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9 Transcriptomics of Industrial Filamentous Fungi: A New View on Regulation, Physiology, and Application

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Fungal Genomics

Part of the book series: The Mycota ((MYCOTA,volume 13))

Abstract

The filamentous fungi Aspergillus niger, A. oryzae, Penicillium chrysogenum and Trichoderma reesei represent an important group of industrial production hosts with unique properties in relation to metabolite and protein production. They serve as a major resource for applications and processes in areas such as food, feed, antibiotics, biofuel and chemical production. With the newly emerged ‘-omics’ era, system-wide insights into the genomic repertoire and physiology of industrial fungi are possible, and the last few years have therefore witnessed great advances in the understanding of their metabolic potential. This review summarizes the transcriptomics insights recently gained into gene regulation and physiology of these industrial cell factories. New concepts and ideas derived from this perspective that aim to engineer fungal metabolism for more sustainable bioprocesses and novel products are highlighted and discussed.

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References

  • Ahmed FE (2006) Microarray RNA transcriptional profiling: part i. Platforms, experimental design and standardization. Expert Rev Mol Diagn 6:535–550. doi:10.1586/14737159.6.4.535

    PubMed  CAS  Google Scholar 

  • Andersen MR, Nielsen ML, Nielsen J (2008a) Metabolic model integration of the bibliome, genome, metabolome and reactome of Aspergillus niger. Mol Syst Biol 4:178. doi:10.1038/msb.2008.12

    PubMed Central  PubMed  Google Scholar 

  • Andersen MR, Vongsangnak W, Panagiotou G, Salazar MP, Lehmann L, Nielsen J (2008b) A trispecies Aspergillus microarray: comparative transcriptomics of three Aspergillus species. Proc Natl Acad Sci U S A 105:4387–4392. doi:10.1073/pnas.0709964105

    PubMed Central  PubMed  CAS  Google Scholar 

  • Andersen MR, Lehmann L, Nielsen J (2009) Systemic analysis of the response of Aspergillus niger to ambient pH. Genome Biol 10:R47. doi:10.1186/gb-2009-10-5-r47

    PubMed Central  PubMed  Google Scholar 

  • Andersen MR, Salazar MP, Schaap PJ, van de Vondervoort PJI, Culley D, Thykaer J, Frisvad JC, Nielsen KF, Albang R, Albermann K, Berka RM, Braus GH, Braus-Stromeyer SA, Corrochano LM, Dai Z, van Dijck PWM, Hofmann G, Lasure LL, Magnuson JK, Menke H, Meijer M, Meijer SL, Nielsen JB, Nielsen ML, van Ooyen AJJ, Pel HJ, Poulsen L, Samson RA, Stam H, Tsang A, van den Brink JM, Atkins A, Aerts A, Shapiro H, Pangilinan J, Salamov A, Lou Y, Lindquist E, Lucas S, Grimwood J, Grigoriev IV, Kubicek CP, Martinez D, van Peij NNME, Roubos JA, Nielsen J, Baker SE (2011) Comparative genomics of citric-acid-producing Aspergillus niger ATCC 1015 versus enzyme-producing CBS 513.88. Genome Res 21:885–897. doi:10.1101/gr.112169.110

    PubMed Central  PubMed  CAS  Google Scholar 

  • Archer DB, Peberdy JE (1997) The molecular biology of secreted enzyme production by fungi. Crit Rev Biotechnol 17:273–306

    PubMed  CAS  Google Scholar 

  • Aro N, Pakula T, Penttilä M (2005) Transcriptional regulation of plant cell wall degradation by filamentous fungi. FEMS Microbiol Rev 29:719–739. doi:10.1016/j.femsre.2004.11.006

    PubMed  CAS  Google Scholar 

  • Arvas M, Pakula T, Lanthaler K, Saloheimo M, Valkonen M, Suortti T, Robson G, Penttilä M (2006) Common features and interesting differences in transcriptional responses to secretion stress in the fungi Trichoderma reesei and Saccharomyces cerevisiae. BMC Genomics 7:32. doi:10.1186/1471-2164-7-32

    PubMed Central  PubMed  Google Scholar 

  • Arvas M, Haiminen N, Smit B, Rautio J, Vitikainen M, Wiebe M, Martinez D, Chee C, Kunkel J, Sanchez C, Nelson MA, Pakula T, Saloheimo M, Penttilä M, Kivioja T (2010) Detecting novel genes with sparse arrays. Gene 467:41–51. doi:10.1016/j.gene.2010.07.009

    PubMed  CAS  Google Scholar 

  • Arvas M, Pakula T, Smit B, Rautio J, Koivistoinen H, Jouhten P, Lindfors E, Wiebe M, Penttilä M, Saloheimo M (2011) Correlation of gene expression and protein production rate – a system wide study. BMC Genomics 12:616. doi:10.1186/1471-2164-12-616

    PubMed Central  PubMed  CAS  Google Scholar 

  • Ashburner M, Ball C, Blake J, Botstein D (2000) Gene Ontology: tool for the unification of biology. Nature 25:25–30

    CAS  Google Scholar 

  • Askenazi M, Driggers EM, Holtzman DA, Norman TC, Iverson S, Zimmer DP, Boers M-E, Blomquist PR, Martinez EJ, Monreal AW, Feibelman TP, Mayorga ME, Maxon ME, Sykes K, Tobin JV, Cordero E, Salama SR, Trueheart J, Royer JC, Madden KT (2003) Integrating transcriptional and metabolite profiles to direct the engineering of lovastatin-producing fungal strains. Nat Biotechnol 21:150–156. doi:10.1038/nbt781

    PubMed  CAS  Google Scholar 

  • Baginsky S, Hennig L, Zimmermann P, Gruissem W (2010) Gene expression analysis, proteomics, and network discovery. Plant Physiol 152:402–410. doi:10.1104/pp. 109.150433

