Transcriptomic analysis of the role of Rim101/PacC in the adaptation of Ustilago maydis to an alkaline environment

Microbiology (United Kingdom)

Volumn 160, Issue PART 9, 2014, Pages 1985-1998

  Franco Frías, Eduardo ^a   Ruiz Herrera, Jose ^b   Aréchiga Carvajal, Elva Teresa ^a  

^a UNIVERSIDAD AUTÓNOMA DE NUEVO LEÓN   (Mexico)

^b DEPARTAMENTO DE INGENIERÍA GENÉTICA   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL POLYSACCHARIDE; FUNGAL PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR RIM101; UNCLASSIFIED DRUG; ALKALI;

ACTIN FILAMENT; ALKALINITY; ARTICLE; CELL BUDDING; CELL POLARITY; FUNGAL CELL WALL; GENE EXPRESSION; GENETIC REGULATION; MEIOSIS; NONHUMAN; PRIORITY JOURNAL; TRANSCRIPTOMICS; USTILAGO MAYDIS; ADAPTATION; DNA SEQUENCE; DRUG EFFECTS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; MICROARRAY ANALYSIS; MOLECULAR GENETICS; PH; PHYSIOLOGICAL STRESS; USTILAGO;

ADAPTATION, PHYSIOLOGICAL; ALKALIES; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, FUNGAL; HYDROGEN-ION CONCENTRATION; MICROARRAY ANALYSIS; MOLECULAR SEQUENCE DATA; SEQUENCE ANALYSIS, DNA; STRESS, PHYSIOLOGICAL; USTILAGO;

EID: 84906877014     PISSN: 13500872     EISSN: 14652080     Source Type: Journal    
DOI: 10.1099/mic.0.076216-0     Document Type: Article

References (54)

