Identification and analysis of genes expressed in the Ustilago maydis dikaryon: Uncovering a novel class of pathogenesis genes

Canadian Journal of Plant Pathology

Volumn 34, Issue 3, 2012, Pages 417-435

  Morrison, Erin N ^a   Donaldson, Michael E ^a   Saville, Barry J ^a  

^a TRENT UNIVERSITY   (Canada)

Author keywords

cDNA library; dikaryon; EST analysis; fungal pathogenesis; noncoding RNAs; Ustilago maydis

Indexed keywords

FUNGI; USTILAGO MAYDIS;

EID: 84864082835     PISSN: 07060661     EISSN: 17152992     Source Type: Journal    
DOI: 10.1080/07060661.2012.697077     Document Type: Article

References (68)

1. Adams, M.D., Kelley, J.M., Gocayne, J.D., Dubnick, M., Polmeropoulos, M.H., Xiao, H. 1991. Complementary DNA sequencing: expressed sequence tags and human genome project. Science, 252: 1651-1656. (Pubitemid 21917081)
2. Ali, S., and, Bakkeren, G. 2011. Fungal and oomycete effectors-strategies to subdue a host. Can. J. Plant Pathol., 33: 425-446.
3. Anderson, J. B., and, Kohn, L. M. 2007. Dikaryons, diploids, and evolution. In Sex in Fungi: Molecular Determination and Evolutionary Implications, Edited by: Heitman, J., Kronstad, J.W., Taylor, J. and Casselton, L. 333-348. Washington, DC: ASM Press.
4. Austin, R., Provart, N.J., Sacadura, N.T., Nugent, K.G., Babu, M., and, Saville, B.J. 2004. A comparative genomic analysis of ESTs from. Ustilago maydis. Funct. Integr. Genomics, 4: 207-218.
5. Avrova, A.O., Whisson, S.C., Pritchard, L., Venter, E., De Luca, S., Hein, I. 2007. A novel non-protein-coding infection-specific gene family is clustered throughout the genome of Phytophthora infestans. Microbiology. 153: 747-759.
6. Babu, M.R., Choffe, K., and, Saville, B.J. 2005. Differential gene expression in filamentous cells of. Ustilago maydis. Curr. Genet., 47: 316-333. (Pubitemid 40723972)
7. Bahn, Y., Kojima, K., Cox, G.M., and, Heitman, J. 2006. A unique fungal two-component system regulates stress responses, drug sensitivity, sexual development, and virulence of. Cryptococcus neoformans. Mol. Biol. Cell, 17: 3122-3135. (Pubitemid 43993514)
8. Banuett, F. 2010. Ustilago maydis and maize: a delightful interaction. In Cellular and Molecular Biology of Filamentous Fungi, Edited by: Borkovich, K.A. and Ebbole, D.J. 622-644. Washington, DC: ASM Press.
9. Banuett, F., and, Herskowitz, I. 1989. Different a alleles are necessary for maintenance of filamentous growth but not for meiosis. Proc. Natl. Acad. Sci. USA, 86: 5878-5882.
10. Banuett, F., and, Herskowitz, I. 1996. Discrete developmental stages during teliospore formation in the corn smut fungus. Ustilago maydis. Development, 122: 2965-2976. (Pubitemid 26371963)
11. Banuett, F., Quintanilla Jr, R.H., and, Reynaga-Peña, C.G. 2008. The machinery for cell polarity, cell morphogenesis, and the cytoskeleton in the Basidiomycete fungus Ustilago maydis-A survey of the genome sequence. Fungal Genet. Biol., 45: S3-S14.
12. Berretta, J., and, Morillon, A. 2009. Pervasive transcription constitutes a new level of eukaryotic genome regulation. EMBO Rep., 10: 973-982.
13. Brachmann, A., König, J., Julius, C., and, Feldbrügge, M. 2004. A reverse genetic approach for generating gene replacement mutants. Ustilago maydis. Mol. Genet. Gen., 272: 216-226. (Pubitemid 39371523)