    PubMed Central  PubMed  CAS  Google Scholar 

  • Bayram O, Krappmann S, Ni M, Bok JW, Helmstaedt K, Valerius O, Braus-Stromeyer S, Kwon N-J, Keller NP, Yu J-H, Braus GH (2008) VelB/VeA/LaeA complex coordinates light signal with fungal development and secondary metabolism. Science (New York, NY) 320:1504–1506. doi:10.1126/science.1155888

    CAS  Google Scholar 

  • Bode HB, Bethe B, Höfs R, Zeeck A (2002) Big effects from small changes: possible ways to explore nature’s chemical diversity. Chembiochem 3:619–627. doi:10.1002/1439-7633(20020703)3:7<619::AID-CBIC619>3.0.CO;2-9

    PubMed  CAS  Google Scholar 

  • Bonaccorsi E, Ferreira A (2006) Transcriptional response of the obligatory aerobe Trichoderma reesei to hypoxia and transient anoxia: implications for energy production and survival in the absence. Biochemistry 45:3912–3924

    PubMed  CAS  Google Scholar 

  • Bourgon R, Gentleman RC, Huber W (2010) Independent filtering increases detection power for high-throughput experiments. Proc Natl Acad Sci U S A 107:9546–9551. doi:10.1073/pnas.0914005107, 0914005107 [pii]

    PubMed Central  PubMed  CAS  Google Scholar 

  • Brakhage A (2013) Regulation of fungal secondary metabolism. Nat Rev Microbiol 11:21–32. doi:10.1038/nrmicro2916

    PubMed  CAS  Google Scholar 

  • Brakhage A, Schroeckh V (2011) Fungal secondary metabolites—strategies to activate silent gene clusters. Fungal Genet Biol 48:15–22. doi:10.1016/j.fgb.2010.04.004

    PubMed  CAS  Google Scholar 

  • Calfon M, Zeng H, Urano F, Till J (2002) IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 415:1–6

    Google Scholar 

  • Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B (2009) The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res 37:D233–D238. doi:10.1093/nar/gkn663

    PubMed Central  PubMed  CAS  Google Scholar 

  • Carvalho N, Jørgensen TR, Arentshorst M, Nitsche BM, van den Hondel CAMJJ, Archer DB, Ram AF (2012) Genome-wide expression analysis upon constitutive activation of the HacA bZIP transcription factor in Aspergillus niger reveals a coordinated cellular response to counteract ER stress. BMC Genomics 13:350. doi:10.1186/1471-2164-13-350

    PubMed Central  PubMed  CAS  Google Scholar 

  • Chen C, Kuo H, Tung S, Hsu P (2012) Blue light acts as a double-edged sword in regulating sexual development of Hypocrea jecorina (Trichoderma reesei). PLoS One 7:9. doi:10.1371/journal.pone.0044969

    Google Scholar 

  • Coutinho PM, Andersen MR, Kolenova K, VanKuyk PA, Benoit I, Gruben BS, Trejo-Aguilar B, Visser H, Van Solingen P, Pakula T (2009) Post-genomic insights into the plant polysaccharide degradation potential of Aspergillus nidulans and comparison to Aspergillus niger and Aspergillus oryzae. Fungal Genet Biol 46:S161–S169. doi:10.1016/j.fgb.2008.07.020

    PubMed  CAS  Google Scholar 

  • De Bekker C, Bruning O, Jonker MJ, Breit TM, Wösten HB (2011a) Single cell transcriptomics of neighboring hyphae of Aspergillus niger. Genome Biol 12:R71. doi:10.1186/gb-2011-12-8-r71

    PubMed Central  PubMed  Google Scholar 

  • De Bekker C, van Veluw GJ, Vinck A, Wiebenga LA, Wösten HAB (2011b) Heterogeneity of Aspergillus niger microcolonies in liquid shaken cultures. Appl Environ Microbiol 77:1263–1267. doi:10.1128/AEM.02134-10

    PubMed Central  PubMed  Google Scholar 

  • De Souza WR, de Gouvea PF, Savoldi M, Malavazi I, de Souza Bernardes L a, Goldman MHS, de Vries RP, de Castro Oliveira JV, Goldman GH (2011) Transcriptome analysis of Aspergillus niger grown on sugarcane bagasse. Biotechnol Biofuels 4:40. doi:10.1186/1754-6834-4-40

    PubMed Central  PubMed  Google Scholar 

  • Delmas S, Pullan ST, Gaddipati S, Kokolski M, Malla S, Blythe MJ, Ibbett R, Campbell M, Liddell S, Aboobaker A, Tucker GA, Archer DB (2012) Uncovering the genome-wide transcriptional responses of the filamentous fungus Aspergillus niger to lignocellulose using RNA sequencing. PLoS Genet 8:e1002875. doi:10.1371/journal.pgen.1002875

    PubMed Central  PubMed  CAS  Google Scholar 

  • Douma RD, Batista JM, Touw KM, Kiel JAKW, Krikken AM, Zhao Z, Veiga T, Klaassen P, Bovenberg RAL, Daran J, Heijnen JJ, Van Gulik WM (2011) Degeneration of penicillin production in ethanol-limited chemostat cultivations of Penicillium chrysogenum: a systems biology approach. BMC Syst Biol 5:132. doi:10.1186/1752-0509-5-132

    PubMed Central  PubMed  CAS  Google Scholar 

  • Fleming A (1929) On the antibacterial action of cultures of a penicillium, with special reference to their use in the isolation of B. influenzae. Br J Exp Pathol 10:226–236

    PubMed Central  CAS  Google Scholar 

  • Foreman PK, Brown D, Dankmeyer L, Dean R, Diener S, Dunn-Coleman NS, Goedegebuur F, Houfek TD, England GJ, Kelley AS, Meerman HJ, Mitchell T, Mitchinson C, Olivares HA, Teunissen PJM, Yao J, Ward M (2003) Transcriptional regulation of biomass-degrading enzymes in the filamentous fungus Trichoderma reesei. J Biol Chem 278:31988–31997. doi:10.1074/jbc.M304750200

