Elucidating how the saprophytic fungus Aspergillus nidulans uses the plant polyester suberin as carbon source

BMC Genomics

Cristina Silva Pereira¹  Jörg D Becker⁵  Jenny Renaut⁴  Ji He³  Rui Ferreira²  Céline C Leclercq⁴  Helga Garcia²  Celso Martins¹  Paula C Alves²  Diego O Hartmann²  Isabel Martins² 

[1] Instituto de Biologia Experimental e Tecnológica (iBET), Av. da República, 2781-901 Oeiras, Portugal;Instituto de Tecnologia Química e Biológica, Universidade Nova de Lisboa, Av. da República, 2780-157 Oeiras, Portugal;Cancer Genomics Research Laboratory, Division of Cancer Epidemiology and Genetics, National Cancer Institute, NIH, DHHS, 8717 Grovemont Circle, 20877 Gaithersburg, MD, USA (previously, the Scientific Computing department, Samuel Roberts Noble Foundation, USA;Proteomics Platform, Centre de Recherche Public - Gabriel Lippmann, Belvaux, Luxembourg;Instituto Gulbenkian de Ciência, Rua da Quinta Grande 6, 2780-156 Oeiras, Portugal

关键词: Whole-genome profiling;    Suberin;    Long chain fatty acids;    Cutinase;    β-oxidation;    Aspergillus nidulans;   

Others  :  1216441
DOI  :  10.1186/1471-2164-15-613

 received in 2014-03-18, accepted in 2014-07-16,  发布年份 2014

【 摘 要 】

Background

Lipid polymers in plant cell walls, such as cutin and suberin, build recalcitrant hydrophobic protective barriers. Their degradation is of foremost importance for both plant pathogenic and saprophytic fungi. Regardless of numerous reports on fungal degradation of emulsified fatty acids or cutin, and on fungi–plant interactions, the pathways involved in the degradation and utilisation of suberin remain largely overlooked. As a structural component of the plant cell wall, suberin isolation, in general, uses harsh depolymerisation methods that destroy its macromolecular structure. We recently overcame this limitation isolating suberin macromolecules in a near-native state.

Results

Suberin macromolecules were used here to analyse the pathways involved in suberin degradation and utilisation by Aspergillus nidulans. Whole-genome profiling data revealed the complex degrading enzymatic machinery used by this saprophytic fungus. Initial suberin modification involved ester hydrolysis and ω-hydroxy fatty acid oxidation that released long chain fatty acids. These fatty acids were processed through peroxisomal β-oxidation, leading to up-regulation of genes encoding the major enzymes of these pathways (e.g. faaB and aoxA). The obtained transcriptome data was further complemented by secretome, microscopic and spectroscopic analyses.

Conclusions

Data support that during fungal growth on suberin, cutinase 1 and some lipases (e.g. AN8046) acted as the major suberin degrading enzymes (regulated by FarA and possibly by some unknown regulatory elements). Suberin also induced the onset of sexual development and the boost of secondary metabolism.

