Advertisement

Biochemical and Molecular Aspects of Dimorphism in Fungi

  • Ejaj K. Pathan
  • Vandana Ghormade
  • Redeemson Panmei
  • Mukund V. Deshpande
Chapter

Abstract

Most of the eukaryotic differentiation processes are unidirectional. However, fungi have the ability to grow reversibly as unicellular yeast (Y) or as filamentous hypha (H) in response to the specific strain-dependent environmental stimuli. Such a phenomenon known as “dimorphism” is not limited to a specific class of fungi. Most of the plant, human, and insect pathogenic fungi show Y-H and reversible morphogenesis, associated with their saprophytic to pathogenic change, for survival and proliferation in the host. In this chapter, we have described the factors stimulating dimorphism, the signal transduction pathways induced by these stimuli, changes in the gene/protein expression patterns due to a cascade of these signals, and, finally, translation of this genotypic effect into phenotypic change, i.e., the morphological outcome. The process of fungal differentiation and formation of tumor cells follow the same regulatory series of events, involving cAMP, MAP, and RAS kinase cascades. Therefore, the molecules inhibiting Y-H transition in fungi can be explored for their anticancer potential.

Keywords

Antifungal Dimorphic stimuli Dimorphism Hyphae Signaling Yeast cells 

Notes

Acknowledgments

MVD is grateful to CSIR, New Delhi, for the Emeritus Scientist Scheme [21(0962)/13/EMR2] and the Department of Biotechnology (DBT-BIRAC), New Delhi, for financial support.

References

  1. Amin A, Joshi M, Deshpande MV (2004) Morphology-associated expression of NADP-dependent glutamate dehydrogenases during yeast-mycelium transition of a dimorphic fungus Benjaminiella poitrasii. Ant van Leeuwenhoek 85:327–334CrossRefGoogle Scholar
  2. Andrade RV, Paes HC, Nicola AM, de Carvalho MJ, Fachin AL, Cardoso RS, Silva SS, Fernandes L, Silva SP, Donadi EA, Sakamoto-Hojo ET, Passos GA, Soares CM, Brígido MM, Felipe MS (2006) Cell organisation, sulphur metabolism and ion transport-related genes are differentially expressed in Paracoccidioides brasiliensis mycelium and yeast cells. BMC Genomics 7:208PubMedPubMedCentralCrossRefGoogle Scholar
  3. Andrews DL, Egan JD, Mayorga ME, Gold SE (2000) The Ustilago maydis ubc4 and ubc5 genes encode members of a MAP kinase cascade required for filamentous growth. Mol Plant-Microbe Interact 13:781–786PubMedCrossRefGoogle Scholar
  4. Anraku Y, Ohya Y, Lida H (1991) Cell cycle control by calcium ad calmodulin in Saccharomyces cerevisiae. Biochem Biophys Acta 1093:169–173PubMedCrossRefGoogle Scholar
  5. Aufavre-Brown A, Mellado E, Gow NAR, Holden DW (1997) Aspergillus fumigatus chsEII: a gene related to CHS3 of Saccharomyces cerevisiae and important for hyphal growth and conidiophores development but not for pathogenecity. Fungal Genet Biol 21:141–152CrossRefGoogle Scholar
  6. Bahn YS, Xue C, Idnurm A, Rutherford JC, Heitman J, Cardenas ME (2007) Sensing the environment: lessons from fungi. Nat Rev Microbiol 5:57–69PubMedCrossRefGoogle Scholar
  7. Bailey DA, Feldmann JFP, Bovey M, Gow NAR, Brown APJ (1996) The Candida albicans HYR1 gene, which is activated in response to hyphal development, belongs to a gene family encoding yeast cell wall proteins. J Bacteriol 178:5353–5360PubMedPubMedCentralCrossRefGoogle Scholar
  8. Barlow AJ, Aldersley T, Chattaway FW (1974) Factors present in serum and seminal plasma, which promote germ tube formation and mycelial growth of Candida albicans. J Gen Microbiol 82:261–272PubMedCrossRefGoogle Scholar
  9. Bartnicki-Garcia S (1963) Mold –yeast dimorphism of Mucor. Bacteriol Rev 27:293–304PubMedPubMedCentralGoogle Scholar
  10. Bartnicki-Garcia S, Nickerson WJ (1962a) Induction of yeast like development in Mucor by carbon dioxide. J Bacteriol 84:829–840PubMedPubMedCentralGoogle Scholar
  11. Bartnicki-Garcia S, Nickerson WJ (1962b) Nutrition, growth and morphogenesis of Mucor rouxii. J Bacteriol 84:841–858PubMedPubMedCentralGoogle Scholar
  12. Becht P, Vollmeister E, Feldbrügge M (2005) Role for RNA-binding proteins implicated in pathogenic development of Ustilago maydis. Eukaryot Cell 4:121–133PubMedPubMedCentralCrossRefGoogle Scholar
  13. Biswas S, Van Dijck P, Datta A (2007) Environmental sensing and signal transduction pathways regulating morphopathogenic determinants of Candida albicans. Microbiol Mol Biol Rev 71:348–376PubMedPubMedCentralCrossRefGoogle Scholar
  14. Blacketer MJ, Madaule P, Myers AM (1994) The Saccharomyces cerevisiae mutation elm4-1 facilitates pseudohyphal differentiation and interacts with a deficiency in phosphoribosyl pyrophosphate synthase activity to cause constitutive pseudohyphal growth. Mol Cell Biol 14:4671–4681PubMedPubMedCentralCrossRefGoogle Scholar
  15. Blackwell M (2011) The fungi: 1, 2, 3... 5.1 million species? Am J Bot 98:426–438PubMedPubMedCentralCrossRefGoogle Scholar
  16. Blasco JL, María A, García-Sánchez M, Ruiz-Herrera J, Eslavaa AP, Iturriaga EA (2002) A gene coding for ornithine decarboxylase (odcA) is differentially expressed during the Mucor circinelloides yeast-to-hypha transition. Res Microbiol 153:155–164PubMedCrossRefGoogle Scholar
  17. Bolker M, Genin S, Lehmier C, Kahmann R (1995) Genetic regulation of mating and dimorphism in Ustilago maydis. Can J Bot 73:320–325CrossRefGoogle Scholar
  18. Borges-Walmsley MI, Walmsley AR (2000) cAMP signalling in pathogenic fungi: control of dimorphic switching and pathogenecity. Trends Microbiol 8:133–141PubMedCrossRefGoogle Scholar
  19. Boyce KJ, Chang H, D’Souza CA, Kronstad JW (2005) An Ustilago maydis septin is required for filamentous growth in culture and for full symptom development on maize. Eukaryot Cell 4:2044–2056PubMedPubMedCentralCrossRefGoogle Scholar
