Transcriptome analysis of a Ustilago maydis ust1 deletion mutant uncovers involvement of laccase and polyketide synthase genes in spore development

Molecular Plant-Microbe Interactions

Volumn 28, Issue 1, 2015, Pages 42-54

  Islamovic, Emir ^a,d   García Pedrajas, María D ^b   Chacko, Nadia ^a,e   Andrews, David L ^a   Covert, Sarah F ^c   Gold, Scott E ^a,f  

^a UNIVERSITY OF GEORGIA   (United States)

^b INSTITUTO DE HORTOFRUTICULTURA SUBTROPICAL Y MEDITERRÁNEA LA MAYORA   (Spain)

^c UNIVERSITY OF GEORGIA   (United States)

^d BASF CORPORATION   (United States)

^e TEXAS A AND M UNIVERSITY   (United States)

^f RUSSELL RESEARCH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGI; USTILAGO MAYDIS; ZEA MAYS;

FUNGAL PROTEIN; LACCASE; POLYKETIDE SYNTHASE; TRANSCRIPTOME;

BIOLOGICAL MODEL; CELL WALL; DNA MICROARRAY; ENZYMOLOGY; FUNGUS SPORE; GENE DELETION; GENE EXPRESSION PROFILING; GENETICS; GROWTH, DEVELOPMENT AND AGING; MAIZE; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PIGMENTATION; PLANT DISEASE; SEEDLING; USTILAGO; VIRULENCE;

CELL WALL; FUNGAL PROTEINS; GENE EXPRESSION PROFILING; LACCASE; MODELS, BIOLOGICAL; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PIGMENTATION; PLANT DISEASES; POLYKETIDE SYNTHASES; SEEDLING; SEQUENCE DELETION; SPORES, FUNGAL; TRANSCRIPTOME; USTILAGO; VIRULENCE; ZEA MAYS;

EID: 84920383220     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-05-14-0133-R     Document Type: Article

References (49)

