Signaling pathways for stress responses and adaptation in Aspergillus species: stress biology in the post-genomic era

References

• Wyatt TT, Wösten HA, Dijksterhuis J. Fungal spores for dispersion in space and time. Adv. Appl. Microbiol. 2013;85:43–91.10.1016/B978-0-12-407672-3.00002-2
   PubMed Web of Science ®Google Scholar
• Adams TH, Yu JH. Coordinate control of secondary metabolite production and asexual sporulation in Aspergillus nidulans. Curr. Opin. Microbiol. 1998;1:674–677.10.1016/S1369-5274(98)80114-8
   PubMed Web of Science ®Google Scholar
• Etxebeste O, Garzia A, Espeso EA, et al. Aspergillus nidulans asexual development: making the most of cellular modules. Trends Microbiol. 2010;18:569–576.10.1016/j.tim.2010.09.007
   PubMed Web of Science ®Google Scholar
• Fischer R, Kües U. Asexual sporulation in mycelial fungi. In: Kües U, Fischer R, editors. The mycota: growth, differentiation and sexuality. Vol. 1. Berlin: Springer; 2006. p. 263–292.
   Google Scholar
• Galagan JE, Calvo SE, Cuomo C, et al. Sequencing of Aspergillus nidulans and comparative analysis with A. fumigatus and A. oryzae. Nature. 2005;438:1105–1115.10.1038/nature04341
   PubMed Web of Science ®Google Scholar
• Machida M, Asai K, Sano M, et al. Genome sequencing and analysis of Aspergillus oryzae. Nature. 2005;438:1157–1161.10.1038/nature04300
   PubMed Web of Science ®Google Scholar
• Nierman WC, Pain A, Anderson MJ, et al. Genomic sequence of the pathogenic and allergenic filamentous fungus Aspergillus fumigatus. Nature. 2005;438:1151–1156.10.1038/nature04332
   PubMed Web of Science ®Google Scholar
• Pel HJ, de Winde JH, Archer DB, et al. Genome sequencing and analysis of the versatile cell factory Aspergillus niger CBS 513.88. Nat. Biotechnol. 2007;25:221–231.10.1038/nbt1282
   PubMed Web of Science ®Google Scholar
• Hohmann S. Osmotic stress signaling and osmoadaptation in yeasts. Microbiol. Mol. Biol. Rev. 2002;66:300–372.10.1128/MMBR.66.2.300-372.2002
   PubMed Web of Science ®Google Scholar
• Chen RE, Thorner J. Function and regulation in MAPK signaling pathways: lessons learned from the yeast Saccharomyces cerevisiae. Biochim. Biophys. Acta. 2007;1773:1311–1340.10.1016/j.bbamcr.2007.05.003
   PubMed Web of Science ®Google Scholar
• Elion EA. Pheromone response, mating and cell biology. Curr. Opin. Microbiol. 2000;3:573–581.10.1016/S1369-5274(00)00143-0
   PubMed Web of Science ®Google Scholar
• Fitzgibbon GJ, Morozov IY, Jones MG, et al. Genetic analysis of the TOR pathway in Aspergillus nidulans. Eukaryotic Cell. 2005;4:1595–1598.10.1128/EC.4.9.1595-1598.2005
   PubMed Web of Science ®Google Scholar
• Conrad M, Schothorst J, Kankipati HN, et al. Nutrient sensing and signaling in the yeast Saccharomyces cerevisiae. FEMS Microbiol. Rev. 2014;38:254–299.10.1111/1574-6976.12065
   PubMed Web of Science ®Google Scholar
• Taj G, Agarwal P, Grant M, et al. MAPK machinery in plants: recognition and response to different stresses through multiple signal transduction pathways. Plant Signal. Behav. 2010;5:1370–1378.10.4161/psb.5.11.13020
   PubMed Web of Science ®Google Scholar
• Schaeffer HJ, Weber MJ. Mitogen-activated protein kinases: specific messages from ubiquitous messengers. Mol. Cell. Biol. 1999;19:2435–2444.10.1128/MCB.19.4.2435
   PubMed Web of Science ®Google Scholar
• Reiser V, Ruis H, Ammerer G. Kinase activity-dependent nuclear export opposes stress-induced nuclear accumulation and retention of hog1 mitogen-activated protein kinase in the budding yeast Saccharomyces cerevisiae. Mol. Biol. Cell. 1999;10:1147–1161.10.1091/mbc.10.4.1147
   PubMed Web of Science ®Google Scholar
• Krisak L, Strich R, Winters RS, et al. SMK1, a developmentally regulated MAP kinase, is required for spore wall assembly in Saccharomyces cerevisiae. Genes Dev. 1994;8:2151–2161.10.1101/gad.8.18.2151
   PubMed Web of Science ®Google Scholar
• Jun SC, Lee SJ, Park HJ, et al. 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. 2011;49:418–430.10.1007/s12275-011-0193-3
   PubMed Web of Science ®Google Scholar
• Kang JY, Chun J, Jun SC, et al. The MpkB MAP kinase plays a role in autolysis and conidiation of Aspergillus nidulans. Fungal Genet. Biol. 2013;61:42–49.10.1016/j.fgb.2013.09.010
   PubMed Web of Science ®Google Scholar
• Atoui A, Bao D, Kaur N, et al. Aspergillus nidulans natural product biosynthesis is regulated by MpkB, a putative pheromone response mitogen-activated protein kinase. Appl. Environ. Microbiol. 2008;74:3596–3600.10.1128/AEM.02842-07
