Skip to main content

Meeting a Challenge: A View on Studying Transcriptional Control of Genes Involved in Plant Biomass Degradation in Aspergillus niger

  • Chapter
  • First Online:

Part of the book series: Grand Challenges in Biology and Biotechnology ((GCBB))

Abstract

Since the rapid developments in genome sequencing and transcriptome analysis technologies, the approaches to study the regulation of gene expression have tremendously changed. Whereas forward genetic screens have remained the most informative approaches, genome- and transcriptome-based methods have completely circumpassed more classical approaches in this field such as genetic linkage analysis and gene complementation studies. Functional analysis of gene regulation has enormously benefited from new gene knockout and overexpression strategies, most notably those based on nonhomologous end joining (NHEJ) mutants and CRISPR-cas technology. Also regarding transcriptional regulation of gene expression, new technologies, in particular RNAseq analysis, have completely taken over earlier transcript analysis methods like northern analysis and microarrays. With a combination of these new technologies, we have been able to address one of the challenges in fungal gene regulation, i.e., transcriptional control of pectin utilization in Aspergillus niger. Pectin degradation is an inherently complex system involving multiple different enzymatic activities, and traditional approaches have not led to the identification of the key factors involved in pectin degradation. However, using a combination of forward genetic screens, genome resequencing of mutant strains and targeted knockout, and overexpression strategies, followed by RNAseq-based transcriptome analysis, allowed the identification of two transcription factor genes, GaaR and GaaX. GaaR is a canonical Zn(II)2Cys6 transcriptional activator, whereas GaaX is a transcriptional repressor interacting with GaaR. Together, GaaR and GaaX consist of one of the more complex transcriptional regulation modules found in A. niger to date. However, genome mining has discovered the presence of similar paralogous modules in A. niger and many other fungi.

This is a preview of subscription content, log in via an institution.

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Al Abdallah Q, Ge W, Fortwendel JR (2017) A simple and universal system for gene manipulation in Aspergillus fumigatus: in vitro-assembled Cas9-guide RNA ribonucleoproteins coupled with microhomology repair templates. mSphere 2(6). https://doi.org/10.1128/mSphere.00446-17

  • Al Abdallah Q, Souza ACO, Martin-Vicente A, Ge W, Fortwendel JR (2018) Whole-genome sequencing reveals highly specific gene targeting by in vitro assembled Cas9-ribonucleoprotein complexes in Aspergillus fumigatus. Fungal Biol Biotechnol 5:11

    Article  PubMed  PubMed Central  Google Scholar 

  • Alazi E, Niu J, Kowalczyk JE, Peng M, Aguilar Pontes MV, van Kan JA, Visser J, de Vries RP, Ram AF (2016) The transcriptional activator GaaR of Aspergillus niger is required for release and utilization of d-galacturonic acid from pectin. FEBS Lett 590(12):1804–1815

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alazi E, Khosravi C, Homan TG, du Pre S, Arentshorst M, di Falco M, Pham TTM, Peng M, Aguilar-Pontes MV, Visser J et al (2017) The pathway intermediate 2-keto-3-deoxy-L-galactonate mediates the induction of genes involved in D-galacturonic acid utilization in Aspergillus niger. FEBS Lett 591(10):1408–1418

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alazi E, Knetsch T, Di Falco M, Reid ID, Arentshorst M, Visser J, Tsang A, Ram AFJ (2018) Inducer-independent production of pectinases in Aspergillus niger by overexpression of the D-galacturonic acid-responsive transcription factor gaaR. Appl Microbiol Biotechnol 102(6):2723–2736

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Andersen MR, Salazar MP, Schaap PJ, van de Vondervoort PJ, Culley D, Thykaer J, Frisvad JC, Nielsen KF, Albang R, Albermann K et al (2011) Comparative genomics of citric-acid-producing Aspergillus niger ATCC 1015 versus enzyme-producing CBS 513.88. Genome Res 21(6):885–897

