Advertisement

Developmental Decisions in Aspergillus nidulans

  • Hee-Soo Park
  • Mi-Kyung Lee
  • Kap-Hoon Han
  • Min-Ju Kim
  • Jae-Hyuk YuEmail author
Chapter
Part of the The Mycota book series (MYCOTA, volume 8)

Abstract

The filamentous fungi (fungi) comprise a universal group of heterotrophic eukaryotic microorganisms living as saprophytes, parasites, or symbionts. Throughout the life cycle, in response to the various external and internal cues, fungi constantly make a decision between vegetative growth and (morphological and chemical) development. The basis for fungal vegetative growth is the continued and coordinated expansion of a series of fungal cell tips into a linear or complex structure. When conditions are met, fungi differentiate into a variety of structures including asexual and sexual spores, which are the effective means of genome protection, survival, and propagation. Spores are also the primary means for infecting host organisms for many human and plant pathogenic fungi. Among fungi, the genus Aspergillus represents the most widespread species in our environment that all reproduce asexually by forming long chains of conidiospores (or conidia) radiating from a central structure known as a conidiophore. The genetic model fungus Aspergillus nidulans has served as an excellent system for studying various biological questions, primarily due to the ease of genetic analysis through meiotic (sexual) recombination and the development of sophisticated molecular tools. These properties have provided a better understanding of the mechanisms controlling growth, development, secondary metabolism, and other aspects of cell biology in fungi. Here, we summarize our current understanding of the mechanisms of making asexual and sexual developmental decision in A. nidulans and present simple models.

Keywords

Development Competence Conidiation Sexual fruiting Cleistothecia Aspergillus nidulans 

Notes

Acknowledgments

The work by HSP and MJK was supported by the National Research Foundation of Korea (NRF) grant to HSP funded by the Korean government (MSIP: No. 2016010945). The work by KHH was supported by the Intelligent Synthetic Biology Center of Global Frontier Projects (2015M3A6A8065838) and by Basic Science Research Program through NRF (NRF-2017R1D1A3B06035312) funded by Korean government. The work by MKL and JHY was supported by the Intelligent Synthetic Biology Center of Global Frontier Project (2011-0031955) funded by the Ministry of Education, Science and Technology grants.

References

  1. Adams TH, Boylan MT, Timberlake WE (1988) brlA is necessary and sufficient to direct conidiophore development in Aspergillus nidulans. Cell 54:353–362PubMedCrossRefGoogle Scholar
  2. Adams TH, Deising H, Timberlake WE (1990) brlA requires both zinc fingers to induce development. Mol Cell Biol 10:1815–1817PubMedPubMedCentralCrossRefGoogle Scholar
  3. Adams TH, Wieser JK, Yu J-H (1998) Asexual sporulation in Aspergillus nidulans. Microbiol Mol Biol Rev 62:35–54PubMedPubMedCentralGoogle Scholar
  4. Aguirre J (1993) Spatial and temporal controls of the Aspergillus brlA developmental regulatory gene. Mol Microbiol 8:211–218PubMedCrossRefGoogle Scholar
  5. Aguirre J, Adams TH, Timberlake WE (1990) Spatial control of developmental regulatory genes in Aspergillus nidulans. Exp Mycol 14:290–293CrossRefGoogle Scholar
  6. Ahmed YL, Gerke J, Park H-S, Bayram O, Neumann P, Ni M, Dickmanns A, Kim SC, Yu J-H, Braus GH et al (2013) The velvet family of fungal regulators contains a DNA-binding domain structurally similar to NF-κB. PLoS Biol 11:e1001750PubMedPubMedCentralCrossRefGoogle Scholar
  7. Alkahyyat F, Ni M, Kim SC, Yu JH (2015) The WOPR domain protein OsaA orchestrates development in Aspergillus nidulans. PLoS One 10:e0137554PubMedPubMedCentralCrossRefGoogle Scholar
  8. Andrianopoulos A, Timberlake WE (1991) ATTS, a new and conserved DNA binding domain. Plant Cell 3:747–748PubMedPubMedCentralCrossRefGoogle Scholar
  9. Andrianopoulos A, Timberlake WE (1994) The Aspergillus nidulans abaA gene encodes a transcriptional activator that acts as a genetic switch to control development. Mol Cell Biol 14:2503–2515PubMedPubMedCentralCrossRefGoogle Scholar
  10. Aramayo R, Timberlake WE (1993) The Aspergillus nidulans yA gene is regulated by abaA. EMBO J 12:2039–2048PubMedPubMedCentralCrossRefGoogle Scholar
  11. Archer DB, Dyer PS (2004) From genomics to post-genomics in Aspergillus. Curr Opin Microbiol 7:499–504PubMedCrossRefGoogle Scholar