  20. Brunn GJ, Williams J, Sabers C, Wiederrecht G, Lawrence JC Jr, Abraham RT (1996) Direct inhibition of the signaling functions of the mammalian target of rapamycin by the phosphoinositide 3-kinase inhibitors, wortmannin and LY 294002. EMBO J 15:5256–5267PubMedPubMedCentralCrossRefGoogle Scholar
  21. Bruno KS, Aramayo R, Minke PF, Metzenberg RL, Plamann M (1996) Loss of growth polarity and mislocalization of septa in a Neurospora mutant altered in the regulatory subunit of cAMP-dependent protein kinase. EMBO J 15:5772–5782PubMedPubMedCentralCrossRefGoogle Scholar
  22. Brunton AH, Gadd GM (1989) The effect of exogenously-supplied nucleosides and nucleotides and the involvement of adenosine 3′-5′-monophosphate (cyclic AMP) in the yeast mycelium transition of Ceratocystis (Ophistoma) ulmi. FEMS Microbiol Lett 60:49–53Google Scholar
  23. Brunton AH, Gadd GM (1991) Evidence for an inositol lipid signal pathway in the yeast-mycelium transition of Ophiostoma ulmi, the dutch elm disease fungus. Mycol Res 95:484–491CrossRefGoogle Scholar
  24. Bulawa CE, Osmond BC (1990) Chitin sunthase I and chitin synthase II are not required in vivo in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 87:7424–7428PubMedPubMedCentralCrossRefGoogle Scholar
  25. Cabib E, Drgonova J, Drgon T (1998) Role of small G proteins in yeast cell polarization and wall biosynthesis. Annu Rev Biochem 67:307–333PubMedPubMedCentralCrossRefGoogle Scholar
  26. Calvo-Mendez C, Martinez-Pacheco M, Ruiz-Herrera J (1987) Regulation of ornithine decarboxylase activity in Mucor bacilliformis and Mucor rouxii. Exp Mycol 11:270–277CrossRefGoogle Scholar
  27. Campos-Góngora E, Palande AS, León-Ramirez C, Pathan EK, Ruiz-Herrera J, Deshpande MV (2018) Determination of the effect of polyamines on an oil-degrading strain of Yarrowia lipolytica using an odc minus mutant. FEMS Yeast Res 18: foy073Google Scholar
  28. Cano-Canchola C, Sosa L, Fonzi W, Sypherd P, Ruiz-Herrera J (1992) Developmental regulation of CUP gene expression through DNA methylation in Mucor spp. J Bacteriol 174:362–366PubMedPubMedCentralCrossRefGoogle Scholar
  29. Casale WL, McConnell DG, Wang SY, Lee YJ, Linz JE (1990) Expression of a gene family in the dimorphic fungus Mucor racemosus which exhibits striking similarity to human ras genes. Mol Cell Biol 10:6654–6663PubMedPubMedCentralCrossRefGoogle Scholar
  30. Casanova M, Cervera AM, Gozalbo D, Martinez JP (1997) Hemin induces germ tube formation in Candida albicans. Infect Immun 65:4360–4364PubMedPubMedCentralGoogle Scholar
  31. Caughey WS, Smiley JD, Hellerman L (1956) L-glutamic acid dehydrogenase: structural requirements for substrate competition: effect of thyroxine. J Biol Chem 224:591–607Google Scholar
  32. Cervantes-Chávez JA, Ruiz-Herrera J (2006) STE11 disruption reveals the central role of a MAPK pathway in dimorphism and mating in Yarrowia lipolytica. FEMS Yeast Res 6:801–815PubMedCrossRefGoogle Scholar
  33. Chacko R, Deshpande MV, Shankar V (1996) Extracellular ribonuclease production by Rhizopus stolonifer: influence of metal ions. Curr Microbiol 32:246–251CrossRefGoogle Scholar
  34. Chaudhary PM, Tupe SG, Deshpande MV (2013) Chitin synthase inhibitors as antifungal agents. Min Rev Med Chem 13:222–236Google Scholar
  35. Chitnis M, Munro CA, Brown AJP, Gooday GW, Gow NAR, Deshpande MV (2002) The zygomycetous fungus, Benjaminiella poitrasii contains large family of differentially regulated chitin synthase genes. Fungal Genet Biol 36:215–223PubMedCrossRefGoogle Scholar
  36. Cho T, Hamatake H, Kaminishi H, Hagihara Y, Watanabe K (1992) The relationship between cyclic adenosine 3′-5′-monophosphate and morphology in exponential phase Candida albicans. J Med Vet Mycol 30:35–42PubMedCrossRefGoogle Scholar
  37. Chou S, Lane S, Liu H (2006) Regulation of mating and filamentation genes by two distinct Ste12 complexes in Saccharomyces cerevisiae. Mol Cell Biol 26:4794–4805PubMedPubMedCentralCrossRefGoogle Scholar
  38. Choudhury R, Punekar NS (2007) Competitive inhibition of glutamate dehydrogenase reaction. FEBS Lett 581:2733–2736PubMedCrossRefGoogle Scholar
  39. Choudhury R, Punekar NS (2009) Aspergillus terreus NADP-glutamate dehydrogenase is kinetically distinct from the allosteric enzyme of other Aspergilli. Mycol Res 113:1121–1126PubMedCrossRefGoogle Scholar
  40. Christodoulidou A, Bouriotis V, Thireos G (1996) Two sporulation-specific chitin deacetylase-encoding genes are required for the ascospore wall rigidity of Saccharomyces cerevisiae. J Biol Chem 271:31420–31425PubMedCrossRefGoogle Scholar
  41. Chung KS, Won M, Lee SB, Jang YJ, Hoe KL, Kim DU (2001) Isolation of a novel gene from Schizosaccharomyces pombe: stm1+ encoding a seven trans membrane loop protein that may couple with the heterotrimeric Galpha 2 protein, Gpa2. J Biol Chem 276:40190–40201PubMedCrossRefGoogle Scholar
  42. Cole GT, Sun SH (1985) Arthroconidium-spherule-endospore transformation in Coccidiodes immitis. In: Szaniszlo PJ (ed) Fungal dimorphism. Plenum Press, New York, pp 281–333CrossRefGoogle Scholar
  43. Cruz MC, Goldstein AL, Blankenship JR, Del Poeta M, Davis D, Cardenas ME, Perfect JR, McCusker JH, Heitman J (2002) Calcineurin is essential for survival during membrane stress in Candida albicans. EMBO J 21:546–559PubMedPubMedCentralCrossRefGoogle Scholar
  44. Csank C, Schroppel K, Leberer E, Harcus D, Mohamed O, Meloche S, Thomas DY, Whiteway M (1998) Roles of the Candida albicans mitogen-activated protein kinase homolog, Cek1p, in hyphal development and systemic candidiasis. Infect Immun 66:2713–2721PubMedPubMedCentralGoogle Scholar
  45. Cullen PJ, Sabbagh WJ, Graham E, Irick MM, van Olden EK, Neal C, Delrow J, Bardwell L, Sprague GFJ (2004) A signaling mucin at the head of the Cdc42- and MAPK-dependent filamentous growth pathway in yeast. Genes Dev 18:1695–1708PubMedPubMedCentralCrossRefGoogle Scholar
  46. Culp DW, Dodge CL, Miao YH, Li L, Sag-Ozkal D, Borgia PT (2000) The chsA gene from Aspergillus nidulans is necessary for maximal conidiation. Curr Microbiol 182:349–353Google Scholar