   PubMed Web of Science ®Google Scholar
• Yoshimi A, Fujioka T, Mizutani O, et al. Mitogen-activated protein kinases MpkA and MpkB independently affect micafungin sensitivity in Aspergillus nidulans. Biosci. Biotechnol. Biochem. 2015;79:836–844.10.1080/09168451.2014.998619
   PubMed Web of Science ®Google Scholar
• Wei H, Requena N, Fischer R. The MAPKK kinase SteC regulates conidiophore morphology and is essential for heterokaryon formation and sexual development in the homothallic fungus Aspergillus nidulans. Mol. Microbiol. 2003;47:1577–1588.10.1046/j.1365-2958.2003.03405.x
   PubMed Web of Science ®Google Scholar
• Bayram Ö, Bayram ÖS, Ahmed YL, et al. The Aspergillus nidulans MAPK module AnSte11-Ste50-Ste7-Fus3 controls development and secondary metabolism. PLoS Genet. 2012;8:e1002816.10.1371/journal.pgen.1002816
   PubMed Web of Science ®Google Scholar
• Jung US, Levin DE. Genome-wide analysis of gene expression regulated by the yeast cell wall integrity signalling pathway. Mol. Microbiol. 1999;34:1049–1057.10.1046/j.1365-2958.1999.01667.x
   PubMed Web of Science ®Google Scholar
• Bussink HJ, Osmani SA. A mitogen-activated protein kinase (MPKA) is involved in polarized growth in the filamentous fungus, Aspergillus nidulans. FEMS Microbiol. Lett. 1999;173:117–125.10.1111/fml.1999.173.issue-1
   PubMed Web of Science ®Google Scholar
• Fujioka T, Mizutani O, Furukawa K, et al. MpkA-dependent and -independent cell wall integrity signaling in Aspergillus nidulans. Eukaryotic Cell. 2007;6:1497–1510.10.1128/EC.00281-06
   PubMed Web of Science ®Google Scholar
• Furukawa K, Hoshi Y, Maeda T. et al. Aspergillus nidulans HOG pathway is activated only by two-component signalling pathway in response to osmotic stress. Mol. Microbiol. 2005;56:1246–1261.10.1111/j.1365-2958.2005.04605.x
   PubMed Web of Science ®Google Scholar
• Bahn YS. Master and commander in fungal pathogens: the two-component system and the HOG signaling pathway. Eukaryotic Cell. 2008;7:2017–2036.10.1128/EC.00323-08
   PubMed Web of Science ®Google Scholar
• Rispail N, Soanes DM, Ant C, et al. Comparative genomics of MAP kinase and calcium-calcineurin signalling components in plant and human pathogenic fungi. Fungal Genet. Biol. 2009;46:287–298.10.1016/j.fgb.2009.01.002
   PubMed Web of Science ®Google Scholar
• Hamel LP, Nicole MC, Duplessis S, et al. Mitogen-activated protein kinase signaling in plant-interacting fungi: distinct messages from conserved messengers. Plant Cell. 2012;24:1327–1351.10.1105/tpc.112.096156
   PubMed Web of Science ®Google Scholar
• Kawasaki L, Sanchez O, Shiozaki K. et al. SakA MAP kinase is involved in stress signal transduction, sexual development and spore viability in Aspergillus nidulans. Mol. Microbiol. 2002;45:1153–1163.10.1046/j.1365-2958.2002.03087.x
   Google Scholar
• Lara-Rojas F, Sánchez O, Kawasaki L. et al. Aspergillus nidulans transcription factor AtfA interacts with the MAPK SakA to regulate general stress responses, development and spore functions. Mol. Microbiol. 2011;80:436–454.10.1111/mmi.2011.80.issue-2
   PubMed Web of Science ®Google Scholar
• Hagiwara D, Takahashi-Nakaguchi A, Toyotome T, et al. NikA/TcsC histidine kinase is involved in conidiation, hyphal morphology, and responses to osmotic stress and antifungal chemicals in Aspergillus fumigatus. PLoS One. 2013;8:e80881.10.1371/journal.pone.0080881
   PubMed Web of Science ®Google Scholar
• Xue T, Nguyen CK, Romans A. et al. A mitogen-activated protein kinase that senses nitrogen regulates conidial germination and growth in Aspergillus fumigatus. Eukaryotic Cell. 2004;3:557–560.10.1128/EC.3.2.557-560.2004
   PubMed Web of Science ®Google Scholar
• de Castro PA, Chen C, de Almeida RS, et al. ChIP-seq reveals a role for CrzA in the Aspergillus fumigatus high-osmolarity glycerol response (HOG) signalling pathway. Mol. Microbiol. 2014;94:655–674.10.1111/mmi.2014.94.issue-3
   PubMed Web of Science ®Google Scholar
• Reyes G, Romans A, Nguyen CK, et al. Novel mitogen-activated protein kinase MpkC of Aspergillus fumigatus is required for utilization of polyalcohol sugars. Eukaryotic Cell. 2006;5:1934–1940.10.1128/EC.00178-06
   PubMed Web of Science ®Google Scholar
• Hagiwara D, Suzuki S, Kamei K, et al. The role of AtfA and HOG MAPK pathway in stress tolerance in conidia of Aspergillus fumigatus. Fungal Genet. Biol. 2014;73:138–149.10.1016/j.fgb.2014.10.011
   PubMed Web of Science ®Google Scholar
• Hoch JA, Silhavy TJ. Two-component signal transduction. Washington DC: ASM Press; 1995.
