Ustilago maydis, a Delicacy of the Aztec Cuisine and a Model for Research

Claudia G. León-Ramírez, José Alejandro Sánchez-Arreguín, José Ruiz-Herrera

Departamento de Ingeniería Genética, Unidad Irapuato, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, Irapuato, Gto, México.

DOI: 10.4236/nr.2014.56024                

Abstract

Ustilago maydis is the causal agent of the disease known as corn smut or Huitlacohe; their natural hosts are maize (Zea mays L.) and its putative ancestor teocintle (Zea mays ssp. parviglumis and ssp. mexicana). In México there is an evidence of its use as human food since pre-hispanic times. Huitlacoche is a typical Mexican food with interesting nutritional properties and distinctive flavor. Its use in cuisine is considered as a culinary delicacy in Mexico and several parts of the world and the current consumption is increasing markedly, mainly due to its exclusive flavor different from any other known food. Huitlacoche contains proteins, carbohydrates, fats, minerals and vitamins that contribute to its nutritional value, also it has been reported that it contains proteins with balanced levels of essential amino acids, something which does not occur in corn having a deficiency mostly in lysine. The fungus also contains compounds with antioxidant properties, consequently it can be included in what are now known as nutraceutical foods. Besides its use in the food, this fungus has been used in different kinds of basic investigation, such as DNA recombination, signaling, cell biology, biotrophic plant-pathogen interactions and others. Its characteristics of dimorphism, and the detailed knowledge we have on its pathogenic development, that we describe in detail, make it an ideal subject for the analysis of fungal differentiation, and for the knowledge of the behavior of the highly aggressive plant pathogens that are members of its taxonomic group, the Ustilaginales. In the present communication we make a thorough review of the nutritional characteristics of U. maydis, its life cycle, and the molecular bases of its differentiation, morpohogenesis and pathogenicity.

Keywords

Ustilago maydis, Huitlacoche, Nutraceutical, Basidiocarps, Virulence

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1]	James, T.Y., Kauff, F., Schoch, C.L., et al. (2006) Reconstructing the Early Evolution of the Fungi Using a Six Gene Phylogeny. Nature, 443, 818-822. http://dx.doi.org/10.1038/nature05110
[2]	Ruiz-Herrera, J., Reynaga-Pena, C.G. and Arechiga-Carvajal, E.T. (2008) Ustilago maydis as a Model for Phytopathogenic Fungal Development. In: Khachatourians, G.G., Arora, D.K., Rajendran, T.P. and Srivastava, A.K., Eds., Agriculturally Important Microorganisms (Vol. 1), Academic World, Bhopal, 107-122.
[3]	Ruiz-Herrera, J. and León-Ramírez, C.G. (2012) Development and Dimorphism of the Pathogenic Basidiomycota Ustilago maydis. In: Ruiz-Herrera, J., Ed., Dimorphic Fungi: Their Importance as Models for Differentiation and Pathogenesis, Bentham E Books, 105-116.
[4]	Holliday, R. (1974) Ustilago maydis. In: King, R.C., Ed., Handbook of Genetics (Vol. 1), Plenum, New York, 575-595.
[5]	Rowell, J.B. (1955) Functional Rate of Compatibility Factors and an in Vitro Test for Sexual Compatibility with Haploid Lines of Ustilago zeae. Phytopathology, 45, 370-374.
[6]	Puhalla, J.E. (1970) Genetic Studies of the b Incompatibility Locus of Ustilago maydis. Genetics Research, 16, 229-232. http://dx.doi.org/10.1017/S0016672300002457
[7]	Trueheart, J. and Herskowitz, I. (1992) The a Locus Governs Cytoduction in Ustilago maydis. Journal of Bacteriology, 174, 7831-7833.