1. Baeza-Montañez, L., Gold, S. E., Espeso, E.,and Garcia-Pedrajas, M. D. 2015. Conserved and distinct functions of the "stunted" (StuA)-homolog Ust1 during cell differentiation in the corn smut fungus Ustilago maydis. Mol. Plant-Microbe Interact. 28:85-101
2. Baker, S. E., Kroken, S., Inderbitzin, P., Asvarak, T., Li, B.Y., Shi, L., Yoder, O. C., and Turgeon, B. G. 2006. Two polyketide synthase-encoding genes are required for biosynthesis of the polyketide virulence factor, T-toxin, by Cochliobolus heterostrophus. Mol. Plant-Microbe Interact. 19:139-149.
3. Banuett F, and Herskowitz, I. 1996. Discrete developmental stages during teliospore formation in the corn smut fungus, Ustilago maydis. Development 122:2965-2976.
4. Barrett, K. J., Gold, S. E., and Kronstad, J. W. 1993. Identification and complementation of a mutation to constitutive filamentous growth in Ustilago maydis. Mol. Plant-Microbe Interact. 6:274-283.
5. Bieszke, J. A., Li, L., and Borkovich, K. A. 2007. The fungal opsin gene nop-1 is negatively-regulated by a component of the blue light sensing pathway and influences conidiation-specific gene expression in Neurospora crassa. Curr. Genet. 52:149-157.
6. Bölker, M., Genin, S., Lehmler, C., and Kahmann, R. 1995. Genetic regulation of mating and dimorphism in Ustilago maydis. Can. J. Bot. 73:320-325.
7. Bölker, M., Basse, C. W., and Schirawski, J. 2008. Ustilago maydis secondary metabolism-From genomics to biochemistry. Fungal Genet. Biol. 45:S88-S93.
8. Chacko, N., and Gold, S. E. 2012. Deletion of the Ustilago maydis ortholog of the Aspergillus sporulation regulator medA affects mating and virulence through pheromone response. Fungal Genet. Biol. 49:426-432.
9. Christensen, J. J. 1963. Corn smut caused by Ustilago maydis. Am. Phytopathol. Soc. Monogr. 2:41.
10. 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 Pathog. 5:e1000290.
11. Durrenberger, F., Laidlaw, R. D., and Kronstad, J. W. 2001. The hgl1 gene is required for dimorphism and teliospore formation in the fungal pathogen Ustilago maydis. Mol. Microbiol. 41:337-348.
12. Dutta, S., Gerhold, D. L., Rice, M., Germann, M., and Kmiec, E. B. 1997. The cloning and overexpression of a cruciform binding protein from Ustilago maydis. Biochim. Biophys. Acta Gene Struct. Expr. 1352:258-266.
13. Eisenman, H. C., and Casadevall, A. 2012. Synthesis and assembly of fungal melanin. Appl. Microb. Biot. 93:931-940.
14. Eisenman, H. C., Mues, M., Weber, S. E., Frases, S., Chaskes, S., Gerfen, G., and Casadevall, A. 2007. Cryptococcus neoformans laccase catalyses melanin synthesis from both D-and L-DOPA. Microbiology 153:3954-3962.
15. Eisenman, H. C., Frases, S., Nicola, A. M., Rodrigues, M. L., and Casadevall, A. 2009. Vesicle-associated melanization in Cryptococcus neoformans. Microbiology 155:3860-3867.
16. García-Pedrajas, M. D., Nadal, M., Kapa, L. B., Perlin, M. H., Andrews, D. L., and Gold, S. E. 2008. DelsGate, a robust and rapid gene deletion construction method. Fungal Genet. Biol. 45:379-388.
17. García-Pedrajas, M. D., Baeza-Montanez, L., and Gold, S. E. 2010. Regulation of Ustilago maydis dimorphism, sporulation, and pathogenic development by a transcription factor with a highly conserved APSES domain. Mol. Plant-Microbe Interact. 23:211-222.
18. Gold, S. E., Brogdon, S. M., Mayorga, M. E., and Kronstad, J. W. 1997. The Ustilago maydis regulatory subunit of a cAMP-dependent protein kinase is required for gall formation in maize. Plant Cell 9:1585-1594.
19. Holliday, R. 1974. Ustilago maydis. Pages 575-595 in: Handbook of Genetics. R. C. King, ed. Plenum, New York.
