago maydis. Plant Cell 2009; 21:3397-412; PMID:19880800; http://dx.doi.org/10.1105/tpc.109.065839.
45. Kaur R, Ma B, Cormack BP. A family of glycosylphosphatidylinositol- linked aspartyl proteases is required for virulence of Candida glabrata. Proc Natl Acad Sci USA 2007; 104:7628-33; PMID:17456602; http://dx.doi.org/10.1073/pnas.0611195104.
46. Richard M, Ibata-Ombetta S, Dromer F, Bordon-Pallier F, Jouault T, Gaillardin C. Complete glycosylphosphatidylinositol anchors are required in Candida albicans for full morphogenesis, virulence and resistance to macrophages. Mol Microbiol 2002; 44:841-53; PMID:11994163; http://dx.doi.org/10.1046/j.1365- 2958.2002.02926.x
47. Lillico S, Field MC, Blundell P, Coombs GH, Mottram JC. Essential roles for GPI-anchored proteins in African trypanosomes revealed using mutants deficient in GPI8. Mol Biol Cell 2003; 14:1182-94; PMID:12631733; http://dx.doi.org/10.1091/mbc.E02-03-0167.
48. Chang T, Milne KG, Güther ML, Smith TK, Ferguson MA. Cloning of Trypanosoma brucei and Leishmania major genes encoding the GlcNAc-phosphatidylinositol de-N-acetylase of glycosylphosphatidylinositol biosynthesis that is essential to the African sleeping sickness parasite. J Biol Chem 2002; 277:50176-82; PMID:12364327; http://dx.doi.org/10.1074/jbc. M208374200.
49. Wösten HA, Bohlmann R, Eckerskorn C, Lottspeich F, Bölker M, Kahmann R. A novel class of small amphipathic peptides affect aerial hyphal growth and surface hydrophobicity in Ustilago maydis. EMBO J 1996; 15:4274-81; PMID:8861956.
50. Mendgen K, Hahn M. Plant infection and the establishment of fungal biotrophy. Trends Plant Sci 2002; 7:352-6; PMID:12167330; http://dx.doi.org/10.1016/S1360-1385(02)02297-5.
51. Banuett F, Herskowitz I. Different a alleles of Ustilago maydis are necessary for maintenance of filamentous growth but not for meiosis. Proc Natl Acad Sci USA 1989; 86:5878-82; PMID:16594058; http://dx.doi.org/10.1073/pnas.86.15.5878.
52. Ruiz-Herrera J, León-Ramírez C, Cabrera-Ponce JL, Martínez-Espinoza AD, Herrera-Estrella L. Completion of the sexual cycle and demonstration of genetic recombination in Ustilago maydis in vitro. Mol Gen Genet 1999; 262:468-72; PMID:10589834; http://dx.doi.org/10.1007/s004380051107.
53. Martin F, Delareulle C, Hilbert JL. An improved ergosterol assay to estimate fungal biomass in ectomycorrhizas. Mycol Res 1990; 94:1059-64; http://dx.doi.org/10.1016/S0953-7562(09)81333-6.
54. Specht CA, Liu Y, Robbins PW, Bulawa CE, Iartchouk N, Winter KR, et al. The chsD and chsE genes of Aspergillus nidulans and their roles in chitin synthesis. Fungal Genet Biol 1996; 20:153-67; PMID:8810520; http://dx.doi.org/10.1006/fgbi.1996.0030.
55. Reissig JL, Storminger JL, Leloir LF. A modified colorimetric method for the estimation of N-acetylamino sugars. J Biol Chem 1955; 217:959-66; PMID:13271455.
56. Bolstad BM, Irizarry RA, Astrand M, Speed TP. A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 2003; 19:185-93; PMID:12538238; http://dx.doi.org/10.1093/bioinformatics/19.2.185.
57. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, et al. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 2003; 4:249-64; PMID:12925520; http://dx.doi.org/10.1093/biostatistics/4.2.249.
58. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc, B 1995; 57:289-300.
59. Ruepp A, Zollner A, Maier D, Albermann K, Hani J, Mokrejs M, et al. The FunCat, a functional annotation scheme for systematic classification of proteins from whole genomes. Nucleic Acids Res 2004; 32:5539-5545; PMID:15486203; http://dx.doi.org/10.1093/nar/gkh894.