[8]	Kronstad, J.W. and Leong, S.A. (1990) The b Mating Type Locus of Ustilago maydis Contains Variable and Constant Regions. Genes & Development, 4, 1384-1395. http://dx.doi.org/10.1101/gad.4.8.1384
[9]	Wangemann-Budde, M. and Schauz, K. (1991) Intraspecific Hybridization of Ustilago maydis Haploids with Compatible and Incompatible Mating Type by Electrofusion and Genetic Analysis of Fusion Products. Experimental Mycology, 15, 159-166. http://dx.doi.org/10.1016/0147-5975(91)90016-7
[10]	Christensen, J.J. (1963) Corn smut Caused by Ustilago maydis. In: American Phytopathology Society Monograph No. 2, American Phytopath Soc., Saint Paul, 1-41.
[11]	Holliday, R. (1961) Induced Mitotic Crossing-Over in Ustilago maydis. Genetics Research, 2, 231-248. http://dx.doi.org/10.1017/S0016672300000720
[12]	Martínez-Espinoza, A.D., García-Pedrajas, M.D. and Gold, S.E. (2001) The Ustilaginales as Plant Pests and Model Systems. Fungal Genetics and Biology, 35, 1-20. http://dx.doi.org/10.1006/fgbi.2001.1301
[13]	Ruiz-Herrera, J., León-Ramírez, C. and Martínez-Espinoza, A.D. (2000) Morphogenesis and Pathogenesis in Ustilago maydis. Recent Research Developments in Microbiology, 4, 585-596.
[14]	Ruiz-Herrera, J., Ortiz-Castellanos, L., Martínez, A.I., et al. (2008) Analysis of the Proteins Involved in the Structure and Synthesis of the Cell Wall of Ustilago maydis. Fungal Genetics and Biology, 45, 571-576. http://dx.doi.org/10.1016/j.fgb.2008.04.010
[15]	Consejo Nacional de Ciencia y Tecnología. Sistema de Fondos FINNOVA. Fondo: C0009 Convocatoria: C0009-2012-02 Solicitud: 000000000191903 Modalidad: A5.
[16]	Guillén-Pérez, L.A., Sánchez-Quintanar, C., Mercado-Domenech, S. and Navarro Garza, H. (2002) Análisis de atribución causal en el uso de semilla criolla y semilla mejorada de maíz. Agrociencia, 36, 377-387.
[17]	Turiján-Altamirano, T., Damián-Huato, M.A., Ramírez-Valverde, B., et al. (2012) Manejo tradicional e innovación tecnológica en cultivo de maíz en San José Chiapa, Puebla. Revista Mexicana de Ciencias Agrícolas, 3, 1085-1110.
[18]	Turrent-Fernández, A., Wise, T.A. and Garvey, E. (2012) Factibilidad de alcanzar el potencial productivo de maíz de México. Mexican Rural Development Research Reports, 24, 1-36.
[19]	Echeverría, M.E. and Arroyo, L.E. (2000) Recetario del Maíz. Cocina Indígena y Popular. Consejo Nacional para las Culturas y las Artes (CONACULTA), México D.F., 441.
[20]	FAOSTAT (2009) Food Supply. Crops Primary Equivalent. Data Base. http://faos-tat3.fao.org/home/index.html
[21]	Serna-Saldívar, S.O. and Amaya-Guerra, C.A. (2008) El papel de la tortilla nixtamalizada en la nutrición y la alimentación. In: Rodríguez-García, M.E., Serna-Saldívar, S.O. and Sánchez-Sinencio, F., Eds., Nixtamalización: del Maíz a la Tortilla. Aspectos Nutrimentales y Toxicológicos, Universidad Autónoma de Querétaro, Querétaro, 105-151.
[22]	Garibay-Orijel, R. (2009) The Zapotec Names for Fungi. Revista Mexicana de Micología, 30.
[23]	Valadez-Azúa, R., Moreno Fuentes, A. and Gómez álvarez, G. (2011) Cujtlacochi. El Cuitlacoche. IIA-UNAM. México D.F., 138 p.
[24]	Beas, F.R., Loarca, G., Guzmán, S.H., Rodriguez, M.G., Vasco, N.L. and Guevara, F. (2011) Potencial nutracéutico de componentes bioactivos presentes en huitlacoche de la zona centro de México. Revista Mexicana de Ciencias Farmacéuticas, 42, 36-44.