   Google Scholar
• Mizuno T. His-Asp phosphotransfer signal transduction. J. Biochem. 1998;123:555–563.10.1093/oxfordjournals.jbchem.a021972
   PubMed Web of Science ®Google Scholar
• Shor E, Chauhan N. A case for two-component signaling systems as antifungal drug targets. PLoS Pathog. 2015;11:e1004632.10.1371/journal.ppat.1004632
   PubMed Web of Science ®Google Scholar
• Defosse TA, Sharma A, Mondal AK, et al. Hybrid histidine kinases in pathogenic fungi. Mol. Microbiol. 2015;95:914–924.10.1111/mmi.12911
   PubMed Web of Science ®Google Scholar
• Nakamichi N, Yamada H, Aoyama K, et al. His-to-Asp phosphorelay circuitry for regulation of sexual development in Schizosaccharomyces pombe. Biosci. Biotechnol. Biochem. 2002;66:2663–2672.10.1271/bbb.66.2663
   PubMed Web of Science ®Google Scholar
• Nakamichi N, Yanada H, Aiba H, et al. Characterization of the Prr1 response regulator with special reference to sexual development in Schizosaccharomyces pombe. Biosci. Biotechnol. Biochem. 2003;67:547–555.10.1271/bbb.67.547
   PubMed Web of Science ®Google Scholar
• Morigasaki S, Shiozaki K. Two-component signaling to the stress MAP kinase cascade in fission yeast. Methods Enzymol. 2010;471:279–289.10.1016/S0076-6879(10)71015-6
   PubMed Web of Science ®Google Scholar
• Kobayashi T, Abe K, Asai K, et al. Genomics of Aspergillus oryzae. Biosci. Biotechnol. Biochem. 2007;71:646–670.10.1271/bbb.60550
   PubMed Web of Science ®Google Scholar
• Hagiwara D, Asano Y, Marui J, et al. The SskA and SrrA response regulators are implicated in oxidative stress responses of hyphae and asexual spores in the phosphorelay signaling network of Aspergillus nidulans. Biosci. Biotechnol. Biochem. 2007;71:1003–1014.10.1271/bbb.60665
   PubMed Web of Science ®Google Scholar
• Vargas-Pérez I, Sánchez O, Kawasaki L. et al. Response regulators SrrA and SskA are central components of a phosphorelay system involved in stress signal transduction and asexual sporulation in Aspergillus nidulans. Eukaryotic Cell. 2007;6:1570–1583.10.1128/EC.00085-07
   PubMed Web of Science ®Google Scholar
• Krems B, Charizanis C, Entian KD. The response regulator-like protein Pos9/Skn7 of Saccharomyces cerevisiae is involved in oxidative stress resistance. Curr. Genet. 1996;29:327–334.10.1007/BF02208613
   PubMed Web of Science ®Google Scholar
• Ohmiya R, Kato C, Yamada H, et al. A fission yeast gene (prr1(+)) that encodes a response regulator implicated in oxidative stress response. J. Biochem. 1999;125:1061–1066.10.1093/oxfordjournals.jbchem.a022387
   PubMed Web of Science ®Google Scholar
• Lee J, Godon C, Lagniel G, et al. Yap1 and Skn7 control two specialized oxidative stress response regulons in yeast. J. Biol. Chem. 1999;274:16040–16046.10.1074/jbc.274.23.16040
   PubMed Web of Science ®Google Scholar
• Kuge S, Arita M, Murayama A, et al. Regulation of the yeast Yap1p nuclear export signal is mediated by redox signal-induced reversible disulfide bond formation. Mol. Cell Biol. 2001;21:6139–6150.10.1128/MCB.21.18.6139-6150.2001
   PubMed Web of Science ®Google Scholar
• Lamarre C, Ibrahim-Granet O, Du C, et al. Characterization of the SKN7 ortholog of Aspergillus fumigatus. Fungal Genet. Biol. 2007;44:682–690.10.1016/j.fgb.2007.01.009
   PubMed Web of Science ®Google Scholar
• Nakamura H, Kikuma T, Jin FJ, et al. AoRim15 is involved in conidial stress tolerance, conidiation and sclerotia formation in the filamentous fungus Aspergillus oryzae. J. Biosci. Bioeng. 2016. doi: 10.1016/j.jbiosc.2015.08.011. Epub ahead of print.
   PubMed Web of Science ®Google Scholar
• Lavín JL, García-Yoldi A, Ramírez L, et al. Two-component signal transduction in Agaricus bisporus: a comparative genomic analysis with other basidiomycetes through the web-based tool BASID2CS. Fungal Genet. Biol. 2013;55:77–84.10.1016/j.fgb.2012.09.012
   PubMed Web of Science ®Google Scholar
• Furukawa K, Katsuno Y, Urao T, et al. Isolation and functional analysis of a gene, tcsB, encoding a transmembrane hybrid-type histidine kinase from Aspergillus nidulans. Appl. Environ. Microbiol. 2002;68:5304–5310.10.1128/AEM.68.11.5304-5310.2002
   PubMed Web of Science ®Google Scholar
• Ji Y, Yang F, Ma D, et al. HOG-MAPK signaling regulates the adaptive responses of Aspergillus fumigatus to thermal stress and other related stress. Mycopathologia. 2012;174:273–282.10.1007/s11046-012-9557-4
   PubMed Web of Science ®Google Scholar
• Virginia M, Appleyard CL, McPheat WL, et al. A novel ‘two-component’ protein containing histidine kinase and response regulator domains required for sporulation in Aspergillus nidulans. Curr. Genet. 2000;37:364–372.