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arentshorst M, Niu J, Ram AFJ (2015) Efficient generation of Aspergillus niger knock out strains by combining NHEJ mutants and a split marker approach. In: van den Berg MA, Maruthachalam K (eds) Genetic transformation systems in fungi, vol 1. Springer, Cham, pp 263–272

    Google Scholar 

  • Arnaud MB, Cerqueira GC, Inglis DO, Skrzypek MS, Binkley J, Chibucos MC, Crabtree J, Howarth C, Orvis J, Shah P et al (2012) The Aspergillus genome database (AspGD): recent developments in comprehensive multispecies curation, comparative genomics and community resources. Nucleic Acids Res 40(Database issue):D653–D659

    Article  CAS  PubMed  Google Scholar 

  • Ashwell G, Wahba AJ, Hickman J (1960) Uronic acid metabolism in bacteria. I. Purification and properties of uronic acid isomerase in Escherichia coli. J Biol Chem 235:1559–1565

    CAS  PubMed  Google Scholar 

  • Beck CF, Mutzel R, Barbe J, Muller W (1982) A multifunctional gene (tetR) controls Tn10-encoded tetracycline resistance. J Bacteriol 150(2):633–642

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Benocci T, Aguilar-Pontes MV, Zhou M, Seiboth B, de Vries RP (2017) Regulators of plant biomass degradation in ascomycetous fungi. Biotechnol Biofuels 10:152

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Benz JP, Protzko RJ, Andrich JMS, Bauer S, Dueber JE, Somerville CR (2014) Identification and characterization of a galacturonic acid transporter from Neurospora crassa and its application for Saccharomyces cerevisiae fermentation processes. Biotechnol Biofuels 7:20

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chang PK, Ehrlich KC (2013) Genome-wide analysis of the Zn(II)(2)Cys(6) zinc cluster-encoding gene family in Aspergillus flavus. Appl Microbiol Biotechnol 97(10):4289–4300

    Article  CAS  PubMed  Google Scholar 

  • Coutinho PM, Andersen MR, Kolenova K, van Kuyk PA, Benoit I, Gruben BS, Trejo-Aguilar B, Visser H, van Solingen P, Pakula T et al (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

    Article  CAS  PubMed  Google Scholar 

  • Craig JP, Coradetti ST, Starr TL, Glass NL (2015) Direct target network of the Neurospora crassa plant cell wall deconstruction regulators CLR-1, CLR-2, and XLR-1. MBio 6(5):e01452–e01415

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Damveld RA, Franken A, Arentshorst M, Punt PJ, Klis FM, van den Hondel CA, Ram AF (2008) A novel screening method for cell wall mutants in Aspergillus niger identifies UDP-galactopyranose mutase as an important protein in fungal cell wall biosynthesis. Genetics 178(2):873–881

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • de Vries RP, Visser J (2001) Aspergillus enzymes involved in degradation of plant cell wall polysaccharides. Microbiol Mol Biol Rev 65(4):497–522

    Article  PubMed  PubMed Central  Google Scholar 

  • de Vries RP, van de Vondervoort PJ, Hendriks L, van de Belt M, Visser J (2002) Regulation of the alpha-glucuronidase-encoding gene (aguA) from Aspergillus niger. Mol Gen Genomics 268(1):96–102

    Article  CAS  Google Scholar 

  • de Vries RP, Riley R, Wiebenga A, Aguilar-Osorio G, Amillis S, Uchima CA, Anderluh G, Asadollahi M, Askin M, Barry K et al (2017) Comparative genomics reveals high biological diversity and specific adaptations in the industrially and medically important fungal genus Aspergillus. Genome Biol 18(1):28

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dean RA, Timberlake WE (1989) Production of cell wall-degrading enzymes by Aspergillus nidulans: a model system for fungal pathogenesis of plants. Plant Cell 1(3):265–273