【 授权许可】

   
2014 Martins et al.; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Heredia A, Matas A, Dominguez E: Investigating plant lipid biopolymers. Biochem Educ 2000, 28(1):50-51.
• [2]Winkler A, Haumaier L, Zech W: Insoluble alkyl carbon components in soils derive mainly from cutin and suberin. Org Geochem 2005, 36(4):519-529.
• [3]Hamer U, Rumpel C, Dignac MF: Cutin and suberin biomarkers as tracers for the turnover of shoot and root derived organic matter along a chronosequence of Ecuadorian pasture soils. Eur J Soil Sci 2012, 63(6):808-819.
• [4]Harms H, Schlosser D, Wick LY: Untapped potential: exploiting fungi in bioremediation of hazardous chemicals. Nat Rev Microbiol 2011, 9(3):177-192.
• [5]Kolattukudy PE, Scheper T, Babel W, Steinbüchel A: Polyesters in higher plants. Biopolyesters 2001, 71:1-49.
• [6]Pereira H: Cork: Biology, Production and Uses. Amsterdam: Elsevier; 2007.
• [7]van Fleet DS: Histochemistry and function of the endodermis. Bot Rev 1961, 27(2):165-220.
• [8]Yeats TH, Rose JKC: The formation and function of plant cuticles. Plant Physiol 2013, 163(1):5-20.
• [9]Schreiber L: Transport barriers made of cutin, suberin and associated waxes. Trends Plant Sci 2010, 15(10):546-553.
• [10]Pollard M, Beisson F, Li YH, Ohlrogge JB: Building lipid barriers: biosynthesis of cutin and suberin. Trends Plant Sci 2008, 13(5):236-246.
• [11]Javelle M, Vernoud V, Rogowsky PM, Ingram GC: Epidermis: the formation and functions of a fundamental plant tissue. New Phytol 2011, 189(1):17-39.
• [12]Kolattukudy PE: Biopolyester membranes of plants: cutin and suberin. Science 1980, 208(4447):990-1000.
• [13]Lulai EC, Corsini DL: Differential deposition of suberin phenolic and aliphatic domains and their roles in resistance to infection during potato tuber (Solanum tuberosum L.) wound-healing. Physiol Mol Plant Pathol 1998, 53(4):209-222.
• [14]Ranathunge K, Schreiber L, Franke R: Suberin research in the genomics era: new interest for an old polymer. Plant Sci 2011, 180(3):399-413.
• [15]Garcia H, Ferreira R, Martins C, Sousa AF, Freire CSR, Silvestre AJD, Kunz W, Rebelo LPN, Silva Pereira C: Ex situ reconstitution of the plant biopolyester suberin as a film. Biomacromolecules 2014, 15(5):1806-1813.
• [16]Graça J, Schreiber L, Rodrigues J, Pereira H: Glycerol and glyceryl esters of ω-hydroxyacids in cutins. Phytochemistry 2002, 61(2):205-215.
• [17]Graça J, Lamosa P: Linear and branched poly(ω-hydroxyacid) esters in plant cutins. J Agr Food Chem 2010, 58(17):9666-9674.
• [18]Fernando G, Zimmermann W, Kolattukudy PE: Suberin-grown Fusarium solani f. sp pisi generates a cutinase-like esterase which depolymerizes the aliphatic components of suberin. Physiol Mol Plant Pathol 1984, 24(2):143-155.
• [19]Kontkanen H, Westerholm-Parvinen A, Saloheimo M, Bailey M, Rättö M, Mattila I, Mohsina M, Kalkkinen N, Nakari-Setälä T, Buchert J: Novel Coprinopsis cinerea polyesterase that hydrolyzes cutin and suberin. Appl Environ Microb 2009, 75(7):2148-2157.
• [20]Garcia Lepe R, Nuero OM, Reyes F, Santamaria F: Lipases in autolysed cultures of filamentous fungi. Lett Appl Microbiol 1997, 25(2):127-130.
• [21]Maggio-Hall LA, Keller NP: Mitochondrial β-oxidation in Aspergillus nidulans. Mol Microbiol 2004, 54(5):1173-1185.