    PubMed  Google Scholar 

  • Gombert A, Veiga T, Puig-Martinez M, Lamboo F, Nijland JG, Driessen a JM, Pronk JT, Daran JM (2011) Functional characterization of the oxaloacetase encoding gene and elimination of oxalate formation in the β-lactam producer Penicillium chrysogenum. Fungal Genet Biol 48:831–839. doi:10.1016/j.fgb.2011.04.007

    PubMed  CAS  Google Scholar 

  • Gouka RJ, Punt PJ, van den Hondel CAMJJ (1997) Glucoamylase gene fusions alleviate limitations for protein production in Aspergillus awamori at the transcriptional and (post) translational levels. Appl Environ Microbiol 63:488–497

    PubMed Central  PubMed  CAS  Google Scholar 

  • Guillemette T, van Peij NNME, Goosen T, Lanthaler K, Robson GD, van den Hondel CAMJJ, Stam H, Archer DB (2007) Genomic analysis of the secretion stress response in the enzyme-producing cell factory Aspergillus niger. BMC Genomics 8:158. doi:10.1186/1471-2164-8-158

    PubMed Central  PubMed  Google Scholar 

  • Häkkinen M, Arvas M, Oja M, Aro N, Penttilä M, Saloheimo M, Pakula TM (2012) Re-annotation of the CAZy genes of Trichoderma reesei and transcription in the presence of lignocellulosic substrates. Microb Cell Fact 11:134. doi:10.1186/1475-2859-11-134

    PubMed Central  PubMed  Google Scholar 

  • Harris DM, van der Krogt ZA, Klaassen P, Raamsdonk LM, Hage S, van den Berg MA, Bovenberg RAL, Pronk JT, Daran J-M (2009a) Exploring and dissecting genome-wide gene expression responses of Penicillium chrysogenum to phenylacetic acid consumption and penicillinG production. BMC Genomics 10:75. doi:10.1186/1471-2164-10-75

    PubMed Central  PubMed  Google Scholar 

  • Harris DM, Westerlaken I, Schipper D, van der Krogt Z a, Gombert AK, Sutherland J, Raamsdonk LM, van den Berg M a, Bovenberg R a L, Pronk JT, Daran J-M (2009b) Engineering of Penicillium chrysogenum for fermentative production of a novel carbamoylated cephem antibiotic precursor. Metab Eng 11:125–137. doi:10.1016/j.ymben.2008.12.003

    PubMed  CAS  Google Scholar 

  • Hesse SJ, Ruijter GJ, Dijkema C, Visser J (2002) Intracellular pH homeostasis in the filamentous fungus Aspergillus niger. Eur J Biochem 269:3485–3494

    PubMed  CAS  Google Scholar 

  • Hoff B, Kamerewerd J, Sigl C, Mitterbauer R, Zadra I, Kürnsteiner H, Kück U (2010a) Two components of a velvet-like complex control hyphal morphogenesis, conidiophore development, and penicillin biosynthesis in Penicillium chrysogenum. Eukaryot Cell 9:1236–1250. doi:10.1128/EC.00077-10

    PubMed Central  PubMed  CAS  Google Scholar 

  • Hoff B, Kamerewerd J, Sigl C, Zadra I, Kück U (2010b) Homologous recombination in the antibiotic producer Penicillium chrysogenum: strain DeltaPcku70 shows up-regulation of genes from the HOG pathway. Appl Microbiol Biotechnol 85:1081–1094. doi:10.1007/s00253-009-2168-4

    PubMed  CAS  Google Scholar 

  • Hrdlicka PJ, Sørensen AB, Poulsen BR, Ruijter GJG, Visser J, Iversen JJL (2004) Characterization of nerolidol biotransformation based on indirect on-line estimation of biomass concentration and physiological state in batch cultures of Aspergillus niger. Biotechnol Prog 20:368–376. doi:10.1021/bp034137f

    PubMed  CAS  Google Scholar 

  • Imanaka H, Tanaka S, Feng B, Imamura K, Nakanishi K (2010) Cultivation characteristics and gene expression profiles of Aspergillus oryzae by membrane-surface liquid culture, shaking-flask culture, and agar-plate culture. J Biosci Bioeng 109:267–273. doi:10.1016/j.jbiosc.2009.09.004

    PubMed  CAS  Google Scholar 

  • Irizarry RA, Bolstad BM, Collin F, Cope LM, Hobbs B, Speed TP (2003) Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res 31:e15

    PubMed Central  PubMed  Google Scholar 

  • Jacobs DI, Olsthoorn MMA, Maillet I, Akeroyd M, Breestraat S, Donkers S, Van Der Hoeven RAM, van den Hondel CAMJJ, Kooistra R, Lapointe T, Menke H, Meulenberg R, Misset M, Müller WH, van Peij NNME, Ram AFJ, Rodriguez S, Roelofs MS, Roubos JA, Van Tilborg MWEM, Verkleij AJ, Pel HJ, Stam H, Sagt CMJ (2009) Effective lead selection for improved protein production in Aspergillus niger based on integrated genomics. Fungal Genet Biol 46:S141–S152. doi:10.1016/j.fgb.2008.08.012

    PubMed  CAS  Google Scholar 

  • Jin FJ, Takahashi T, Utsushikawa M, Furukido T, Nishida M, Ogawa M, Tokuoka M, Koyama Y (2010) A trial of minimization of chromosome 7 in Aspergillus oryzae by multiple chromosomal deletions. Mol Genet Genomics 283:1–12. doi:10.1007/s00438-009-0494-y

    PubMed  CAS  Google Scholar 

  • Jørgensen TR, Goosen T, van den Hondel CAMJJ, Ram AFJ, Iversen JJL (2009) Transcriptomic comparison of Aspergillus niger growing on two different sugars reveals coordinated regulation of the secretory pathway. BMC Genomics 10:44. doi:10.1186/1471-2164-10-44

    PubMed Central  PubMed  Google Scholar 

  • Jørgensen TR, Nitsche BM, Lamers GEM, Arentshorst M, van den Hondel CAMJJ, Ram AFJ (2010) Transcriptomic insights into the physiology of Aspergillus niger approaching a specific growth rate of zero. Appl Environ Microbiol 76:5344–5355. doi:10.1128/AEM.00450-10, AEM.00450-10 [pii]

