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

References

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 issueD136–D140 [View Article][PubMed]
   [Google Scholar]
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 [View Article][PubMed]
   [Google Scholar]
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 [View Article][PubMed]
   [Google Scholar]
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 [View Article][PubMed]
   [Google Scholar]
5. Barth G., Gaillardin C. ( 1996). Yarrowia lipolytica. Non-conventional Yeasts in Biotechnology: a Handbook313–388 Wolf K. Berlin: Springer-Verlag; [View Article]
   [Google Scholar]
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 [View Article][PubMed]
   [Google Scholar]
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 [View Article][PubMed]
   [Google Scholar]
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 [View Article][PubMed]
   [Google Scholar]
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 [View Article][PubMed]
   [Google Scholar]
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[PubMed]
    [Google Scholar]
11. Davis D., Edwards J. E. Jr, Mitchell A. P., Ibrahim A. S. ( 2000). Candida albicans RIM101 pH response pathway is required for host-pathogen interactions. Infect Immun 68:5953–5959 [View Article][PubMed]
    [Google Scholar]
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 [View Article][PubMed]
    [Google Scholar]
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 [View Article][PubMed]
    [Google Scholar]
14. Fischer M., Kaldenhoff R. ( 2008). On the pH regulation of plant aquaporins. J Biol Chem 283:33889–33892 [View Article][PubMed]
    [Google Scholar]
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 [View Article]
    [Google Scholar]
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 [View Article][PubMed]
    [Google Scholar]
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 [View Article][PubMed]
    [Google Scholar]
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 [View Article][PubMed]
    [Google Scholar]
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[PubMed]
    [Google Scholar]
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 [View Article][PubMed]
    [Google Scholar]
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 issueD436–D441 [View Article][PubMed]
    [Google Scholar]
22. Holliday R. ( 1961). The genetics of Ustilago maydis. Genet Res 2:204–230 [View Article]
    [Google Scholar]
23. Huang C., Chang A. ( 2011). pH-dependent cargo sorting from the Golgi. J Biol Chem 286:10058–10065 [View Article][PubMed]
    [Google Scholar]
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[PubMed]
    [Google Scholar]
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 [View Article][PubMed]
    [Google Scholar]
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[PubMed]
    [Google Scholar]
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 [View Article][PubMed]
    [Google Scholar]
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 [View Article][PubMed]
    [Google Scholar]
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 [View Article][PubMed]
    [Google Scholar]
30. Li R., Murray A. W. ( 1991). Feedback control of mitosis in budding yeast. Cell 66:519–531 [View Article][PubMed]
    [Google Scholar]
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 [View Article]
    [Google Scholar]
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 [View Article][PubMed]
    [Google Scholar]
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 issueD132–D136 [View Article][PubMed]
    [Google Scholar]
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 [View Article][PubMed]
    [Google Scholar]
35. Nakamura N., Tanaka S., Teko Y., Mitsui K., Kanazawa H. ( 2005). Four Na⁺/H⁺ exchanger isoforms are distributed to Golgi and post-Golgi compartments and are involved in organelle pH regulation. J Biol Chem 280:1561–1572 [View Article][PubMed]
    [Google Scholar]
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 [View Article][PubMed]
    [Google Scholar]
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 [View Article][PubMed]
    [Google Scholar]
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 [View Article][PubMed]
    [Google Scholar]
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 [View Article][PubMed]
    [Google Scholar]
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 [View Article][PubMed]
    [Google Scholar]
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 issueD290–D301 [View Article][PubMed]
    [Google Scholar]
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 [View Article]
    [Google Scholar]
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 [View Article][PubMed]
    [Google Scholar]
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[PubMed]
    [Google Scholar]
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 [View Article][PubMed]
    [Google Scholar]
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 issueD446–D451 [View Article][PubMed]
    [Google Scholar]
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 issueD161–D166 [View Article][PubMed]
    [Google Scholar]
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 acid- and alkaline-expressed genes by ambient pH. EMBO J 14:779–790[PubMed]
    [Google Scholar]
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 [View Article][PubMed]
    [Google Scholar]
50. UniProt Consortium ( 2012). Reorganizing the protein space at the Universal Protein Resource (UniProt). Nucleic Acids Res 40:Database issueD71–D75 [View Article][PubMed]
    [Google Scholar]
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 [View Article][PubMed]
    [Google Scholar]
52. Wang T., Bretscher A. ( 1995). The rho-GAP encoded by BEM2 regulates cytoskeletal structure in budding yeast. Mol Biol Cell 6:1011–1024 [View Article][PubMed]
    [Google Scholar]
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 [View Article][PubMed]
    [Google Scholar]
54. You B. J., Chung K. R. ( 2007). Phenotypic characterization of mutants of the citrus pathogen Colletotrichum acutatum defective in a PacC-mediated pH regulatory pathway. FEMS Microbiol Lett 277:107–114 [View Article][PubMed]
    [Google Scholar]