   PubMed Web of Science ®Google Scholar
• Tüncher A, Reinke H, Martic G, et al. A basic-region helix-loop-helix protein-encoding gene (devR) involved in the development of Aspergillus nidulans. Mol. Microbiol. 2004;52:227–241.10.1111/j.1365-2958.2003.03961.x
   PubMed Web of Science ®Google Scholar
• Aoyama K, Aiba H, Mizuno T. Genetic analysis of the His-to-Asp phosphorelay implicated in mitotic cell cycle control: involvement of histidine-kinase genes of Schizosaccharomyces pombe. Biosci. Biotechnol. Biochem. 2001;65:2347–2352.10.1271/bbb.65.2347
   PubMed Web of Science ®Google Scholar
• Hayashi S, Yoshioka M, Matsui T, et al. Control of reactive oxygen species (ROS) production through histidine kinases in Aspergillus nidulans under different growth conditions. FEBS Open Bio. 2014;4:90–95.10.1016/j.fob.2014.01.003
   PubMed Web of Science ®Google Scholar
• Meena N, Kaur H, Mondal AK. Interactions among HAMP domain repeats act as an osmosensing molecular switch in group III hybrid histidine kinases from fungi. J. Biol. Chem. 2010;285:12121–12132.10.1074/jbc.M109.075721
   PubMed Web of Science ®Google Scholar
• El-Mowafy M, Bahgat MM, Bilitewski U. Deletion of the HAMP domains from the histidine kinase CaNik1p of Candida albicans or treatment with fungicides activates the MAP kinase Hog1p in S. cerevisiae transformants. BMC Microbiol. 2013;13:209.10.1186/1471-2180-13-209
   PubMed Web of Science ®Google Scholar
• Hagiwara D, Mizuno T, Abe K. Characterization of NikA histidine kinase and two response regulators with special reference to osmotic adaptation and asexual development in Aspergillus nidulans. Biosci. Biotechnol. Biochem. 2009;73:1566–1571.10.1271/bbb.90063
   PubMed Web of Science ®Google Scholar
• Motoyama T, Ohira T, Kadokura K. et al. An Os-1 family histidine kinase from a filamentous fungus confers fungicide-sensitivity to yeast. Curr. Genet. 2005;47:298–306.10.1007/s00294-005-0572-6
   PubMed Web of Science ®Google Scholar
• Dongo A, Bataillé-Simoneau N, Campion C, et al. The group III two-component histidine kinase of filamentous fungi is involved in the fungicidal activity of the bacterial polyketide ambruticin. Appl. Environ. Microbiol. 2009;75:127–134.10.1128/AEM.00993-08
   PubMed Web of Science ®Google Scholar
• Hagiwara D, Matsubayashi Y, Marui J, et al. Characterization of the NikA histidine kinase implicated in the phosphorelay signal transduction of Aspergillus nidulans, with special reference to fungicide responses. Biosci. Biotechnol. Biochem. 2007;71:844–847.10.1271/bbb.70051
   PubMed Web of Science ®Google Scholar
• Izumitsu K, Yoshimi A, Tanaka C. Two-component response regulators Ssk1p and Skn7p additively regulate high-osmolarity adaptation and fungicide sensitivity in Cochliobolus heterostrophus. Eukaryotic Cell. 2007;6:171–181.10.1128/EC.00326-06
   PubMed Web of Science ®Google Scholar
• Rispail N, Di Pietro A. The two-component histidine kinase Fhk1 controls stress adaptation and virulence of Fusarium oxysporum. Mol. Plant Pathol. 2010;11:395–407.10.1111/mpp.2010.11.issue-3
   PubMed Web of Science ®Google Scholar
• Viaud M, Fillinger S, Liu W, et al. A class III histidine kinase acts as a novel virulence factor in Botrytis cinerea. Mol. Plant Microbe Interact. 2006;19:1042–1050.10.1094/MPMI-19-1042
   PubMed Web of Science ®Google Scholar
• Brandt S, von Stetten D, Gunther M, et al. The fungal phytochrome FphA from Aspergillus nidulans. J. Biol. Chem. 2008;283:34605–34614.10.1074/jbc.M805506200
   PubMed Web of Science ®Google Scholar
• Blumenstein A, Vienken K, Tasler R, et al. The Aspergillus nidulans phytochrome FphA represses sexual development in red light. Curr. Biol. 2005;15:1833–1838.10.1016/j.cub.2005.08.061
   PubMed Web of Science ®Google Scholar
• Purschwitz J, Müller S, Kastner C, et al. Functional and physical interaction of blue- and red-light sensors in Aspergillus nidulans. Curr. Biol. 2008;18:255–259.10.1016/j.cub.2008.01.061
   PubMed Web of Science ®Google Scholar
• Suzuki A, Kanamaru K, Azuma N, et al. GFP-tagged expression analysis revealed that some histidine kinases of Aspergillus nidulans show temporally and spatially different expression during the life cycle. Biosci. Biotechnol. Biochem. 2008;72:428–434.10.1271/bbb.70543
   PubMed Web of Science ®Google Scholar