14. Christensen, J.J. 1931. Studies on the genetics of. Ustilago zeae. Phytopathology, 4: 129-188.
15. Day, P.R., and, Anagnostakis, S.L. 1971. Corn smut dikaryon in culture. Nat. New Biol., 231: 19-20.
16. Doehlemann, G., van der Linde, K., Assmann, D., Schwammbach, D., Hof, A., Mohanty, A. 2009. Pep1, a secreted effector protein of Ustilago maydis, is required for successful invasion of plant cells. PLoS Path., 5: e1000290
17. Donaldson, M.E., and, Saville, B.J. 2008. Bioinformatic identification of Ustilago maydis meiosis genes. Fungal Genet. Biol., 45: S47-S53.
18. Doyle, C.E., Donaldson, M.E., Morrison, E.N., and, Saville, B.J. 2011. Ustilago maydis transcript features identified through full-length cDNA analysis. Mol. Genet. Gen., 286: 143-159.
19. Drinnenberg, I.A., Weinberg, D.E., Xie, K.T., Mower, J.P., Wolfe, K.H., Fink, G.R. 2009. RNAi in budding yeast. Science, 326: 544-550.
20. Eisenberg, E., and, Levanon, E.Y. 2003. Human housekeeping genes are compact. Trends Genet., 19: 362-365. (Pubitemid 36794535)
21. 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. (Pubitemid 28174098)
22. Guénin, S., Mauriat, M., Pelloux, J., Van Wuytswinkel, O., Bellini, C., and, Gutierrez, L. 2009. Normalization of qRT-PCR data: the necessity of adopting a systematic, experimental conditions-specific, validation of references. J. Exp. Bot., 60: 487-493.
23. Gullerova, M., and, Proudfoot, N.J. 2010. Transcriptional interference and gene orientation in yeast: noncoding RNA connections. Cold Spring Harbor Symposium, 75: 299-311.
24. Harrison, B.R., Yazgan, O., and, Krebs, J.E. 2009. Life without RNAi: noncoding RNAs and their functions in Saccharomyces cerevisiae. Biochem. Cell Biol., 87: 767-779.
25. Heimel, K., Scherer, M., Vranes, M., Wahl, R., Pothiratana, C., Schuler, D. 2010. The transcription factor Rbf1 is the master regulator for b-mating type controlled pathogenic development. Ustilago maydis. PLoS Pathog., 6: e1001035
26. Ho, E.C., Cahill, M.H., and, Saville, B.J. 2007. Gene discovery and transcript analyses in the corn smut pathogen Ustilago maydis: expressed sequence tag and genome sequence comparison. BMC Genomics, 8: 334
27. Hoffman, C.S., and, Winston, F. 1987. A ten-minute DNA preparation from yeast efficiently releases autonomous plasmids for transformation of. Escherichia coli. Gene, 57: 267-272. (Pubitemid 18007116)
28. Holliday, R. 1961. The genetics of Ustilago maydis. Genet. Res., 2: 204-230.
29. Holliday, R. 1974. Ustilago maydis. In Handbook of Genetics. First, Edited by: King, R.C. 575-595. New York: Plenum.
30. 4 photosynthesis. J. Plant Physiol., 165: 19-28. (Pubitemid 350266912)
31. Iida, Y., Ohara, T., and, Tsuge, T. 2006. Identification of genes up-regulated during conidiation of Fusarium oxysporum through expressed sequence tag analysis. Fungal Genet. Biol., 43: 179-189. (Pubitemid 43357968)
32. Kahmann, R., and, Kämper, J. 2004. Ustilago maydis: how its biology relates to pathogenic development. New Phytol., 164: 31-42. (Pubitemid 39260327)
33. Kämper, J. 2004. A PCR-based system for highly efficient generation of gene replacement mutants in Ustilago maydis. Mol. Genet. Gen., 271: 103-110. (Pubitemid 38299691)
34. Kämper, J., Kahmann, R., Bölker, M., Ma, L.J., Brefort, T., Saville, B.J. 2006. Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature, 444: 97-101. (Pubitemid 44684763)
