Chapter 30 : How Fungi Sense Sugars, Alcohols, and Amino Acids

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Zoom in

How Fungi Sense Sugars, Alcohols, and Amino Acids, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555816636/9781555814731_Chap30-1.gif /docserver/preview/fulltext/10.1128/9781555816636/9781555814731_Chap30-2.gif


G-protein-coupled receptors (GPCRs) are an important receptor gene family and play important roles in sensing sugars in eukaryotic organisms, including fungi. Recent studies on the interactions between and plants, a major environmental niche, reveal that -inositol, produced and secreted by plants, is sensed by the fungus and promotes fungal sexual reproduction, providing a potential explanation for how this organism completes its life cycle in nature. Several fusel alcohols, such as 1-butanol and isoamyl alcohol, stimulate filamentous growth of haploid cells. A recent study showed that aromatic alcohols (such as tryptophol and phenylethanol) secreted by yeast cells function as quorum-sensing molecules and stimulate filamentous growth through a Flo11-dependent mechanism. Amino acids are important nutrients for fungi and are detected by specialized sensor systems, which include the general amino acid permease Gap1, the Ssy1-Ptr3-Ssy5 (SPS) system, GPCRs, and the target of rapamycin (TOR). In , three transport systems have been described based on the analysis of the kinetics of amino acid uptake and the patterns of competitive inhibition between amino acids. The Gap1 homolog in is encoded by the locus, which can transport all L-amino acids except proline. Besides this system, two other transport systems have also been identified. One is encoded by the MTR gene and transports neutral and aromatic amino acids. The other is encoded by the PMB gene and transports basic amino acids, such as arginine and lysine.

Citation: Xue* C, Ebbole D, Heitman J. 2010. How Fungi Sense Sugars, Alcohols, and Amino Acids, p 469-479. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch30
Highlighted Text: Show | Hide
Loading full text...

Full text loading...


Image of FIGURE 1

Carbon sensors in yeast. utilizes multiple sensory systems to sense and import carbon sources from the environment. A Gpr1 GPCR system senses extracellular sugars and activates the Gpa2-cAMP-PKA signaling pathway to control pseudohyphal differentiation. Glucose can also be sensed by a transporter-like receptor system that involves Snf3 and Rgt2, which regulate the expression of the major hexose transporter gene family (HXT). The HXT proteins import glucose to undergo glycolysis, and its intermediate, glucose-6-phosphate, also triggers the activation of cAMP-PKA signaling. Yeasts may also sense -inositol through the -inositol transporter gene family and utilize inositol as a precursor for many metabolic and catabolic processes that play critical roles in signaling regulation and cell developmental processes. A variety of alcohol-related products (such as fusel alcohols, aromatic alcohols, and farnesol-related molecules) that are produced by yeasts themselves provide an autoregulatory machinery to regulate yeast cell population and filamentation processes.

Citation: Xue* C, Ebbole D, Heitman J. 2010. How Fungi Sense Sugars, Alcohols, and Amino Acids, p 469-479. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch30
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 2

Amino acid sensory systems. Fungal cells require nitrogen sources, including amino acids, from the extracellular environment through a sophisticated sensory network, which involves the general amino acid permease Gap1 to uptake a broad range of amino acids, the SPS system to sense more specific amino acids groups, and two permease systems to respond to oligopeptides, including the PTR system, which imports di/tripeptides, and the OPT system, which transports oligopeptides. This amino acid permease network is highly coordinated through regulation between members and some common regulators, such as Cup9. In addition to the amino acid permeases, GPCR receptors that sense certain amino acids as signaling molecules have also been identified in the pathogenic yeasts and . Also, the Tor protein complex is important for sensing nutrient signals, including amino acids, and regulating the stability of some amino acid permeases, as well as many transcriptional and translational processes.

Citation: Xue* C, Ebbole D, Heitman J. 2010. How Fungi Sense Sugars, Alcohols, and Amino Acids, p 469-479. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch30
Permissions and Reprints Request Permissions
Download as Powerpoint


1. Abraham, R. T. 2004. mTOR as a positive regulator of tumor cell responses to hypoxia. Curr. Top. Microbiol. Immunol. 279: 299319.