• Hagiwara D, Asano Y, Marui J, et al. Transcriptional profiling for Aspergillus nidulans HogA MAPK signaling pathway in response to fludioxonil and osmotic stress. Fungal Genet. Biol. 2009;46:868–878.10.1016/j.fgb.2009.07.003
   PubMed Web of Science ®Google Scholar
• Losada L, Barker BM, Pakala S, et al. Large-scale transcriptional response to hypoxia in Aspergillus fumigatus observed using RNAseq identifies a novel hypoxia regulated ncRNA. Mycopathologia. 2014;178:331–339.10.1007/s11046-014-9779-8
   PubMed Web of Science ®Google Scholar
• Posas F, Wurgler-Murphy SM, Maeda T, et al. Yeast HOG1 MAP kinase cascade is regulated by a multistep phosphorelay mechanism in the SLN1–YPD1–SSK1 “two-component” osmosensor. Cell. 1996;86:865–875.10.1016/S0092-8674(00)80162-2
   PubMed Web of Science ®Google Scholar
• Aoyama K, Mitsubayashi Y, Aiba H, et al. Spy1, a histidine-containing phosphotransfer signaling protein, regulates the fission yeast cell cycle through the Mcs4 response regulator. J. Bacteriol. 2000;182:4868–4874.10.1128/JB.182.17.4868-4874.2000
   PubMed Web of Science ®Google Scholar
• Nguyen AN, Lee A, Place W, et al. Multistep phosphorelay proteins transmit oxidative stress signals to the fission yeast stress-activated protein kinase. Mol. Biol. Cell. 2000;11:1169–1181.10.1091/mbc.11.4.1169
   PubMed Web of Science ®Google Scholar
• Mavrianos J, Desai C, Chauhan N. Two-component histidine phosphotransfer protein ypd1 is not essential for viability in Candida albicans. Eukaryotic Cell. 2014;13:452–460.10.1128/EC.00243-13
   PubMed Web of Science ®Google Scholar
• Banno S, Noguchi R, Yamashita K, et al. Roles of putative His-to-Asp signaling modules HPT-1 and RRG-2, on viability and sensitivity to osmotic and oxidative stresses in Neurospora crassa. Curr. Genet. 2007;51:197–208.10.1007/s00294-006-0116-8
   PubMed Web of Science ®Google Scholar
• Jacob S, Foster AJ, Yemelin A, et al. High osmolarity glycerol (HOG) signalling in Magnaporthe oryzae: identification of MoYPD1 and its role in osmoregulation, fungicide action, and pathogenicity. Fungal Biol. 2015;119:580–594.10.1016/j.funbio.2015.03.003
   PubMed Web of Science ®Google Scholar
• Wong Sak Hoi J, Dumas B. Ste12 and Ste12-like proteins, fungal transcription factors regulating development and pathogenicity. Eukaryotic Cell. 2010;9:480–485.
   PubMed Web of Science ®Google Scholar
• Vallim MA, Miller KY, Miller BL. Aspergillus SteA (Sterile12-like) is a homeodomain-C2/H2-Zn+2 finger transcription factor required for sexual reproduction. Mol. Microbiol. 2000;36:290–301.10.1046/j.1365-2958.2000.01874.x
   PubMed Web of Science ®Google Scholar
• Morita H, Hatamoto O, Masuda T, et al. Function analysis of steA homolog in Aspergillus oryzae. Fungal Genet. Biol. 2007;44:330–338.10.1016/j.fgb.2006.10.009
   PubMed Web of Science ®Google Scholar
• Proft M, Serrano R. Repressors and upstream repressing sequences of the stress-regulated ENA1 gene in saccharomyces cerevisiae: bZIP protein Sko1p confers HOG-dependent osmotic regulation. Mol. Cell. Biol. 1999;19:537–546.10.1128/MCB.19.1.537
   PubMed Web of Science ®Google Scholar
• Rep M, Reiser V, Gartner U, et al. Osmotic stress-induced gene expression in Saccharomyces cerevisiae requires Msn1p and the novel nuclear factor Hot1p. Mol. Cell. Biol. 1999;19:5474–5485.10.1128/MCB.19.8.5474
   PubMed Web of Science ®Google Scholar
• Proft M, Struhl K. Hog1 kinase converts the Sko1-Cyc8-Tup1 repressor complex into an activator that recruits SAGA and SWI/SNF in response to osmotic stress. Mol. Cell. 2002;9:1307–1317.10.1016/S1097-2765(02)00557-9
   PubMed Web of Science ®Google Scholar
• Rep M, Krantz M, Thevelein JM, et al. The transcriptional response of Saccharomyces cerevisiae to osmotic shock. Hot1p and Msn2p/Msn4p are required for the induction of subsets of high osmolarity glycerol pathway-dependent genes. J. Biol. Chem. 2000;275:8290–8300.10.1074/jbc.275.12.8290
   PubMed Web of Science ®Google Scholar
• Shiozaki K, Russell P. Conjugation, meiosis, and the osmotic stress response are regulated by Spc1 kinase through Atf1 transcription factor in fission yeast. Genes Dev. 1996;10:2276–2288.10.1101/gad.10.18.2276
   PubMed Web of Science ®Google Scholar
• Wilkinson MG, Samuels M, Takeda T, et al. The Atf1 transcription factor is a target for the Sty1 stress-activated MAP kinase pathway in fission yeast. Genes Dev. 1996;10:2289–2301.10.1101/gad.10.18.2289