  12. Arratia-Quijada J, Sanchez O, Scazzocchio C, Aguirre J (2012) FlbD, a Myb transcription factor of Aspergillus nidulans, is uniquely involved in both asexual and sexual differentiation. Eukaryot Cell 11:1132–1142PubMedPubMedCentralCrossRefGoogle Scholar
  13. Atoui A, Bao D, Kaur N, Grayburn WS, Calvo AM (2008) Aspergillus nidulans natural product biosynthesis is regulated by mpkB, a putative pheromone response mitogen-activated protein kinase. Appl Environ Microbiol 74:3596–3600PubMedPubMedCentralCrossRefGoogle Scholar
  14. Atoui A, Kastner C, Larey CM, Thokala R, Etxebeste O, Espeso EA, Fischer R, Calvo AM (2010) Cross-talk between light and glucose regulation controls toxin production and morphogenesis in Aspergillus nidulans. Fungal Genet Biol 47:962–972PubMedPubMedCentralCrossRefGoogle Scholar
  15. Axelrod DE, Gealt M, Pastushok M (1973) Gene control of developmental competence in Aspergillus nidulans. Dev Biol 34:9–15PubMedCrossRefGoogle Scholar
  16. Bahn YS, Xue CY, Idnurm A, Rutherford JC, Heitman J, Cardenas ME (2007) Sensing the environment: lessons from fungi. Nat Rev Microbiol 5:57–69PubMedCrossRefGoogle Scholar
  17. Bayram O, Braus GH (2012) Coordination of secondary metabolism and development in fungi: the velvet family of regulatory proteins. FEMS Microbiol Rev 36:1–24PubMedCrossRefGoogle Scholar
  18. Bayram O, Krappmann S, Ni M, Bok JW, Helmstaedt K, Valerius O, Braus-Stromeyer S, Kwon N-J, Keller NP, Yu J-H et al (2008) VelB/VeA/LaeA complex coordinates light signal with fungal development and secondary metabolism. Science 320:1504–1506PubMedCrossRefGoogle Scholar
  19. Bayram O, Braus GH, Fischer R, Rodriguez-Romero J (2010) Spotlight on Aspergillus nidulans photosensory systems. Fungal Genet Biol 47:900–908PubMedCrossRefGoogle Scholar
  20. Bayram O, Bayram OS, Ahmed YL, Maruyama J, Valerius O, Rizzoli SO, Ficner R, Irniger S, Braus GH (2012) The Aspergillus nidulans MAPK module AnSte11-Ste50-Ste7-Fus3 controls development and secondary metabolism. PLoS Genet 8:e1002816PubMedPubMedCentralCrossRefGoogle Scholar
  21. Bayram O, Feussner K, Dumkow M, Herrfurth C, Feussner I, Braus GH (2016) Changes of global gene expression and secondary metabolite accumulation during light-dependent Aspergillus nidulans development. Fungal Genet Biol 87:30–53PubMedCrossRefGoogle Scholar
  22. Bennett JW, Fernholz FA, Lee LS (1978) Effect of light on aflatoxins, anthraquinones, and sclerotia in Aspergillus flavus and A. parasiticus. Mycologia 70:104–116PubMedCrossRefGoogle Scholar
  23. Blumenstein A, Vienken K, Tasler R, Purschwitz J, Veith D, Frankenberg-Dinkel N, Fischer R (2005) The Aspergillus nidulans phytochrome FphA represses sexual development in red light. Curr Biol 15:1833–1838PubMedCrossRefGoogle Scholar
  24. Boylan MT, Mirabito PM, Willett CE, Zimmerman CR, Timberlake WE (1987) Isolation and physical characterization of three essential conidiation genes from Aspergillus nidulans. Mol Cell Biol 7:3113–3118PubMedPubMedCentralCrossRefGoogle Scholar
  25. Braus GH, Irniger S, Bayram O (2010) Fungal development and the COP9 signalosome. Curr Opin Microbiol 13:672–676PubMedCrossRefGoogle Scholar
  26. Brodhun F, Feussner I (2011) Oxylipins in fungi. FEBS J 278:1047–1063PubMedCrossRefGoogle Scholar
  27. Busby TM, Miller KY, Miller BL (1996) Suppression and enhancement of the Aspergillus nidulans medusa mutation by altered dosage of the bristle and stunted genes. Genetics 143:155–163PubMedPubMedCentralGoogle Scholar
  28. Busch S, Eckert SE, Krappmann S, Braus GH (2003) The COP9 signalosome is an essential regulator of development in the filamentous fungus Aspergillus nidulans. Mol Microbiol 49:717–730PubMedCrossRefGoogle Scholar
  29. Busch S, Schwier EU, Nahlik K, Bayram O, Helmstaedt K, Draht OW, Krappmann S, Valerius O, Lipscomb WN, Braus GH (2007) An eight-subunit COP9 signalosome with an intact JAMM motif is required for fungal fruit body formation. Proc Natl Acad Sci U S A 104:8089–8094PubMedPubMedCentralCrossRefGoogle Scholar
  30. Calvo AM, Bok J, Brooks W, Keller NP (2004) veA is required for toxin and sclerotial production in Aspergillus parasiticus. Appl Environ Microbiol 70:4733–4739PubMedPubMedCentralCrossRefGoogle Scholar
  31. Casselton L, Zolan M (2002) The art and design of genetic screens: filamentous fungi. Nat Rev Genet 3:683–697PubMedCrossRefGoogle Scholar
  32. Chang YC, Timberlake WE (1993) Identification of Aspergillus brlA response elements (BREs) by genetic selection in yeast. Genetics 133:29–38PubMedPubMedCentralGoogle Scholar