[25]	Juárez-Montiel, M., Ruiloba de León, S., Chávez-Camarillo, G., Hernández-Rodríguez, C. and Villa-Tanaca, L. (2011) Huitlacoche (Corn Smut), Caused by the Phytopathogenic Fungus Ustilago maydis, as a Functional Food. Revista Iberoamericana de Micología, 28, 69-73. http://dx.doi.org/10.1016/j.riam.2011.01.001
[26]	FAO/WHO/UNU (1985) Energy and Protein Requirements. Report of a Joint FAO/WHO/UNU Expert Consultation. WHO Technical Report Series, No. 724.
[27]	Lizárraga-Guerra, R. and López, M.G. (1996) Content of Free Amino Acids in Huitlacoche (Ustilago maydis). Journal of Agricultural and Food Chemistry, 44, 2556-2559. http://dx.doi.org/10.1021/jf960017u
[28]	Valverde, M.E., Paredes-López, O., Pataky, J.K., Guevara-Laraa, F. and Pineda, T.S. (1995) Huitlacoche (Ustilago maydis) as a Food Source-Biology, Composition, and Production. Critical Reviews in Food Science and Nutrition, 35, 191-229. http://dx.doi.org/10.1080/10408399509527699
[29]	Lizárraga-Guerra, R., Guth, H. and López, M.G. (1997) Identification of the Most Potent Odorants in Huitlacoche (Ustilago maydis) and Austern Pilzen (Pleurotus sp.) by Aroma Extract Dilution Analysis and Static Head-Space Samples. Journal of Agricultural and Food Chemistry, 45, 1329-1332. http://dx.doi.org/10.1021/jf960650f
[30]	Lizárraga-Guerra, R. (1995) Extracción y caracterización de compuestos saborizantes en huitlacoche (Ustilago maydis) Tesis de maestría. Universidad Autónoma de Sinaloa, 30-34, 57-70.
[31]	Lobato-Salinas, V., Martínez-Flores, H., Lucas-Huacuz, S., et al. (2010) Alternativa tecnológica para el uso del hongo huitlacoche (Ustilago maydis) Subdirección de Innovación y Apropiación de Tecnologías para el Desarrollo del Centro de Investigación y Desarrollo del Estado de Michoacán. Calzada Juárez 1446, Col. Villa Universidad, C.P. 58060, Morelia, Michoacán.
[32]	Jacobs, C.W., Mattichak, S.J. and Knowles, J.F. (1994) Budding Patterns during Cell Cycle of the Maize Smut Pathogen Ustilago maydis. Canadian Journal of Botany, 72, 1675-1680. http://dx.doi.org/10.1139/b94-205
[33]	Snetselaar, K.M. (1993) Microscopic Observation of Ustilago maydis Mating Interactions. Experimental Mycology, 17, 345-355. http://dx.doi.org/10.1006/emyc.1993.1033
[34]	Garcia-Muse, T., Steinberg, G. and Perez-Martin, J. (2003) Pheromone-Induced G2 Arrest in the Phytopathogenic Fungus Ustilago maydis. Eukaryotic Cell, 2, 494-500. http://dx.doi.org/10.1128/EC.2.3.494-500.2003
[35]	Urban, M., Kahmann, R. and Bolker, M. (1996) Identification of the Pheromone Response Element in Ustilago maydis. Molecular and General Genetics, 251, 31-37.