20. Huber, S. M., Lottspeich, F., and Kamper, J. 2002. A gene that encodes a product with similarity to dioxygenases is highly expressed in teliospores of Ustilago maydis. Mol. Genet. Genomics 267:757-771.
21. Kamper, J., Kahmann, R., Bölker, M., Ma, L.-J., Brefort, T., Saville, B. J., Banuett, F., Kronstad, J. W., Gold, S. E., Muller, O., Perlin, M. H., Wosten, H. A. B., de Vries, R., Ruiz-Herrera, J., Reynaga-Pena, C. G., Snetselaar, K., McCann, M., Perez-Martin, J., Feldbrugge, M., Basse, C. W., Steinberg, G., Ibeas, J. I., Holloman, W., Guzman, P., Farman, M., Stajich, J. E., Sentandreu, R., Gonzalez-Prieto, J. M., Kennell, J. C., Molina, L., Schirawski, J., Mendoza-Mendoza, A., Greilinger, D., Munch, K., Rossel, N., Scherer, M., Vranes, M., Ladendorf, O., Vincon, V., Fuchs, U., Sandrock, B., Meng, S., Ho, E. C. H., Cahill, M. J., Boyce, K. J., Klose, J., Klosterman, S. J., Deelstra, H. J., Ortiz-Castellanos, L., Li, W., Sanchez-Alonso, P., Schreier. P. H., Hauser-Hahn, I., Vaupel, M., Koopmann, E., Friedrich, G., Voss, H., Schluter, T., Margolis, J., Platt, D., Swimmer, C., Gnirke, A., Chen, F., Vysotskaia, V., Mannhaupt, G., Guldener, U., Munsterkotter, M., Haase, D., Oesterheld, M., Mewes, H.-W., Mauceli, E. W., DeCaprio, D., Wade, C. M., Butler, J., Young, S., Jaffe, D. B., Calvo, S., Nusbaum, C., Galagan, J., and Birren, B. W. 2006. Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 444:97-101.
22. Keon, J. P., White, G. A., and Hargreaves, J. A. 1991. Isolation, characterization and sequence of a gene conferring resistance to the systemic fungicide carboxin from the maize smut pathogen, Ustilago maydis. Curr. Genet. 19:475-481.
23. Khaldi, N., Collemare, J., Lebrun, M. H., and Wolfe, K. H. 2008. Evidence for horizontal transfer of a secondary metabolite gene cluster between fungi. Genome Biol. 9:R18.
24. Kruger, J., Loubradou, G., Wanner, G., Regenfelder, E., Feldbrugge, M., and Kahmann, R. 2000. Activation of the cAMP pathway in Ustilago maydis reduces fungal proliferation and teliospore formation in plant tumors. Mol. Plant-Microbe Interact. 13:1034-1040.
25. Kumar, S., and Punekar, N. S. 1997. The metabolism of 4-aminobutyrate (GABA) in fungi. Mycol. Res. 101:403-409.
26. Kusch, G., and Schauz, K. 1989. Light and electron microscopic studies of chlamydospore development in Ustilago maydis. Cryptogamic Bot. 1:230-235.
27. Langfelder, K., Philippe, B., Jahn, B., Latge, J. P., and Brakhage, A. A. 2001. Differential expression of the Aspergillus fumigatus pksP gene detected in vitro and in vivo with green fluorescent protein. Infect. Immun. 69:6411-6418.
28. Langfelder, K., Streibel, M., Jahn, B., Haase, G., and Brakhage, A. A. 2003. Biosynthesis of fungal melanins and their importance for human pathogenic fungi. Fungal Genet. Biol. 38:143-158.
29. Lin, S. Y., Okuda, S., Ikeda, K., Okuno, T., and Takano, Y. 2012. LAC2 encoding a secreted laccase is involved in appressorial melanization and conidial pigmentation in Colletotrichum orbiculare. Mol. Plant-Microbe Interact. 25:1552-1561.
30. Litvintseva, A. P., and Henson, J. M. 2002. Cloning, characterization, and transcription of three laccase genes from Gaeumannomyces graminis var. tritici, the Take-All fungus. Appl. Environ. Microbiol. 68:1305-1311.
31. Marita, J. M., Vermerris, W., Ralph, J., and Hatfield, R. D. 2003. Variations in the cell wall composition of maize brown midrib mutants. J. Agric. Food Chem. 51:1313-1321.
32. Martínez-Salgado, J. L., León-Ramírez, C. G., Pacheco, A. B., Ruiz-Herrera, J., and de la Rosa, A. P. B. 2013. Analysis of the regulation of the Ustilago maydis proteome by dimorphism, pH or MAPK and GCN5 genes. J. Proteom. 79:251-262.