   PubMed Web of Science ®Google Scholar
• Hagiwara D, Asano Y, Yamashino T, et al. Characterization of bZip-type transcription factor AtfA with reference to stress responses of conidia of Aspergillus nidulans. Biosci. Biotechnol. Biochem. 2008;72:2756–2760.10.1271/bbb.80001
   PubMed Web of Science ®Google Scholar
• Damveld RA, Arentshorst M, Franken A, et al. The Aspergillus niger MADS-box transcription factor RlmA is required for cell wall reinforcement in response to cell wall stress. Mol. Microbiol. 2005;58:305–319.10.1111/j.1365-2958.2005.04827.x
   PubMed Web of Science ®Google Scholar
• Ji H, Lu X, Wang C, et al. Identification of a novel HOG1 homologue from an industrial glycerol producer Candida glycerinogenes. Curr. Microbiol. 2014;69:909–914.10.1007/s00284-014-0670-0
   PubMed Web of Science ®Google Scholar
• Zajc J, Kogej T, Galinski EA, et al. Osmoadaptation strategy of the most halophilic fungus, Wallemia ichthyophaga, growing optimally at salinities above 15% NaCl. Appl. Environ. Microbiol. 2014;80:247–256.10.1128/AEM.02702-13
   PubMed Web of Science ®Google Scholar
• Kayingo G, Wong B. The MAP kinase Hog1p differentially regulates stress-induced production and accumulation of glycerol and D-arabitol in Candida albicans. Microbiology. 2005;151:2987–2999.10.1099/mic.0.28040-0
   PubMed Web of Science ®Google Scholar
• Miskei M, Karányi Z, Pócsi I. Annotation of stress-response proteins in the aspergilli. Fungal Genet. Biol. 2008;46 (Suppl 1):S105–S120.
   Google Scholar
• Fillinger S, Ruijter G, Tamás MJ, et al. Molecular and physiological characterization of the NAD-dependent glycerol 3-phosphate dehydrogenase in the filamentous fungus Aspergillus nidulans. Mol. Microbiol. 2001;39:145–157.10.1046/j.1365-2958.2001.02223.x
   PubMed Web of Science ®Google Scholar
• Furukawa K, Yoshimi A, Furukawa T, et al. Novel reporter gene expression systems for monitoring activation of the Aspergillus nidulans HOG pathway. Biosci. Biotechnol. Biochem. 2007;71:1724–1730.10.1271/bbb.70131
   PubMed Web of Science ®Google Scholar
• Witteveen CFB, Visser J. Polyol pools in Aspergillus niger. FEMS Microbiol. Lett. 1995;134:57–62.10.1111/fml.1995.134.issue-1
   PubMed Web of Science ®Google Scholar
• Beever RE, Laracy EP. Osmotic adjustment in the filamentous fungus Aspergillus nidulans. J. Bacteriol. 1986;168:1358–1365.
   PubMed Web of Science ®Google Scholar
• Redkar RJ, Locy RD, Singh NK. Biosynthetic pathways of glycerol accumulation under salt stress in Aspergillus nidulans. Exp. Mycol. 1995;19:241–246.10.1006/emyc.1995.1030
   PubMedGoogle Scholar
• Kelavkar UP, Chhatpar HS. Polyol concentrations in Aspergillus repens grown under salt stress. World J. Microbiol. Biotechnol. 1993;9:579–582.10.1007/BF00386298
   PubMed Web of Science ®Google Scholar
• Mellon JE, Dowd MK, Cotty PJ. Time course study of substrate utilization by Aspergillus flavus in medium simulating corn (Zea mays) kernels. J. Agric. Food Chem. 2002;50:648–652.10.1021/jf011048e
   PubMed Web of Science ®Google Scholar
• Ross SJ, Findlay VJ, Malakasi P, et al. Thioredoxin peroxidase is required for the transcriptional response to oxidative stress in budding yeast. Mol. Biol. Cell. 2000;11:2631–2642.10.1091/mbc.11.8.2631
   PubMed Web of Science ®Google Scholar
• Moye-Rowley WS. Regulation of the transcriptional response to oxidative stress in fungi: similarities and differences. Eukaryotic Cell. 2003;2:381–389.10.1128/EC.2.3.381-389.2003
   PubMed Web of Science ®Google Scholar
• Ikner A, Shiozaki K. Yeast signaling pathways in the oxidative stress response. Mutat. Res. 2005;569:13–27.10.1016/j.mrfmmm.2004.09.006
   PubMed Web of Science ®Google Scholar
• Asano Y, Hagiwara D, Yamashino T, et al. Characterization of the bZip-type transcription factor NapA with reference to oxidative stress response in Aspergillus nidulans. Biosci. Biotechnol. Biochem. 2007;71:1800–1803.10.1271/bbb.70133
   PubMed Web of Science ®Google Scholar
• Lessing F, Kniemeyer O, Wozniok I, et al. The Aspergillus fumigatus transcriptional regulator AfYap1 represents the major regulator for defense against reactive oxygen intermediates but is dispensable for pathogenicity in an intranasal mouse infection model. Eukaryotic Cell. 2007;6:2290–2302.10.1128/EC.00267-07
   PubMed Web of Science ®Google Scholar