2. Allen, K. E.,, M. T. McNally,, H. S. Lowendorf,, C. W. Slay-man, and, S. J. Free. 1989. Deoxyglucose-resistant mutants of Neurospora crassa: isolation, mapping, and biochemical characterization. J. Bacteriol. 171: 5358.
3. Andreasson, C.,, E. P. Neve, and, P. O. Ljungdahl. 2004. Four permeases import proline and the toxic proline analogue azetidine-2-carboxylate into yeast. Yeast 21: 193199.
4. Andreasson, C.,, S. Heessen, and, P. O. Ljungdahl. 2006. Regulation of transcription factor latency by receptor-activated proteolysis. Genes Dev. 20: 15631568.
5. Ashe, M. P.,, J. W. Slaven,, S. K. De Long,, S. Ibrahimo, and, A. B. Sachs. 2001. A novel eIF2B-dependent mechanism of translational control in yeast as a response to fusel alcohols. EMBO J. 20: 64646474.
6. Attwood, T. K., and, J. B. Findlay. 1994. Fingerprinting G-protein-coupled receptors. Protein Eng. 7: 195203.
7. Bahn, Y. S.,, C. Xue,, A. Idnurm,, J. C. Rutherford,, J. Heitman, and, M. E. Cardenas. 2007. Sensing the environment: lessons from fungi. Nat. Rev. Microbiol. 5: 5769.
8. Beck, T.,, A. Schmidt, and, M. N. Hall. 1999. Starvation induces vacuolar targeting and degradation of the tryptophan permease in yeast. J. Cell Biol. 146: 12271238.
9. Brega, E.,, R. Zufferey, and, C. B. Mamoun. 2004. Candida albicans Csy1p is a nutrient sensor important for activation of amino acid uptake and hyphal morphogenesis. Eukaryot. Cell 3: 135143.
10. Brown, V.,, J. Sabina, and, M. Johnston. 2009. Specialized sugar sensing in diverse fungi. Curr. Biol. 19: 436441.
11. Byrd, C.,, G. C. Turner, and, A. Varshavsky. 1998. The N-end rule pathway controls the import of peptides through degradation of a transcriptional repressor. EMBO J. 17: 269277.
12. Calvert, C. M., and, D. Sanders. 1995. Inositol trisphosphate-dependent and -independent Ca 2+ mobilization pathways at the vacuolar membrane of Candida albicans. J. Biol. Chem. 270: 72727280.
13. Cardenas, M. E.,, N. S. Cutler,, M. C. Lorenz,, C. J. Di Como, and, J. Heitman. 1999. The TOR signaling cascade regulates gene expression in response to nutrients. Genes Dev. 13: 32713279.
14. Chen, C., and, M. B. Dickman. 2005. Proline suppresses apoptosis in the fungal pathogen Colletotrichum trifolii. Proc. Natl. Acad. Sci. USA 102: 34593464.
15. Chen, H.,, M. Fujita,, Q. Feng,, J. Clardy, and, G. R. Fink. 2004. Tyrosol is a quorum-sensing molecule in Candida albicans. Proc. Natl. Acad. Sci. USA 101: 50485052.
16. Chen, H., and, G. R. Fink. 2006. Feedback control of morphogenesis in fungi by aromatic alcohols. Genes Dev. 20: 11501161.
17. Chen, J. C., and, T. Powers. 2006. Coordinate regulation of multiple and distinct biosynthetic pathways by TOR and PKA kinases in S. cerevisiae. Curr. Genet. 49: 281293.
18. Chen, Y. L.,, S. Kauffman, and, T. B. Reynolds. 2008. Candida albicans uses multiple mechanisms to acquire the essential metabolite inositol during infection. Infect. Immun. 76: 27932801.
19. Colombo, S.,, D. Ronchetti,, J. M. Thevelein,, J. Winderickx, and, E. Martegani. 2004. Activation state of the Ras2 protein and glucose-induced signaling in Saccharomyces cerevisiae. J. Biol. Chem. 279: 4671546722.