  47. Cunliffe D, Leason M, Parkin D, Lea P (1983) The inhibition of glutamate dehydrogenase by derivatives of isophthalic acid. Phytochemistry 22:1357–1360CrossRefGoogle Scholar
  48. Da Silva SP, Borges-Walmsley MI, Pereira IS, Soares CMDA, Walmsley AR, Felipe MSS (1999) Differential expression of an hsp70 gene during transition from the mycelial to the infective yeast form of the human pathogenic fungus Paracoccidioides brasiliensis. Mol Microbiol 31:1039–1050PubMedCrossRefGoogle Scholar
  49. Davis TR, Zucchi PC, Kumamoto CA (2013) Calmodulin binding to Dfi1p promotes invasiveness of Candida albicans. PLoS One 8:e76239PubMedPubMedCentralCrossRefGoogle Scholar
  50. de Carvalho MJ, Amorim Jesuino RS, Daher BS, Silva-Pereira I, de Freitas SM, Soares CM, Felipe MS (2003) Functional and genetic characterization of calmodulin from the dimorphic and pathogenic fungus Paracoccidioides brasiliensis. Fungal Genet Biol 39:204–210PubMedCrossRefGoogle Scholar
  51. de Oliveira JCF, Borges ACC, Marques MV, Gomes SL (1997) Cloning and characterisation of the gene for the catalytic subunit of cAMP-dependent protein kinase in the aquatic fungus Blastocladiella emersonii. Eur J Biochem 219:555–562CrossRefGoogle Scholar
  52. Dean RA (1997) Signal pathways and appressorium morphogenesis. Annu Rev Phytopathol 35:211–234PubMedCrossRefGoogle Scholar
  53. Deshpande MV (1996) The effect of morphological changes in fungal pathogenesis. Ind J Med Microbiol 14:1–9Google Scholar
  54. Deshpande MV (1998) Biochemical basis of fungal differentiation. In: Verma A (ed) Microbes: for health, wealth and sustainable environment. Malhotra Publishing House, India, pp 241–252Google Scholar
  55. Dohlman HG, Thorner JW (2001) Regulation of G protein-initiated signal transduction in yeast: paradigms and principles. Annu Rev Biochem 70:703–754PubMedCrossRefGoogle Scholar
  56. Doiphode N (2007) Dimorphism in Benjaminiella poitrasii: role of NAD-dependent glutamate dehydrogenase in yeast-hypha transition A PhD thesis submitted to University of Pune, Pune, IndiaGoogle Scholar
  57. Domer JE (1985) Blastomyces dermatitidis. In: Szaniszlo PJ (ed) Fungal dimorphism. Plenum Press, New York, pp 51–67CrossRefGoogle Scholar
  58. Elias-Villalobos A, Fernández-Álvarez A, Ibeas JI (2011) The general transcriptional repressor Tup1 is required for dimorphism and virulence in a fungal plant pathogen. PLoS Pathog 7:e1002235PubMedPubMedCentralCrossRefGoogle Scholar
  59. Feng Q, Summers E, Guo B, Fink G (1999) Ras signaling is required for serum-induced hyphal differentiation in Candida albicans. J Bacteriol 181:6339–6346PubMedPubMedCentralGoogle Scholar
  60. Fernandes L, Paes HC, Tavares AH et al (2008) Transcriptional profile of ras1 and ras2 and the potential role of farnesylation in the dimorphism of the human pathogen Paracoccidioides brasiliensis. FEMS Yeast Res 8:300PubMedCrossRefGoogle Scholar
  61. Gadd GM (1995) Signal transduction in fungi. In: Gow NAR, Gadd GM (eds) The growing fungus. Chapman and Hall, London, pp 183–210CrossRefGoogle Scholar
  62. Gancedo JM, Mazon MJ, Eraso P (1985) Biological roles for cyclic AMP: similarities and differences between organisms. Trends Biochem Sci 10:210–212CrossRefGoogle Scholar
  63. Garcia JR, Hiatt WR, Peters J, Sypherd PS (1980) S-Adenosylmethionine levels and protein methylation during morphogenesis of Mucor racemosus. J Bacteriol 142:196–201PubMedPubMedCentralGoogle Scholar
  64. Garrison RG, Boyd KS (1974) Ultrastructural studies of induced morphogenesis by Aspergillus parasiticus. J Bacteriol 154:524–528Google Scholar
  65. Geis PA, Jacobs CW (1985) Polymorphism of Wangiella dermatitidis. In: Szaniszlo PJ (ed) Fungal dimorphism: with emphasis on fungi pathogenic for humans. Plenum Press, New York, pp 205–233CrossRefGoogle Scholar
  66. Georgopapadakou NH, Walsh TJ (1994) Human mycoses: drugs and targets for emerging pathogens. Science 264:371–373PubMedCrossRefGoogle Scholar
  67. Ghormade V, Deshpande MV (2000) Fungal spore germination into yeast or mycelium: possible implications of dimorphism in evolution and human pathogenesis. Naturwissenschaften 87:236–240PubMedCrossRefGoogle Scholar
  68. Ghormade V, Joshi CV, Deshpande MV (2005) Regulation of polyamines: a possible model for signal transduction pathway leading to dimorphism in Benjaminiella poitrasii. J Mycol Pl Pathol 35:442–450Google Scholar
  69. Ghormade V, Pathan E, Deshpande MV (2012) Yeast-hypha dimorphism in zygomycetous fungi. In: Ruiz-Herrera J (ed) Dimorphic fungi: their importance as models for differentiation and fungal pathogenesis. Bentham Science Publishers, USA, pp 118–139Google Scholar
  70. Gimeno CJ, Fink GR (1994) Induction of pseudohyphal growth by over-expression of PHD1, a Saccharomyces cerevisiae gene related to transcriptional regulators of fungal development. Mol Cell Biol 14:2100–2112PubMedPubMedCentralCrossRefGoogle Scholar
  71. Gimeno CJ, Ljungdah PO, Styles CA, Fink GR (1992) Unipolar cell divisions in yeast S. cerevisiae lead to filamentous growth regulation by starvation and RAS. Cell 68:1077–1090PubMedCrossRefGoogle Scholar
  72. Gold S, Duncan G, Barrett K, Kronstad J (1994) cAMP regulates morphogenesis in the fungal pathogen Ustilago maydis. Gen Dev 8:2805–2816CrossRefGoogle Scholar
  73. Görlach J, Fox DS, Cutler NS, Cox GM, Perfect JR, Heitman J (2000) Identification and characterization of a highly conserved calcineurin binding protein, CBP1/calcipressin, in Cryptococcus neoformans. EMBO J 19:3618–3629PubMedPubMedCentralCrossRefGoogle Scholar
  74. Gow NAR (1995) Yeast-hyphal dimorphism. In: Gow NAR, Gadd GM (eds) The growing fungus. Chapman and Hall, London, pp 403–422CrossRefGoogle Scholar
  75. Gow NAR, Swoboda R, Bertram G, Gooday GW, Brown APJ (1993) In: Bossche VH (ed) Dimorphic fungi in biology and medicine. Plenum Press, New York, pp 61–712Google Scholar