60. Mueller O, Kahmann R, Aguilar G, Trejo-Aguilar B, Wu A, de Vries RP. The secretome of the maize pathogen Ustilago maydis. Fungal Genet Biol 2008; 45:S63-S70; PMID:18456523; http://dx.doi.org/10.1016/j.fgb.2008.03.012.
61. Ruiz-Herrera J, Ortiz-Castellanos L, Martínez AI, León-Ramírez C, Sentandreu R. Analysis of the proteins involved in the structure and synthesis of the cell wall of Ustilago maydis. Fungal Genet Biol 2008; 45:S71-S76; PMID:18508396; http://dx.doi.org/10.1016/j.fgb.2008.04.010.
62. Robledo-Briones M, Ruiz-Herrera J. Regulation of genes involved in cell wall synthesis and structure during Ustilago maydis dimorphism. FEMS Yeast Res 2013; 13:74-84; PMID:23167842; http://dx.doi.org/10.1111/1567-1364.12011.
63. UniProt Consortium. Update on activities at the Universal Protein Resource (UniProt) in 2013. Nucleic Acids Res 2013; 41:D43-7; PMID:23161681; http://dx.doi.org/10.1093/nar/gks1068.
64. Ogata H, Goto S, Sato K, Fujibuchi W, Bono H, Kanehisa M. KEEG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res 1999; 27:29-34; PMID:9847135; http://dx.doi.org/10.1093/nar/27.1.29.
65. Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C, et al. The Pfam protein families database. Nucleic Acids Res 2012; 40:290-301; PMID:21896617; http://dx.doi.org/10.1093/nar/gkr1065.
66. Gough J, Karplus K, Hughey R, Chothia C. Assignment of homology to genome sequences using a library of hidden Markov models that represent all proteins of known structure. J Mol Biol 2001; 313:903-919; PMID:11697912; http://dx.doi.org/10.1006/jmbi.2001.5080.
67. Dürrenberger F, Laidlaw RD, Kronstad JW. The hgl1 gene is required for dimorphism and teliospore formation in the fungal pathogen Ustilago maydis. Mol Microbiol 2001; 41:337-48; PMID:11489122; http://dx.doi.org/10.1046/j.1365-2958.2001.02528.x
68. Mendoza-Mendoza A, Eskova A, Weise C, Czajkowski R, Kahmann R. Hap2 regulates the pheromone response transcription factor prf1 in Ustilago maydis. Mol Microbiol 2009; 72:683-98; PMID:19400774; http://dx.doi.org/10.1111/j.1365-2958.2009.06676.x
69. Molina L, Kahmann R. An Ustilago maydis gene involved in H2O2 detoxification is required for virulence. Plant Cell 2007; 19:2293-309; PMID:17616735; http://dx.doi.org/10.1105/tpc.107.052332.
70. Wahl R, Wippel K, Goos S, Kämper J, Sauer N. A novel high-affinity sucrose transporter is required for virulence of the plant pathogen Ustilago maydis. PLoS Biol 2010; 8:e1000303; PMID:20161717; http://dx.doi.org/10.1371/journal.pbio.1000303.
71. Mayorga ME, Gold SE. Characterization and molecular genetic complementation of mutants affecting dimorphism in the fungus ustilago maydis. Fungal Genet Biol 1998; 24:364-76; PMID:9756717; http://dx.doi.org/10.1006/fgbi.1998.1078.
72. Abramovitch RB, Yang G, Kronstad JW. The ukb1 gene encodes a putative protein kinase required for bud site selection and pathogenicity in Ustilago maydis. Fungal Genet Biol 2002; 37:98-108; PMID:12223194; http://dx.doi.org/10.1016/S1087-1845(02)00030-0.
73. Andrews DL, Egan JD, Mayorga ME, Gold SE. The Ustilago maydis ubc4 and ubc5 genes encode members of a MAP kinase cascade required for filamentous growth. Mol Plant Microbe Interact 2000; 13:781-786; PMID:10875339; http://dx.doi.org/10.1094/MPMI.2000.13.7.781.