20. Coons, D. M.,, R. B. Boulton, and, L. F. Bisson. 1995. Computer-assisted nonlinear regression analysis of the multicomponent glucose uptake kinetics of Saccharomyces cerevisiae. J. Bacteriol. 177: 32513258.
21. Crespo, J. L.,, T. Powers,, B. Fowler, and, M. N. Hall. 2002. The TOR-controlled transcription activators GLN3, RTG1, and RTG3 are regulated in response to intracellular levels of glutamine. Proc. Natl. Acad. Sci. USA 99: 67846789.
22. Cutler, N. S.,, X. Pan,, J. Heitman, and, M. E. Cardenas. 2001. The TOR signal transduction cascade controls cellular differentiation in response to nutrients. Mol. Biol. Cell 12: 41034113.
23. D’Alessio, M., and, M. C. Brandriss. 2000. Cross-pathway regulation in Saccharomyces cerevisiae: activation of the pro-line utilization pathway by Gal4p in vivo. J. Bacteriol. 182: 37483753.
24. Des Etages, S. A.,, D. Saxena,, H. L. Huang,, D. A. Falvey,, D. Barber, and, M. C. Brandriss. 2001. Conformational changes play a role in regulating the activity of the proline utilization pathway-specific regulator in Saccharomyces cerevisiae. Mol. Microbiol. 40: 890899.
25. Dickinson, J. R. 1996. ‘Fusel’ alcohols induce hyphal-like extensions and pseudohyphal formation in yeasts. Microbiology 142: 13911397.
26. Dickinson, J. R. 2008. Filament formation in Saccharomyces cerevisiae: a review. Folia Microbiol. (Praha) 53: 314.
27. Di Como, C. J., and, K. T. Arndt. 1996. Nutrients, via the Tor proteins, stimulate the association of Tap42 with type 2A phosphatases. Genes Dev. 10: 19041916.
28. Didion, T.,, B. Regenberg,, M. U. Jorgensen,, M. C. Kielland-Brandt, and, H. A. Andersen. 1998. The permease homologue Ssy1p controls the expression of amino acid and peptide transporter genes in Saccharomyces cerevisiae. Mol. Microbiol. 27: 643650.
29. Dlugai, S.,, S. Hippler,, R. Wieczorke, and, E. Boles. 2001. Glucose-dependent and -independent signalling functions of the yeast glucose sensor Snf3. FEBS Lett. 505: 389392.
30. Donaton, M. C.,, I. Holsbeeks,, O. Lagatie,, G. Van Zeebroeck,, M. Crauwels,, J. Winderickx, and, J. M. Thevelein. 2003. The Gap1 general amino acid permease acts as an amino acid sensor for activation of protein kinase A targets in the yeast Saccharomyces cerevisiae. Mol. Microbiol. 50: 911929.
31. Forsberg, H., and, P. O. Ljungdahl. 2001. Sensors of extracellular nutrients in Saccharomyces cerevisiae. Curr. Genet. 40: 91109.
32. Franzot, S. P., and, T. L. Doering. 1999. Inositol acylation of glycosylphosphatidylinositols in the pathogenic fungus Cryptococcus neoformans and the model yeast Saccharomyces cerevisiae. Biochem. J. 340: 2532.
33. Gancedo, J. M. 2008. The early steps in glucose signalling in yeast. FEMS Microbiol. Rev. 32: 673704.
34. Garrett, J. M. 2008. Amino acid transport through the Saccharomyces cerevisiae Gap1 permease is controlled by the Ras/cAMP pathway. Int. J. Biochem. Cell Biol. 40: 496502.
35. Gimeno, C. J.,, P. O. Ljungdahl,, C. A. Styles, and, G. R. Fink. 1992. Unipolar cell divisions in the yeast S. cerevisiae lead to filamentous growth: regulation by starvation and RAS. Cell 68: 10771090.
36. Han, K. H.,, J. A. Seo, and, J. H. Yu. 2004. A putative G protein-coupled receptor negatively controls sexual development in Aspergillus nidulans. Mol. Microbiol. 51: 13331345.
37. Harding, M. W.,, A. Galat,, D. E. Uehling, and, S. L. Schreiber 1989. A receptor for the immunosuppressant FK506 is a cis-trans peptidyl-prolyl isomerase. Nature 341: 758760.