  33. Chang MH, Chae KS, Han DM, Jahng KY (2004) The GanB Galpha-protein negatively regulates asexual sporulation and plays a positive role in conidial germination in Aspergillus nidulans. Genetics 167:1305–1315PubMedPubMedCentralCrossRefGoogle Scholar
  34. Clutterbuck AJ (1969) A mutational analysis of conidial development in Aspergillus nidulans. Genetics 63:317–327PubMedPubMedCentralGoogle Scholar
  35. d’Enfert C (1997) Fungal spore germination: Insights from the molecular genetics of Aspergillus nidulans and Neurospora crassa. Fungal Genet Biol 21:163–172CrossRefGoogle Scholar
  36. D’Souza CA, Lee BN, Adams TH (2001) Characterization of the role of the FluG protein in asexual development of Aspergillus nidulans. Genetics 158:1027–1036PubMedPubMedCentralGoogle Scholar
  37. De Souza CP, Hashmi SB, Osmani AH, Andrews P, Ringelberg CS, Dunlap JC, Osmani SA (2013) Functional analysis of the Aspergillus nidulans kinome. PLoS One 8:e58008PubMedPubMedCentralCrossRefGoogle Scholar
  38. Duran RM, Cary JW, Calvo AM (2007) Production of cyclopiazonic acid, aflatrem, and aflatoxin by Aspergillus flavus is regulated by veA, a gene necessary for sclerotial formation. Appl Microbiol Biotechnol 73:1158–1168PubMedCrossRefGoogle Scholar
  39. Dutton JR, Johns S, Miller BL (1997) StuAp is a sequence-specific transcription factor that regulates developmental complexity in Aspergillus nidulans. EMBO J 16:5710–5721PubMedPubMedCentralCrossRefGoogle Scholar
  40. Dyer PS, O’Gorman CM (2011) A fungal sexual revolution: Aspergillus and Penicillium show the way. Curr Opin Microbiol 14:649–654PubMedCrossRefGoogle Scholar
  41. Dyer PS, O’Gorman CM (2012) Sexual development and cryptic sexuality in fungi: insights from Aspergillus species. FEMS Microbiol Rev 36:165–192PubMedCrossRefGoogle Scholar
  42. Dyer PS, Paoletti M, Archer DB (2003) Genomics reveals sexual secrets of Aspergillus. Microbiology 149:2301–2303PubMedCrossRefGoogle Scholar
  43. Ebbole DJ (2010) The conidium. In: Cellular and molecular biology of filamentous fungi. ASM Press, Washington, DC, pp 577–590Google Scholar
  44. Etxebeste O, Herrero-Garcia E, Araujo-Bazan L, Rodriguez-Urra AB, Garzia A, Ugalde U, Espeso EA (2009) The bZIP-type transcription factor FlbB regulates distinct morphogenetic stages of colony formation in Aspergillus nidulans. Mol Microbiol 73:775–789PubMedCrossRefGoogle Scholar
  45. Etxebeste O, Garzia A, Espeso EA, Ugalde U (2010) Aspergillus nidulans asexual development: making the most of cellular modules. Trends Microbiol 18:569–576PubMedCrossRefGoogle Scholar
  46. Fisher MC, Henk DA, Briggs CJ, Brownstein JS, Madoff LC, McCraw SL, Gurr SJ (2012) Emerging fungal threats to animal, plant and ecosystem health. Nature 484:186–194PubMedCrossRefGoogle Scholar
  47. Galagan JE, Calvo SE, Cuomo C, Ma LJ, Wortman JR, Batzoglou S, Lee SI, Basturkmen M, Spevak CC, Clutterbuck J et al (2005) Sequencing of Aspergillus nidulans and comparative analysis with A. fumigatus and A. oryzae. Nature 438:1105–1115PubMedCrossRefGoogle Scholar
  48. Garzia A, Etxebeste O, Herrero-Garcia E, Fischer R, Espeso EA, Ugalde U (2009) Aspergillus nidulans FlbE is an upstream developmental activator of conidiation functionally associated with the putative transcription factor FlbB. Mol Microbiol 71:172–184PubMedCrossRefGoogle Scholar
  49. Garzia A, Etxebeste O, Herrero-Garcia E, Ugalde U, Espeso EA (2010) The concerted action of bZip and cMyb transcription factors FlbB and FlbD induces brlA expression and asexual development in Aspergillus nidulans. Mol Microbiol 75:1314–1324PubMedCrossRefGoogle Scholar
  50. Geiser DM (2009) Sexual structures in Aspergillus: morphology, importance and genomics. Med Mycol 47(Suppl 1):S21–S26PubMedCrossRefGoogle Scholar
  51. Grahl N, Shepardson KM, Chung D, Cramer RA (2012) Hypoxia and fungal pathogenesis: to air or not to air? Eukaryot Cell 11:560–570PubMedPubMedCentralCrossRefGoogle Scholar
  52. Gugnani HC (2003) Ecology and taxonomy of pathogenic aspergilli. Front Biosci 8:s346–s357PubMedCrossRefGoogle Scholar
  53. Han KH (2009) Molecular Genetics of Emericella nidulans Sexual Development. Mycobiology 37:171–182PubMedPubMedCentralCrossRefGoogle Scholar
  54. Han S, Adams TH (2001) Complex control of the developmental regulatory locus brlA in Aspergillus nidulans. Mol Gen Genomics 266:260–270CrossRefGoogle Scholar