    PubMed Central  PubMed  Google Scholar 

  • Jørgensen TR, Nielsen KF, Arentshorst M, Park J, van den Hondel CAMJJ, Frisvad JC, Ram AFJ (2011) Submerged conidiation and product formation by Aspergillus niger at low specific growth rates are affected in aerial developmental mutants. Appl Environ Microbiol 77:5270–5277. doi:10.1128/AEM.00118-11

    PubMed Central  PubMed  Google Scholar 

  • Karaffa L, Kubicek CP (2003) Aspergillus niger citric acid accumulation: do we understand this well working black box? Appl Environ Microbiol 61:189–196. doi:10.1007/s00253-002-1201-7

    CAS  Google Scholar 

  • Kardos N, Demain AL (2011) Penicillin: the medicine with the greatest impact on therapeutic outcomes. Appl Environ Microbiol 92:677–687. doi:10.1007/s00253-011-3587-6

    CAS  Google Scholar 

  • Karimi-Aghcheh R, Bok JW, Phatale P a, Smith KM, Baker SE, Lichius A, Omann M, Zeilinger S, Seiboth B, Rhee C, Keller NP, Freitag M, Kubicek CP (2013) Functional analyses of Trichoderma reesei LAE1 reveal conserved and contrasting roles of this regulator. G3 (Bethesda) 3:369–378. doi:10.1534/g3.112.005140

    CAS  Google Scholar 

  • Kimura S, Maruyama J, Takeuchi M, Kitamoto K (2008) Monitoring global gene expression of proteases and improvement of human lysozyme production in the nptB Gene disruptant of Aspergillus oryzae. Biosci Biotechnol Biochem 72:499–505. doi:10.1271/bbb.70582

    PubMed  CAS  Google Scholar 

  • Koetsier MJ, Gombert AK, Fekken S, Bovenberg RAL, van den Berg MA, Kiel JAKW, Jekel PA, Janssen DB, Pronk JT, van der Klei IJ, Daran J-M (2010) The Penicillium chrysogenum aclA gene encodes a broad-substrate-specificity acyl-coenzyme A ligase involved in activation of adipic acid, a side-chain precursor for cephem antibiotics. Fungal Genet Biol 47:33–42. doi:10.1016/j.fgb.2009.10.003

    PubMed  CAS  Google Scholar 

  • Kwon MJ, Arentshorst M, Roos ED, van den Hondel CAMJJ, Meyer V, Ram AFJ (2011) Functional characterization of Rho GTPases in Aspergillus niger uncovers conserved and diverged roles of Rho proteins within filamentous fungi. Mol Microbiol 79:1151–1167. doi:10.1111/j.1365-2958.2010.07524.x

    PubMed  CAS  Google Scholar 

  • Kwon MJ, Jørgensen TR, Nitsche BM, Arentshorst M, Park J, Ram AFJ, Meyer V (2012) The transcriptomic fingerprint of glucoamylase over-expression in Aspergillus niger. BMC Genomics. doi:10.1186/1471-2164-13-701

    Google Scholar 

  • Kwon MJ, Nitsche BM, Arentshorst M, Jørgensen TR, Ram AFJ, Meyer V (2013) The transcriptomic signature of RacA activation and inactivation provides new insights into the morphogenetic network of Aspergillus niger. PLoS One 8:68946

    Google Scholar 

  • Levin AM, de Vries RP, Conesa A, de Bekker C, Talon M, Menke HH, van Peij NNME, Wösten HAB (2007) Spatial differentiation in the vegetative mycelium of Aspergillus niger. Eukaryot Cell 6:2311–2322. doi:10.1128/EC.00244-07

    PubMed Central  PubMed  CAS  Google Scholar 

  • Li A, van Luijk N, ter Beek M, Caspers M, Punt PJ, van der Werf M (2011) A clone-based transcriptomics approach for the identification of genes relevant for itaconic acid production in Aspergillus. Fungal Genet Biol 48:602–611. doi:10.1016/j.fgb.2011.01.013

    PubMed  CAS  Google Scholar 

  • Lubertozzi D, Keasling JD (2009) Developing Aspergillus as a host for heterologous expression. Biotechnol Adv 27:53–75. doi:10.1016/j.biotechadv.2008.09.001

    PubMed  CAS  Google Scholar 

  • Määttänen P, Gehring K, Bergeron JJM, Thomas DY (2010) Protein quality control in the ER: the recognition of misfolded proteins. Semin Cell Dev Biol 21:500–511. doi:10.1016/j.semcdb.2010.03.006

    PubMed  Google Scholar 

  • Machida M, Asai K, Sano M, Tanaka T, Kumagai T et al (2005) Genome sequencing and analysis of Aspergillus oryzae. Nature 438:1157–1161. doi:10.1038/nature04300

    PubMed  Google Scholar 

  • MacKenzie DA, Guillemette T, Al-Sheikh H, Watson AJ, Jeenes DJ, Wongwathanarat P, Dunn-Coleman NS, van Peij NNME, Archer DB (2005) UPR-independent dithiothreitol stress-induced genes in Aspergillus niger. Mol Genet Genomics 274:410–418. doi:10.1007/s00438-005-0034-3

    PubMed  CAS  Google Scholar 

  • Maeda H, Sano M, Maruyama Y, Tanno T, Akao T, Totsuka Y, Endo M, Sakurada R, Yamagata Y, Machida M, Akita O, Hasegawa F, Abe K, Gomi K, Nakajima T, Iguchi Y (2004) Transcriptional analysis of genes for energy catabolism and hydrolytic enzymes in the filamentous fungus Aspergillus oryzae using cDNA microarrays and expressed sequence tags. Appl Microbiol Biotechnol 65:74–83. doi:10.1007/s00253-004-1608-4

    PubMed  CAS  Google Scholar 

  • Martens-Uzunova ES, Schaap PJ (2008) An evolutionary conserved d-galacturonic acid metabolic pathway operates across filamentous fungi capable of pectin degradation. Fungal Genet Biol 45:1449–1457. doi:10.1016/j.fgb.2008.08.002