35. Kessler, M.M., Willins, D.A., Zeng, Q., Del Mastro, R.G., Cook, R., Doucette-Stamm, L. 2002. The use of direct cDNA selection to rapidly and effectively identify genes in the fungus Aspergillus fumigatus. Fungal Genet. Biol., 36: 59-70.
36. Kojic, M., Kostrub, C.F., Buchman, A.R., and, Holloman, W.K. 2002. BRCA2 homolog required for proficiency in DNA repair, recombination, and genome stability in Ustilago maydis. Mol. Cell, 10: 683-691. (Pubitemid 35284183)
37. Lakshminarayan, M.I., Anantharaman, V., Wolf, M.Y., and, Aravind, L. 2008. Comparative genomics of transcription factors and chromatin proteins in parasitic protists and other eukaryotes. Int. J. Parasitol., 38: 1-31. (Pubitemid 350251386)
38. Laurie, J.D., Linning, R., and, Bakkeren, G. 2008. Hallmarks of RNA silencing are found in the smut fungus Ustilago hordei but not in its close relative Ustilago maydis. Curr. Genet., 53: 49-58. (Pubitemid 50006392)
39. Martínez-Espinoza, A.D., García-Pedrajas, M.D., and, Gold, S.E. 2002. The Ustilaginales as plant pests and model systems. Fungal Genet. Biol., 35: 1-20.
40. Mewes, H.W., Dietmann, S., Frishman, D., Gregory, R., Mannhaupt, G., Mayer, K.F. 2008. MIPS: analysis and annotation of genome information in 2007. Nucleic Acids Res., 36: D196-D201.
41. Morton, C.O., Varga, J.J., Hornbach, A., Mezger, M., Sennefelder, H., Kneitz, S. 2011. The temporal dynamics of differential gene expression in Aspergillus fumigatus interacting with human immature dendritic cells in vitro. PloS One, 6: e1606
42. 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 Genet. Biol., 45: S63-70.
43. Nugent, K.G., Choffe, K., and, Saville, B.J. 2004. Gene expression during Ustilago maydis diploid filamentous growth: EST library creation and analyses. Fungal Genet. Biol., 41: 349-360. (Pubitemid 38169454)
44. Ozsolak, F., and, Milos, P.M. 2011. RNA sequencing: advances, challenges and opportunities. Nat. Rev. Genet., 12: 87-98.
45. Qi, W., Kwon, C., and, Trail, F. 2006. Microarray analysis of transcript accumulation during perithecium development in the filamentous fungus Gibberella zeae (anamorph Fusarium graminearum). Mol. Genet. Gen., 276: 87-100. (Pubitemid 43946096)
46. Rozen, S., and, Skaletsky, H.J. 2000. Primer3 on the WWW for general users and for biologist programmers. In Bioinformatics Methods and Protocols: Methods in Molecular Biology, Edited by: Krawetz, S. and Misener, S. 365-386. Totowa, NJ: Humana Press.
47. Ruepp, A., Zollner, A., Maier, D., Albermann, K., Hani, J., Mokrejs, M. 2004. The FunCat, a functional annotation scheme for systematic classification of proteins from whole genomes. Nucleic Acids Res., 32: 5539-5545. (Pubitemid 39545671)
48. Sacadura, N.T., and, Saville, B.J. 2003. Gene expression and EST analyses of Ustilago maydis germinating teliospores. Fungal Genet. Biol., 40: 47-64. (Pubitemid 37013497)
49. Sambrook, J., and, Russell, D.W. 2001. Molecular Cloning: A Laboratory Manual, 3rd, Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
50. Schauwecker, F., Wanner, G., and, Kahmann, R. 1995. Filament-specific expression of a cellulose gene in the dimorphic fungus Ustilago maydis. Biol. Chem. H.-S., 376: 617-625.