  76. Gow NAR, van de Veerdonk FL, Brown APJ, Netea MG (2012) Candida albicans morphogenesis and host defence: discriminating invasion from colonization. Nat Rev Microbiol 10:112–122CrossRefGoogle Scholar
  77. Guevara-Olvera L, Calvo-Mendez C, Ruiz-Herrera J (1993) The role of polyamine metabolism in dimorphism of Yarrowia Lipolytica. Microbiology 139:485–493Google Scholar
  78. Harold FM (1995) From morphogenes to morphogenesis. Microbiology 141:2765–2778PubMedCrossRefGoogle Scholar
  79. Herrero AB, López MC, García S, Schmidt A, Spaltmann F, Ruiz-Herrera J, Dominguez A (1999) Control of filament formation in Candida albicans by polyamine levels. Infect Immun 67:4870–4878PubMedPubMedCentralGoogle Scholar
  80. Herrero AB, Magnelli P, Mansour MK, Levitz SM, Bussey H, Abeijon C (2004) KRE5 gene null mutant strains of Candida albicans are avirulent and have altered cell wall composition and hypha formation properties. Eukaryot Cell 3:1423–1432PubMedPubMedCentralCrossRefGoogle Scholar
  81. Hiramoto F, Nomura N, Furumai T, Oki T, Igarashi Y (2003) Apoptosis-like cell death of Saccharomyces cerevisiae induced by a mannose-binding antifungal antibiotic, pradimicin. J Antibiot 56:768–772PubMedCrossRefGoogle Scholar
  82. Holmes AR, Cannon RD, Shepherd MG (1991) Effect of calcium ion uptake on Candida albicans morphology. FEMS Microbiol Lett 77:187–194CrossRefGoogle Scholar
  83. Houghton-Larsen J, Pedersen PA (2003) Cloning and characterization of a glucoamylase gene (GlaM) from the dimorphic zygomycte Mucor circinelloides. Appl Microbiol Biotechnol 62:210–217PubMedCrossRefGoogle Scholar
  84. Hube B, Monod M, Schofield DA, Brown APJ, Gow NAR (1994) Expression of seven members of the gene family encoding secretory aspartyl proteinase in Candida albicans. Mol Microbiol 14:87–99PubMedCrossRefGoogle Scholar
  85. Hurtado CA, Rachubinski RA (1999) MHY1 encodes a C2H2-type zinc finger protein that promotes dimorphic transition in the yeast Yarrowia lipolytica. J Bacteriol 181:3051–3057PubMedPubMedCentralGoogle Scholar
  86. Hurtado CA, Rachubinski RA (2002) Isolation and characterization of YlBEM1, a gene required for cell polarization and differentiation in the dimorphic yeast Yarrowia lipolytica. Eukaryot Cell 1:526–537PubMedPubMedCentralCrossRefGoogle Scholar
  87. Jacobsen ID, Wilson D, Wächtler B, Brunke S, Naglik JR, Hube B (2012) Candida albicans dimorphism as a therapeutic target. Expert Rev Anti-Infect Ther 10:85–93PubMedCrossRefGoogle Scholar
  88. Jeraj N, Kunic B, Lenasi H, Breskvar K (2006) Purification and molecular characterization of chitin deacetylase from Rhizopus nigricans. Enz Microbial Technol 39:1294–1299CrossRefGoogle Scholar
  89. Johnson CH, Klotz MG, York JL, Kruft V, McEwen JE (2002) Redundancy, phylogeny and differential expression of Histoplasma capsulatum catalases. Microbiology 148:1129–1142PubMedCrossRefGoogle Scholar
  90. Johnson C, Kweon HK, Sheidy D, Shively CA, Mellacheruvu D, Nesvizhskii AI, Andrews PC, Kumar A (2014) The yeast Sks1p kinase signaling network regulates pseudohyphal growth and glucose response. PLoS Genet 10:e1004183PubMedPubMedCentralCrossRefGoogle Scholar
  91. Joshi CV, Pathan EK, Punekar NS, Tupe SG, Kapadnis BP, Deshpande MV (2013) A biochemical correlate of dimorphism in a zygomycete Benjaminiella poitrasii: characterization of purified NAD-dependent glutamate dehydrogenase, a target for antifungal agents. Antonie Van Leeuwenhoek 104:25–36PubMedCrossRefGoogle Scholar
  92. Juan-Francisco JB, Ruiz-Herrera J, Dominguez A (2001) Disruption of gene YlODC reveals absolute requirement of polyamines for mycelial development in Yarrowia lipolytica. FEMS Yeast Res 1:195–204Google Scholar
  93. Kafetzopoulos D, Thireos G, Vournakis JN, Bouriotis V (1993) The primary structure of a fungal deacetylase reveals the function for two bacterial products. Proc Natl Acad Sci U S A 90:8005–8008PubMedPubMedCentralCrossRefGoogle Scholar
  94. Karakkat BB, Gold SE, Covert SF (2013) Two members of the Ustilago maydis velvet family influence teliospore development and virulence on maize seedlings. Fungal Genet Biol 61:111–119PubMedCrossRefGoogle Scholar
  95. Kaur S, Mishra P, Prasad R (1988) Dimorphism-associated changes in amino acid transport of Candida albicans. FEMS Microbiol Lett 50:97–100CrossRefGoogle Scholar
  96. Khale A (1990) Dimorphism in fungi. A PhD thesis submitted to University of Pune, Pune, IndiaGoogle Scholar
  97. Khale A, Srinivasan MC, Deshmukh SS, Deshpande MV (1990) Dimorphism of Benjaminiella poitrasii: isolation and biochemical studies of morphological mutants. Antonie Van Leeuwenhoek 57:37–41PubMedCrossRefGoogle Scholar
  98. Khale A, Srinivasan MC, Deshpande MV (1992) Significance of NADP-/NAD- glutamate dehydrogenase ratio in the dimorphic behavior of Benjaminiella poitrasii. J Bacteriol 174:3723–3728PubMedPubMedCentralCrossRefGoogle Scholar
  99. Khale-Kumar A, Deshpande MV (1993) Possible involvement of cyclic adenosine 3′- 5′-monophosphate in the regulation of NADP-/ NAD – glutamate dehydrogenase ratio and yeast –mycelium transition of Benjaminiella poitrasii. J Bacteriol 175:6052–6055PubMedPubMedCentralCrossRefGoogle Scholar
  100. King L, Butler G (1998) Ace2p, a regulator of CTS1 (chitinase) expression, affects pseudohyphal production in Saccharomyces cerevisiae. Curr Genet 34:183–191PubMedCrossRefGoogle Scholar
  101. Köhler JR, Fink GR (1996) Candida albicans strains heterozygous and homozygous for mutations in mitogen-activated protein kinase signaling components have defects in hyphal development. Proc Natl Acad Sci U S A 93:13223–13228PubMedPubMedCentralCrossRefGoogle Scholar
  102. Kronstad J, de Maria A, Funnell D, Laidlaw RD, Lee N, de Sa MM, Ramesh M (1998) Signalling via cAMP in fungi: interconnections with mitogen-activated protein kinase pathway. Arch Microbiol 170:395–404PubMedCrossRefGoogle Scholar