38. Hauser, M.,, V. Narita,, A. M. Donhardt,, F. Naider, and, J. M. Becker. 2001. Multiplicity and regulation of genes encoding peptide transporters in Saccharomyces cerevisiae. Mol. Membr. Biol. 18: 105112.
39. Healy, M. E.,, C. L. Dillavou, and, G. E. Taylor. 1977. Diagnostic medium containing inositol, urea, and caffeic acid for selective growth of Cryptococcus neoformans. J. Clin. Microbiol. 6: 387391.
40. Heitman, J.,, N. R. Movva, and, M. N. Hall. 1991. Targets for cell cycle arrest by the immunosuppressant rapamycin in yeast. Science 253: 905909.
41. Hoffman, C. S. 2005. Glucose sensing via the protein kinase A pathway in Schizosaccharomyces pombe. Biochem. Soc. Trans. 33: 257260.
42. Hogan, D. A. 2006. Talking to themselves: autoregulation and quorum sensing in fungi. Eukaryot. Cell 5: 613619.
43. Huang, H. L., and, M. C. Brandriss. 2000. The regulator of the yeast proline utilization pathway is differentially phosphorylated in response to the quality of the nitrogen source. Mol. Cell. Biol. 20: 892899.
44. Jacinto, E. 2007. Phosphatase targets in TOR signaling. Methods Mol. Biol. 365: 323334.
45. Jauniaux, J. C., and, M. Grenson. 1990. GAP1, the general amino acid permease gene of Saccharomyces cerevisiae. Nucleotide sequence, protein similarity with the other bakers yeast amino acid permeases, and nitrogen catabolite repression. Eur. J. Biochem. 190: 3944.
46. Jin, J. H., and, A. Seyfang. 2003. High-affinity myo-inositol transport in Candida albicans: substrate specificity and pharmacology. Microbiology. 149: 33713381.
47. Kanter, U.,, M. Becker,, E. Friauf, and, R. Tenhaken. 2003. Purification, characterization and functional cloning of inositol oxygenase from Cryptococcus. Yeast 20: 13171329.
48. Klasson, H.,, G. R. Fink, and, P. O. Ljungdahl. 1999. Ssy1p and Ptr3p are plasma membrane components of a yeast system that senses extracellular amino acids. Mol. Cell. Biol. 19: 54055416.
49. Kolakowski, L. F., Jr. 1994. GCRDb: a G-protein-coupled receptor database. Recept. Channels 2: 17.
50. Kraakman, L.,, K. Lemaire,, P. Ma,, A. W. Teunissen,, M. C. Donaton,, P. Van Dijck,, J. Winderickx,, J. H. de Winde, and, J. M. Thevelein. 1999. A Saccharomyces cerevisiae G-protein coupled receptor, Gpr1, is specifically required for glucose activation of the cAMP pathway during the transition to growth on glucose. Mol. Microbiol. 32: 10021012.
51. Kruppa, M.,, B. P. Krom,, N. Chauhan,, A. V. Bambach,, R. L. Cihlar, and, R. A. Calderone. 2004. The two-component signal transduction protein Chk1p regulates quorum sensing in Candida albicans. Eukaryot. Cell 3: 10621065.
52. Kulkarni, R. D.,, M. R. Thon,, H. Pan, and, R. A. Dean. 2005. Novel G-protein-coupled receptor-like proteins in the plant pathogenic fungus Magnaporthe grisea. Genome Biol. 6: R24.
53. Lai, K.,, C. P. Bolognese,, S. Swift, and, P. McGraw. 1995. Regulation of inositol transport in Saccharomyces cerevisiae involves inositol-induced changes in permease stability and endocytic degradation in the vacuole. J. Biol. Chem. 270: 25252534.
54. Lasko, P., and, M. C. Brandriss. 1981. Proline transport in Saccharomyces cerevisiae. J. Bacteriol. 148: 241247.
55. Lauwers, E.,, G. Grossmann, and, B. Andre. 2007. Evidence for coupled biogenesis of yeast Gap1 permease and sphingolipids: essential role in transport activity and normal control by ubiquitination. Mol. Biol. Cell. 18: 30683080.