    CAS  PubMed  PubMed Central  Google Scholar 

  • Diep CQ, Tao X, Pilauri V, Losiewicz M, Blank TE, Hopper JE (2008) Genetic evidence for sites of interaction between the Gal3 and Gal80 proteins of the Saccharomyces cerevisiae GAL gene switch. Genetics 178(2):725–736

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Doudna JA, Charpentier E (2014) Genome editing. The new frontier of genome engineering with CRISPR-Cas9. Science 346(6213):1258096

    Article  PubMed  CAS  Google Scholar 

  • Downes DJ, Chonofsky M, Tan K, Pfannenstiel BT, Reck-Peterson SL, Todd RB (2014) Characterization of the mutagenic spectrum of 4-nitroquinoline 1-oxide (4-NQO) in Aspergillus nidulans by whole genome sequencing. G3 (Bethesda) 4(12):2483–2492

    Article  PubMed Central  Google Scholar 

  • Fairhead C, Llorente B, Denis F, Soler M, Dujon B (1996) New vectors for combinatorial deletions in yeast chromosomes and for gap-repair cloning using ‘split-marker’ recombination. Yeast 12(14):1439–1457

    Article  CAS  PubMed  Google Scholar 

  • Fedorova ND, Khaldi N, Joardar VS, Maiti R, Amedeo P, Anderson MJ, Crabtree J, Silva JC, Badger JH, Albarraq A et al (2008) Genomic islands in the pathogenic filamentous fungus Aspergillus fumigatus. PLoS Genet 4(4):e1000046

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Galagan JE, Calvo SE, Borkovich KA, Selker EU, Read ND, Jaffe D, FitzHugh W, Ma LJ, Smirnov S, Purcell S et al (2003) The genome sequence of the filamentous fungus Neurospora crassa. Nature 422(6934):859–868

    Article  CAS  PubMed  Google Scholar 

  • 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(7071):1105–1115

    Article  CAS  PubMed  Google Scholar 

  • Geever RF, Huiet L, Baum JA, Tyler BM, Patel VB, Rutledge BJ, Case ME, Giles NH (1989) DNA sequence, organization and regulation of the qa gene cluster of Neurospora crassa. J Mol Biol 207(1):15–34

    Article  CAS  PubMed  Google Scholar 

  • Goswami RS (2012) Targeted gene replacement in fungi using a split-marker approach. Methods Mol Biol 835:255–269

    Article  CAS  PubMed  Google Scholar 

  • Haber JE (2000) Recombination: a frank view of exchanges and vice versa. Curr Opin Cell Biol 12(3):286–292

    Article  CAS  PubMed  Google Scholar 

  • Harholt J, Suttangkakul A, Vibe Scheller H (2010) Biosynthesis of pectin. Plant Physiol 153(2):384–395

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hilditch S, Berghall S, Kalkkinen N, Penttilä M, Richard P (2007) The missing link in the fungal D-galacturonate pathway – identification of the L-threo-3-deoxy-hexulosonate aldolase. J Biol Chem 282(36):26195–26201

    Article  CAS  PubMed  Google Scholar 

  • Horvath P, Barrangou R (2010) CRISPR/Cas, the immune system of bacteria and archaea. Science 327(5962):167–170

    Article  CAS  PubMed  Google Scholar 

  • Hruby M, Filippov SK, Panek J, Novakova M, Mackova H, Kucka J, Ulbrich K (2010) Thermoresponsive micelles for radionuclide delivery. J Control Release 148(1):e60–e62

    Article  CAS  PubMed  Google Scholar 

  • Hsiao YM, Zheng MH, Hu RM, Yang TC, Tseng YH (2008) Regulation of the pehA gene encoding the major polygalacturonase of Xanthomonas campestris by Clp and RpfF. Microbiology 154(Pt 3):705–713

    Article  CAS  PubMed  Google Scholar 

  • Hsu PD, Lander ES, Zhang F (2014) Development and applications of CRISPR-Cas9 for genome engineering. Cell 157(6):1262–1278