[36]	Flor-Parra, I., Vranes, M., Kamper, J. and Pérez-Martín, J. (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. http://dx.doi.org/10.1105/tpc.106.042754
[37]	Day, P.R. and Anagnostakis, S.L. (1971) Corn Smut Dikaryon in Culture. Nature, 231, 19-20. http://dx.doi.org/10.1038/newbio231019a0
[38]	Banuett, F. and Herskowitz, I. (1989) Different Alleles of Ustilago maydis Are Necessary for Maintenance of Filamentous Growth but Not for Meiosis. Proceedings of the National Academy of Sciences of the United States of America, 86, 5878-5882. http://dx.doi.org/10.1073/pnas.86.15.5878
[39]	Banuett, F. and Herskowitz, I. (1994b) Morphological Transitions in the Life Cycle of Ustilago maydis and Their Genetic Control by the a and b Loci. Experimental Mycology, 18, 247-266. http://dx.doi.org/10.1006/emyc.1994.1024
[40]	Ruiz-Herrera, J., León-Ramírez, C., Cabrera-Ponce, J.L., Martínez-Espinoza, A.D. and Herrera-Estrella, L. (1999) Completion of the Sexual Cycle and Demonstration of Genetic Recombination of Ustilago maydis in Vitro. Molecular and General Genetics, 262, 468-472. http://dx.doi.org/10.1007/s004380051107
[41]	Alexopoulous, C.J. and Mims, C.W. (1979) Introductory Mycology. 3rd Edition, John Wiley and Sons, New York.
[42]	Cabrera-Ponce, J.L., León-Ramírez, C.G., Verver-Vargas, A., Palma-Tiradob, L. and Ruiz-Herrera, J. (2012) Metamorphosis of the Basidiomycota Ustilago maydis: Transformation of Yeast-Like Cells into Basidiocarps. Fungal Genetics and Biology, 49, 765-767. http://dx.doi.org/10.1016/j.fgb.2012.07.005
[43]	Thomas, P.L. (1991) Genetics of Small Grain Smuts. Annual Review of Phytopathology, 29, 137-148. http://dx.doi.org/10.1146/annurev.py.29.090191.001033
[44]	Martínez-Espinoza, A.D., Ruiz-Herrera, J., León-Ramírez, C. and Gold, S.E. (2004) MAP Kinase and cAMP Signaling Pathways Modulate the pH-Induced Yeast-to-Mycelium Dimorphic Transition in the Corn Smut Ustilago maydis. Current Microbiology, 49, 274-281. http://dx.doi.org/10.1007/s00284-004-4315-6
[45]	Bolker, M., Urban, M. and Kahmann, R. (1992) The a Mating Type Locus of U. maydis Specifies Cell Signaling Components. Cell, 68, 441-450. http://dx.doi.org/10.1016/0092-8674(92)90182-C
[46]	Fedler, M., Luh, K.S., Stelter, K., Nieto-Jacobo, F. and Basse, C.W. (2009) The a2 Mating-Type Locus Genes lga2 and rga2 Direct Uniparental mtDNA Inheritance and Constrain Mitochondrial DNA Recombination during Sexual Development of Ustilago maydis. Genetics, 181, 847-860. http://dx.doi.org/10.1534/genetics.108.096859
[47]	Garcia-Pedrajas, M.D., Nadal, M., Bolker, M., Gold, S.E. and Perlin, M.H. (2008) Sending Mixed Signals: Redundancy vs. Uniqueness of Signaling Components in the Plant Pathogen, Ustilago maydis. Fungal Genetics and Biology, 45, S22-S30. http://dx.doi.org/10.1016/j.fgb.2008.04.007
[48]	Klosterman, S.J., Perlin, M.H., Garcia-Pedrajas, M., Covert, S.F. and Gold, S.E. (2007) Genetics of Morphogenesis and Pathogenic Development of Ustilago maydis. Advances in Genetics, 57, 1-47. http://dx.doi.org/10.1016/S0065-2660(06)57001-4