• [22]Hynes MJ, Murray SL, Duncan A, Khew GS, Davis MA: Regulatory genes controlling fatty acid catabolism and peroxisomal functions in the filamentous fungus Aspergillus nidulans. Eukaryot Cell 2006, 5(5):794-805.
• [23]Purdy R, Kolattukudy P: Hydrolysis of plant cuticle by plant pathogens. Properties of cutinase I, cutinase II, and a nonspecific esterase isolated from Fusarium solani pisi. Biochemistry 1975, 14(13):2832-2840.
• [24]Fan C-Y, Köller W: Diversity of cutinases from plant pathogenic fungi: diferential and sequential expression of cutinolytic esterases by Alternaria brassicicola. FEMS Microbiol Lett 1998, 158(1):33-38.
• [25]Bonnen AM, Hammerschmidt R: Cutinolytic enzymes from Colletotrichum lagenarium. Physiol Mol Plant Pathol 1989, 35(6):463-474.
• [26]Li D, Sirakova T, Rogers L, Ettinger WF, Kolattukudy PE: Regulation of constitutively expressed and induced cutinase genes by different zinc finger transcription factors in Fusarium solani f. sp. pisi (Nectria haematococca). J Biol Chem 2002, 277:7905-7912.
• [27]Castro-Ochoa D, Peña-Montes C, González-Canto A, Alva-Gasca A, Esquivel-Bautista R, Navarro-Ocaña A, Farrés A: ANCUT2, an extracellular cutinase from Aspergillus nidulans induced by olive oil. Appl Biochem Biotechnol 2012, 166:1275-1290.
• [28]Yang S, Xu H, Yan Q, Liu Y, Zhou P, Jiang Z: A low molecular mass cutinase of Thielavia terrestris efficiently hydrolyzes poly(esters). J Ind Microbiol Biotechnol 2013, 40:217-226.
• [29]Garcia H, Ferreira R, Petkovic M, Ferguson JL, Leitão MC, Gunaratne HQ, Seddon K, Rebelo L, Silva Pereira C: Dissolution of cork biopolymers in biocompatible ionic liquids. Green Chem 2010, 12:367-369.
• [30]Ferreira R, Garcia H, Sousa AF, Freire CSR, Silvestre AJD, Rebelo LPN, Silva Pereira C: Isolation of suberin from birch outer bark and cork using ionic liquids: a new source of macromonomers. Ind Crop Prod 2013, 44:520-527.
• [31]Ferreira R, Garcia H, Sousa AF, Guerreiro M, Duarte FJS, Freire CSR, Calhorda MJ, Silvestre AJD, Rebelo LPN, Silva Pereira C: Unravelling the dual role of cholinium hexanoate ionic liquid as solvent and catalyst in suberin depolymerization. RSC Adv 2014, 4(1):2993-3002.
• [32]Ferreira R, Garcia H, Sousa AF, Petkovic M, Lamosa P, Freire CSR, Silvestre AJD, Rebelo LPN, Silva Pereira C: Suberin isolation from cork using ionic liquids: characterisation of ensuing products. New J Chem 2012, 36(10):2014-2024.
• [33]Carvalho MB, Martins I, Medeiros J, Tavares S, Planchon S, Renaut J, Nuñez O, Gallart-Ayala H, Galceran MT, Hursthouse A, Silva Pereira C: The response of Mucor plumbeus to pentachlorophenol: a toxicoproteomics study. J Proteomics 2013, 78:159-171.
• [34]Petkovic M, Hartmann DO, Adamová G, Seddon KR, Rebelo LPN, Silva Pereira C: Unravelling the mechanism of toxicity of alkyltributylphosphonium chlorides in Aspergillus nidulans conidia. New J Chem 2012, 36(1):56-63.
• [35]Seidler M, Salvenmoser S, Müller FM: In vitro effects of micafungin against Candida biofilms on polystyrene and central venous catheter sections. Int J Antimicrob Agents 2006, 28(6):568-573.
• [36]Carvalho MB, Martins I, Leitão MC, Garcia H, Rodrigues C, Romão VS, McLellan I, Hursthouse A, Silva Pereira C: Screening pentachlorophenol degradation ability by environmental fungal strains belonging to the phyla Ascomycota and Zygomycota. J Ind Microbiol Biotechnol 2009, 36(10):1249-1256.
• [37]Hartmann DO, Silva Pereira C: A molecular analysis of the toxicity of alkyltributylphosphonium chlorides in Aspergillus nidulans. New J Chem 2013, 37(5):1569-1577.