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huisjes EH, Luttik MA, Almering MJ, Bisschops MM, Dang DH, Kleerebezem M, Siezen R, van Maris AJ, Pronk JT (2012) Toward pectin fermentation by Saccharomyces cerevisiae: expression of the first two steps of a bacterial pathway for D-galacturonate metabolism. J Biotechnol 162(2–3):303–310

    Article  CAS  PubMed  Google Scholar 

  • Jiang F, Frey BR, Evans ML, Friel JC, Hopper JE (2009) Gene activation by dissociation of an inhibitor from a transcriptional activation domain. Mol Cell Biol 29(20):5604–5610

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johnson DS, Mortazavi A, Myers RM, Wold B (2007) Genome-wide mapping of in vivo protein-DNA interactions. Science 316(5830):1497–1502

    Article  CAS  PubMed  Google Scholar 

  • Kerstens HHD (2010) Bioinformatics approaches to detect genetic variation in whole genome sequencing data. Wageningen University, Wageningen

    Google Scholar 

  • Kowalczyk JE, Benoit I, de Vries RP (2014) Regulation of plant biomass utilization in Aspergillus. Adv Appl Microbiol 88:31–56

    Article  CAS  PubMed  Google Scholar 

  • Kuivanen J, Mojzita D, Wang YM, Hilditch S, Penttila M, Richard P, Wiebe MG (2012) Engineering filamentous fungi for conversion of D-galacturonic acid to L-galactonic acid. Appl Environ Microbiol 78(24):8676–8683

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kuorelahti S, Kalkkinen N, Penttilä M, Londesborough J, Richard P (2005) Identification in the mold Hypocrea jecorina of the first fungal D-galacturonic acid reductase. Biochemistry 44(33):11234–11240

    Article  CAS  PubMed  Google Scholar 

  • Kuorelahti S, Jouhten P, Maaheimo H, Penttilä M, Richard P (2006) L-galactonate dehydratase is part of the fungal path for D-galacturonic acid catabolism. Mol Microbiol 61(4):1060–1068

    Article  CAS  PubMed  Google Scholar 

  • Kurella M, Hsiao LL, Yoshida T, Randall JD, Chow G, Sarang SS, Jensen RV, Gullans SR (2001) DNA microarray analysis of complex biologic processes. J Am Soc Nephrol 12(5):1072–1078

    CAS  PubMed  Google Scholar 

  • Lamb HK, Moore JD, Lakey JH, Levett LJ, Wheeler KA, Lago H, Coggins JR, Hawkins AR (1996a) Comparative analysis of the QUTR transcription repressor protein and the three C-terminal domains of the pentafunctional AROM enzyme. Biochem J 313(Pt 3):941–950

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lamb HK, Newton GH, Levett LJ, Cairns E, Roberts CF, Hawkins AR (1996b) The QUTA activator and QUTR repressor proteins of Aspergillus nidulans interact to regulate transcription of the quinate utilization pathway genes (vol 142, pg 1477, 1996). Microbiol-UK 142:2983–2983

    Article  CAS  Google Scholar 

  • Laver T, Harrison J, O'Neill PA, Moore K, Farbos A, Paszkiewicz K, Studholme DJ (2015) Assessing the performance of the Oxford Nanopore technologies MinION. Biomol Detect Quantif 3:1–8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leijdekkers AG, Huang JH, Bakx EJ, Gruppen H, Schols HA (2015) Identification of novel isomeric pectic oligosaccharides using hydrophilic interaction chromatography coupled to traveling-wave ion mobility mass spectrometry. Carbohydr Res 404:1–8

    Article  CAS  PubMed  Google Scholar 

  • Levesley I, Newton GH, Lamb HK, van Schothorst E, Dalgleish RW, Samson AC, Roberts CF, Hawkins AR (1996) Domain structure and function within the QUTA protein of Aspergillus nidulans: implications for the control of transcription. Microbiology 142(Pt 1):87–98