[49]	Nadal, M., García-Pedrajas, M.D. and Gold, S.E. (2008) Dimorphism in Fungal Plant Pathogens. FEMS Microbiology Letters, 284, 127-134. http://dx.doi.org/10.1111/j.1574-6968.2008.01173.x
[50]	Regenfelder, E., Spellig, T., Hartmann, A., Lauenstein, S., Bolker, M. and Kahmann, R. (1997) G Proteins in Ustilago maydis: Transmission of Multiple Signals. EMBO Journal, 16, 1934-1942. http://dx.doi.org/10.1093/emboj/16.8.1934
[51]	Krüger, J., Loubradou, G., Regenfelder, E., Hartmann, A. and Kahmann, R. (1998) Crosstalk between cAMP and Pheromone Signalling Pathways in Ustilago maydis. Molecular and General Genetics, 260, 193-198. http://dx.doi.org/10.1007/s004380050885
[52]	Kaffarnik, F., Müller, P., Leibundgut, M., Kahmann, R. and Feldbrügge, M. (2003) PKA and MAPK Phosphorylation of Prf1 Allows Promoter Discrimination in Ustilago maydis. EMBO Journal, 22, 5817-5826. http://dx.doi.org/10.1093/emboj/cdg554
[53]	Müller, P., Weinzierl, G., Brachmann, A., Feldbrügge, M. and Kahmann, R. (2003) Mating and Pathogenic Development of the Smut Fungus Ustilago maydis Are Regulated by One Mitogen-Activated Protein Kinase. Eukaryotic Cell, 2, 1187-1199. http://dx.doi.org/10.1128/EC.2.6.1187-1199.2003
[54]	Brefort, T., Doehlemann, G., Mendoza-Mendoza, A., Reissman, S., Djamei, A. and Kahmann, R. (2009) Ustilago maydis as a Pathogen. Annual Review of Phytopathology, 47, 423-445. http://dx.doi.org/10.1146/annurev-phyto-080508-081923
[55]	Schulz, B., Banuett, F., Dahl, M., Schlesinger, R., Schafer, W., Martin, T., Herskowitz, I. and Kahmann, R. (1990) The b Alleles of U. maydis Whose Combinations Program Pathogenic Development, Code for Polypeptides Containing a Homeodomain-Related Motif. Cell, 60, 295-306. http://dx.doi.org/10.1016/0092-8674(90)90744-Y
[56]	Gillissen, B., Bergmann, J., Sandman, C., Schroeer, B., Bolker, M. and Kahmann, R. (1992) A Two Component Regulatory System for Self/Non-Self Recognition in U. maydis. Cell, 68, 647-657. http://dx.doi.org/10.1016/0092-8674(92)90141-X
[57]	Kamper, J., Reichmann, M., Romeis, T., Bolker, M. and Kahmann, R. (1995) Multiallelic Recognition: Nonself-Dependent Dimerization of the bE and bW Homeodomain Proteins in Ustilago maydis. Cell, 81, 73-83. http://dx.doi.org/10.1016/0092-8674(95)90372-0
[58]	Laity, C., Giasson, L., Campbell, R. and Kronstad, J. (1995) Heterozygosity at the b Mating-Type Locus Attenuates Fusion in Ustilago maydis. Current Genetics, 27, 451-459. http://dx.doi.org/10.1007/BF00311215
[59]	Gold, S., Duncan, G., Barret, K. and Kronstad, J. (1994) cAMP Regulates Morphogenesis in the Fungal Pathogen Ustilago maydis. Genes & Development, 8, 2805-2816. http://dx.doi.org/10.1101/gad.8.23.2805
[60]	Ruiz-Herrera, J., León, C.G., Guevara-Olvera, L. and Cárabez-Trejo, A. (1995) Yeast-Mycelial Dimorphism of Haploid and Diploid Strains of Ustilago maydis. Microbiology, 141, 695-703. http://dx.doi.org/10.1099/13500872-141-3-695
[61]	Klose, J., Moniz de Sá, M. and Kronstad, J.W. (2004) Lipid-Induced Filamentous Growth in Ustilago maydis. Molecular Microbiology, 52, 823-835. http://dx.doi.org/10.1111/j.1365-2958.2004.04019.x