56. Lee, H.,, Y. C. Chang, and, K. J. Kwon-Chung. 2005. TUP1 disruption reveals biological differences between MAT a and MAT alpha strains of Cryptococcus neoformans. Mol. Micro-biol. 55: 12221232.
57. Lee, H.,, Y. C. Chang,, G. Nardone, and, K. J. Kwon-Chung. 2007. TUP1 disruption in Cryptococcus neoformans uncovers a peptide-mediated density-dependent growth phenomenon that mimics quorum sensing. Mol. Microbiol. 64: 591601.
58. Lee, S. C., and, Y. H. Lee. 1998. Calcium/calmodulin-dependent signaling for appressorium formation in the plant pathogenic fungus Magnaporthe grisea. Mol. Cells 8: 698704.
59. Lemaire, K.,, S. Van de Velde,, P. Van Dijck, and, J. M. Thevelein. 2004. Glucose and sucrose act as agonist and mannose as antagonist ligands of the G protein-coupled receptor Gpr1 in the yeast Saccharomyces cerevisiae. Mol. Cell 16: 293299.
60. Li, L., and, K. A. Borkovich. 2006. GPR-4 is a predicted G-protein-coupled receptor required for carbon source-dependent asexual growth and development in Neurospora crassa. Eukaryot. Cell 5: 12871300.
61. Liu, Z.,, J. Thornton,, M. Spirek, and, R. A. Butow. 2008. Activation of the SPS amino acid-sensing pathway in Saccharomyces cerevisiae correlates with the phosphorylation state of a sensor component, Ptr3. Mol. Cell. Biol. 28: 551563.
62. Loewith, R.,, E. Jacinto,, S. Wullschleger,, A. Lorberg,, J. L. Crespo,, D. Bonenfant,, W. Oppliger,, P. Jenoe, and, M. N. Hall. 2002. Two TOR complexes, only one of which is rapamycin sensitive, have distinct roles in cell growth control. Mol. Cell 10: 457468.
63. Lorenz, M. C.,, N. S. Cutler, and, J. Heitman. 2000a. Characterization of alcohol-induced filamentous growth in Saccharomyces cerevisiae. Mol. Biol. Cell 11: 183199.
64. Lorenz, M. C.,, X. Pan,, T. Harashima,, M. E. Cardenas,, Y. Xue,, J. P. Hirsch, and, J. Heitman. 2000b. The G protein-coupled receptor Gpr1 is a nutrient sensor that regulates pseudohyphal differentiation in Saccharomyces cerevisiae. Genetics 154: 609622.
65. Lubkowitz, M. A.,, D. Barnes,, M. Breslav,, A. Burchfield,, F. Naider, and, J. M. Becker. 1998. Schizosaccharomyces pombe isp4 encodes a transporter representing a novel family of oligopeptide transporters. Mol. Microbiol. 28: 729741.
66. Madi, L.,, S. A. McBride,, L. A. Bailey, and, D. J. Ebbole. 1997. rco-3, a gene involved in glucose transport and conidiation in Neurospora crassa. Genetics 146: 499508.
67. Madi, L.,, D. J. Ebbole,, B. T. White, and, C. Yanofsky. 1994. Mutants of Neurospora crassa that alter gene expression and conidia development. Proc. Natl. Acad. Sci. USA 91: 62266230.
68. Maidan, M. M.,, L. De Rop,, J. Serneels,, S. Exler,, S. Rupp,, H. Tournu,, J. M. Thevelein, and, P. Van Dijck. 2005a. The G protein-coupled receptor Gpr1 and the Galpha protein Gpa2 act through the cAMP-protein kinase A pathway to induce morphogenesis in Candida albicans. Mol. Biol. Cell 16: 19711986.
69. Maidan, M. M.,, J. M. Thevelein, and, P. Van Dijck. 2005b. Carbon source induced yeast-to-hypha transition in Candida albicans is dependent on the presence of amino acids and on the G-protein-coupled receptor Gpr1. Biochem. Soc. Trans. 33: 291293.