    Article  CAS  PubMed  Google Scholar 

  • Levett LJ, Si-Hoe SM, Liddle S, Wheeler K, Smith D, Lamb HK, Newton GH, Coggins JR, Hawkins AR (2000) Identification of domains responsible for signal recognition and transduction within the QUTR transcription repressor protein. Biochem J 350:189–197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liepins J, Kuorelahti S, Penttilä M, Richard P (2006) Enzymes for the NADPH-dependent reduction of dihydroxyacetone and D-glyceraldehyde and L-glyceraldehyde in the mould Hypocrea jecorina. FEBS J 273(18):4229–4235

    Article  CAS  PubMed  Google Scholar 

  • Lister R, Gregory BD, Ecker JR (2009) Next is now: new technologies for sequencing of genomes, transcriptomes, and beyond. Curr Opin Plant Biol 12(2):107–118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Machida M, Asai K, Sano M, Tanaka T, Kumagai T, Terai G, Kusumoto K, Arima T, Akita O, Kashiwagi Y et al (2005) Genome sequencing and analysis of Aspergillus oryzae. Nature 438(7071):1157–1161

    Article  PubMed  Google Scholar 

  • MacPherson S, Larochelle M, Turcotte B (2006) A fungal family of transcriptional regulators: the zinc cluster proteins. Microbiol Mol Biol Rev 70(3):583–604

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mannhaupt G, Montrone C, Haase D, Mewes HW, Aign V, Hoheisel JD, Fartmann B, Nyakatura G, Kempken F, Maier J et al (2003) What’s in the genome of a filamentous fungus? Analysis of the Neurospora genome sequence. Nucleic Acids Res 31(7):1944–1954

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Margulies M, Egholm M, Altman WE, Attiya S, Bader JS, Bemben LA, Berka J, Braverman MS, Chen YJ, Chen Z et al (2005) Genome sequencing in microfabricated high-density picolitre reactors. Nature 437(7057):376–380

    Article  CAS  PubMed  PubMed Central  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(11):1449–1457

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Meyer V, Arentshorst M, Flitter SJ, Nitsche BM, Kwon MJ, Reynaga-Pena CG, Bartnicki-Garcia S, van den Hondel CA, Ram AF (2009) Reconstruction of signaling networks regulating fungal morphogenesis by transcriptomics. Eukaryot Cell 8(11):1677–1691

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meyer V, Wanka F, van Gent J, Arentshorst M, van den Hondel CA, Ram AF (2011) Fungal gene expression on demand: an inducible, tunable, and metabolism-independent expression system for Aspergillus niger. Appl Environ Microbiol 77(9):2975–2983

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Michelmore RW, Paran I, Kesseli RV (1991) Identification of markers linked to disease-resistance genes by bulked segregant analysis: a rapid method to detect markers in specific genomic regions by using segregating populations. Proc Natl Acad Sci U S A 88(21):9828–9832

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mikheyev AS, Tin MM (2014) A first look at the Oxford Nanopore MinION sequencer. Mol Ecol Resour 14(6):1097–1102

    Article  CAS  PubMed  Google Scholar 

  • Mohnen D (2008) Pectin structure and biosynthesis. Curr Opin Plant Biol 11(3):266–277

    Article  CAS  PubMed  Google Scholar 

  • Mojzita D, Wiebe M, Hilditch S, Boer H, Penttila M, Richard P (2010) Metabolic engineering of fungal strains for conversion of D-galacturonate to meso-galactarate. Appl Environ Microbiol 76(1):169–175

    Article  CAS  PubMed  Google Scholar 

  • Nielsen ML, Albertsen L, Lettier G, Nielsen JB, Mortensen UH (2006) Efficient PCR-based gene targeting with a recyclable marker for Aspergillus nidulans. Fungal Genet Biol 43(1):54–64

    Article  CAS  PubMed  Google Scholar 

  • Ninomiya Y, Suzuki K, Ishii C, Inoue H (2004) Highly efficient gene replacements in Neurospora strains deficient for nonhomologous end-joining. Proc Natl Acad Sci U S A 101(33):12248–12253