33. Moriwaki, A., Kihara, J., Kobayashi, T., Tokunaga, T., Arase, S., and Honda, Y. 2004. Insertional mutagenesis and characterization of a polyketide synthase gene PKS1 required for melanin biosynthesis in Bipolaris oryzae. FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Lett. 238:1-8.
34. Oh, Y., Donofrio, N., Pan, H., Coughlan, S., Brown, D. E., Meng, S., Mitchell, T., and Dean, R. A. 2008. Transcriptome analysis reveals new insight into appressorium formation and function in the rice blast fungus Magnaporthe oryzae. Genome Biol. 9:R85.
35. Pfaffl, M. W. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29:e45.
36. Piattelli, M., Fattorusso, E., Magno, S., and Nicolaus, R. A. 1963. Ustilago melanin, a naturally occurring catechol melanin. Tetrahedron Lett. 4:997-998.
37. Quadbeck-Seeger, C., Wanner, G., Huber, S., Kahmann, R., and Kamper, J. 2000. A protein with similarity to the human retinoblastoma binding protein 2 acts specifically as a repressor for genes regulated by the b mating type locus in Ustilago maydis. Mol. Microbiol. 38:154-166.
38. Reichmann, M., Jamnischek, A., Weinzierl, G., Ladendorf, O., Huber, S., Kahmann, R., and Kamper, J. 2002. The histone deacetylase Hda1 from Ustilago maydis is essential for spore development. Mol. Microbiol. 46:1169-1182.
39. Ruepp, A., Zollner, A., Maier, D., Albermann, K., Hani, J., Mokrejs, M., Tetko, I., Guldner, U., Mannhaupt, G., Munsterkotter, M., and Mewes, H. W. 2004. The FunCat, a functional annotation scheme for systematic classification of proteins from whole genomes. Nucleic Acid Res. 32:5539-5545.
40. Scherer, M., Heimel, K., Starke, V., and Kamper, J. 2006. The Clpl protein is required for clamp formation and pathogenic development of Ustilago maydis. Plant Cell 18:2388-2401.
41. Skibbe, D. S., Doehlemann, G., Fernandes, J., and Walbot, V. 2010. Maize tumors caused by Ustilago maydis require organ-specific genes in host and pathogen. Science 328:89-92.
42. Smith, D. G., Garcia-Pedrajas, M. D., Hong, W., Yu, Z., Gold, S. E., and Perlin, M. H. 2004. An ste20 homologue in Ustilago maydis plays a role in mating and pathogenicity. Eukaryot. Cell 3:180-189.
43. Snetselaar, K. M., and Mims, C. W. 1994. Light and electron-microscopy of Ustilago maydis hyphae in maize. Mycol. Res. 98:347-355.
44. Sugareva, V., Härtl, A., Brock, M., Hübner, K., Rohde, M., Heinekamp, T., and Brakhage, A. A. 2006. Characterisation of the laccase-encoding gene abr2 of the dihydroxynaphthalene-like melanin gene cluster of Aspergillus fumigatus. Arch. Microbiol. 186:345-355.
45. Tsai, H. F., Wheeler, M. H., Chang, Y. C., and Kwon-Chung, K. J. 1999. A developmentally regulated gene cluster involved in conidial pigment biosythesisy in Aspergillus fumigatus. J. Bacteriol. 181:6469-6477.
46. Tsai, H. F., Fujii, I., Watanabe, A., Wheeler, M. H., Chang, Y. C., Yasuoka, Y., Ebizuka, Y., and Kwong-Chung, K. J. 2001. Pentaketide melanin biosynthesis in Aspergillus fumigatus requires chain-length shortening of a heptaketide precursor. J. Biol. Chem. 276:29292-29298.
47. Tsukuda, T., Carleton, S., Fotheringham, S., and Holloman, W. 1988. Isolation and characterization of an autonomously replicating sequence from Ustilago maydis. Mol. Cell. Biol. 8:3703-3709.
48. Woo, P. C., Tam, E. W., Chong, K. T., Cai, J. J., Tung, E. T., Ngan, A. H., Lau, S. K., and Yuen, K. Y. 2010. High diversity of polyketide synthase genes and the melanin biosynthesis gene cluster in Penicillium marneffei. FEBS (Fed. Eur. Biochem. Soc.) J. 277:3750-3758.
49. Zhu, X., and Williamson, P. R. 2004. Role of laccase in the biology and virulence of Cryptococcus neoformans. FEMS (Fed. Eur. Microbiol. Soc.) Yeast Res. 5:1-10.