  55. Han DM, Han YJ, Lee YH, Jahng KY, Jahng SH, Chae KS (1990) Inhibitory conditions of asexual development and their application for the screening of mutants defective in sexual development. Kor J Mycol 18:225–232Google Scholar
  56. Han S, Navarro J, Greve RA, Adams TH (1993) Translational repression of brlA expression prevents premature development in Aspergillus. EMBO J 12:2449–2457PubMedPubMedCentralCrossRefGoogle Scholar
  57. Han DM, Han YJ, Kim JH, Jahng KY, Chung YS, Chung JH, Chae KS (1994) Isolation and characterization of NSD mutants in Aspergillus nidulans. Kor J Mycol 22:1–7Google Scholar
  58. Han KH, Cheong SS, Hoe HS, Han DM (1998) Characterization of several NSD mutants of Aspergillus nidulans that never undergo sexual development. Kor J Genet 20:257–264Google Scholar
  59. Han KH, Han KY, Yu JH, Chae KS, Jahng KY, Han DM (2001) The nsdD gene encodes a putative GATA-type transcription factor necessary for sexual development of Aspergillus nidulans. Mol Microbiol 41:299–309PubMedCrossRefGoogle Scholar
  60. Han KH, Lee DB, Kim JH, Kim MS, Han KY, Kim WS, Park YS, Kim HB, Han DM (2003) Environmental factors affecting development of Aspergillus nidulans. J Microbiol 41:34–40Google Scholar
  61. Han KH, Seo JA, Yu JH (2004a) A putative G protein-coupled receptor negatively controls sexual development in Aspergillus nidulans. Mol Microbiol 51:1333–1345PubMedCrossRefGoogle Scholar
  62. Han KH, Seo JA, Yu JH (2004b) Regulators of G-protein signalling in Aspergillus nidulans: RgsA downregulates stress response and stimulates asexual sporulation through attenuation of GanB (Galpha) signalling. Mol Microbiol 53:529–540PubMedCrossRefGoogle Scholar
  63. Harris SD (2006) Cell polarity in filamentous. Int Rev Cytol 251:41–77PubMedCrossRefGoogle Scholar
  64. Harris SD (2008) Branching of fungal hyphae: regulation, mechanisms and comparison with other branching systems. Mycologia 100:823–832PubMedCrossRefGoogle Scholar
  65. Harris SD (2011) Hyphal morphogenesis: an evolutionary perspective. Fungal Biol 115:475–484PubMedCrossRefGoogle Scholar
  66. Hicks JK, Yu J-H, Keller NP, Adams TH (1997) Aspergillus sporulation and mycotoxin production both require inactivation of the FadA G alpha protein-dependent signaling pathway. EMBO J 16:4916–4923PubMedPubMedCentralCrossRefGoogle Scholar
  67. Hoffmann B, Wanke C, Lapaglia SK, Braus GH (2000) c-Jun and RACK1 homologues regulate a control point for sexual development in Aspergillus nidulans. Mol Microbiol 37:28–41PubMedCrossRefGoogle Scholar
  68. Ichinomiya M, Ohta A, Horiuchi H (2005) Expression of asexual developmental regulator gene abaA is affected in the double mutants of classes I and II chitin synthase genes, chsC and chsA, of Aspergillus nidulans. Curr Genet 48:171–183PubMedCrossRefGoogle Scholar
  69. Jun SC, Lee SJ, Park HJ, Kang JY, Leem YE, Yang TH, Chang MH, Kim JM, Jang SH, Kim HG et al (2011) The MpkB MAP kinase plays a role in post-karyogamy processes as well as in hyphal anastomosis during sexual development in Aspergillus nidulans. J Microbiol 49:418–430PubMedCrossRefGoogle Scholar
  70. Kafer E (1965) Origins of translocations in Aspergillus nidulans. Genetics 52:217–232PubMedPubMedCentralGoogle Scholar
  71. Kang JY, Chun J, Jun SC, Han DM, Chae KS, Jahng KY (2013) The MpkB MAP kinase plays a role in autolysis and conidiation of Aspergillus nidulans. Fungal Genet Biol 61:42–49PubMedCrossRefGoogle Scholar
  72. Kawasaki L, Sanchez O, Shiozaki K, Aguirre J (2002) SakA MAP kinase is involved in stress signal transduction, sexual development and spore viability in Aspergillus nidulans. Mol Microbiol 45:1153–1163PubMedCrossRefGoogle Scholar
  73. Keller NP, Turner G, Bennett JW (2005) Fungal secondary metabolism – From biochemistry to genomics. Nat Rev Microbiol 3:937–947PubMedCrossRefGoogle Scholar
  74. Kim H, Han K, Kim K, Han D, Jahng K, Chae K (2002) The veA gene activates sexual development in Aspergillus nidulans. Fungal Genet Biol 37:72–80PubMedCrossRefGoogle Scholar
  75. Kim HR, Chae KS, Han KH, Han DM (2009) The nsdC gene encoding a putative C2H2-type transcription factor is a key activator of sexual development in Aspergillus nidulans. Genetics 182:771–783PubMedPubMedCentralCrossRefGoogle Scholar
  76. Kim YJ, Yu YM, Maeng PJ (2017) Differential control of asexual development and sterigmatocystin biosynthesis by a novel regulator in Aspergillus nidulans. Sci Rep 7:46340PubMedPubMedCentralCrossRefGoogle Scholar
  77. Kong Q, Wang L, Liu Z, Kwon N-J, Kim SC, Yu J-H (2013) Gbeta-like CpcB plays a crucial role for growth and development of Aspergillus nidulans and Aspergillus fumigatus. PLoS One 8:e70355PubMedPubMedCentralCrossRefGoogle Scholar
