title: Oxygen and an extracellular phase transition independently control central regulatory genes and conidiogenesis in Aspergillus fumigatus.
abstract: Conidiogenesis is the primary process for asexual reproduction in filamentous fungi. As the conidia resulting from the conidiogenesis process are primarily disseminated via air currents and/or water, an outstanding question has been how fungi recognize aerial environments suitable for conidial development. In this study, we documented the somewhat complex development of the conidia-bearing structures, termed conidiophores, from several Aspergillus species in a subsurface (gel-phase) layer of solid media. A subset of the isolates studied was able to develop conidiophores in a gel-phase environment, but exposure to the aeriform environment was required for the terminal developmental transition from phialide cells to conidia. The remaining Aspergilli could not initiate the conidiogenesis process until they were exposed to the aeriform environment. Our observations of conidiophore development in high or low oxygen conditions in both aeriform and gel-phase environments revealed that oxygen and the aeriform state are positive environmental factors for inducing conidiogenesis in most of the aspergilli tested in this study. Transcriptional analysis using A. fumigatus strain AF293 confined to either the aeriform or gel-phase environments revealed that expression of a key regulatory gene for conidiophore development (AfubrlA) is facilitated by oxygen while expression of another regulatory gene controlling conidia formation from phialides (AfuabaA) was repressed regardless of oxygen levels in the gel-embedded environment. Furthermore, by comparing the developmental behavior of conidiation-defective mutants lacking genes controlling various regulatory checkpoints throughout the conidiogenesis pathway, we propose that this aerial response by the fungus requires both oxygen and the phase transition (solid to aeriform), with these environmental signals integrating into the upstream regulatory pathway and central regulatory pathway of conidiogenesis, respectively. Our findings provide not only novel insight into how fungi respond to an aerial environment to trigger development for airborne conidia production but also the relationship between environmental factors and conidiogenesis regulation in aspergilli.
authors.affiliation: Plant Biology Division, Samuel Roberts Noble Foundation, Ardmore, Oklahoma, United States of America.
authors.forename: Myoung-Hwan
authors.initials: MH
authors.lastname: Chi
authors.forename: Kelly D
authors.initials: KD
authors.lastname: Craven
mesh_terms: D001232:Aspergillus fumigatus / Q000235:genetics* / Q000502:physiology*; D003470:Culture Media / Q000737:chemistry; D005656:Fungal Proteins / Q000235:genetics; D015966:Gene Expression Regulation, Fungal; D005800:Genes, Fungal; D009154:Mutation; D010100:Oxygen / Q000737:chemistry*; D012100:Reproduction, Asexual / Q000235:genetics; D020133:Reverse Transcriptase Polymerase Chain Reaction; D013172:Spores, Fungal / Q000502:physiology
chemical_list: D003470:Culture Media; D005656:Fungal Proteins; D010100:Oxygen
references.citation: J Biosci. 2010 Mar;35(1):119-26
references.pmid: 20413916
references.citation: Mycologia. 2008 Mar-Apr;100(2):205-26
references.pmid: 18595197
references.citation: Mol Cell Biol. 1994 Apr;14(4):2503-15
references.pmid: 8139553
references.citation: PLoS Genet. 2008 Apr 11;4(4):e1000046
references.pmid: 18404212
references.citation: Dev Biol. 1990 Apr;138(2):499-508
references.pmid: 2180753
references.citation: Science. 2008 Jun 13;320(5882):1504-6
references.pmid: 18556559
references.citation: Eukaryot Cell. 2006 Oct;5(10):1577-84
references.pmid: 17030989