  103. Kuchin S, Vyas VK, Carlson M (2002) Snf1 protein kinase and the repressors Nrg1 and Nrg2 regulate FLO11, haploid invasive growth, and diploid pseudohyphal differentiation. Mol Cell Biol 22:3994–4000PubMedPubMedCentralCrossRefGoogle Scholar
  104. Kuchin S, Vyas VK, Carlson M (2003) Role of the yeast Snf1 protein kinase in invasive growth. Biochem Soc Trans 31:175–177PubMedCrossRefGoogle Scholar
  105. Lambrechts MG, Bauer FF, Marmur J, Pretorius IS (1996) Muc1, a mucin-like protein that is regulated by Mss10, is critical for pseudohyphal differentiation in yeast. Proc Natl Acad Sci U S A 93:8419–8424PubMedPubMedCentralCrossRefGoogle Scholar
  106. Lee YH, Dean RA (1993) cAMP regulates infection structure formation in the plant pathogenic fungus. Magnaporthe grisea. Plant Cell 5:693–700PubMedPubMedCentralCrossRefGoogle Scholar
  107. Lee SC, Li A, Calo S, Inoue M, Tonthat NK, Bain JM, Louw J, Shinohara ML, Erwig LP, Schumachr MA, Ko DC, Heitman J (2015) Calcineurin orchestrates dimorphic transitions, antifungal drug responses and host–pathogen interactions of the pathogenic mucoralean fungus Mucor circinelloides. Mol Microbiol 97:844–865PubMedPubMedCentralCrossRefGoogle Scholar
  108. Lengeler KB, Davidson RC, D’Souza C, Harashima T, Shen WC, Wang P, Pan X, Waugh M, Heitman J (2000) Signal transduction cascades regulating fungal development and virulence. Microbiol Mol Biol Rev 64:746–785PubMedPubMedCentralCrossRefGoogle Scholar
  109. Li L, Wright SJ, Krystofova S, Park G, Borkovich KA (2007) Heterotrimeric G protein signaling in filamentous fungi. Annu Rev Microbiol 61:423–452PubMedCrossRefGoogle Scholar
  110. Linz JE, Katayama C, Sypherd PS (1986) Three genes for the elongation factor EF-lα in Mucor racemosus. Mol Cell Biol 6:593–600PubMedPubMedCentralCrossRefGoogle Scholar
  111. Litcher A, Mills D (1997) Fill, a G-protein alpha-subunit that acts upstream of cAMP and is essential for dimorphic switching in haploid cells of Ustilago hordei. Mol Gen Genet 256:426–435CrossRefGoogle Scholar
  112. Liu H, Kohler J, Fink GR (1994) Suppression of hyphal formation in Candida albicans by mutation of a STE12 homolog. Science 266:1723–1736PubMedCrossRefGoogle Scholar
  113. Lo WS, Dranginis AM (1998) The cell surface flocculin Flo11 is required for pseudohyphae formation and invasion by Saccharomyces cerevisiae. Mol Biol Cell 9:161–171PubMedPubMedCentralCrossRefGoogle Scholar
  114. Lorenz MC, Heitman J (1997) Yeast pseudohyphal growth is regulated by GPA2, a G protein alpha homolog. EMBO J 16:7008–7018PubMedPubMedCentralCrossRefGoogle Scholar
  115. Lorenz MC, Pan X, Harashima T, Cardenas ME, Xue Y, Hirsch JP, Heitman J (2000) The G protein coupled receptor gpr1 is a nutrient sensor that regulates pseudohyphal differentiation in Saccharomyces cerevisiae. Genetics 154:609–622PubMedPubMedCentralGoogle Scholar
  116. Madeo F, Herker E, Maldener C, Wissing S, Lächelt S, Herlan M, Fehr M, Lauber K, Sigrist SJ, Wesselborg S, Fröhlich KU (2002) A caspase-related protease regulates apoptosis in yeast. Mol Cell 9:911–917PubMedCrossRefGoogle Scholar
  117. Madzak C, Blanchin-Roland S, Cordero-Otero RR, Gaillardin C (1999) Functional analysis of upstream regulating regions from the Yarrowia lipolytica XPR2 promoter. Microbiology 145:75–87PubMedCrossRefGoogle Scholar
  118. Maeda T, Watanabe Y, Kunitomo H, Yamamoto M (1994) Cloning of pka1 gene encoding the catalytic subunit of the cAMP-dependent protein kinase in Schizosaccharomyces pombe. J Biol Chem 269:9632–9637PubMedGoogle Scholar
  119. Magee PT (1997) Which came first, the hypha or the yeast? Science 277:52–53PubMedCrossRefGoogle Scholar
  120. Maidan MM, Thevelein JM, Van Dijck P (2005) 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 33:291–293PubMedCrossRefGoogle Scholar
  121. Malathi K, Ganesan K, Datta A (1994) Identification of a putative transcription factor in Candida albicans that can complement the mating defect of Saccharomyces cerevisiae ste12 mutants. J Biol Chem 269:22945–22951PubMedGoogle Scholar
  122. Maresca B, Kobayashi GS (1989) Dimorphism in Histoplasma capsulatum: a model for the study of cell differentiation in pathogenic fungi. Microbiol Mol Biol Rev 53:186–209Google Scholar
  123. Maresca B, Kobayashi GS (2000) Dimorphism in Histoplasma capsulatum and Blastomyces dermatitidis. Contrib Microbiol 5:201–216PubMedCrossRefGoogle Scholar
  124. Martinez-Espinoza AD, Ruiz-Herrera J, Leon Ramirez CG, Gold SE (2004) MAP kinase and cAMP signaling pathways modulate the pH- induced yeast to mycelium dimorphic transition in the corn smut fungus Ustilago maydis. Curr Microbiol 49:274–281PubMedCrossRefGoogle Scholar
  125. Mattia E, Carruba G, Angiolella L, Cassone A (1982) Induction of germ tube formation by N-acetyl-D-glucosamine in Candida albicans: uptake of inducer and germinative response. J Bacteriol 152:555–562PubMedPubMedCentralGoogle Scholar
  126. Maw T, Tan TK, Khor E, Wong SM (2002) Complete cDNA sequence of chitin deacetylase from Gongronella butleri and its phylogenetic analysis revealed clusters corresponding to taxonomic classification of fungi. J Biosci Bioeng 93:376–381PubMedCrossRefGoogle Scholar
  127. Mayorga ME, Gold SE (1999) A MAP kinase encoded by the ubc3 gene of Ustilago maydis is required for filamentous growth and full virulence. Mol Microbiol 34:485–449PubMedCrossRefGoogle Scholar
  128. McCreath KJ, Specht CA, Robbins PW (1995) Molecular cloning and characterization of chitinase genes from Candida albicans. Proc Natl Acad Sci U S A 92:2544–2548PubMedPubMedCentralCrossRefGoogle Scholar
  129. Medoff G, Kobayashi GS, Painter A, Travis S (1987) Morphogenesis and pathogenecity of Histoplasma capsulatum. Infect Immun 55:1355–1358PubMedPubMedCentralGoogle Scholar