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nitsche BM, Crabtree J, Cerqueira GC, Meyer V, Ram AF, Wortman JR (2011) New resources for functional analysis of omics data for the genus Aspergillus. BMC Genomics 12:486

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Niu J, Arentshorst M, Nair PD, Dai Z, Baker SE, Frisvad JC, Nielsen KF, Punt PJ, Ram AF (2015) Identification of a classical mutant in the industrial host Aspergillus niger by systems genetics: LaeA is required for citric acid production and regulates the formation of some secondary metabolites. G3 (Bethesda) 6(1):193–204

    Article  CAS  Google Scholar 

  • Niu J, Arentshorst M, Seelinger F, Ram AF, Ouedraogo JP (2016) A set of isogenic auxotrophic strains for constructing multiple gene deletion mutants and parasexual crossings in Aspergillus niger. Arch Microbiol 198(9):861–868

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Niu J, Alazi E, Reid ID, Arentshorst M, Punt PJ, Visser J, Tsang A, Ram AF (2017) An evolutionarily conserved transcriptional activator-repressor module controls expression of genes for D-galacturonic acid utilization in Aspergillus niger. Genetics 205(1):169–183

    Article  CAS  PubMed  Google Scholar 

  • Nodvig CS, Nielsen JB, Kogle ME, Mortensen UH (2015) A CRISPR-Cas9 system for genetic engineering of filamentous Fungi. PLoS One 10(7):e0133085

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nodvig CS, Hoof JB, Kogle ME, Jarczynska ZD, Lehmbeck J, Klitgaard DK, Mortensen UH (2018) Efficient oligo nucleotide mediated CRISPR-Cas9 gene editing in Aspergilli. Fungal Genet Biol 115:78–89

    Article  PubMed  CAS  Google Scholar 

  • Payne SH, Loomis WF (2006) Retention and loss of amino acid biosynthetic pathways based on analysis of whole-genome sequences. Eukaryot Cell 5(2):272–276

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pel HJ, de Winde JH, Archer DB, Dyer PS, Hofmann G, Schaap PJ, Turner G, de Vries RP, Albang R, Albermann K et al (2007) Genome sequencing and analysis of the versatile cell factory Aspergillus niger CBS 513.88. Nat Biotechnol 25(2):221–231

    Article  PubMed  Google Scholar 

  • Platt A, Ross HC, Hankin S, Reece RJ (2000) The insertion of two amino acids into a transcriptional inducer converts it into a galactokinase. Proc Natl Acad Sci U S A 97(7):3154–3159

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pohl C, Kiel JA, Driessen AJ, Bovenberg RA, Nygard Y (2016) CRISPR/Cas9 based genome editing of Penicillium chrysogenum. ACS Synth Biol 5(7):754–764

    Article  CAS  PubMed  Google Scholar 

  • Punt PJ, Schuren FH, Lehmbeck J, Christensen T, Hjort C, van den Hondel CA (2008) Characterization of the Aspergillus niger prtT, a unique regulator of extracellular protease encoding genes. Fungal Genet Biol 45(12):1591–1599

    Article  CAS  PubMed  Google Scholar 

  • Ren B, Robert F, Wyrick JJ, Aparicio O, Jennings EG, Simon I, Zeitlinger J, Schreiber J, Hannett N, Kanin E et al (2000) Genome-wide location and function of DNA binding proteins. Science 290(5500):2306–2309

    Article  CAS  PubMed  Google Scholar 

  • Rhoads A, Au KF (2015) PacBio sequencing and its applications. Genom Proteom Bioinform 13(5):278–289

    Article  Google Scholar 

  • Robertson G, Hirst M, Bainbridge M, Bilenky M, Zhao Y, Zeng T, Euskirchen G, Bernier B, Varhol R, Delaney A et al (2007) Genome-wide profiles of STAT1 DNA association using chromatin immunoprecipitation and massively parallel sequencing. Nat Methods 4(8):651–657