70. Margolis-Clark, E.,, I. Hunt,, S. Espinosa, and, B. J. Bowman. 2001. Identification of the gene at the pmg locus, encoding system II, the general amino acid transporter in Neurospora crassa. Fungal Genet. Biol. 33: 127135.
71. Martinez, P., and, P. O. Ljungdahl. 2005. Divergence of Stp1 and Stp2 transcription factors in Candida albicans places virulence factors required for proper nutrient acquisition under amino acid control. Mol. Cell. Biol. 25: 94359446.
72. Martinez-Anaya, C.,, J. R. Dickinson, and, P. E. Sudbery. 2003. In yeast, the pseudohyphal phenotype induced by isoamyl alcohol results from the operation of the morphogenesis checkpoint. J. Cell Sci. 116: 34233431.
73. Moriya, H., and, M. Johnston. 2004. Glucose sensing and signaling in Saccharomyces cerevisiae through the Rgt2 glucose sensor and casein kinase I. Proc. Natl. Acad. Sci. USA 101: 15721577.
74. Miwa, T.,, Y. Takagi,, M. Shinozaki,, C. W. Yun,, W. A. Schell,, J. R. Perfect,, H. Kumagai, and, H. Tamaki. 2004. Gpr1, a putative G-protein-coupled receptor, regulates morphogenesis and hypha formation in the pathogenic fungus Candida albicans. Eukaryot. Cell 3: 919931.
75. Navarathna, D. H.,, K. W. Nickerson,, G. E. Duhamel,, T. R. Jerrels, and, T. M. Petro. 2007. Exogenous farnesol interferes with the normal progression of cytokine expression during candidiasis in a mouse model. Infect. Immun. 75: 40064011.
76. Nickerson, K. W.,, A. L. Atkin, and, J. M. Hornby. 2006. Quorum sensing in dimorphic fungi: farnesol and beyond. Appl. Environ. Microbiol. 72: 38053813.
77. Niederberger, C.,, R. Graub,, A. M. Schweingruber,, H. Fankhauser,, M. Rusu,, M. Poitelea,, L. Edenharter, and, M.E. Schweingruber. 1998. Exogenous inositol and genes responsible for inositol transport are required for mating and sporulation in Schizosaccharomyces pombe. Curr. Genet. 33: 255261.
78. Nikawa, J.,, Y. Tsukagoshi, and, S. Yamashita. 1991. Isolation and characterization of two distinct myo-inositol transporter genes of Saccharomyces cerevisiae. J. Biol. Chem. 266: 1118411191.
79. Nikawa, J.,, K., Hosaka, and, S. Yamashita. 1993. Differential regulation of two myo-inositol transporter genes of Saccharomyces cerevisiae. Mol. Microbiol. 10: 955961.
80. Ozcan, S.,, J. Dover, and, M. Johnston. 1998. Glucose sensing and signaling by two glucose receptors in the yeast Saccharomyces cerevisiae. EMBO J. 17: 25662573.
81. Pall, M. L. 1969. Amino acid transport in Neurospora crassa. I. Properties of two amino acid transport systems. Biochim. Biophys. Acta 173: 113127.
82. Pall, M.L. 1970. Amino acid transport in Neurospora crassa. II. Properties of a basic amino acid transport system. Biochim. Biophys. Acta 203: 139149.
83. Pan, X., and, J. Heitman. 1999. Cyclic AMP-dependent protein kinase regulates pseudohyphal differentiation in Saccharomyces cerevisiae. Mol. Cell. Biol. 19: 48744887.
84. Puria, R.,, S. A. Zurita-Martinez, and, M. E. Cardenas. 2008. Nuclear translocation of Gln3 in response to nutrient signals requires Golgi-to-endosome trafficking in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 105: 71947199.
85. Raught, B.,, A. C. Gingras, and, N. Sonenberg. 2001. The target of rapamycin (TOR) proteins. Proc. Natl. Acad. Sci. USA 98: 70377044.
86. Reuss, O., and, J. Morschhäuser. 2006. A family of oligopep-tide transporters is required for growth of Candida albicans on proteins. Mol. Microbiol. 60: 795812.