51. Schirawski, J., Mannhaupt, G., Münch, K., Brefort, T., Schipper, K., Doehlemann, G. 2010. Pathogenicity determinants in smut fungi revealed by genome comparison. Science, 330: 1546-1548.
52. Seidl, M.F., Van den Ackerveken, G., Govers, F., and, Snel, B. 2011. A domain-centric analysis of Oomycete plant pathogen genomes reveals unique protein organization. Plant Physiol., 155: 628-644.
53. Smith, C.A., Robertson, D., Yates, B., Nielsen, D.M., Brown, D., Dean, R.A. 2008. The effect of temperature on Natural Antisense Transcript (NAT) expression. Aspergillus flavus. Curr. Genet., 54: 241-269.
54. Smith, T.L., and, Leong, S.A. 1990. Isolation and characterization of an Ustilago maydis glyceraldehyde-3-phosphate dehydrogenase-encoding gene. Gene, 93: 111-117. (Pubitemid 20353090)
55. 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.
56. Snetselaar, K.M., and, Mims, C.W. 1994. Light and electron microscopy of Ustilago maydis hyphae in maize. Mycol. Res., 98: 347-355. (Pubitemid 2070604)
57. Spellig, T., Regenfelder, E., and, Reichmann, M. 1994. Control of mating and development in Ustilago maydis. Antonie van Leeuwenhoek. 65: 191-197.
58. Stergiopoulos, I., and, de Wit, P.J.G.M. 2009. Fungal effector proteins. Annu. Rev. Phytopathol., 47: 233-263.
59. van den Berg, M.A., Albang, R., Albermann, K., Badger, J.H., Daran, J.M., Driessen, A.J.M. 2008. Genome sequencing and analysis of the filamentous fungus Penicillium chrysogenum. Nat. Biotechnol., 26: 1161-1168.
60. Verdun, R.E., Di Paulo, N., Urmenya, T.P., Rondinelli, E., Frasch, A.C., and, Sanchez, D.O. 1998. Gene discovery through expressed sequence tag sequencing in Trypanosoma cruzi. Infect. Immun., 66: 5393-5398. (Pubitemid 29044636)
61. Wilusz, J.E., Sunwoo, H., and, Spector, D.L. 2009. Long noncoding RNAs: functional surprises from the RNA world. Gene Dev., 23: 1494-1504.
62. Yamamoto, M. 2010. The selective elimination of messenger RNA underlies the mitosis-meiosis switch in fission yeast. Proc. Jpn. Acad. Ser. B Phys. Biol. Sci., 86: 788-797.
63. Yang, D., Tang, Z.H., Zhang, L.P., Zhao, C.P., and, Zheng, Y.L. 2009. Construction, characterization, and expressed sequence tag (EST) analysis of normalized cDNA library of thermo-photoperiod-sensitive genic male sterile (TPGMS) wheat from spike developmental stages. Plant Mol. Biol. Rep., 27: 117-125.
64. Yee, A.R. 1998. Specificity at the b mating type locus of Ustilago maydis, Vancouver, Canada: PhD Thesis. The University of British Columbia.
65. Yu, M., de Carvalho, L.P.S., Sun, G., and, Blanchard, J.S. 2006. Activity-based substrate profiling for Gcn5-related N-acetyltransferases: the use of chloroacetyl-Coenzyme A to identify protein substrates. J. Am. Chem. Soc., 128: 15356-15357. (Pubitemid 44875995)
66. Zahiri, A.R., Babu, M.R., and, Saville, B.J. 2005. Differential gene expression during teliospore germination. Ustilago maydis. Mol. Genet. Gen., 273: 394-403. (Pubitemid 40922404)
67. Zarnack, K. 2006. Die Auswirkung der posttranslationellen Aktivierung des Transkriptionsfaktors Prf1 auf die Pheromonantwort in Ustilago maydis, Marburg, Germany: PhD Thesis, Philipps-University.
68. Zarnack, K., Eichhorn, H., Kahmann, R., and, Feldbrügge, M. 2008. Pheromone-regulated target genes respond differentially to MAPK phosphorylation of transcription factor Prf1. Mol. Microbiol., 69: 1041-1053. (Pubitemid 352033321)