    Article  CAS  PubMed  Google Scholar 

  • Sander JD, Joung JK (2014) CRISPR-Cas systems for editing, regulating and targeting genomes. Nat Biotechnol 32(4):347–355

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sarkari P, Marx H, Blumhoff ML, Mattanovich D, Sauer M, Steiger MG (2017) An efficient tool for metabolic pathway construction and gene integration for Aspergillus niger. Bioresour Technol 245(Pt B):1327–1333

    Article  CAS  PubMed  Google Scholar 

  • Schneeberger K (2014) Using next-generation sequencing to isolate mutant genes from forward genetic screens. Nat Rev Genet 15(10):662–676

    Article  CAS  PubMed  Google Scholar 

  • Schneeberger K, Ossowski S, Lanz C, Juul T, Petersen AH, Nielsen KL, Jorgensen JE, Weigel D, Andersen SU (2009) SHOREmap: simultaneous mapping and mutation identification by deep sequencing. Nat Methods 6(8):550–551

    Article  CAS  PubMed  Google Scholar 

  • Shelest E (2017) Transcription factors in fungi: TFome dynamics, three major families, and dual-specificity TFs. Front Genet 8:53

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sloothaak J, Schilders M, Schaap PJ, de Graaff LH (2014) Overexpression of the Aspergillus niger GatA transporter leads to preferential use of D-galacturonic acid over D-xylose. AMB Express 4:66

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Song L, Ouedraogo JP, Kolbusz M, Nguyen TTM, Tsang A (2018) Efficient genome editing using tRNA promoter-driven CRISPR/Cas9 gRNA in Aspergillus niger. PLoS One 13(8):e0202868

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Srivatsan A, Han Y, Peng J, Tehranchi AK, Gibbs R, Wang JD, Chen R (2008) High-precision, whole-genome sequencing of laboratory strains facilitates genetic studies. PLoS Genet 4(8):e1000139

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tan K, Roberts AJ, Chonofsky M, Egan MJ, Reck-Peterson SL (2014) A microscopy-based screen employing multiplex genome sequencing identifies cargo-specific requirements for dynein velocity. Mol Biol Cell 25(5):669–678

    Article  PubMed  PubMed Central  Google Scholar 

  • Timson DJ, Ross HC, Reece RJ (2002) Gal3p and Gal1p interact with the transcriptional repressor Gal80p to form a complex of 1: 1 stoichiometry. Biochem J 363:515–520

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Todd RB, Andrianopoulos A (1997) Evolution of a fungal regulatory gene family: the Zn(II)2Cys6 binuclear cluster DNA binding motif. Fungal Genet Biol 21(3):388–405

    Article  CAS  PubMed  Google Scholar 

  • Todd RB, Zhou M, Ohm RA, Leeggangers HA, Visser L, de Vries RP (2014) Prevalence of transcription factors in ascomycete and basidiomycete fungi. BMC Genomics 15:214

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Verwaal R, Buiting-Wiessenhaan N, Dalhuijsen S, Roubos JA (2018) CRISPR/Cpf1 enables fast and simple genome editing of Saccharomyces cerevisiae. Yeast 35(2):201–211

    Article  CAS  PubMed  Google Scholar 

  • Vesth TC, Nybo JL, Theobald S, Frisvad JC, Larsen TO, Nielsen KF, Hoof JB, Brandl J, Salamov A, Riley R et al (2018) Investigation of inter- and intraspecies variation through genome sequencing of Aspergillus section Nigri. Nat Genet 50(12):1688–1695

    Article  CAS  PubMed  Google Scholar 

  • Vogt K, Bhabhra R, Rhodes JC, Askew DS (2005) Doxycycline-regulated gene expression in the opportunistic fungal pathogen Aspergillus fumigatus. BMC Microbiol 5:1