    PubMed  CAS  Google Scholar 

  • Martens-Uzunova E, Schaap P (2009) Assessment of the pectin degrading enzyme network of Aspergillus niger by functional genomics. Fungal Genet Biol 46(Suppl 1):S170–S179

    PubMed  CAS  Google Scholar 

  • Martens-Uzunova ES, Zandleven JS, Benen JA, Awad H, Kools HJ, Beldman G, Voragen AG, van den Berg JA, Schaap PJ (2006) A new group of exo-acting family 28 glycoside hydrolases of Aspergillus niger that are involved in pectin degradation. Biochem J 400:43–52. doi:10.1042/BJ20060703, BJ20060703 [pii]

    PubMed Central  PubMed  CAS  Google Scholar 

  • Masai K, Maruyama J, Sakamoto K, Nakajima H, Akita O, Kitamoto K (2006) Square-plate culture method allows detection of differential gene expression and screening of novel, region-specific genes in Aspergillus oryzae. Appl Microbiol Biotechnol 71:881–891. doi:10.1007/s00253-006-0429-z

    PubMed  CAS  Google Scholar 

  • Mela F, Fritsche K, de Boer W, van Veen J a, de Graaff LH, van den Berg M, Leveau JHJ (2011) Dual transcriptional profiling of a bacterial/fungal confrontation: Collimonas fungivorans versus Aspergillus niger. ISME J 5:1494–1504. doi:10.1038/ismej.2011.29

    PubMed Central  PubMed  CAS  Google Scholar 

  • Metz B, Seidl-Seiboth V, Haarmann T, Kopchinskiy A, Lorenz P, Seiboth B, Kubicek CP (2011) Expression of biomass-degrading enzymes is a major event during conidium development in Trichoderma reesei. Eukaryot Cell 10:1527–1535. doi:10.1128/EC.05014-11

    PubMed Central  PubMed  CAS  Google Scholar 

  • Meyer V (2008) Genetic engineering of filamentous fungi—progress, obstacles and future trends. Biotechnol Adv 26:177–185. doi:10.1016/j.biotechadv.2007.12.001

    PubMed  CAS  Google Scholar 

  • Meyer V, Damveld RA, Arentshorst M, Stahl U, van den Hondel CAMJJ, Ram AFJ (2007) Survival in the presence of antifungals: genome-wide expression profiling of Aspergillus niger in response to sublethal concentrations of caspofungin and fenpropimorph. J Biol Chem 282:32935–32948. doi:10.1074/jbc.M705856200, M705856200 [pii]

    PubMed  CAS  Google Scholar 

  • Meyer V, Arentshorst M, Flitter SJ, Nitsche BM, Kwon MJ, Reynaga-Pena CG, Bartnicki-Garcia S, van den Hondel CAMJJ, Ram AFJ, Reynaga-Peña CG (2009) Reconstruction of signaling networks regulating fungal morphogenesis by transcriptomics. Eukaryot Cell 8:1677–1691. doi:10.1128/EC.00050-09, EC.00050-09 [pii]

    PubMed Central  PubMed  CAS  Google Scholar 

  • Mulder HJ, Nikolaev I, Madrid SM (2006) HACA, the transcriptional activator of the unfolded protein response (UPR) in Aspergillus niger, binds to partly palindromic UPR elements of the consensus sequence 5′-CAN(G/A)NTGT/GCCT-3′. Fungal Genet Biol 43:560–572. doi:10.1016/j.fgb.2006.02.005

    PubMed  CAS  Google Scholar 

  • Murooka Y, Yamshita M (2008) Traditional healthful fermented products of Japan. J Ind Microbiol Biotechnol 35:791–798. doi:10.1007/s10295-008-0362-5

    PubMed  CAS  Google Scholar 

  • Nitsche BM, Crabtree J, Cerqueira GC, Meyer V, Ram AFJ, Wortman JR, Fj A (2011) New resources for functional analysis of omics data for the genus Aspergillus. BMC Genomics 12:486. doi:10.1186/1471-2164-12-486

    PubMed Central  PubMed  CAS  Google Scholar 

  • Nitsche BM, Jørgensen TR, Akeroyd M, Meyer V, Ram AFJ (2012) The carbon starvation response of Aspergillus niger during submerged cultivation: insights from the transcriptome and secretome. BMC Genomics 13:380. doi:10.1186/1471-2164-13-380

    PubMed Central  PubMed  CAS  Google Scholar 

  • Noguchi Y, Sano M, Kanamaru K, Ko T, Takeuchi M, Kato M, Kobayashi T (2009) Genes regulated by AoXlnR, the xylanolytic and cellulolytic transcriptional regulator, in Aspergillus oryzae. Appl Microbiol Biotechnol 85:141–154. doi:10.1007/s00253-009-2236-9

    PubMed  CAS  Google Scholar 

  • Novodvorska M, Hayer K, Pullan S (2013) Transcriptional landscape of Aspergillus niger at breaking of conidial dormancy revealed by RNA-sequencing. BMC Genomics 14:246

    PubMed Central  PubMed  CAS  Google Scholar 

  • Ogawa M, Tokuoka M, Jin FJ, Takahashi T, Koyama Y (2010) Genetic analysis of conidiation regulatory pathways in koji-mold Aspergillus oryzae. Fungal Genet Biol 47:10–18. doi:10.1016/j.fgb.2009.10.004

    PubMed  CAS  Google Scholar 

  • Ogawa M, Kobayashi T, Koyama Y (2012) ManR, a novel Zn(II)(2)Cys(6) transcriptional activator, controls the β-mannan utilization system in Aspergillus oryzae. Fungal Genet Biol 49:987–995. doi:10.1016/j.fgb.2012.09.006

    PubMed  CAS  Google Scholar 

  • Ohno A, Maruyama J, Nemoto T, Arioka M, Kitamoto K (2011) A carrier fusion significantly induces unfolded protein response in heterologous protein production by Aspergillus oryzae. Appl Microbiol Biotechnol 92:1197–1206. doi:10.1007/s00253-011-3487-9