[62]	Klose, J. and Kronstad, J.W. (2006) The Multifunctional Beta-Oxidation Enzyme Is Requiered for Full Symptom Development by the Biotrophic Maize Pathogen Ustilago maydis. Eukaryotic Cell, 5, 2047-2061. http://dx.doi.org/10.1128/EC.00231-06
[63]	Aréchiga-Carvajal, E.T. and Ruiz-Herrera, J. (2005) The RIM101/pacC Homologue from the Basidiomycete Ustilago maydis Is Functional in Multiple pH-Sensitive Phenomena. Eukaryotic Cell, 4, 999-1008. http://dx.doi.org/10.1128/EC.4.6.999-1008.2005
[64]	Guevara-Olvera, L., Xoconostle-Cazares, B. and Ruiz-Herrera, J. (1997) Cloning and Disruption of the Ornithine Decarboxilase Gene in Ustilago maydis: Evidence for the Role of Polyamines in Its Dimorphic Transition. Microbiology, 143, 2237-2245. http://dx.doi.org/10.1099/00221287-143-7-2237
[65]	Martínez-Soto, D. and Ruiz-Herrera, J. (2013) Transcriptomic Analysis of the Dimorphic Transition of Ustilago maydis Induced in Vitro by a Change in pH. Fungal Genetics and Biology, 58-59, 116-125. http://dx.doi.org/10.1016/j.fgb.2013.08.011
[66]	Robledo-Briones, M. and Ruiz-Herrera, J. (2013) Regulation of Genes Involved in Cell Wall Synthesis and Structure during Ustilago maydis Dimorphism. FEMS Yeast Research, 13, 74-84. http://dx.doi.org/10.1111/1567-1364.12011
[67]	Mendoza-Mendoza, A., Djamei, A., Weise, C., Linne, U., Marahiel, M., Vranes, M., Kamper, J. and Kahmann, R. (2009) Physical-Chemical Plant-Derived Signals Induce Differentiation in Ustilago maydis. Molecular Microbiology, 71, 895-911. http://dx.doi.org/10.1111/j.1365-2958.2008.06567.x
[68]	Brachmann, A., Weinzierl, G., Kamper, J. and Kahmann, R. (2001) Identification of Genes in the bW/bE Regulatory Cascade in Ustilago maydis. Molecular Microbiology, 42, 1047-1063. http://dx.doi.org/10.1046/j.1365-2958.2001.02699.x
[69]	Heimel, K., Scherer, M., Vranes, M., et al. (2010) The Transcription Factor Rbf1 Is the Master Regulator for b-Mating Type Controlled Pathogenic Development in Ustilago maydis. PLoS Pathogens, 6, Article ID: e1001035.
[70]	Snetselaar, K.M. and Mims, C.W. (1992) Sporidial Fusion and Infection of Maize Seedlings by the Smut Fungus Ustilago maydis. Mycologia, 84, 193-203. http://dx.doi.org/10.2307/3760250
[71]	White, D.G. (1999) Compendium of Corn Diseases. 3rd Edition, APS Press, St. Paul.
[72]	Brachmann, A., Schirawski, J., Müller, P. and Kahmann, R. (2003) An Unusual MAP Kinase Is Required for Efficient Penetration of the Plant Surface by Ustilago maydis. EMBO Journal, 22, 2199-2210. http://dx.doi.org/10.1093/emboj/cdg198
[73]	Mueller, O., Kahmann, R., Aguilar, G., Trejo-Aguilar, B., Wu, A. and de Vries, R.P. (2008) The Secretome of the Maize Pathogen Ustilago maydis. Fungal Genetics and Biology, 45, S63-S70. http://dx.doi.org/10.1016/j.fgb.2008.03.012
[74]	Gold, S.E. and Kronstad, J.W. (1994) Disruption of Two Genes for Chitin Synthase in the Phytopathogenic Fungus Ustilago maydis. Molecular Microbiology, 11, 897-902. http://dx.doi.org/10.1111/j.1365-2958.1994.tb00368.x
[75]	Xoconostle-Cázares, B., León-Ramírez, C. and Ruiz-Herrera, J. (1996) Two Chitin Synthase Genes from Ustilago maydis. Microbiology, 142, 377-387. http://dx.doi.org/10.1099/13500872-142-2-377