• [38]Edgar R, Domrachev M, Lash AE: Gene expression omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 2002, 30(1):207-210.
• [39]Li C, Wong WH: Model-based analysis of oligonucleotide arrays: expression index computation and outlier detection. Proc Natl Acad Sci U S A 2001, 98(1):31-36.
• [40]Li C, Wong WH: Model-based analysis of oligonucleotide arrays: model validation, design issues and standard error application. Genome Biol 2001, 2(8):1-11.
• [41]Priebe S, Linde J, Albrecht D, Guthke R, Brakhage AA: FungiFun: a web-based application for functional categorization of fungal genes and proteins. Fungal Genet Biol 2011, 48(4):353-358.
• [42]Emri T, Szilágyi M, László K, M-Hamvas M, Pócsi I: PepJ is a new extracellular proteinase of Aspergillus nidulans. Folia Microbiol 2009, 54(2):105-109.
• [43]Szilágyi M, Kwon NJ, Bakti F, M-Hamvas M, Jámbrik K, Park H, Pócsi I, Yu JH, Emri T: Extracellular proteinase formation in carbon starving Aspergillus nidulans cultures - physiological function and regulation. J Basic Microbiol 2011, 51(6):625-634.
• [44]Pusztahelyi T, Molnár Z, Emri T, Klement É, Miskei M, Kerékgyártó J, Balla J, Pócsi I: Comparative studies of differential expression of chitinolytic enzymes encoded by chiA, chiB, chiC and nagA genes in Aspergillus nidulans. Folia Microbiol 2006, 51(6):547-554.
• [45]Shin KS, Kwon NJ, Kim YH, Park HS, Kwon GS, Yu JH: Differential roles of the ChiB chitinase in autolysis and cell death of Aspergillus nidulans. Eukaryot Cell 2009, 8(5):738-746.
• [46]Szilágyi M, Kwon NJ, Dorogi C, Pócsi I, Yu JH, Emri T: The extracellular β-1,3-endoglucanase EngA is involved in autolysis of Aspergillus nidulans. J Appl Microbiol 2010, 109(5):1498-1508.
• [47]Szilágyi M, Miskei M, Karányi Z, Lenkey B, Pócsi I, Emri T: Transcriptome changes initiated by carbon starvation in Aspergillus nidulans. Microbiol (UK) 2013, 159:176-190.
• [48]Muzzarelli RAA, Miliani M, Cartolari M, Tarsi R, Tosi G, Muzzarelli C: Polyuronans obtained by regiospecific oxidation of polysaccharides from Aspergillus niger, Trichoderma reesei and Saprolegnia sp. Carbohyd Polym 2000, 43(1):55-61.
• [49]Tsiatsiani L, Van Breusegem F, Gallois P, Zavialov A, Lam E, Bozhkov PV: Metacaspases. Cell Death Differ 2011, 18(8):1279-1288.
• [50]Uren AG, O’Rourke K, Aravind L, Pisabarro MT, Seshagiri S, Koonin EV, Dixit VM: Identification of paracaspases and metacaspases: two ancient families of caspase-like proteins, one of which plays a key role in MALT lymphoma. Mol Cell 2000, 6(4):961-967.
• [51]Savoldi M, Malavazi I, Soriani FM, Capellaro JL, Kitamoto K, da Silva Ferreira ME, Goldman MHS, Goldman GH: Farnesol induces the transcriptional accumulation of the Aspergillus nidulans Apoptosis Inducing Factor (AIF) like mitochondrial oxidoreductase. Mol Microbiol 2008, 70(1):44-59.
• [52]Ren Q, Chen K, Paulsen IT: TransportDB: a comprehensive database resource for cytoplasmic membrane transport systems and outer membrane channels. Nucleic Acids Res 2007, 35:D274-D279.
• [53]Inglis DO, Binkley J, Skrzypek MS, Arnaud MB, Cerqueira GC, Shah P, Wymore F, Wortman JR, Sherlock G: Comprehensive annotation of secondary metabolite biosynthetic genes and gene clusters of Aspergillus nidulans, A. fumigatus, A. niger and A. oryzae. BMC Microbiol 2013, 13:91.