    PubMed  CAS  Google Scholar 

  • Pakula TM, Laxell M, Huuskonen A, Uusitalo J, Saloheimo M, Penttilä M (2003) The effects of drugs inhibiting protein secretion in the filamentous fungus Trichoderma reesei. Evidence for down-regulation of genes that encode secreted proteins in the stressed cells. J Biol Chem 278:45011–45020. doi:10.1074/jbc.M302372200

    PubMed  CAS  Google Scholar 

  • Panagiotou G, Andersen MR, Grotkjaer T, Regueira TB, Nielsen J, Olsson L (2009) Studies of the production of fungal polyketides in Aspergillus nidulans by using systems biology tools. Appl Environ Microbiol 75:2212–2220. doi:10.1128/AEM.01461-08

    PubMed Central  PubMed  CAS  Google Scholar 

  • Papagianni M (2004) Fungal morphology and metabolite production in submerged mycelial processes. Biotechnol Adv 22:189–259. doi:10.1016/j.biotechadv.2003.09.005

    PubMed  CAS  Google Scholar 

  • Papagianni M, Mattey M (2006) Morphological development of Aspergillus niger in submerged citric acid fermentation as a function of the spore inoculum level. Application of neural network and cluster analysis for characterization of mycelial morphology. Microb Cell Fact 5:3

    PubMed Central  PubMed  Google Scholar 

  • Pel HJ, de Winde JH, Archer DB, Dyer PS, Hofmann G et al (2007) Genome sequencing and analysis of the versatile cell factory Aspergillus niger CBS 513.88. Nat Biotechnol 25:221–231

    PubMed  Google Scholar 

  • Portnoy T, Margeot A, Linke R, Atanasova L, Fekete E, Sándor E, Hartl L, Karaffa L, Druzhinina IS, Seiboth B, Le Crom S, Kubicek CP (2011) The CRE1 carbon catabolite repressor of the fungus Trichoderma reesei: a master regulator of carbon assimilation. BMC Genomics 12:269. doi:10.1186/1471-2164-12-269

    PubMed Central  PubMed  CAS  Google Scholar 

  • Poulsen L, Andersen MR, Lantz AE, Thykaer J (2012) Identification of a transcription factor controlling pH-dependent organic acid response in Aspergillus niger. PLoS One 7:e50596. doi:10.1371/journal.pone.0050596

    PubMed Central  PubMed  CAS  Google Scholar 

  • Römisch K (1999) Surfing the Sec61 channel: bidirectional protein translocation across the ER membrane. J Cell Sci 112:4185–4191

    PubMed  Google Scholar 

  • Ruijter GJG, Kubicek CP, Visser J (2002) Production of organic acids by fungi. In: Osiewacz HD (ed) The Mycota X industrial applications. Springer, Berlin, pp 213–230

    Google Scholar 

  • Rumbold K, van Buijsen HJJ, Overkamp KM, van Groenestijn JW, Punt PJ, van der Werf MJ (2009) Microbial production host selection for converting second-generation feedstocks into bioproducts. Microb Cell Fact 8:64. doi:10.1186/1475-2859-8-64

    PubMed Central  PubMed  Google Scholar 

  • Sainani KL (2009) The problem of multiple testing. PMR 1:1098–1103. doi:10.1016/j.pmrj.2009.10.004, S1934-1482(09)01460-9 [pii]

    Google Scholar 

  • Sakamoto K, Arima T, Iwashita K, Yamada O, Gomi K, Akita O (2008) Aspergillus oryzae atfB encodes a transcription factor required for stress tolerance in conidia. Fungal Genet Biol 45:922–932. doi:10.1016/j.fgb.2008.03.009

    PubMed  CAS  Google Scholar 

  • Sakamoto K, Iwashita K, Yamada O, Kobayashi K, Mizuno A, Akita O, Mikami S, Shimoi H, Gomi K (2009) Aspergillus oryzae atfA controls conidial germination and stress tolerance. Fungal Genet Biol 46:887–897. doi:10.1016/j.fgb.2009.09.004

    PubMed  CAS  Google Scholar 

  • Salazar M, Vongsangnak W, Panagiotou G, Andersen MR, Nielsen J (2009) Uncovering transcriptional regulation of glycerol metabolism in Aspergilli through genome-wide gene expression data analysis. Mol Genet Genomics 282:571–586. doi:10.1007/s00438-009-0486-y

    PubMed  CAS  Google Scholar 

  • Saloheimo M, Pakula TM (2012) The cargo and the transport system: secreted proteins and protein secretion in Trichoderma reesei (Hypocrea jecorina). Microbiology 158:46–57. doi:10.1099/mic.0.053132-0

    PubMed  CAS  Google Scholar 

  • Seiboth B, Karimi RA, Phatale PA, Linke R, Hartl L, Sauer DG, Smith KM, Baker SE, Freitag M, Kubicek CP (2012) The putative protein methyltransferase LAE1 controls cellulase gene expression in Trichoderma reesei. Mol Microbiol 84:1150–1164. doi:10.1111/j.1365-2958.2012.08083.x

    PubMed Central  PubMed  CAS  Google Scholar 

  • Semova N, Storms R, John T, Gaudet P, Ulycznyj P, Min XJ, Sun J, Butler G, Tsang A (2006) Generation, annotation, and analysis of an extensive Aspergillus niger EST collection. BMC Microbiol 6:7. doi:10.1186/1471-2180-6-7

    PubMed Central  PubMed  Google Scholar 

  • Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504. doi:10.1101/gr.1239303, 13/11/2498 [pii]

    PubMed Central  PubMed  CAS  Google Scholar 

  • Sidrauski C, Walter P (1997) The transmembrane kinase Ire1p is a site-specific endonuclease that initiates mRNA splicing in the unfolded protein response. Cell 90:1009–1031

    Google Scholar 

  • Sigl C, Haas H, Specht T, Pfaller K, Kürnsteiner H, Zadra I (2011) Among developmental regulators, StuA but not BrlA is essential for penicillin V production in Penicillium chrysogenum. Appl Environ Microbiol 77:972–982. doi:10.1128/AEM.01557-10