87. Reynolds, T. B. 2009. Strategies for acquiring the phospholipid metabolite inositol in pathogenic bacteria, fungi and protozoa: making it and taking it. Microbiology 155 (Pt. 5): 13861396.
88. Rohde, J.,, J. Heitman, and, M. E. Cardenas. 2001. The TOR kinases link nutrient sensing to cell growth. J. Biol. Chem. 276: 95839586.
89. Rohde, J. R., and, M. E. Cardenas. 2003. The Tor pathway regulates gene expression by linking nutrient sensing to his-tone acetylation. Mol. Cell. Biol. 23: 629635.
90. Rohde, J. R.,, S. Campbell,, S. A. Zurita-Martinez,, N. S. Cutler,, M. Ashe, and, M. E. Cardenas. 2004. TOR controls transcriptional and translational programs via Sap-Sit4 protein phosphatase signaling effectors. Mol. Cell. Biol. 24: 83328341.
91. Rolland, F.,, J. H. de Winde,, K. Lemaire,, E. Boles,, J. M. Thevelein, and, J. Winderickx. 2000. Glucose-induced cAMP signaling in yeast requires both a G-protein coupled receptor system for extracellular glucose detection and a separable hexose kinase-dependent sensing process. Mol. Microbiol. 38: 348358.
92. Rolland, F.,, V. Wanke,, L. Cauwenberg,, P. Ma,, E. Boles,, M. Vanoni,, J. H. de Winde,, J. M. Thevelein, and, J. Winder-ickx. 2001. The role of hexose transport and phosphorylation in cAMP signaling in the yeast Saccharomyces cerevisiae. FEMS Yeast Res. 1: 3345.
93. Rolland, F.,, J. Winderickx, and, J. M. Thevelein. 2002. Glucose-sensing and -signalling mechanisms in yeast. FEMS Yeast Res. 2: 183201.
94. Schmelzle, T.,, T. Beck,, D. E. Martin, and, M. N. Hall. 2004. Activation of the RAS/cyclic AMP pathway suppresses a TOR deficiency in yeast. Mol. Cell. Biol. 24: 338351.
95. Schmidt, A.,, T. Beck,, A. Koller,, J. Kunz, and, M. N. Hall. 1998. The TOR nutrient signalling pathway phosphorylates NPR1 and inhibits turnover of the tryptophan permease. EMBO J. 17: 69246931.
96. Seeds, A. M., and, J. D. York. 2007. Inositol polyphosphate kinases: regulators of nuclear function. Biochem. Soc. Symp. 74: 183197.
97. Semighini, C. P.,, J. M. Hornby,, R. Dumitru,, K. W. Nicker-son, and, S. D. Harris. 2006. Farnesol-induced apoptosis in Aspergillus nidulans reveals a possible mechanism for antagonistic interactions between fungi. Mol. Microbiol. 59: 753764.
98. Shaw, B. D., and, H. C. Hoch. 2000. Ca 2+ regulation of Phyllosticta ampelicida pycnidiospore germination and appressorium formation. Fungal Genet. Biol. 31: 4353.
99. Siekierka, J. J.,, M. J. Staruch,, S. H. Hung, and, N. H. Sigal. 1989. FK-506, a potent novel immunosuppressive agent, binds to a cytosolic protein which is distinct from the cyclosporin A-binding protein, cyclophilin. J. Immunol. 143: 15801583.
100. Silverman-Gavrila, L. B., and, R. R. Lew. 2002. An IP 3-activated Ca 2+ channel regulates fungal tip growth. J. Cell Sci. 115: 50135025.
101. Silverman-Gavrila, L. B., and, R. R. Lew. 2003. Calcium gradient dependence of Neurospora crassa hyphal growth. Microbiology 149: 24752485.
102. Smirnova, J. B.,, J. N. Selley,, F. Sanchez-Cabo,, K. Carroll,, A. A. Eddy,, J. E. McCarthy,, S. J. Hubbard,, G. D. Pavitt,, C. M. Grant, and, M. P. Ashe. 2005. Global gene expression profiling reveals widespread yet distinctive translational responses to different eukaryotic translation initiation factor 2B-targeting stress pathways. Mol. Cell. Biol. 25: 93409349.