  130. Miles S, Li L, Davison J, Breeden LL (2013) Xbp1 directs global repression of budding yeast transcription during the transition to quiescence and is important for the longevity and reversibility of the quiescent state. PLoS Genet 9:e1003854PubMedPubMedCentralCrossRefGoogle Scholar
  131. Mio T, Yabe T, Sudoh M, Satoh Y, Nakajima T, Arisawa M, Yamada-Okabe H (1996) Role of three chitin synthase genes in the growth of Candida albicans. J Bacteriol 178:2416–2419PubMedPubMedCentralCrossRefGoogle Scholar
  132. Mishra C, Semino C, Mckreath K, De La Vega H, Jones BJ, Specht CA, Robbins P (1997) Cloning and expression of two chitin deacetylase genes of Saccharomyces cerevisiae. Yeast 13:327–336PubMedCrossRefGoogle Scholar
  133. Munro CA, Winter K, Buchan A, Henry K, Becker JM, Brown AJ, Bulawa CE, Gow NAR (2001) Chs1 of Candida albicans is an essential chitin synthase required for synthesis of the septum and cell integrity. Mol Microbiol 39:1414–1426PubMedCrossRefGoogle Scholar
  134. Muthukumar G, Nickerson KW (1984) Ca(II)- calmodulin regulation of fungal dimorphism in Ceratocystis ulmi. J Bacteriol 159:390–392PubMedPubMedCentralGoogle Scholar
  135. Muthukumar G, Nickerson AW, Nickerson KW (1987) Calmodulin levels in yeasts and filamentous fungi. FEMS Microbiol Lett 41:253–255CrossRefGoogle Scholar
  136. Naglik JR, Challacombe SJ, Hube B (2003) Candida albicans secreted aspartyl proteinases in virulence and pathogenesis. Microbiol Mol Biol Rev 67:400–428PubMedPubMedCentralCrossRefGoogle Scholar
  137. Nagy G, Farkas A, Csernetics Á, Bencsik O, Szekeres A, Nyilasi I, Vágvölgyi C, Papp T (2014) Transcription of the three HMG-CoA reductase genes of Mucor circinelloides. BMC Microbiol 14:93PubMedPubMedCentralCrossRefGoogle Scholar
  138. Nantel A, Dignard D, Bachewich C, Harcus D, Marcil A, Bouin A, Sensen CW, Hogues H, Hoog M, Gordon P, Rigby T, Benoit F, Tessier DC, Thomas DY, Whiteway M (2002) Transcription profiling of Candida albicans cells undergoing the yeast-to-hyphal transition. Mol Biol Cell 13:3452–3465PubMedPubMedCentralCrossRefGoogle Scholar
  139. Niimi M (1996) Dibutyryl cyclic AMP-enhanced germ tube formation in exponentially growing Candida albicans cells. Fungal Genet Biol 20:79–83PubMedCrossRefGoogle Scholar
  140. Niimi M, Niimi K, Cannon RD (1997) Temperature-related expression of the vacuolar aspartic proteinase (APR1) gene and beta-N-acetylglucosaminidase (HEX1) gene during Candida albicans morphogenesis. FEMS Microbiol Lett 148:247–254PubMedCrossRefGoogle Scholar
  141. Noor S, Punekar NS (2005) Allosteric NADP-glutamate dehydrogenase from Aspergilli: purification, characterization and implications for metabolic regulation at the carbon-nitrogen interface. Microbiology 151:1409–1419PubMedCrossRefGoogle Scholar
  142. Ocampo J, McCormack B, Navarro E, Moreno S, Garre V, Rossi S (2012) Protein kinase a regulatory subunit isoforms regulate growth and differentiation in Mucor circinelloides: essential role of PKAR4. Eukaryot Cell 11:989–1002PubMedPubMedCentralCrossRefGoogle Scholar
  143. Odds FC (1988) Candida and candidosis. Balliere Tindall, LondonGoogle Scholar
  144. Orlowski M (1991) Mucor dimorphism. Microbiol Rev 55:234–258PubMedPubMedCentralGoogle Scholar
  145. Palande AS, Kulkarni SV, León-Ramirez C, Campos-Góngora E, Ruiz-Herrera J, Deshpande MV (2014) Dimorphism and hydrocarbon metabolism in Yarrowia lipolytica var. indica. Arch Microbiol 196:545–556PubMedCrossRefGoogle Scholar
  146. Paranjpe V, Gupta-Roy B, Datta A (1990) Involvement of calcium, calmodulin and protein phosphorylation in morphogenesis of Candia albicans. J Bacteriol 154:524–528Google Scholar
  147. Park JH, Kim H, Kim SH (2018) Azole antifungal drugs induce cell death by suppressing mTOR through PI3K/Akt inhibition in human breast cancer. In: proceedings of the American Association for Cancer Research annual meeting. Chicago, ILGoogle Scholar
  148. Pathan EK (2017) Molecular characterization of NAD- and NADP-dependent glutamate dehydrogenases to understand their cause-effect relationship in dimorphic zygomycete Benjaminiella poitrasii and its evaluation as an antifungal target. A PhD thesis submitted to Academy of Scientific and Innovative Research (AcSIR), New Delhi, IndiaGoogle Scholar
  149. Pathan EK, Ghormade V, Deshpande MV (2017) Selection of reference genes for quantitative real-time RT-PCR assays in different morphological forms of dimorphic zygomycetous fungus Benjaminiella poitrasii. PLoS One 12:e0179454PubMedPubMedCentralCrossRefGoogle Scholar
  150. Phillips AJ, Sudbery I, Ramsdale M (2003) Apoptosis induced by environmental stresses and amphotericin B in Candida albicans. Proc Natl Acad Sci U S A 100:14327–14332PubMedPubMedCentralCrossRefGoogle Scholar
  151. Pillonel C (2005) Evaluation of phenylaminopyrimidines as antifungal protein kinase inhibitors. Pest Manag Sci 61:1069–1076PubMedCrossRefGoogle Scholar
  152. Pine L, Peacock CL (1958) Studies on the growth of Histoplasma capsulatum. IV. Factors influencing conversion of the mycelium phase to the yeast phase. J Bacteriol 75:167–174PubMedPubMedCentralGoogle Scholar
  153. Ramon AM, Porta A, Fonzi WA (1999) Effect of environmental pH on morphological development of Candida albicans is mediated via the PacC-related transcription factor encoded by PRR2. J Bacteriol 181:7524–7530PubMedPubMedCentralGoogle Scholar
  154. Rangel-Porras RA, Meza-Carmen V, Martinez-Cadena G, Torres-Guzmán JC, González-Hernández GA, Arnau J, Gutiérrez-Corona JF (2005) Molecular analysis of an NAD-dependent alcohol dehydrogenase from the zygomycete Mucor circinelloides. Mol Gen Genomics 274:354–363CrossRefGoogle Scholar
  155. Richard M, Quijano RR, Bezzate S, Bordon-Pallier F, Gaillardin C (2001) Tagging morphogenetic genes by insertional mutagenesis in the yeast Yarrowia lipolytica. J Bacteriol 183:3098–3107PubMedPubMedCentralCrossRefGoogle Scholar