    PubMed Central  PubMed  CAS  Google Scholar 

  • Snoek ISI, van der Krogt ZA, Touw H, Kerkman R, Pronk JT, Bovenberg RAL, van den Berg MA, Daran JM (2009) Construction of an hdfA Penicillium chrysogenum strain impaired in non-homologous end-joining and analysis of its potential for functional analysis studies. Fungal Genet Biol 46:418–426. doi:10.1016/j.fgb.2009.02.008

    PubMed  CAS  Google Scholar 

  • Taheri-talesh N, Horio T, Araujo-baza L, Dou X, Espeso EA, Pen MA, Osmani SA, Oakley BR (2008) The tip growth apparatus of Aspergillus nidulans. Mol Biol Cell 19:1439–1449. doi:10.1091/mbc.E07

    PubMed Central  PubMed  CAS  Google Scholar 

  • Tamano K, Sano M, Yamane N, Terabayashi Y, Toda T, Sunagawa M, Koike H, Hatamoto O, Umitsuki G, Takahashi T, Koyama Y, Asai R, Abe K, Machida M (2008) Transcriptional regulation of genes on the non-syntenic blocks of Aspergillus oryzae and its functional relationship to solid-state cultivation. Fungal Genet Biol 45:139–151. doi:10.1016/j.fgb.2007.09.005

    PubMed  CAS  Google Scholar 

  • Terabayashi Y, Sano M, Yamane N, Marui J, Tamano K, Sagara J, Dohmoto M, Oda K, Ohshima E, Tachibana K, Higa Y, Ohashi S, Koike H, Machida M (2010) Identification and characterization of genes responsible for biosynthesis of kojic acid, an industrially important compound from Aspergillus oryzae. Fungal Genet Biol 47:953–961. doi:10.1016/j.fgb.2010.08.014

    PubMed  CAS  Google Scholar 

  • Terabayashi Y, Shimizu M, Kitazume T, Masuo S, Fujii T, Takaya N (2012) Conserved and specific responses to hypoxia in Aspergillus oryzae and Aspergillus nidulans determined by comparative transcriptomics. Appl Microbiol Biotechnol 93:305–317. doi:10.1007/s00253-011-3767-4

    PubMed  Google Scholar 

  • Thykaer J, Nielsen J (2003) Metabolic engineering of β-lactam production. Metab Eng 5:56–69. doi:10.1016/S1096-7176(03)00003-X

    PubMed  CAS  Google Scholar 

  • Tisch D, Kubicek CP, Schmoll M (2011) The phosducin-like protein PhLP1 impacts regulation of glycoside hydrolases and light response in Trichoderma reesei. BMC Genomics 12:613. doi:10.1186/1471-2164-12-613

    PubMed Central  PubMed  CAS  Google Scholar 

  • Tsuchiya K, Nagashima T (1994) High level secretion of calf chymosin using a glucoamylase-prochymosin fusion gene in Aspergillus oryzae. Biosci Biotechnol Biochem 58:895–899

    PubMed  CAS  Google Scholar 

  • Tsukagoshi N, Kobayashi T, Kato M (2001) Regulation of the amylolytic and (hemi-)cellulolytic genes in aspergilli. J Gen Appl Microbiol 47:1–19

    PubMed  CAS  Google Scholar 

  • Valkonen SM (2004) The ire1 and ptc2 genes involved in the unfolded protein response pathway in the filamentous fungus Trichoderma reesei. Mol Genet Genomics 272:443–451. doi:10.1007/s00438-004-1070-0

    PubMed  CAS  Google Scholar 

  • Van de Vondervoort PJI, Langeveld SMJ, Visser J, van Peij NNME, Pel HJ, van den Hondel CAMJJ, Ram AFJ (2007) Identification of a mitotic recombination hotspot on chromosome III of the asexual fungus Aspergillus niger and its possible correlation with [corrected] elevated basal transcription. Curr Genet 52:107–114. doi:10.1007/s00294-007-0143-0

    PubMed Central  PubMed  CAS  Google Scholar 

  • Van den Berg MA, Albang R, Albermann K, Badger JH, Daran J-M, Driessen AJM, Garcia-Estrada C, Fedorova ND, Harris DM, Heijne WHM, Joardar V, Kiel J a KW, Kovalchuk A, Martín JF, Nierman WC, Nijland JG, Pronk JT, Roubos JA, van der Klei IJ, van Peij NNME, Veenhuis M, von Döhren H, Wagner C, Wortman J, Bovenberg R a L (2008) Genome sequencing and analysis of the filamentous fungus Penicillium chrysogenum. Nat Biotechnol 26:1161–1168. doi:10.1038/nbt.1498

    PubMed  CAS  Google Scholar 

  • Van den Berg RA, Braaksma M, van der Veen D, van der Werf MJ, Punt PJ, van der Oost J, de Graaff LH (2010) Identification of modules in Aspergillus niger by gene co-expression network analysis. Fungal Genet Biol 47:539–550. doi:10.1016/j.fgb.2010.03.005, S1087-1845(10)00046–0 [pii]

    PubMed  Google Scholar 

  • Van den Brink HJM, Petersen SG, Rahbek-Nielsen H, Hellmuth K, Harboe M (2006) Increased production of chymosin by glycosylation. J Biotechnol 125:304–310. doi:10.1016/j.jbiotec.2006.02.024

    PubMed  Google Scholar 

  • Van der Veen D, Oliveira JM, van den Berg W a M, de Graaff LH (2009) Analysis of variance components reveals the contribution of sample processing to transcript variation. Appl Environ Microbiol 75:2414–2422. doi:10.1128/AEM.02270-08

    PubMed Central  PubMed  Google Scholar 

  • Veening J-W, Smits WK, Kuipers OP (2008) Bistability, epigenetics, and bet-hedging in bacteria. Annu Rev Microbiol 62:193–210. doi:10.1146/annurev.micro.62.081307.163002