  78. Kovacs Z, Szarka M, Kovacs S, Boczonadi I, Emri T, Abe K, Pocsi I, Pusztahelyi T (2013) Effect of cell wall integrity stress and RlmA transcription factor on asexual development and autolysis in Aspergillus nidulans. Fungal Genet Biol 54:1–14PubMedCrossRefGoogle Scholar
  79. Krijgsheld P, Bleichrodt R, van Veluw GJ, Wang F, Muller WH, Dijksterhuis J, Wosten HA (2013) Development in Aspergillus. Stud Mycol 74:1–29PubMedCrossRefGoogle Scholar
  80. Kwon N-J, Garzia A, Espeso EA, Ugalde U, Yu J-H (2010a) FlbC is a putative nuclear C2H2 transcription factor regulating development in Aspergillus nidulans. Mol Microbiol 77:1203–1219PubMedCrossRefGoogle Scholar
  81. Kwon N-J, Shin K-S, Yu J-H (2010b) Characterization of the developmental regulator FlbE in Aspergillus fumigatus and Aspergillus nidulans. Fungal Genet Biol 47:981–993PubMedCrossRefGoogle Scholar
  82. Kwon N-J, Park H-S, Jung S, Kim SC, Yu J-H (2012) The putative guanine nucleotide exchange factor RicA mediates upstream signaling for growth and development in Aspergillus. Eukaryot Cell 11:1399–1412PubMedPubMedCentralCrossRefGoogle Scholar
  83. Lafon A, Seo JA, Han KH, Yu J-H, d’Enfert C (2005) The heterotrimeric G-protein GanB(alpha)-SfaD(beta)-GpgA(gamma) is a carbon source sensor involved in early cAMP-dependent germination in Aspergillus nidulans. Genetics 171:71–80PubMedPubMedCentralCrossRefGoogle Scholar
  84. Lara-Rojas F, Sanchez O, Kawasaki L, Aguirre J (2011) Aspergillus nidulans transcription factor AtfA interacts with the MAPK SakA to regulate general stress responses, development and spore functions. Mol Microbiol 80:436–454PubMedPubMedCentralCrossRefGoogle Scholar
  85. Lee BN, Adams TH (1994) The Aspergillus nidulans fluG gene is required for production of an extracellular developmental signal and is related to prokaryotic glutamine synthetase I. Genes Dev 8:641–651PubMedCrossRefGoogle Scholar
  86. Lee BN, Adams TH (1996) FluG and flbA function interdependently to initiate conidiophore development in Aspergillus nidulans through brlA beta activation. EMBO J 15:299–309PubMedPubMedCentralCrossRefGoogle Scholar
  87. Lee JY, Kim LH, Kim HE, Park JS, Han KH, Han DM (2013) A putative APSES transcription factor is necessary for normal growth and development of Aspergillus nidulans. J Microbiol 51:800–806PubMedCrossRefGoogle Scholar
  88. Lee MK, Kwon NJ, Choi JM, Lee IS, Jung S, Yu JH (2014) NsdD is a key repressor of asexual development in Aspergillus nidulans. Genetics 197:159–173PubMedPubMedCentralCrossRefGoogle Scholar
  89. Lee MK, Kwon NJ, Lee IS, Jung S, Kim SC, Yu JH (2016) Negative regulation and developmental competence in Aspergillus. Sci Rep 6:28874PubMedPubMedCentralCrossRefGoogle Scholar
  90. 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
  91. Lew RR (2011) How does a hypha grow? The biophysics of pressurized growth in fungi. Nat Rev Microbiol 9:509–518PubMedCrossRefGoogle Scholar
  92. Marshall MA, Timberlake WE (1991) Aspergillus nidulans wetA activates spore-specific gene expression. Mol Cell Biol 11:55–62PubMedPubMedCentralCrossRefGoogle Scholar
  93. Martinelli S (1976) Conidiation of Aspergillus nidulans in submerged culture. Trans Br Mvcol Soc 67(1):121–128CrossRefGoogle Scholar
  94. Mirabito PM, Adams TH, Timberlake WE (1989) Interactions of three sequentially expressed genes control temporal and spatial specificity in Aspergillus development. Cell 57:859–868PubMedCrossRefGoogle Scholar
  95. Mooney JL, Yager LN (1990) Light is required for conidiation in Aspergillus nidulans. Genes Dev 4:1473–1482PubMedCrossRefGoogle Scholar
  96. Morton AG (1961) The induction of sporulation in mould fungi. Proc R Soc London Ser B 153:548–569CrossRefGoogle Scholar
  97. Nahlik K, Dumkow M, Bayram O, Helmstaedt K, Busch S, Valerius O, Gerke J, Hoppert M, Schwier E, Opitz L et al (2010) The COP9 signalosome mediates transcriptional and metabolic response to hormones, oxidative stress protection and cell wall rearrangement during fungal development. Mol Microbiol 78:964–979PubMedCrossRefGoogle Scholar
  98. Nevalainen H, Peterson R (2014) Making recombinant proteins in filamentous fungi – are we expecting too much? Front Microbiol 5:75PubMedPubMedCentralGoogle Scholar
  99. Ni M, Yu JH (2007) A novel regulator couples sporogenesis and trehalose biogenesis in Aspergillus nidulans. PLoS One 2:e970PubMedPubMedCentralCrossRefGoogle Scholar