references.citation: Microbiology (Reading). 2007 Jun;153(Pt 6):1677-1692
references.pmid: 17526826
references.citation: Cell. 1989 Jun 2;57(5):859-68
references.pmid: 2655931
references.citation: Eukaryot Cell. 2006 Aug;5(8):1328-36
references.pmid: 16896216
references.citation: Trends Microbiol. 2005 Mar;13(3):111-8
references.pmid: 15737729
references.citation: Nature. 2005 Dec 22;438(7071):1105-15
references.pmid: 16372000
references.citation: Nature. 2009 Jan 22;457(7228):471-4
references.pmid: 19043401
references.citation: J Infect Dis. 1990 Nov;162(5):1151-8
references.pmid: 1977804
references.citation: PLoS One. 2012;7(9):e45935
references.pmid: 23049895
references.citation: Infect Immun. 1996 Oct;64(10):4401-5
references.pmid: 8926121
references.citation: Cell. 1988 Jul 29;54(3):353-62
references.pmid: 3293800
references.citation: Fungal Genet Biol. 2010 Dec;47(12):981-93
references.pmid: 20817115
references.citation: Fungal Genet Biol. 2004 Apr;41(4):443-53
references.pmid: 14998527
references.citation: Microbiology (Reading). 1995 Jan;141 ( Pt 1):21-8
references.pmid: 7894714
references.citation: Curr Biol. 2005 Jul 12;15(13):1242-8
references.pmid: 16005299
references.citation: Mol Microbiol. 1994 Oct;14(2):323-34
references.pmid: 7830576
references.citation: Genes Dev. 1994 Mar 15;8(6):641-51
references.pmid: 7926755
references.citation: Genes Dev. 1995 Feb 15;9(4):491-502
references.pmid: 7883170
references.citation: Eukaryot Cell. 2010 Nov;9(11):1711-23
references.pmid: 20852021
references.citation: Genetics. 1993 Jan;133(1):29-38
references.pmid: 8417986
references.citation: EMBO J. 1996 Oct 1;15(19):5184-90
references.pmid: 8895563
references.citation: J Gen Microbiol. 1969 Nov;59(1):31-45
references.pmid: 5365366
references.citation: Microbiology (Reading). 2011 Feb;157(Pt 2):313-326
references.pmid: 20966095
references.citation: Nature. 2005 Dec 22;438(7071):1151-6
references.pmid: 16372009
references.citation: Dev Biol. 1973 Sep;34(1):9-15
references.pmid: 4595499
references.citation: Adv Genet. 1977;19:33-131
references.pmid: 327767
references.citation: Mol Microbiol. 2012 Nov;86(4):937-53
references.pmid: 22970834
references.citation: Microbiol Mol Biol Rev. 1998 Mar;62(1):35-54
references.pmid: 9529886
references.citation: Mycologia. 2005 Nov-Dec;97(6):1316-29
references.pmid: 16722222
references.citation: PLoS Genet. 2010 Dec 02;6(12):e1001226
references.pmid: 21152013
references.citation: Methods. 2001 Dec;25(4):402-8
references.pmid: 11846609
references.citation: Mol Microbiol. 2010 Sep;77(5):1203-19
references.pmid: 20624219
references.citation: Clin Microbiol Rev. 1999 Apr;12(2):310-50
references.pmid: 10194462
references.citation: Eukaryot Cell. 2006 Oct;5(10):1585-95
references.pmid: 17030990
references.citation: Eukaryot Cell. 2008 Jan;7(1):38-48
references.pmid: 17993569
references.citation: Curr Genet. 1994 Dec;27(1):62-9
references.pmid: 7750148
references.citation: Curr Opin Microbiol. 2012 Dec;15(6):669-77
references.pmid: 23092920
references.citation: Antimicrob Agents Chemother. 1997 Jun;41(6):1364-8
references.pmid: 9174200
references.citation: Genetics. 2006 Mar;172(3):1535-44
references.pmid: 16387865
references.citation: J Clin Microbiol. 1996 Jan;34(1):87-93
references.pmid: 8748280
references.citation: PLoS One. 2007 Oct 03;2(10):e970
references.pmid: 17912349
references.citation: J Antimicrob Chemother. 1997 Sep;40(3):401-14
references.pmid: 9338494
references.citation: Plant Cell. 1990 Aug;2(8):731-9
references.pmid: 2152124
references.citation: Mol Cell Biol. 1991 Jan;11(1):55-62
references.pmid: 1986246
references.citation: ACS Chem Biol. 2012 Mar 16;7(3):599-606
references.pmid: 22234162
references.citation: Genetics. 2001 Feb;157(2):591-600
references.pmid: 11156981