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Voragen AGJ, Pilnik W (1989) Pectin-degrading enzymes in fruit and vegetable processing. In: Whitaker JR, Sonnet PE (eds) Biocatalysis in agricultural biotechnology. American Chemical Society, Washington, DC, pp 93–155

    Chapter  Google Scholar 

  • Wang Z, Gerstein M, Snyder M (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 10(1):57–63

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wanka F, Cairns T, Boecker S, Berens C, Happel A, Zheng X, Sun J, Krappmann S, Meyer V (2016) Tet-on, or Tet-off, that is the question: advanced conditional gene expression in Aspergillus. Fungal Genet Biol 89:72–83

    Article  CAS  PubMed  Google Scholar 

  • Watts C, Si-Hoe SM, Lamb HK, Levett LJ, Coggins JR, Hawkins AR (2002) Kinetic analysis of the interaction between the QutA and QutR transcription-regulating proteins. Proteins 48(2):161–168

    Article  CAS  PubMed  Google Scholar 

  • Wiebe MG, Mojzita D, Hilditch S, Ruohonen L, Penttilä M (2010) Bioconversion of D-galacturonate to keto-deoxy-L-galactonate (3-deoxy-L-threo-hex-2-ulosonate) using filamentous fungi. BMC Biotechnol 10:63. https://doi.org/10.1186/1472-6750-10-63

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wiedenheft B, Sternberg SH, Doudna JA (2012) RNA-guided genetic silencing systems in bacteria and archaea. Nature 482(7385):331–338

    Article  CAS  PubMed  Google Scholar 

  • Zhang LS, Thiewes H, van Kan JAL (2011) The D-galacturonic acid catabolic pathway in Botrytis cinerea. Fungal Genet Biol 48(10):990–997

    Article  CAS  PubMed  Google Scholar 

  • Zhang L, Hua C, Stassen JH, Chatterjee S, Cornelissen M, van Kan JA (2014) Genome-wide analysis of pectate-induced gene expression in Botrytis cinerea: identification and functional analysis of putative d-galacturonate transporters. Fungal Genet Biol 72:182–191

    Article  CAS  PubMed  Google Scholar 

  • Zhang XH, Tee LY, Wang XG, Huang QS, Yang SH (2015) Off-target effects in CRISPR/Cas9-mediated genome engineering. Mol Ther Nucleic Acids 4:e264

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang L, Lubbers RJ, Simon A, Stassen JH, Vargas Ribera PR, Viaud M, van Kan JA (2016) A novel Zn2 Cys6 transcription factor BcGaaR regulates D-galacturonic acid utilization in Botrytis cinerea. Mol Microbiol 100(2):247–262

    Article  CAS  PubMed  Google Scholar 

  • Zheng YM, Lin FL, Gao H, Zou G, Zhang JW, Wang GQ, Chen GD, Zhou ZH, Yao XS, Hu D (2017) Development of a versatile and conventional technique for gene disruption in filamentous fungi based on CRISPR-Cas9 technology. Sci Rep 7(1):9250

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zheng X, Zheng P, Zhang K, Cairns TC, Meyer V, Sun J, Ma Y (2018) 5S rRNA promoter for guide RNA expression enabled highly efficient CRISPR/Cas9 genome editing in Aspergillus niger. ACS Synth Biol 8(7):1568–1574

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Peter J. Punt .

Editor information

Editors and Affiliations

Ethics declarations

JN was supported by a grant from the Chinese Scholarship Council.

Rights and permissions

Reprints and permissions

Copyright information

© 2020 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Niu, J., Ram, A.F.J., Punt, P.J. (2020). Meeting a Challenge: A View on Studying Transcriptional Control of Genes Involved in Plant Biomass Degradation in Aspergillus niger . In: Nevalainen, H. (eds) Grand Challenges in Fungal Biotechnology. Grand Challenges in Biology and Biotechnology. Springer, Cham. https://doi.org/10.1007/978-3-030-29541-7_8

Download citation

Publish with us

Policies and ethics