1. Abdulrehman, D., Monteiro, P. T., Teixeira, M. C., Mira, N. P., Lourenço, A. B., dos Santos, S. C., Cabrito, T. R., Francisco, A. P., Madeira, S. C. & other authors (2011). YEASTRACT: providing a programmatic access to curated transcriptional regulatory associations in Saccharomyces cerevisiae through a web services interface. Nucleic Acids Res 39 (Database issue), D136-D140.
2. Aréchiga-Carvajal, E. T. & Ruiz-Herrera, J. (2005). The RIM101/PacC homologue from the basidiomycete Ustilago maydis is functional in multiple pH-sensitive phenomena. Eukaryot Cell 4, 999-1008.
3. Arst, H. N., Jr, Bignell, E. & Tilburn, J. (1994). Two new genes involved in signalling ambient pH in Aspergillus nidulans. Mol Gen Genet 245, 787-790.
4. Banuett, F. & Herskowitz, I. (1989). Different a alleles of Ustilago maydis are necessary for maintenance of filamentous growth but not for meiosis. Proc Natl Acad Sci U S A 86, 5878-5882.
5. Barth, G. & Gaillardin, C. (1996). Yarrowia lipolytica. In Nonconventional Yeasts in Biotechnology: a Handbook, pp. 313-388. Edited by K. Wolf. Berlin: Springer-Verlag.
6. Benito, B., Garciadeblás, B., Pérez-Martín, J. & Rodríguez-Navarro, A. (2009). Growth at high pH and sodium and potassium tolerance in media above the cytoplasmic pH depend on ENA ATPases in Ustilago maydis. Eukaryot Cell 8, 821-829.
7. Burge, S., Kelly, E., Lonsdale, D., Mutowo-Muellenet, P., McAnulla, C., Mitchell, A., Sangrador-Vegas, A., Yong, S. Y., Mulder, N. & Hunter, S. (2012). Manual GO annotation of predictive protein signatures: the InterPro approach to GO curation. Database (Oxford) 2012, bar068.
8. Caddick, M. X., Brownlee, A. G. & Arst, H. N., Jr (1986). Regulation of gene expression by pH of the growth medium in Aspergillus nidulans. Mol Gen Genet 203, 346-353.
9. Cervantes-Chávez, J. A., Ortiz-Castellanos, L., Tejeda-Sartorius, M., Gold, S. & Ruiz-Herrera, J. (2010). Functional analysis of the pH responsive pathway Pal/Rim in the phytopathogenic basidiomycete Ustilago maydis. Fungal Genet Biol 47, 446-457.
10. Chen, H., Crabb, J. W. & Kinsey, J. A. (1998). The Neurospora aab-1 gene encodes a CCAAT binding protein homologous to yeast HAP5. Genetics 148, 123-130.
11. Davis, D., Edwards, J. E., Jr, Mitchell, A. P. & Ibrahim, A. S. (2000). Candida albicans RIM101 pH response pathway is required for hostpathogen interactions. Infect Immun 68, 5953-5959.
12. Eisendle, M., Oberegger, H., Buttinger, R., Illmer, P. & Haas, H. (2004). Biosynthesis and uptake of siderophores is controlled by the PacC-mediated ambient-pH regulatory system in Aspergillus nidulans. Eukaryot Cell 3, 561-563.
13. Espeso, E. A. & Peñalva, M. A. (1996). Three binding sites for the Aspergillus nidulans PacC zinc-finger transcription factor are necessary and sufficient for regulation by ambient pH of the isopenicillin N synthase gene promoter. J Biol Chem 271, 28825-28830.
14. Fischer, M. & Kaldenhoff, R. (2008). On the pH regulation of plant aquaporins. J Biol Chem 283, 33889-33892.
15. Fonseca-García, C., López, M. G., Aréchiga-Carvajal, E. T. & Ruiz-Herrera, J. (2011). A novel polysaccharide secreted by pal/rim mutants of the phytopathogen fungus Ustilago maydis. Carbohydr Polym 86, 1646-1650.
16. Fonseca-García, C., León-Ramírez, C. G. & Ruiz-Herrera, J. (2012). The regulation of different metabolic pathways through the Pal/Rim pathway in Ustilago maydis. FEMS Yeast Res 12, 547-556.
17. Frías, J. E. & Flores, E. (2010). Negative regulation of expression of the nitrate assimilation nirA operon in the heterocyst-forming cyanobacterium Anabaena sp. strain PCC 7120. J Bacteriol 192, 2769-2778.
18. Fujita, A., Lord, M., Hiroko, T., Hiroko, F., Chen, T., Oka, C., Misumi, Y. & Chant, J. (2004). Rax1, a protein required for the establishment of the bipolar budding pattern in yeast. Gene 327, 161-169.
