The regulation of different metabolic pathways through the Pal/Rim pathway in Ustilago maydis

FEMS Yeast Research

Volumn 12, Issue 5, 2012, Pages 547-556

  Fonseca García, Citlali ^a   León Ramírez, Claudia G ^a   Ruiz Herrera, José ^a  

^a DEPARTAMENTO DE INGENIERÍA GENÉTICA   (Mexico)

Author keywords

Cell wall; Pal Rim pathway; PH regulation; Stress response; Ustilago maydis

Indexed keywords

ARTICLE; CELL PH; CELL WALL; CONTROLLED STUDY; FUNGAL GENE; FUNGAL STRAIN; METABOLISM; MUTANT; NONHUMAN; PHENOTYPE; RIM13 GENE; STRESS; USTILAGO MAYDIS; WILD TYPE;

CELL WALL; CULTURE MEDIA; CYTOSOL; GENE DELETION; GENE EXPRESSION REGULATION, FUNGAL; HYDROGEN-ION CONCENTRATION; METABOLIC NETWORKS AND PATHWAYS; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; USTILAGO;

FUNGI; USTILAGO MAYDIS;

EID: 84863622707     PISSN: 15671356     EISSN: 15671364     Source Type: Journal    
DOI: 10.1111/j.1567-1364.2012.00805.x     Document Type: Article

References (51)