74. Regenfelder E, Spellig T, Hartmann A, Lauenstein S, Bölker M, Kahmann R. G proteins in Ustilago maydis: transmission of multiple signals? EMBO J 1997; 16:1934-42; PMID:9155019; http://dx.doi.org/10.1093/emboj/16.8.1934.
75. Fernández-Álvarez A, Marín-Menguiano M, Lanver D, Jiménez-Martín A, Elías-Villalobos A, Pérez-Pulido AJ, et al. Identification of O-mannosylated virulence factors in Ustilago maydis. PLoS Pathog 2012; 8:e1002563; PMID:22416226; http://dx.doi.org/10.1371/journal.ppat.1002563.
76. Mayorga ME, Gold SE. The ubc2 gene of Ustilago maydis encodes a putative novel adaptor protein required for filamentous growth, pheromone response and virulence. Mol Microbiol 2001; 41:1365-79; PMID:11580841; http://dx.doi.org/10.1046/j.1365-2958.2001.02606.x
77. Valdés-Santiago L, Cervantes-Chávez JA, Ruiz-Herrera J. Ustilago maydis spermidine synthase is encoded by a chimeric gene, required for morphogenesis, and indispensable for survival in the host. FEMS Yeast Res 2009; 9:923-35; PMID:19624748; http://dx.doi.org/10.1111/j.1567-1364.2009.00539.x
78. Valdés-Santiago L, Guzmán-de-Peña D, Ruiz-Herrera J. Life without putrescine: disruption of the gene-encoding polyamine oxidase in Ustilago maydis odc mutants. FEMS Yeast Res 2010; 10:928-40; PMID:20840600; http://dx.doi.org/10.1111/j.1567-1364.2010.00675.x
79. Valdés-Santiago L, Cervantes-Chávez JA, Winkler R, León-Ramírez CG, Ruiz-Herrera J. Phenotypic comparison of samdc and spe mutants reveals complex relationships of polyamine metabolism in Ustilago maydis. Microbiology 2012; 158:674-84; PMID:22222500; http://dx.doi.org/10.1099/mic.0.055954-0.
80. Müller P, Katzenberger JD, Loubradou G, Kahmann R. Guanyl nucleotide exchange factor Sql2 and Ras2 regulate filamentous growth in Ustilago maydis. Eukaryot Cell 2003; 2:609-17; PMID:12796306; http://dx.doi.org/10.1128/EC.2.3.609-617.2003.
81. Garrido E, Voss U, Müller P, Castillo-Lluva S, Kahmann R, Pérez-Martín J. The induction of sexual development and virulence in the smut fungus Ustilago maydis depends on Crk1, a novel MAPK protein. Genes Dev 2004; 18:3117-30; PMID:15601825; http://dx.doi.org/10.1101/gad.314904.
82. Orth AB, Rzhetskaya M, Pell EJ, Tien M. A serine (threonine) protein kinase confers fungicide resistance in the phytopathogenic fungus Ustilago maydis. Appl Environ Microbiol 1995; 61:2341-5; PMID:7793954.
83. Zavrel M, Majer O, Kuchler K, Rupp S. Transcription factor Efg1 shows a haploinsufficiency phenotype in modulating the cell wall architecture and immunogenicity of Candida albicans. Eukaryot Cell 2012; 11:129-40; PMID:22140230; http://dx.doi.org/10.1128/EC.05206-11.
84. Shah JC, Clancy MJ. IME4, a gene that mediates MAT and nutritional control of meiosis in Saccharomyces cerevisiae. Mol Cell Biol 1992; 12:1078-1086; PMID:1545790.
85. Aréchiga-Carvajal ET, Ruiz-Herrera J. The RIM101/ pacC homolog from the basidiomycete Ustilago maydis is functional in multiple pH-sensitive phenomena. Eukaryot Cell 2005; 4:999-1008; PMID:15947192; http://dx.doi.org/10.1128/EC.4.6.999-1008.2005.
86. Brefort T, Müller P, Kahmann R. The high-mobilitygroup domain transcription factor Rop1 is a direct regulator of prf1 in Ustilago maydis. Eukaryot Cell 2005; 4:379-91; PMID:15701800; http://dx.doi.org/10.1128/EC.4.2.379-391.2005