103. Springael, J. Y., and, B. Andre. 1998. Nitrogen-regulated ubiquitination of the Gap1 permease of Saccharomyces cerevisiae. Mol. Biol. Cell 9: 12531263.
104. Stanbrough, M., and, B. Magasanik. 1995. Transcriptional and posttranslational regulation of the general amino acid permease of Saccharomyces cerevisiae. J. Bacteriol. 177: 94102.
105. Uppuluri, P.,, S. Mekala, and, W. L. Chaffin. 2007. Farnesol-mediated inhibition of Candida albicans yeast growth and rescue by a diacylglycerol analogue. Yeast 24: 681693.
106. Versele, M.,, K. Lemaire, and, J. M. Thevelein. 2001. Sex and sugar in yeast: two distinct GPCR systems. EMBO Rep. 2: 574579.
107. Vincent, V. L., and, L. S. Klig. 1995. Unusual effect of myoinositol on phospholipid biosynthesis in Cryptococcus neofor-mans. Microbiology 141: 18291837.
108. Voicu, P. M.,, M. Poitelea,, E. Schweingruber, and, M. Rusu. 2002. Inositol is specifically involved in the sexual program of the fission yeast Schizosaccharomyces pombe. Arch. Micro-biol. 177: 251258.
109. Wedaman, K. P.,, A. Reinke,, S. Anderson,, J. Yates III,, J. M. McCaffery, and, T. Powers. 2003. Tor kinases are in distinct membrane-associated protein complexes in Saccharomyces cerevisiae. Mol. Biol. Cell 14: 12041220.
110. Welton, R. M., and, C. S. Hoffman. 2000. Glucose monitoring in fission yeast via the gpa2 Galpha, the git5 Gbeta and the git3 putative glucose receptor. Genetics 156: 513521.
111. Wiles, A. M.,, H. Cai,, F. Naider, and, J. M. Becker. 2006. Nutrient regulation of oligopeptide transport in Saccharomyces cerevisiae. Microbiology 152: 31333145.
112. Wu, B.,, K. Ottow,, P. Poulsen,, R. F. Gaber,, E. Albers, and, M. C. Kielland-Brandt. 2006. Competitive intra- and extracellular nutrient sensing by the transporter homologue Ssy1p. J. Cell Biol. 173: 327331.
113. Xin, X.,, H. H. Wilkinson,, A. Correa,, Z. A. Lewis,, D. Bell-Pedersen, and, D. J. Ebbole. 2004. Transcriptional response to glucose starvation and functional analysis of a glucose transporter of Neurospora crassa. Fungal Genet. Biol. 41: 11041119.
114. Xue, C.,, Y. S. Bahn,, G. M. Cox, and, J. Heitman. 2006. G protein-coupled receptor Gpr4 senses amino acids and activates the cAMP-PKA pathway in Cryptococcus neoformans. Mol. Biol. Cell 17: 667679.
115. Xue, C.,, Y. Tada,, X. Dong, and, J. Heitman. 2007. The human fungal pathogen Cryptococcus can complete its sexual cycle during a pathogenic association with plants. Cell Host Microbe 1: 263273.
116. Xue, Y.,, M. Batlle, and, J. P. Hirsch, 1998. GPR1 encodes a putative G protein-coupled receptor that associates with the Gpa2p Galpha subunit and functions in a Ras-independent pathway. EMBO J. 17: 19962007.
117. Zeitlinger, J.,, I. Simon,, C. T. Harbison,, N. M. Hannett,, T. L. Volkert,, G. R. Fink, and, R. A. Young. 2003. Program-specific distribution of a transcription factor dependent on partner transcription factor and MAPK signaling. Cell 113: 395404.
118. Zhang, L. H., and, Y. H. Dong. 2004. Quorum sensing and signal interference: diverse implications. Mol. Microbiol. 53: 15631571.
119. Zurita-Martinez, S. A., and, M. E. Cardenas. 2005. Tor and cyclic AMP-protein kinase A: two parallel pathways regulating expression of genes required for cell growth. Eukaryot. Cell 4: 6371.

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error