  100. Ni M, Gao N, Kwon N-J, Shin K-S, Yu J-H (2010) Regulation of Aspergillus Conidiation. In: Cellular and Molecular Biology of Filamentous Fungi, pp 559–576CrossRefGoogle Scholar
  101. Noble LM, Andrianopoulos A (2013) Reproductive competence: a recurrent logic module in eukaryotic development. Proc R Soc B Biol Sci 280Google Scholar
  102. Oiartzabal-Arano E, Garzia A, Gorostidi A, Ugalde U, Espeso EA, Etxebeste O (2015) Beyond asexual development: modifications in the gene expression profile caused by the absence of the Aspergillus nidulans transcription factor FlbB. Genetics 199:1127–1142PubMedPubMedCentralCrossRefGoogle Scholar
  103. Palmer DA, Thompson JK, Li L, Prat A, Wang P (2006) Gib2, a novel Gbeta-like/RACK1 homolog, functions as a Gbeta subunit in cAMP signaling and is essential in Cryptococcus neoformans. J Biol Chem 281:32596–32605PubMedCrossRefGoogle Scholar
  104. Paoletti M, Seymour FA, Alcocer MJ, Kaur N, Calvo AM, Archer DB, Dyer PS (2007) Mating type and the genetic basis of self-fertility in the model fungus Aspergillus nidulans. Curr Biol 17:1384–1389PubMedCrossRefGoogle Scholar
  105. Park HS, Yu JH (2012) Genetic control of asexual sporulation in filamentous fungi. Curr Opin Microbiol 15:669–677PubMedCrossRefGoogle Scholar
  106. Park BC, Park YH, Park HM (2003) Activation of chsC transcription by AbaA during asexual development of Aspergillus nidulans. FEMS Microbiol Lett 220:241–246PubMedCrossRefGoogle Scholar
  107. Park HS, Ni M, Jeong KC, Kim YH, Yu JH (2012) The role, interaction and regulation of the velvet regulator VelB in Aspergillus nidulans. PLoS One 7:e45935PubMedPubMedCentralCrossRefGoogle Scholar
  108. Park H-S, Nam TY, Han KH, Kim SC, Yu J-H (2014) VelC positively controls sexual development in Aspergillus nidulans. PLoS One 9:e89883PubMedPubMedCentralCrossRefGoogle Scholar
  109. Park HS, Yu YM, Lee MK, Maeng PJ, Kim SC, Yu JH (2015) Velvet-mediated repression of beta-glucan synthesis in Aspergillus nidulans spores. Sci Rep 5:10199PubMedPubMedCentralCrossRefGoogle Scholar
  110. Park HS, Jun SC, Han KH, Hong SB, Yu JH (2017) Diversity, Application, and Synthetic Biology of Industrially Important Aspergillus Fungi. Adv Appl Microbiol 100:161–202PubMedCrossRefGoogle Scholar
  111. Prade RA, Timberlake WE (1993) The Aspergillus nidulans brlA regulatory locus consists of overlapping transcription units that are individually required for conidiophore development. EMBO J 12:2439–2447PubMedPubMedCentralCrossRefGoogle Scholar
  112. Purschwitz J, Muller S, Kastner C, Schoser M, Haas H, Espeso EA, Atoui A, Calvo AM, Fischer R (2008) Functional and physical interaction of blue- and red-light sensors in Aspergillus nidulans. Curr Biol 18:255–259PubMedCrossRefGoogle Scholar
  113. Purschwitz J, Muller S, Fischer R (2009) Mapping the interaction sites of Aspergillus nidulans phytochrome FphA with the global regulator VeA and the White Collar protein LreB. Mol Gen Genomics 281:35–42CrossRefGoogle Scholar
  114. Rai JN, Tewari JP, Sinha AK (1967) Effect of environmental conditions on sclerotia and cleistothecia production in Aspergillus. Mycopathol Mycol Appl 31:209–224PubMedCrossRefGoogle Scholar
  115. Ramamoorthy V, Dhingra S, Kincaid A, Shantappa S, Feng X, Calvo AM (2013) The putative C2H2 transcription factor MtfA is a novel regulator of secondary metabolism and morphogenesis in Aspergillus nidulans. PLoS One 8:e74122PubMedPubMedCentralCrossRefGoogle Scholar
  116. Rauscher S, Pacher S, Hedtke M, Kniemeyer O, Fischer R (2016) A phosphorylation code of the Aspergillus nidulans global regulator VelvetA (VeA) determines specific functions. Mol Microbiol 99:909–924PubMedCrossRefGoogle Scholar
  117. Riquelme M (2013) Tip Growth in Filamentous Fungi: A Road Trip to the Apex. Annual Rev Microbiol 67:587–609CrossRefGoogle Scholar
  118. Rodriguez-Romero J, Hedtke M, Kastner C, Muller S, Fischer R (2010) Fungi, hidden in soil or up in the air: light makes a difference. Annu Rev Microbiol 64:585–610PubMedCrossRefGoogle Scholar
  119. Rodriguez-Urra AB, Jimenez C, Nieto MI, Rodriguez J, Hayashi H, Ugalde U (2012) Signaling the induction of sporulation involves the interaction of two secondary metabolites in Aspergillus nidulans. ACS Chem Biol 7:599–606PubMedCrossRefGoogle Scholar
  120. Rohrig J, Yu Z, Chae KS, Kim JH, Han KH, Fischer R (2017) The Aspergillus nidulans Velvet-interacting protein, VipA, is involved in light-stimulated heme biosynthesis. Mol Microbiol 105:825–838PubMedCrossRefGoogle Scholar