• Hon T, Dodd A, Dirmeier R, et al. A mechanism of oxygen sensing in yeast: Multiple oxygen-responsive steps in the heme biosynthetic pathway affect hap1 activity. J. Biol. Chem. 2003;278:50771–50780.10.1074/jbc.M303677200
   PubMed Web of Science ®Google Scholar
• Davies BS, Rine J. A role for sterol levels in oxygen sensing in Saccharomyces cerevisiae. Genetics. 2006;174:191–201.10.1534/genetics.106.059964
   PubMed Web of Science ®Google Scholar
• Masuo S, Terabayashi Y, Shimizu M, et al. Global gene expression analysis of Aspergillus nidulans reveals metabolic shift and transcription suppression under hypoxia. Mol. Genet. Genomics. 2010;284:415–424.10.1007/s00438-010-0576-x
   PubMed Web of Science ®Google Scholar
• Vödisch M, Scherlach K, Winkler R, et al. Analysis of the Aspergillus fumigatus proteome reveals metabolic changes and the activation of the pseurotin a biosynthesis gene cluster in response to hypoxia. J. Proteome Res. 2011;10:2508–2524.10.1021/pr1012812
   PubMed Web of Science ®Google Scholar
• Willger SD, Puttikamonkul S, Kim KH, et al. A sterol-regulatory element binding protein is required for cell polarity, hypoxia adaptation, azole drug resistance, and virulence in Aspergillus fumigatus. PLoS Pathog. 2008;4:e1000200.10.1371/journal.ppat.1000200
   PubMed Web of Science ®Google Scholar
• Chung D, Barker BM, Carey CC, et al. ChIP-seq and in vivo transcriptome analyses of the Aspergillus fumigatus SREBP SrbA reveals a new regulator of the fungal hypoxia response and virulence. PLoS Pathog. 2014;10:e1004487.10.1371/journal.ppat.1004487
   Google Scholar
• Grahl N, Shepardson KM, Chung D, et al. Hypoxia and fungal pathogenesis: to air or not to air? Eukaryotic Cell. 2012;11:560–570.10.1128/EC.00031-12
   PubMed Web of Science ®Google Scholar
• Chun CD, Liu OW, Madhani HD. A link between virulence and homeostatic responses to hypoxia during infection by the human fungal pathogen Cryptococcus neoformans. PLoS Pathog. 2007;3:e22.10.1371/journal.ppat.0030022
   PubMed Web of Science ®Google Scholar
• Kroll K, Pähtz V, Hillmann F, et al. Identification of hypoxia-inducible target genes of Aspergillus fumigatus by transcriptome analysis reveals cellular respiration as an important contributor to hypoxic survival. Eukaryotic Cell. 2014;13:1241–1253.10.1128/EC.00084-14
   PubMed Web of Science ®Google Scholar
• Kozakiewicsz Z, Smith D. Physiology of Aspergillus. In: Smith JE, editor. Biotechnology handbooks – 7: Aspergillus. New York, NY: Plenum Press; 1994. p. 23–40.
   Google Scholar
• Burnie JP, Carter TL, Hodgetts SJ, et al. Fungal heat-shock proteins in human disease. FEMS Microbiol. Rev. 2006;30:53–88.10.1111/j.1574-6976.2005.00001.x
   PubMed Web of Science ®Google Scholar
• Li ZW, Li X, Yu QY, et al. The small heat shock protein (sHSP) genes in the silkworm, Bombyx mori, and comparative analysis with other insect sHSP genes. BMC Evol. Biol. 2009;9:215.10.1186/1471-2148-9-215
   PubMed Web of Science ®Google Scholar
• Freitas JS, Silva EM, Leal J, et al. Transcription of the Hsp30, Hsp70, and Hsp90 heat shock protein genes is modulated by the PalA protein in response to acid pH-sensing in the fungus Aspergillus nidulans. Cell Stress Chaperones. 2011;16:565–572.10.1007/s12192-011-0267-5
   PubMed Web of Science ®Google Scholar
• Lamoth F, Juvvadi PR, Fortwendel JR, et al. Heat shock protein 90 is required for conidiation and cell wall integrity in Aspergillus fumigatus. Eukaryotic Cell. 2012;11:1324–1332.10.1128/EC.00032-12
   PubMed Web of Science ®Google Scholar
• Wu J, Wang M, Zhou L, et al. Small heat shock proteins, phylogeny in filamentous fungi and expression analyses in Aspergillus nidulans. Gene. 2016;575:675–679.10.1016/j.gene.2015.09.044
   PubMed Web of Science ®Google Scholar
• Al-Bader N, Vanier G, Liu H, et al. Role of trehalose biosynthesis in Aspergillus fumigatus development, stress response, and virulence. Infect. Immun. 2010;78:3007–3018.10.1128/IAI.00813-09
   PubMed Web of Science ®Google Scholar
• Fillinger S, Chaveroche MK, van Dijck P, et al. Trehalose is required for the acquisition of tolerance to a variety of stresses in the filamentous fungus Aspergillus nidulans. Microbiology. 2001;147:1851–1862.10.1099/00221287-147-7-1851
   PubMed Web of Science ®Google Scholar
• An MZ, Tang YQ, Mitsumasu K, et al. Enhanced thermotolerance for ethanol fermentation of Saccharomyces cerevisiae strain by overexpression of the gene coding for trehalose-6-phosphate synthase. Biotechnol. Lett. 2011;33:1367–1374.10.1007/s10529-011-0576-x