  156. Richardson CM, Williamson DS, Parratt MJ, Borgognoni J, Cansfield AD, Dokurno P, Francis GL, Howes R, Moore JD, Murray JB, Robertson A, Surgenor AE, Torrance CJ (2006) Triazolo[1,5- a]pyrimidines as novel CDK2 inhibitors: protein structure guided design and SAR. Bioorg Medl Chem Lett 16:1353–1357CrossRefGoogle Scholar
  157. Rivera-Rodriguez N, Rodriguez-del Valle N (1992) Effects of calcium ions on the germination of Sporothrix schenckii conidia. J Med Vet Mycol 30:185–195PubMedCrossRefGoogle Scholar
  158. Robson GD, Weibe MG, Trinci APJ (1991) Exogenous cAMP and cGMP modulate branching in Fusarium graminearum. J Bacteriol 154:524–528Google Scholar
  159. Rodriguez-Caban J, Gonzalez-Velazquez W, Perez-Sanchez L, Gonzalez-Mendez R, Rodriguez-del Valle N (2011) Calcium/calmodulin kinase1 and its relation to thermotolerance and HSP90 in Sporothrix schenckii: an RNAi and yeast two-hybrid study. BMC Microbiol 11:162PubMedPubMedCentralCrossRefGoogle Scholar
  160. Rogers KS (1971) Molecular interaction of competitive inhibitors with bovine liver glutamate dehydrogenase. J Biol Chem 246:2004–2009PubMedGoogle Scholar
  161. Rogers KS, Boots MR, Boots SG (1972) Molecular interaction of six aromatic competitive inhibitors with bovine liver glutamate dehydrogenase. Biochim Biophys Acta 258:343–350PubMedCrossRefGoogle Scholar
  162. Ruiz-Herrera J (1994) Polyamines, DNA methylation and fungal differentiation. Crit Rev Microbiol 20:143–150CrossRefGoogle Scholar
  163. Ruiz-Herrera J, Martinez-Espinoza AD (1998) The fungus Ustilago maydis, from the Aztec cuisine to the research laboratory. Int J Microbiol 1:149–158Google Scholar
  164. Ruiz-Herrera J, Sentrandreu R (2002) Different effectors of dimorphism in Yarrowia lipolytica. Arch Microbiol 178:477–483PubMedCrossRefGoogle Scholar
  165. Ruiz-Herrera J, Ruiz A, Lopez-Romero E (1983) Isolation and biochemical analysis of Mucor bacilliformis monomorphic mutants. J Bacteriol 156:264–272PubMedPubMedCentralGoogle Scholar
  166. Ruiz-Herrera J, Leon CG, Guevera-Olvera L, Carabez-Trejo A (1995) Yeast-mycelial dimorphism of haploid and diploid strains of Ustilago maydis in liquid culture. Microbiol. 141:695–703CrossRefGoogle Scholar
  167. Ryan O, Shapiro RS, Kurat CF, Mayhew D, Baryshnikova A, Chin B, Lin ZY, Cox MJ, Vizeacoumar F, Cheung D, Bahr S, Tsui K, Tebbji F, Sellam A, Istel F, Schwarzmüller T, Reynolds TB, Kuchler K, Gifford DK, Whiteway M, Giaever G, Nislow C, Costanzo M, Gingras AC, Mitra RD, Andrews B, Fink GR, Cowen LE, Boone C (2012) Global gene deletion analysis exploring yeast filamentous growth. Science 337:1353–1356PubMedCrossRefGoogle Scholar
  168. Ryley JF, Ryley NG (1990) Candida albicans: do mycelia matter? J Med Vet Mycol 28:225–239PubMedCrossRefGoogle Scholar
  169. Sabie FT, Gadd GM (1990) Effect of zinc on the yeast mycelium transition of Candida albicans and examination of zinc uptake at different stages of growth. Mycol Res 94:952–958CrossRefGoogle Scholar
  170. San-Blas F, San-Blas G (1985) Paracoccidioides brasiliensis. In: Szaniszlo PJ (ed) Fungal dimorphism. Plenum Press, New York, pp 93–120CrossRefGoogle Scholar
  171. Saudohar M, Bencina M, van de Vondervoort PJ, Panneman H, Legisa M, Visser J, Ruijter GJ (2002) Cyclic AMP-dependent protein kinase is involved in morphogenesis of Aspergillus niger. Microbiol. 148:2635–2645CrossRefGoogle Scholar
  172. Schulz BE, Kraepelin G, Hinkel-Mann W (1974) Factors affecting dimorphism in Mycotypha (Mucorales): correlation with the fermentation /respiration equilibrium. J Gen Microbiol 82:1–13PubMedCrossRefGoogle Scholar
  173. Sebghati TS, Engle JT, Goldman WE (2000) Intracellular parasitism by Histoplasma capsulatum: fungal virulence and calcium dependence. Science 290:1368–1372PubMedCrossRefGoogle Scholar
  174. Seike T, Nakamura T, Shimoda C (2013) Distal and proximal actions of peptide pheromone M-factor control different conjugation steps in fission yeast. PLoS One 8:e69491PubMedPubMedCentralCrossRefGoogle Scholar
  175. Sentandreu M, Elorza MV, Sentandreu R, Fonzi WA (1998) Cloning and characterization of PRA1, a gene encoding a novel pH-regulated antigen of Candida albicans. J Bacteriol 180:282–289PubMedPubMedCentralGoogle Scholar
  176. Shapiro RS, Robbins N, Cowen LE (2007) Regulatory circuitry governing fungal development, drug resistance, and disease. Microbiol Mol Biol Rev 75:213–267CrossRefGoogle Scholar
  177. Shepherd MG, Yin YC, Ram SP, Sullivan PA (1980) Germ tube induction in Candida albicans. Can J Microbiol 26:21–26PubMedCrossRefGoogle Scholar
  178. Silverman SJ, Sburlati A, Slater ML, Cabib E (1988) Chitin synthetase is essential for septum formation and cell division in Saccaharomyces ceevisiae. Proc Natl Acad Sci U S A 87:7424–7428Google Scholar
  179. Soares DA, Oliveira MB, Evangelista AF, Venancio EJ, Andrade RV, Felipe MS, Petrofeza S (2013) Phospholipase gene expression during Paracoccidioides brasiliensis morphological transition and infection. Mem Inst Oswaldo Cruz 108:808–811PubMedPubMedCentralCrossRefGoogle Scholar
  180. Soberanes-Gutiérrez CV, Juárez-Montiel M, Olguín-Rodríguez O, Hernández-Rodríguez C, Ruiz-Herrera J, Villa-Tanaca L (2015) The pep4 gene encoding proteinase A is involved in dimorphism and pathogenesis of Ustilago maydis. Mol Plant Pathol 16:837–846PubMedPubMedCentralCrossRefGoogle Scholar
  181. Steinbach WJ, Cramer RA Jr, Perfect BZ, Asfaw YG, Sauer TC, Najvar LK, Kirkpatrick WR, Patterson TF, Benjamin DK Jr, Heitman J, Perfect JR (2006) Calcineurin controls growth, morphology, and pathogenicity in Aspergillus fumigatus. Eukaryot Cell 5:1091–1103PubMedPubMedCentralCrossRefGoogle Scholar
  182. Steinbach WJ, Reedy JL, Cramer RA Jr, Perfect JR, Heitman J (2007) Harnessing calcineurin as a novel anti-infective agent against invasive fungal infections. Nat Rev Microbiol 5:418–430PubMedCrossRefGoogle Scholar
  183. Stevens L, Duncan D, Robertson P (1989) Purification and characterization of NAD-glutamate dehydrogenase from Aspergillus nidulans. FEMS Microbiol Lett 48:173–178PubMedCrossRefGoogle Scholar