    PubMed  CAS  Google Scholar 

  • Veiga T, Gombert AK, Landes N, Verhoeven MD, Kiel J a KW, Krikken AM, Nijland JG, Touw H, Luttik M a H, van der Toorn JC, Driessen AJM, Bovenberg R a L, van den Berg M a, van der Klei IJ, Pronk JT, Daran J-M (2012a) Metabolic engineering of β-oxidation in Penicillium chrysogenum for improved semi-synthetic cephalosporin biosynthesis. Metab Eng 14:437–448. doi:10.1016/j.ymben.2012.02.004

    PubMed  CAS  Google Scholar 

  • Veiga T, Nijland JG, Driessen AJM, Bovenberg R a L, Touw H, van den Berg M a, Pronk JT, Daran J-M (2012b) Impact of velvet complex on transcriptome and penicillin G production in glucose-limited chemostat cultures of a β-lactam high-producing Penicillium chrysogenum strain. OMICS 16:320–333. doi:10.1089/omi.2011.0153

    PubMed Central  PubMed  CAS  Google Scholar 

  • Veiga T, Solis-Escalante D, Romagnoli G, ten Pierick A, Hanemaaijer M, Deshmuhk A, Wahl A, Pronk JT, Daran J-M (2012c) Resolving phenylalanine metabolism sheds light on natural synthesis of penicillin G in Penicillium chrysogenum. Eukaryotic Cell 11:238–249. doi:10.1128/EC.05285-11

    PubMed Central  PubMed  CAS  Google Scholar 

  • Vinck A, Terlou M, Pestman WR, Martens EP, Ram AFJ, van den Hondel CAMJJ, Wösten HAB (2005) Hyphal differentiation in the exploring mycelium of Aspergillus niger. Mol Microbiol 58:693–699. doi:10.1111/j.1365-2958.2005.04869.x

    PubMed  CAS  Google Scholar 

  • Vinck A, de Bekker C, Ossin A, Ohm RA, de Vries RP, Wösten HAB (2011) Heterogenic expression of genes encoding secreted proteins at the periphery of Aspergillus niger colonies. Environ Microbiol 13:216–225. doi:10.1111/j.1462-2920.2010.02322.x

    PubMed  CAS  Google Scholar 

  • Vitikainen M, Arvas M, Pakula T, Oja M, Penttilä M, Saloheimo M (2010) Array comparative genomic hybridization analysis of Trichoderma reesei strains with enhanced cellulase production properties. BMC Genomics 11:441. doi:10.1186/1471-2164-11-441

    PubMed Central  PubMed  Google Scholar 

  • Vongsangnak W, Salazar M, Hansen K, Nielsen J (2009) Genome-wide analysis of maltose utilization and regulation in aspergilli. Microbiology 155:3893–3902. doi:10.1099/mic.0.031104-0

    PubMed  CAS  Google Scholar 

  • Vongsangnak W, Nookaew I, Salazar M, Nielsen J (2010) Analysis of genome-wide coexpression and coevolution of Aspergillus oryzae and Aspergillus niger. OMICS 14:165–175. doi:10.1089/omi.2009.0118

    PubMed  CAS  Google Scholar 

  • Vongsangnak W, Hansen K, Nielsen J (2011) Integrated analysis of the global transcriptional response to α-amylase over-production by Aspergillus oryzae. Biotechnol Bioeng 108:1130–1139. doi:10.1002/bit.23033

    PubMed  CAS  Google Scholar 

  • Wada R, Maruyama J-I, Yamaguchi H, Yamamoto N, Wagu Y, Paoletti M, Archer DB, Dyer PS, Kitamoto K (2012) Presence and functionality of mating type genes in the supposedly asexual filamentous fungus Aspergillus oryzae. Appl Environ Microbiol 78:2819–2829. doi:10.1128/AEM.07034-11

    PubMed Central  PubMed  CAS  Google Scholar 

  • Wang Z, Gerstein M, Snyder M (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 10:57–63. doi:10.1038/nrg2484

    PubMed Central  PubMed  CAS  Google Scholar 

  • Wang B, Guo G, Wang C, Lin Y, Wang X, Zhao M, Guo Y, He M, Zhang Y, Pan L (2010) Survey of the transcriptome of Aspergillus oryzae via massively parallel mRNA sequencing. Nucleic Acids Res 38:5075–5087. doi:10.1093/nar/gkq256

    PubMed Central  PubMed  CAS  Google Scholar 

  • Wösten HAB, Moukha SM, Sietsma JH, Wessels JG (1991) Localization of growth and secretion of proteins in Aspergillus niger. J Gen Microbiol 137:2017–2023

    PubMed  Google Scholar 

  • Yoon J, Kimura S, Maruyama J, Kitamoto K (2009) Construction of quintuple protease gene disruptant for heterologous protein production in Aspergillus oryzae. Appl Microbiol Biotechnol 82:691–701. doi:10.1007/s00253-008-1815-5

    PubMed  CAS  Google Scholar 

  • Yuan XL, Roubos JA, van den Hondel CAMJJ, Ram AFJ (2007) Identification of InuR, a new Zn(II)2Cys6 transcriptional activator involved in the regulation of inulinolytic genes in Aspergillus niger. Mol Genet Genomics 279:11–26. doi:10.1007/s00438-007-0290-5

    PubMed Central  PubMed  Google Scholar 

  • Yuan X, Van Der Kaaij R, van den Hondel CAMJJ, Punt PJ, van der Maarel MJEC, Dijkhuizen L, Ram AFJ (2008) Aspergillus niger genome-wide analysis reveals a large number of novel alpha-glucan acting enzymes with unexpected expression profiles. Mol Genet Genomics 279:545–561. doi:10.1007/s00438-008-0332-7

    PubMed Central  PubMed  CAS  Google Scholar 

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Nitsche, B.M., Meyer, V. (2014). 9 Transcriptomics of Industrial Filamentous Fungi: A New View on Regulation, Physiology, and Application. In: Nowrousian, M. (eds) Fungal Genomics. The Mycota, vol 13. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-45218-5_9

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