19. Garí, E., Volpe, T., Wang, H., Gallego, C., Futcher, B. & Aldea, M. (2001). Whi3 binds the mRNA of the G1 cyclin CLN3 to modulate cell fate in budding yeast. Genes Dev 15, 2803-2808.
20. Gong, T., Liao, Y., He, F., Yang, Y., Yang, D.-D., Chen, X.-D. & Gao, X.-D. (2013). Control of polarized growth by the Rho-family GTPase Rho4 in budding yeast: requirement of the N-terminal extension of Rho4 and regulation by the Rho GTPase-activating protein Bem2. Eukaryot Cell 12, 368-377.
21. Güldener, U., Münsterkötter, M., Oesterheld, M., Pagel, P., Ruepp, A., Mewes, H. W. & Stümpflen, V. (2006). MPact: the MIPS protein interaction resource on yeast. Nucleic Acids Res 34 (Database issue), D436-D441.
22. Holliday, R. (1961). The genetics of Ustilago maydis. Genet Res 2, 204-230.
23. Huang, C. & Chang, A. (2011). pH-dependent cargo sorting from the Golgi. J Biol Chem 286, 10058-10065.
24. Imai, J., Toh-e, A. & Matsui, Y. (1996). Genetic analysis of the Saccharomyces cerevisiae RHO3 gene, encoding a rho-type small GTPase, provides evidence for a role in bud formation. Genetics 142, 359-369.
25. Jain, R., Valiante, V., Remme, N., Docimo, T., Heinekamp, T., Hertweck, C., Gershenzon, J., Haas, H. & Brakhage, A. A. (2011). The MAP kinase MpkA controls cell wall integrity, oxidative stress response, gliotoxin production and iron adaptation in Aspergillus fumigatus. Mol Microbiol 82, 39-53.
26. Jones, J. D. G., Dunsmuir, P. & Bedbrook, J. (1985). High level expression of introduced chimaeric genes in regenerated transformed plants. EMBO J 4, 2411-2418.
27. Kulmburg, P., Mathieu, M., Dowzer, C., Kelly, J. & Felenbok, B. (1993). Specific binding sites in the alcR and alcA promoters of the ethanol regulon for the CREA repressor mediating carbon catabolite repression in Aspergillus nidulans. Mol Microbiol 7, 847-857.
28. Lamb, T. M. & Mitchell, A. P. (2003). The transcription factor Rim101p governs ion tolerance and cell differentiation by direct repression of the regulatory genes NRG1 and SMP1 in Saccharomyces cerevisiae. Mol Cell Biol 23, 677-686.
29. Lamb, T. M., Xu, W., Diamond, A. Y. & Mitchell, A. P. (2001). Alkaline response genes of Saccharomyces cerevisiae and their relationship to the RIM101 pathway. J Biol Chem 276, 1850-1856.
30. Li, R. & Murray, A. W. (1991). Feedback control of mitosis in budding yeast. Cell 66, 519-531.
31. Martin, S. A. (1992). Effects of extracellular pH and phenolic monomers on glucose uptake by Fibrobacter succinogenes S85. Lett Appl Microbiol 15, 26-28.
32. Martínez-Muñoz, G. A. & Kane, P. (2008). Vacuolar and plasma membrane proton pumps collaborate to achieve cytosolic pH homeostasis in yeast. J Biol Chem 283, 20309-20319.
33. Monteiro, P. T., Mendes, N. D., Teixeira, M. C., d'Orey, S., Tenreiro, S., Mira, N. P., Pais, H., Francisco, A. P., Carvalho, A. M. & other authors (2008). YEASTRACT-DISCOVERER: new tools to improve the analysis of transcriptional regulatory associations in Saccharomyces cerevisiae. Nucleic Acids Res 36 (Database issue), D132-D136.
34. Morey, J. S., Ryan, J. C. & Van Dolah, F. M. (2006). Microarray validation: factors influencing correlation between oligonucleotide microarrays and real-time PCR. Biol Proced Online 8, 175-193.
35. + exchanger isoforms are distributed to Golgi and post-Golgi compartments and are involved in organelle pH regulation. J Biol Chem 280, 1561-1572.
36. Németh-Cahalan, K. L. & Hall, J. E. (2000). pH and calcium regulate the water permeability of aquaporin 0. J Biol Chem 275, 6777-6782.
37. Nobile, C. J., Solis, N., Myers, C. L., Fay, A. J., Deneault, J. S., Nantel, A., Mitchell, A. P. & Filler, S. G. (2008). Candida albicans transcription factor Rim101 mediates pathogenic interactions through cell wall functions. Cell Microbiol 10, 2180-2196.