  121. Rosen S, Yu J-H, Adams TH (1999) The Aspergillus nidulans sfaD gene encodes a G protein beta subunit that is required for normal growth and repression of sporulation. EMBO J 18:5592–5600PubMedPubMedCentralCrossRefGoogle Scholar
  122. Ruger-Herreros C, Rodriguez-Romero J, Fernandez-Barranco R, Olmedo M, Fischer R, Corrochano LM, Canovas D (2011) Regulation of conidiation by light in Aspergillus nidulans. Genetics 188:809–822PubMedPubMedCentralCrossRefGoogle Scholar
  123. Samson RA, Visagie CM, Houbraken J, Hong SB, Hubka V, Klaassen CH, Perrone G, Seifert KA, Susca A, Tanney JB et al (2014) Phylogeny, identification and nomenclature of the genus Aspergillus. Stud Mycol 78:141–173PubMedPubMedCentralCrossRefGoogle Scholar
  124. Sarikaya Bayram O, Bayram O, Valerius O, Park HS, Irniger S, Gerke J, Ni M, Han KH, Yu JH, Braus GH (2010) LaeA control of velvet family regulatory proteins for light-dependent development and fungal cell-type specificity. PLoS Genet 6:e1001226PubMedPubMedCentralCrossRefGoogle Scholar
  125. Saxena RK, Sinha U (1973) Conidiation of Aspergillus nidulans in submerged liquid culture. Gen Appl Microbiol 19:141–146CrossRefGoogle Scholar
  126. Scherer M, Fischer R (1998) Purification and characterization of laccase II of Aspergillus nidulans. Arch Microbiol 170:78–84PubMedCrossRefGoogle Scholar
  127. Schoustra S, Rundle HD, Dali R, Kassen R (2010) Fitness-associated sexual reproduction in a filamentous fungus. Curr Biol 20:1350–1355PubMedCrossRefGoogle Scholar
  128. Seo JA, Guan Y, Yu JH (2003) Suppressor mutations bypass the requirement of fluG for asexual sporulation and sterigmatocystin production in Aspergillus nidulans. Genetics 165:1083–1093PubMedPubMedCentralGoogle Scholar
  129. Seo JA, Han KH, Yu JH (2004) The gprA and gprB genes encode putative G protein-coupled receptors required for self-fertilization in Aspergillus nidulans. Mol Microbiol 53:1611–1623PubMedCrossRefGoogle Scholar
  130. Seo JA, Han KH, Yu JH (2005) Multiple roles of a heterotrimeric G-protein gamma-subunit in governing growth and development of Aspergillus nidulans. Genetics 171:81–89PubMedPubMedCentralCrossRefGoogle Scholar
  131. Seo JA, Guan Y, Yu JH (2006) FluG-dependent asexual development in Aspergillus nidulans occurs via derepression. Genetics 172:1535–1544PubMedPubMedCentralCrossRefGoogle Scholar
  132. Sewall TC, Mims CW, Timberlake WE (1990a) abaA controls phialide differentiation in Aspergillus nidulans. Plant Cell 2:731–739PubMedPubMedCentralCrossRefGoogle Scholar
  133. Sewall TC, Mims CW, Timberlake WE (1990b) Conidium differentiation in Aspergillus nidulans wild-type and wet-white (wetA) mutant strains. Dev Biol 138:499–508PubMedCrossRefGoogle Scholar
  134. Shimizu K, Keller NP (2001) Genetic involvement of a cAMP-dependent protein kinase in a G protein signaling pathway regulating morphological and chemical transitions in Aspergillus nidulans. Genetics 157:591–600PubMedPubMedCentralGoogle Scholar
  135. Si H, Rittenour WR, Xu K, Nicksarlian M, Calvo AM, Harris SD (2012) Morphogenetic and developmental functions of the Aspergillus nidulans homologues of the yeast bud site selection proteins Bud4 and Axl2. Mol Microbiol 85:252–270PubMedCrossRefGoogle Scholar
  136. Skromne I, Sanchez O, Aguirre J (1995) Starvation stress modulates the expression of the Aspergillus nidulans brlA regulatory gene. Microbiology 141:21–28PubMedCrossRefGoogle Scholar
  137. Sohn KT, Yoon KS (2002) Ultrastructural Study on the Cleistothecium Development in Aspergillus nidulans. Mycobiology 30:117–127CrossRefGoogle Scholar
  138. Song MH, Nah JY, Han YS, Han DM, Chae KS (2001) Promotion of conidial head formation in Aspergillus oryzae by a salt. Biotechnol Lett 23:689–691CrossRefGoogle Scholar
  139. Steinberg G (2007) Hyphal growth: a tale of motors, lipids, and the Spitzenkorper. Eukaryot Cell 6:351–360PubMedPubMedCentralCrossRefGoogle Scholar
  140. Stinnett SM, Espeso EA, Cobeno L, Araujo-Bazan L, Calvo AM (2007) Aspergillus nidulans VeA subcellular localization is dependent on the importin alpha carrier and on light. Mol Microbiol 63:242–255PubMedCrossRefGoogle Scholar
  141. Timberlake WE (1990) Molecular genetics of Aspergillus development. Annu Rev Genet 24:5–36PubMedCrossRefGoogle Scholar
  142. Tisch D, Schmoll M (2010) Light regulation of metabolic pathways in fungi. Appl Microbiol Biotechnol 85:1259–1277PubMedCrossRefGoogle Scholar