[76]	Xoconostle-Cázares, B., Specht, C.A., Robbins, P.W., Liu, Y.L., León, C. and Ruiz-Herrera, J. (1997) Umchs5, a Gene Coding for a Class IV Chitin Synthase in Ustilago maydis. Fungal Genetics and Biology, 22, 199-208. http://dx.doi.org/10.1006/fgbi.1997.1014
[77]	Garcerá-Teruel, A., Xoconostle-Cázares, B., Rosas-Quijano, R., et al. (2004) Loss of Virulence in Ustilago maydis by Umchs6 Gene Disruption. Research in Microbiology, 155, 87-97. http://dx.doi.org/10.1016/j.resmic.2003.11.005
[78]	Weber, I., Assman, D., Thines, E. and Steinberg, G. (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. http://dx.doi.org/10.1105/tpc.105.037341
[79]	Fernández-álvarez, A., Elías-Villalobos, A. and Ibeas, J.I. (2009) The O-Mannosyltransferase PMT4 Is Essential for Normal Appressorium Formation and Penetration in Ustilago maydis. Plant Cell, 21, 3397-3412. http://dx.doi.org/10.1105/tpc.109.065839
[80]	Ruiz-Herrera, J., Robledo-Briones, M. and Martínez-Soto, D. (2013) Experimental Pathosystems as a Tool for the Identification of Virulence Factors in Pathogenic Fungi. In: Deshpande, M. and Ruiz-Herrera, J., Eds., Biotechnology: Beyond Borders, CSIR-National Chemical Laboratory, Pune, 30-38.
[81]	Kamper, J., Kahmann, R., Bolker, M., et al. (2006) Insights from the Genome of the Biotrophic Fungal Plant Pathogen Ustilago maydis. Nature, 444, 97-101. http://dx.doi.org/10.1038/nature05248
[82]	Doehlemann, G., Van der Linde, K., Assmann, D., Schwammbach, D., Hof, A., Mohanty, A., Jackson, D. and Kahmann, R. (2009) Pep1, a Secreted Effector Protein of Ustilago maydis, Is Required for Successful Invasion of Plant Cells. PLoS Pathogens, 5, Article ID: e100029.
[83]	Hemetsberger, C., Herrberger, C., Zechmann, B., Hillmer, M. and Doehlemann, G. (2012) The Ustilago maydis Effector Pep1 Suppresses Plant Immunity by Inhibition of Host Peroxidase Activity. PLoS Pathogens, 8, Article ID: e1002684. http://dx.doi.org/10.1371/journal.ppat.1002684
[84]	Doehlemann, G., Reissmann, S., Assmann, D., Fleckenstein, M. and Kahmann, R. (2011) Two Linked Genes Encoding a Secreted Effector and a Membrane Protein Are Essential for Ustilago maydis—Induced Tumour Formation. Molecular Microbiology, 81, 751-766. http://dx.doi.org/10.1111/j.1365-2958.2011.07728.x
[85]	Banuett, F. and Herskowitz, I. (1996) Discrete Developmental Stages during Teliospore Formation in the Corn Smut Fungus, Ustilago maydis. Development, 122, 2965-2976.
[86]	León-Ramírez, C.G., Cabrera-Ponce, J.L., Martínez-Espinoza, A.D., Herrera-Estrella, L., Méndez, L., Reynaga-Pena, C.G. and Ruiz-Herrera, J. (2004) Infection of Alternative Host Plant Species by Ustilago maydis. New Phytologist, 164, 337-346. http://dx.doi.org/10.1111/j.1469-8137.2004.01171.x
[87]	Méndez-Morán, L., Reynaga-Pena, C.G., Springer, P.S. and Ruiz-Herrera, J. (2005) Ustilago maydis Infection of the Non-Natural Host Arabidopsis thaliana. Phytopathology, 95, 480-488.
[88]	Martínez-Soto, D., Robledo-Briones, A.M., Estrada-Luna, A. and Ruiz-Herrera, J. (2013) Transcriptomic Analysis of Ustilago maydis Infecting Arabidopsis Reveals Important Aspects of the Fungus Pathogenic Mechanisms. Plant Signaling & Behavior, 8, Article ID: e25059.