1. Antonsson B, Montessuit S, Friedli L, Payton MA & Paravicini G (1994) Protein kinase C in yeast. Characteristics of the Saccharomyces cerevisiae PKC1 gene product. J Biol Chem 269: 16821-16828.
2. Aréchiga-Carvajal ET & 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 HN Jr & Peñalva MA (2004) pH regulation in Aspergillus and parallels with higher eukaryotic regulatory systems. Trends Genet 19: 224-231.
4. Balgi AD, Diering GH, Donohue E, Lam KK, Fonseca BD, Zimmerman C, Numata M & Roberge M (2011) Regulation of mTORC1 signaling by pH. PLoS ONE 6: e21549.
5. Banuett F & Herskowitz I (1989) Different a alleles of Ustilago maydis are necessary for maintenance of filamentous growth but not for meiosis. P Natl Acad Sci USA 86: 5878-5882.
6. Benito B, Garciadeblás B, Pérez-Martín J & Rodríguez-Navarro A (2009) Growth at high pH, and sodium and potassium tolerance in above cytoplasmic pH media depend on ENA ATPases in Ustilago maydis. Eukaryot Cell 8: 821-829.
7. Bensen ES, Martin SJ, Li M, Berman J & Davis DA (2004) Transcriptional profiling in Candida albicans reveals new adaptive responses to extracellular pH and functions for Rim101p. Mol Microbiol 54: 1335-1351.
8. Blanchin-Roland S, Da Costa G & Gaillardin C (2005) ESCRT-I components of the endocytic machinery are required for Rim101-dependent ambient pH regulation in the yeast Yarrowia lipolytica. Microbiology 151: 3627-3637.
9. Blanchin-Roland S, Da Costa G & Gaillardin C (2008) Ambient pH signalling in the yeast Yarrowia lipolytica involves YlRim23p/PalC, which interacts with Snf7p/Vps32p, but does not require the long C terminus of YlRim9p/PalI. Microbiology 154: 1668-1676.
10. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding. Anal Biochem 72: 248-254.
11. Bravo R & Macdonald-Bravo H (1986) Effect of pH on the induction of competence and progression to the S-phase in mouse fibroblasts. FEBS Lett 195: 309-312.
12. Butcher RW & Sutherland EW (1962) Adenosine 3′, 5′-phosphate in biological materials. I. Purification and properties of cyclic 3′, 5′-nucleotide phosphodiesterase and use of this enzyme to characterize adenosine 3′, 5′-phosphate in human urine. J Biol Chem 237: 1244-1250.
13. Caracuel Z, Roncero MI, Espeso EA, González-Verdejo CI, García-Maceira FI & Di Pietro A (2003) The pH signalling transcription factor PacC controls virulence in the plant pathogen Fusarium oxysporum. Mol Microbiol 48: 65-779.
14. Castrejon F, Gomez A, Sanz M, Duran A & Roncero C (2006) The rim101 pathway contributes to yeast cell wall assembly and its function becomes essential in the absence of mitogen-activated protein kinase slt2p. Eukaryot Cell 5: 507-517.
15. Cervantes-Chávez 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.
16. Chambard JC & Pouyssegur J (1986) Intracellular pH controls growth factorinduced ribosomal protein S6 phosphorylation and protein synthesis in the G0-G1 transition of fibroblasts. Exp Cell Res 164: 282-294.
17. Chiche J, Ilc K, Laferriere J, Trottier E, Dayan F, Mazure NM, Brahimi-Horn MC & Pouyssegur J (2009) Hypoxiainducible carbonic anhydrases IX and XII promote tumor cell growth by counteracting acidosis through the regulation of the intracellular pH. Cancer Res 69: 358-368.
18. Cornet M, Bidard F, Schwarz P, Da Costa G, Blanchin-Roland S, Dromer F & Gaillardin C (2005) Deletions of endocytic components VPS28 and VPS32 affect growth at alkaline pH and virulence through both RIM101-dependent and RIM101-independent pathways in Candida albicans. Infect Immun 73: 7977-7987.
19. Davenport KR, Sohaskey M, Kamada Y, Levin DE & Gustin MC (1995) A second osmosensing signal transduction pathway in yeast. Hypotonic shock activates the PKC1 protein kinase-regulated cell integrity pathway. J Biol Chem 270: 30157-30161.
20. Davis D (2003) Adaptation to environmental pH in Candida albicans and its relation to pathogenesis. Curr Genet 44: 1-7.
21. Davis DA, Edwards JE Jr, Mitchell AP & Ibrahim AS (2000) Candida albicans rim101 pH response pathway is required for host-pathogen interactions. Infect Immun 68: 5953-5959.
22. Dimler RJ, Schaeffer WC, Wise CS & Rist CE (1952) Quantitative paper chromatography of D-glucose and its oligosaccharides. Anal Chem 24: 1411-1414.
23. Dische Z (1962) Color reactions of hexosamines. Methods in Carbohydrate Chemistry, Vol. 1 (Whistler RL & Wolfram ML, eds), pp. 507-512. Academic Press, New York.
24. Fonseca-García C, López MG, Aréchiga-Carvajal ET & Ruiz-Herrera J (2011) A novel polysaccharide secreted by pal/rim mutants of the phytopathogen fungus Ustilago maydis. Carbohydr Polym 86: 1646-1650.
25. González-López CL, Szabo R, Blanchin-Roland S & Gaillardin C (2002) Genetic control of extracellular protease synthesis in the yeast Yarrowia lipolytica. Genetics 160: 417-427.
26. Gustin MC, Albertyn J, Alexander M & Davenport K (1998) MAP Kinase pathways in the yeast Saccharomyces cerevisiae. Microbiol Mol Biol Rev 62: 1264-1300.
27. Holliday R (1961) The genetics of Ustilago maydis. Genet Res 2: 203-230.
28. Jolicoeur M, Germette S, Gaudette M, Perrier M & Becard G (1998) Intracellular pH in arbuscular mycorrhizal fungi. A symbiotic physiological marker. Plant Physiol 116: 1279-1288.
29. Klose J, de Sá MM & Kronstad JW (2004) Lipid-induced filamentous growth in Ustilago maydis. Mol Microbiol 52: 823-835.
30. Kullas AL, Martin SJ & Davis D (2007) Adaptation to environmental pH: integrating the Rim101 and calcineurin signal transduction pathways. Mol Microbiol 66: 858-871.
31. Lamb TM & Mitchell AP (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.
32. Lamb TM, Xu W, Diamond A & Mitchell AP (2001) Alkaline response genes of Saccharomyces cerevisiae and their relationship to the RIM101 pathway. J Biol Chem 276: 1850-1856.
33. Latge JP (1999) Aspergillus fumigatus and aspergillosis. Clin Microbiol Rev 12: 310-350.
34. Levin DE (2005) Cell wall integrity signaling in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 69: 262-291.
35. Martínez-Espinoza AD, León C, Elizarraraz G & Ruiz-Herrera J (1997) Monomorphic nonpathogenic mutants of Ustilago maydis. Phytopathology 87: 259-265.
36. Musgrove E, Seaman M & Hedley D (1987) Relationship between cytoplasmic pH and proliferation during exponential growth and cellular quiescence. Exp Cell Res 172: 65-75.
37. Negrutskii BS & El'skaya AV (1998) Eukaryotic translation elongation factor 1 alpha: structure, expression, functions, and possible role in aminoacyl-tRNA channeling. Prog Nucleic Acid Res Mol Biol 60: 47-78.
38. Orejas M, Espeso EA, Tilburn J, Sarkar S, Arst HN Jr & Peñalva MA (1995) Activation of the Aspergillus PacC transcription factor in response to alkaline ambient pH requires proteolysis of the carboxy-terminal moiety. Genes Dev 9: 1622-1632.
39. Peñalva MA & Arst HN Jr (2002) Regulation of gene expression by ambient pH in filamentous fungi and yeasts. Microbiol Mol Biol Rev 66: 426-446.
40. Peñalva MA & Arst HN Jr (2004) Recent advances in the characterization of ambient pH regulation of gene expression in filamentous fungi and yeasts. Annu Rev Microbiol 58: 425-451.
41. Peñalva MA, Tilburn J, Bignell E & Arst HN Jr (2008) Ambient pH gene regulation in fungi: making connections. Trends Microbiol 16: 291-300.
42. +-ATPase of Saccharomyces cerevisiae: influence on its expression and activity. Biochemistry (Mosc) 75: 1055-1063.
43. Pouyssegur J, Franchi A, L'Allemain G & Paris S (1985) Cytoplasmic pH, a key determinant of growth factor-induced DNA synthesis in quiescent fibroblasts. FEBS Lett 190: 115-119.
44. Rollins JA (2003) The Sclerotinia sclerotiorum pac1 gene is required for sclerotial development and virulence. Mol Plant Microbe Interact 16: 785-795.
45. Rollins JA & Dickman MB (2001) pH signaling in Sclerotinia sclerotiorum: identification of a pacC/RIM1 Homolog. Appl Environ Microbiol 67: 75-81.
46. Ruiz-Herrera J, León C, Carabez-Trejo A & Reyes-Salinas E (1996) Structure and chemical composition of the cell walls from the haploid yeast and mycelial forms of Ustilago maydis. Fungal Genet Biol 20: 133-142.
47. Su SS & Mitchell AP (1993) Molecular characterization of the yeast meiotic regulatory gene RIM1. Nucleic Acids Res 21: 3789-3797.
48. Tilburn J, Sarkar S, Widdick DA, Espeso EA, Orejas M, Mungroo J, Peñalva MA & Arst HN 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.
49. von Tigerstrom RG & Stelmaschuk S (1989) The use of Tween 20 in a sensitive turbidimetric assay of lipolytic enzymes. Can J Microbiol 35: 511-514.
50. Xu W, Smith FJ Jr, Subaran R & Mitchell AP (2004) Multivesicular body escort components function in pH response regulation in Saccharomyces cerevisiae and Candida albicans. Mol Biol Cell 15: 5528-5537.
51. You BJ & Chung KR (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.