  184. Stewart E, Gow NAR, Bowen DV (1988) Cytoplasmic alkalinization during germ tube formation in Candida albicans. J Gen Microbiol 134:1079–1087PubMedGoogle Scholar
  185. Stoldt VR, Sonneborn A, Leuker CE, Ernst JF (1997) Efg1p, an essential regulator of morphogenesis of the human pathogen Candida albicans, is a member of a conserved class of bHLH proteins regulating morphogenetic processes in fungi. EMBO J 16:1982–1991PubMedPubMedCentralCrossRefGoogle Scholar
  186. Sudoh M, Tatsuno K, Ono N, Ohta A, Chibana H, YamadaOkabe H, Arisawa M (1999) The Candida albicans CHS4 gene complements a Saccharomyces cerevisiae skt5/chs4 mutation and is involved in chitin biosynthesis. Microbiology 145:1613–1622PubMedCrossRefGoogle Scholar
  187. Sypherd PS, Borgia PT, Paznokas JL (1978) Biochemistry of dimorphism in the fungus Mucor. Adv Microb Physiol 18:67–104PubMedCrossRefGoogle Scholar
  188. Szabo R, Stofanikova V (2002) Presence of organic sources of nitrogen is critical for filament formation and pH-dependent morphogenesis in Yarrowia lipolytica. FEMS Microbiol Lett 206:45–50PubMedCrossRefGoogle Scholar
  189. Tabor CW, Tabor H (1985) Polyamines in microorganisms. Microbiol Rev 49:81–99PubMedPubMedCentralGoogle Scholar
  190. Tani Y, Yamada Y, Kamihara T (1979) Morphological change in Candida tropicalis pK 233 caused by ethanol and its prevention by myo-inositol. Biochem Biophys Res Commun 91:351–355PubMedCrossRefGoogle Scholar
  191. Terenzi HF, Flawia MM, Tellenzinon MT, Tores HN (1976) The control of Neurospora crassa morphology by cyclic adenosine 3′, 5′- monophosphate and dibutyryl cyclic adenosine 3′, 5′-monophosphate. J Bacteriol 154:524–528Google Scholar
  192. Thykaer J, Rueksomtawin K, Noorman H, Nielsen J (2009) Disruption of the NADPH-dependent glutamate dehydrogenase affects the morphology of two industrial strains of Penicillium chrysogenum. J Biotechnol 139:280–282PubMedCrossRefGoogle Scholar
  193. Tian X, Shearer G Jr (2002) The mold specific MS8 gene is required for normal hypha formation in the dimorphic pathogenic fungus Histoplasma capsulatum. Eukaryot Cell 1:249–256PubMedPubMedCentralCrossRefGoogle Scholar
  194. Travassos LR (1985) Sporothrix schenckii. In: Szaniszlo PJ (ed) Fungal dimorphism. Plenum Press, New York, pp 121–163CrossRefGoogle Scholar
  195. Tupe SG, Kulkarni RR, Shirazi F, Sant DG, Joshi SP, Deshpande MV (2015) Possible mechanism of antifungal phenazine-1-carboxamide from Pseudomonas sp. against dimorphic fungi Benjaminiella poitrasii and human pathogen Candida albicans. J Appl Microbiol 118:39–48PubMedCrossRefGoogle Scholar
  196. Valle-Maldonado MI, Jacome-Galarza IE, Gutierrez-Corona F, Ramirez-Diaz MI, Campos-Garcia J, Meza-Carmen V (2015) Selection of reference genes for quantitative real-time RT-PCR during dimorphism in zygomycete Mucor circinelloides. Mol Biol Rep 42:705–711PubMedCrossRefGoogle Scholar
  197. Veronese FM, Nyc JF, Degani Y, Brown DM, Smith EL (1974) Nicotinamide adenine dinucleotide-specific glutamate dehydrogenase of Neurospora: purification and molecular properties. J Biol Chem 249:7922–7928PubMedGoogle Scholar
  198. Villalobos-Duno H, San-Blas G, Paulinkevicius M, Sánchez-Martín Y, Nino-Vega G (2013) Biochemical characterization of Paracoccidioides brasiliensis α-1,3-glucanase Agn1p, and its functionality by heterologous expression in Schizosaccharomyces pombe. PLoS One 8:e66853PubMedPubMedCentralCrossRefGoogle Scholar
  199. Wang P, Heitman J (1999) Signal transduction cascades regulating mating, filamentation and virulence in Cryptococcus neoformans. Curr Opin Microbiol 2:358–362PubMedCrossRefGoogle Scholar
  200. Wang LC, Montalvo-Munoz F, Tsai YC, Liang CY, Chang CC, Lo WS (2015) The histone acetyltransferase Gcn5 regulates ncRNA-ICR1 and FLO11 expression during pseudohyphal development in Saccharomyces cerevisiae. Biomed Res Int 2015:284692PubMedPubMedCentralGoogle Scholar
  201. Webster RH, Sil A (2008) Conserved factors Ryp2 and Ryp3 control cell morphology and infectious spore formation in the fungal pathogen Histoplasma capsulatum. Proc Natl Acad Sci U S A 105:14573–14578PubMedPubMedCentralCrossRefGoogle Scholar
  202. Wolff A, Appel K, Petersen J, Poulsen U, Arnau J, Jacobsen M (2002) Recombinant dimorphic fungal cell. WO/2002/070721Google Scholar
  203. Xu JR, Hamer JE (1996) MAP kinase and cAMP signaling regulate infection structure formation and pathogenic growth in the rice blast fungus Magnaporthe grisea. Genes Dev 10:2696–2706PubMedCrossRefGoogle Scholar
  204. Xue C, Bahn YS, Cox GM, Heitman J (2006) G protein-coupled receptor Gpr4 senses amino acids and activates the cAMP-PKA pathway in Cryptococcus neoformans. Mol Biol Cell 17:667–679PubMedPubMedCentralCrossRefGoogle Scholar
  205. Ying S, Feng M, Keyhani NO (2013) B. bassiana G-protein coupled receptor. Environ Microbiol 15:2902–2921PubMedGoogle Scholar
  206. Zacchi LF, Gomez-Raja J, Davis DA (2010) Mds3 regulates morphogenesis in Candida albicans through the TOR pathway. Mol Cell Biol 30:3695–3710PubMedPubMedCentralCrossRefGoogle Scholar
  207. Zhao X, Kim Y, Park G, Xu JR (2005) A mitogen-activated protein kinase cascade regulating infection-related morphogenesis in Magnaporthe grisea. Plant Cell 17:1317–1329PubMedPubMedCentralCrossRefGoogle Scholar
  208. Zinjarde SS, Pant A, Deshpande MV (1998) Dimorphic transition in Yarrowia lipolytica from oil polluted seawater. Mycol Res 102:553–558CrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  • Ejaj K. Pathan
    • 1
  • Vandana Ghormade
    • 2
  • Redeemson Panmei
    • 1
  • Mukund V. Deshpande
    • 3
  1. 1.Biochemical Sciences DivisionCSIR-National Chemical LaboratoryPuneIndia
  2. 2.NanobioscienceAgharkar Research InstitutePuneIndia
  3. 3.Division of Biological SciencesCSIR-National Chemical LaboratoryPuneIndia

Personalised recommendations