38. Novacky, A., Ullrich-Eberius, C. I. & Lüttge, U. (1980). pH and membrane-potential changes during glucose uptake in Lemna gibba G1 and their response to light. Planta 149, 321-326.
39. O'Meara, T. R., Norton, D., Price, M. S., Hay, C., Clements, M. F., Nichols, C. B. & Alspaugh, J. A. (2010). Interaction of Cryptococcus neoformans Rim101 and protein kinase A regulates capsule. PLoS Pathog 6, e1000776.
40. Peñalva, M. A., Tilburn, J., Bignell, E. & Arst, H. N., Jr (2008). Ambient pH gene regulation in fungi: making connections. Trends Microbiol 16, 291-300.
41. Punta, M., Coggill, P. C., Eberhardt, R. Y., Mistry, J., Tate, J., Boursnell, C., Pang, N., Forslund, K., Ceric, G. & other authors (2012). The Pfam protein families database. Nucleic Acids Res 40 (Database issue), D290-D301.
42. Ruiz-Herrera, J., León, C. G., Guevara-Olvera, L. & Cárabez-Trejo, A. (1995). Yeast-mycelial dimorphism of haploid and diploid strains of Ustilago maydis. Microbiology 141, 695-703.
43. Soontorngun, N., Larochelle, M., Drouin, S., Robert, F. & Turcotte, B. (2007). Regulation of gluconeogenesis in Saccharomyces cerevisiae is mediated by activator and repressor functions of Rds2. Mol Cell Biol 27, 7895-7905.
44. Su, S. S. & Mitchell, A. P. (1993). Identification of functionally related genes that stimulate early meiotic gene expression in yeast. Genetics 133, 67-77.
45. Teertstra, W. R., van der Velden, G. J., de Jong, J. F., Kruijtzer, J. A. W., Liskamp, R. M. J., Kroon-Batenburg, L. M., Müller, W. H., Gebbink, M. F. B. G. & Wösten, H. A. B. (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.
46. Teixeira, M. C., Monteiro, P., Jain, P., Tenreiro, S., Fernandes, A. R., Mira, N. P., Alenquer, M., Freitas, A. T., Oliveira, A. L. & Sá-Correia, I. (2006). The YEASTRACT database: a tool for the analysis of transcription regulatory associations in Saccharomyces cerevisiae. Nucleic Acids Res 34 (Database issue), D446-D451.
47. Teixeira, M. C., Monteiro, P. T., Guerreiro, J. F., Gonçalves, J. P., Mira, N. P., dos Santos, S. C., Cabrito, T. R., Palma, M., Costa, C. & other authors (2014). The YEASTRACT database: an upgraded information system for the analysis of gene and genomic transcription regulation in Saccharomyces cerevisiae. Nucleic Acids Res 42 (Database issue), D161-D166.
48. Tilburn, J., Sarkar, S., Widdick, D. A., Espeso, E. A., Orejas, M., Mungroo, J., Peñalva, M. A. & Arst, H. N., Jr (1995). The Aspergillus PacC zinc finger transcription factor mediates regulation of both acidand alkaline-expressed genes by ambient pH. EMBO J 14, 779-790.
49. Tsuchiya, D., Gonzalez, C. & Lacefield, S. (2011). The spindle checkpoint protein Mad2 regulates APC/C activity during prometaphase and metaphase of meiosis I in Saccharomyces cerevisiae. Mol Biol Cell 22, 2848-2861.
50. UniProt Consortium (2012). Reorganizing the protein space at the Universal Protein Resource (UniProt). Nucleic Acids Res 40 (Database issue), D71-D75.
51. Vylkova, S., Carman, A. J., Danhof, H. A., Collette, J. R., Zhou, H. & Lorenz, M. C. (2011). The fungal pathogen Candida albicans autoinduces hyphal morphogenesis by raising extracellular pH. MBio 2, e00055-e11.
52. Wang, T. & Bretscher, A. (1995). The rho-GAP encoded by BEM2 regulates cytoskeletal structure in budding yeast. Mol Biol Cell 6, 1011-1024.
53. Weiss, E. L., Kurischko, C., Zhang, C., Shokat, K., Drubin, D. G. & Luca, F. C. (2002). The Saccharomyces cerevisiae Mob2p-Cbk1p kinase complex promotes polarized growth and acts with the mitotic exit network to facilitate daughter cell-specific localization of Ace2p transcription factor. J Cell Biol 158, 885-900.
54. You, B. J. & Chung, K. R. (2007). Phenotypic characterization of mutants of the citrus pathogen Colletotrichum acutatum defective in a PacCmediated pH regulatory pathway. FEMS Microbiol Lett 277, 107-114.