  143. Todd RB, Davis MA, Hynes MJ (2007) Genetic manipulation of Aspergillus nidulans: heterokaryons and diploids for dominance, complementation and haploidization analyses. Nat Protoc 2:822–830PubMedCrossRefGoogle Scholar
  144. Treseder KK, Lennonb JT (2015) Fungal Traits That Drive Ecosystem Dynamics on Land. Microbiol Mol Biol R 79:243–262CrossRefGoogle Scholar
  145. Tsitsigiannis DI, Keller NP (2007) Oxylipins as developmental and host-fungal communication signals. Trends Microbiol 15:109–118PubMedCrossRefGoogle Scholar
  146. Tsitsigiannis DI, Zarnowski R, Keller NP (2004) The lipid body protein, PpoA, coordinates sexual and asexual sporulation in Aspergillus nidulans. J Biol Chem 279:11344–11353PubMedCrossRefGoogle Scholar
  147. Tsitsigiannis DI, Kowieski TM, Zarnowski R, Keller NP (2005) Three putative oxylipin biosynthetic genes integrate sexual and asexual development in Aspergillus nidulans. Microbiology 151:1809–1821PubMedCrossRefGoogle Scholar
  148. Vallim MA, Miller KY, Miller BL (2000) Aspergillus SteA (sterile12-like) is a homeodomain-C2/H2-Zn2+ finger transcription factor required for sexual reproduction. Mol Microbiol 36:290–301PubMedCrossRefGoogle Scholar
  149. van Burik JAH, Magee PT (2001) Aspects of fungal pathogenesis in humans. Annu Rev Microbiol 55:743–772PubMedCrossRefGoogle Scholar
  150. Vienken K, Fischer R (2006) The Zn(II)2Cys6 putative transcription factor NosA controls fruiting body formation in Aspergillus nidulans. Mol Microbiol 61:544–554PubMedCrossRefGoogle Scholar
  151. Vienken K, Scherer M, Fischer R (2005) The Zn(II)2Cys6 putative Aspergillus nidulans transcription factor repressor of sexual development inhibits sexual development under low-carbon conditions and in submersed culture. Genetics 169:619–630PubMedPubMedCentralCrossRefGoogle Scholar
  152. Wei H, Requena N, Fischer R (2003) The MAPKK kinase SteC regulates conidiophore morphology and is essential for heterokaryon formation and sexual development in the homothallic fungus Aspergillus nidulans. Mol Microbiol 47:1577–1588PubMedCrossRefGoogle Scholar
  153. Wieser J, Lee BN, Fondon J III, Adams TH (1994) Genetic requirements for initiating asexual development in Aspergillus nidulans. Curr Genet 27:62–69PubMedCrossRefGoogle Scholar
  154. Wieser J, Yu J-H, Adams TH (1997) Dominant mutations affecting both sporulation and sterigmatocystin biosynthesis in Aspergillus nidulans. Curr Genet 32:218–224PubMedCrossRefGoogle Scholar
  155. Wong KH, Hynes MJ, Todd RB, Davis MA (2009) Deletion and overexpression of the Aspergillus nidulans GATA factor AreB reveals unexpected pleiotropy. Microbiology 155:3868–3880PubMedCrossRefGoogle Scholar
  156. Wu J, Miller BL (1997) Aspergillus asexual reproduction and sexual reproduction are differentially affected by transcriptional and translational mechanisms regulating stunted gene expression. Mol Cell Biol 17:6191–6201PubMedPubMedCentralCrossRefGoogle Scholar
  157. Xu JR (2000) Map kinases in fungal pathogens. Fungal Genet Biol 31:137–152PubMedCrossRefGoogle Scholar
  158. Yager LN, Kurtz MB, Champe SP (1982) Temperature-shift analysis of conidial development in Aspergillus nidulans. Dev Biol 93:92–103PubMedCrossRefGoogle Scholar
  159. Yu J-H (2006) Heterotrimeric G protein signaling and RGSs in Aspergillus nidulans. J Microbiol 44:145–154PubMedGoogle Scholar
  160. Yu J-H (2010) Regulation of Development in Aspergillus nidulans and Aspergillus fumigatus. Mycobiology 38:229–237PubMedPubMedCentralCrossRefGoogle Scholar
  161. Yu JH, Wieser J, Adams TH (1996) The Aspergillus FlbA RGS domain protein antagonizes G protein signaling to block proliferation and allow development. EMBO J 15:5184–5190PubMedPubMedCentralCrossRefGoogle Scholar
  162. Zonneveld BJM (1988) Effect of carbon dioxide on fruiting in Aspergillus nidulans. Trans Br Mycol Soc 91:625CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Hee-Soo Park
    • 1
  • Mi-Kyung Lee
    • 2
  • Kap-Hoon Han
    • 3
  • Min-Ju Kim
    • 1
  • Jae-Hyuk Yu
    • 4
    • 5
    Email author
  1. 1.School of Food Science and Biotechnology, Institute of Agricultural Science and TechnologyKyungpook National UniversityDaeguRepublic of Korea
  2. 2.Biological Resource Center (BRC)Korea Research Institute of Bioscience and Biotechnology (KRIBB)Jeongeup-siRepublic of Korea
  3. 3.Department of Pharmaceutical EngineeringWoosuk UniversityWanjuRepublic of Korea
  4. 4.Department of BacteriologyUniversity of WisconsinMadisonUSA
  5. 5.Department of Systems BiotechnologyKonkuk UniversitySeoulRepublic of Korea

Personalised recommendations