   PubMed Web of Science ®Google Scholar
• Albrecht D, Guthke R, Brakhage AA, et al. Integrative analysis of the heat shock response in Aspergillus fumigatus. BMC Genomics. 2010;11:32.10.1186/1471-2164-11-32
   PubMed Web of Science ®Google Scholar
• Do JH, Yamaguchi R, Miyano S. Exploring temporal transcription regulation structure of Aspergillus fumigatus in heat shock by state space model. BMC Genomics. 2009;10:306.10.1186/1471-2164-10-306
   PubMed Web of Science ®Google Scholar
• Futagami T, Mori K, Wada S, et al. Transcriptomic analysis of temperature responses of Aspergillus kawachii during barley koji production. Appl. Environ. Microbiol. 2015;81:1353–1363.10.1128/AEM.03483-14
   PubMed Web of Science ®Google Scholar
• Aimanianda V, Bayry J, Bozza S, et al. Surface hydrophobin prevents immune recognition of airborne fungal spores. Nature. 2009;460:1117–1121.10.1038/nature08264
   PubMed Web of Science ®Google Scholar
• Grünbacher A, Throm T, Seidel C, et al. Six hydrophobins are involved in hydrophobin rodlet formation in Aspergillus nidulans and contribute to hydrophobicity of the spore surface. PLoS One. 2014;9:e94546.10.1371/journal.pone.0094546
   PubMed Web of Science ®Google Scholar
• Braga GU, Rangel DE, Fernandes ÉK, et al. Molecular and physiological effects of environmental UV radiation on fungal conidia. Curr. Genet. 2015;61:405–425.10.1007/s00294-015-0483-0
   PubMed Web of Science ®Google Scholar
• Chiang YM, Meyer KM, Praseuth M, et al. Characterization of a polyketide synthase in Aspergillus niger whose product is a precursor for both dihydroxynaphthalene (DHN) melanin and naphtho-γ-pyrone. Fungal Genet. Biol. 2011;48:430–437.10.1016/j.fgb.2010.12.001
   PubMed Web of Science ®Google Scholar
• Esbelin J, Mallea S, Ram AF, et al. Role of pigmentation in protecting Aspergillus niger conidiospores against pulsed light radiation. Photochem. Photobiol. 2013;89:758–761.10.1111/php.2013.89.issue-3
   PubMed Web of Science ®Google Scholar
• Heinekamp T, Thywißen A, Macheleidt J, et al. Aspergillus fumigatus melanins: interference with the host endocytosis pathway and impact on virulence. Front. Microbiol. 2013;3:440.
   PubMed Web of Science ®Google Scholar
• Thywißen A, Heinekamp T, Dahse HM, et al. Conidial dihydroxynaphthalene melanin of the human pathogenic fungus Aspergillus fumigatus interferes with the host endocytosis pathway. Front. Microbiol. 2011;2:96.
   PubMed Web of Science ®Google Scholar
• Volling K, Thywissen A, Brakhage AA, et al. Phagocytosis of melanized Aspergillus conidia by macrophages exerts cytoprotective effects by sustained PI3K/Akt signalling. Cell. Microbiol. 2011;13:1130–1148.10.1111/cmi.2011.13.issue-8
   PubMed Web of Science ®Google Scholar
• Hillmann F, Novohradská S, Mattern DJ, et al. Virulence determinants of the human pathogenic fungus Aspergillus fumigatus protect against soil amoeba predation. Environ. Microbiol. 2015;17:2858–2869.10.1111/1462-2920.12808
   PubMed Web of Science ®Google Scholar
• Navarro RE, Stringer MA, Hansberg W. et al. catA, a new Aspergillus nidulans gene encoding a developmentally regulated catalase. Curr. Genet. 1996;29:352–359.
   PubMed Web of Science ®Google Scholar
• Paris S, Wysong D, Debeaupuis JP, et al. Catalases of Aspergillus fumigatus. Infect. Immun. 2003;71:3551–3562.10.1128/IAI.71.6.3551-3562.2003
   PubMed Web of Science ®Google Scholar
• Hisada H, Hata Y, Kawato A, et al. Cloning and expression analysis of two catalase genes from Aspergillus oryzae. J. Biosci. Bioeng. 2005;99:562–568.10.1263/jbb.99.562
   PubMed Web of Science ®Google Scholar
• Sakamoto K, Iwashita K, Yamada O, et al. Aspergillus oryzae atfA controls conidial germination and stress tolerance. Fungal Genet. Biol. 2009;46:887–897.10.1016/j.fgb.2009.09.004
   PubMed Web of Science ®Google Scholar
• Sakamoto K, Arima TH, Iwashita K, et al. Aspergillus oryzae atfB encodes a transcription factor required for stress tolerance in conidia. Fungal Genet. Biol. 2008;45:922–932.10.1016/j.fgb.2008.03.009
   PubMed Web of Science ®Google Scholar
• Ruijter GJ, Bax M, Patel H, et al. Mannitol is required for stress tolerance in Aspergillus niger conidiospores. Eukaryotic Cell. 2003;2:690–698.10.1128/EC.2.4.690-698.2003
   PubMed Web of Science ®Google Scholar