• [54]Forment JV, Flipphi M, Ramón D, Ventura L, MacCabe AP: Identification of the mstE gene encoding a glucose inducible, low affinity glucose transporter in Aspergillus nidulans. J Biol Chem 2006, 281(13):8339-8346.
• [55]Dowzer CEA, Kelly JM: Analysis of the CreA gene, a regulator of carbon catabolite repression in Aspergillus nidulans. Mol Cell Biol 1991, 11(11):5701-5709.
• [56]David H, Krogh AM, Roca C, Akesson M, Nielsen J: CreA influences the metabolic fluxes of Aspergillus nidulans during growth on glucose and xylose. Microbiol (UK) 2005, 151:2209-2221.
• [57]Strauss J, Horvath HK, Abdallah BM, Kindermann J, Mach RL, Kubicek CP: The function of CreA, the carbon catabolite repressor of Aspergillus nidulans, is regulated at the transcriptional and post-transcriptional level. Mol Microbiol 1999, 32(1):169-178.
• [58]Hynes MJ, Szewczyk E, Murray SL, Suzuki Y, Davis MA, Lewis HMS: Transcriptional control of gluconeogenesis in Aspergillus nidulans. Genetics 2007, 176(1):139-150.
• [59]Meijer S, Panagiotou G, Olsson L, Nielsen J: Physiological characterization of xylose metabolism in Aspergillus niger under oxygen-limited conditions. Biotechnol Bioeng 2007, 98(2):462-475.
• [60]Felenbok B, Sequeval D, Mathieu M, Sibley S, Gwynne DI, Davies RW: The ethanol regulon in Aspergillus nidulans - characterization and sequence of the positive regulatory gene alcR. Gene 1988, 73(2):385-396.
• [61]Macios M, Caddick MX, Weglenski P, Scazzocchio C, Dzikowska A: The GATA factors AREA and AREB together with the co-repressor NMRA, negatively regulate arginine catabolism in Aspergillus nidulans in response to nitrogen and carbon source. Fungal Genet Biol 2012, 49(3):189-198.
• [62]Wong KH, Hynes MJ, Davis MA: Recent advances in nitrogen regulation: a comparison between Saccharomyces cerevisiae and filamentous fungi. Eukaryot Cell 2008, 7(6):917-925.
• [63]Berger H, Basheer A, Böck S, Reyes-Dominguez Y, Dalik T, Altmann F, Strauss J: Dissecting individual steps of nitrogen transcription factor cooperation in the Aspergillus nidulans nitrate cluster. Mol Microbiol 2008, 69(6):1385-1398.
• [64]Schinko T, Berger H, Lee W, Gallmetzer A, Pirker K, Pachlinger R, Buchner I, Reichenauer T, Güldener U, Strauss J: Transcriptome analysis of nitrate assimilation in Aspergillus nidulans reveals connections to nitric oxide metabolism. Mol Microbiol 2010, 78(3):720-738.
• [65]Muszkieta L, Beauvais A, Pähtz V, Gibbons JG, Anton Leberre V, Beau R, Shibuya K, Rokas A, Francois JM, Kniemeyer O, Brakhage AA, Latge JP: Investigation of Aspergillus fumigatus biofilm formation by various “omics” approaches. Front Microbiol 2013, 4:13.
• [66]Wei HJ, Scherer M, Singh A, Liese R, Fischer R: Aspergillus nidulans α-1,3 glucanase (mutanase), mutA, is expressed during sexual development and mobilizes mutan. Fungal Genet Biol 2001, 34(3):217-227.
• [67]Arnaud M, Chibucos M, Costanzo M, Crabtree J, Inglis D, Lotia A, Orvis J, Shah P, Skrzypek M, Binkley G, Miyasato SR, Wortman JR, Sherlock G: The Aspergillus Genome Database, a curated comparative genomics resource for gene, protein and sequence information for the Aspergillus research community. Nucleic Acids Res 2010, 38(Database issue):D420-427.
• [68]Apweiler R, Martin MJ, O’Donovan C, Magrane M, Alam-Faruque Y, Alpi E, Antunes R, Arganiska J, Casanova EB, Bely B, Apweiler R, Martin MJ, O’Donovan C, Magrane M, Alam-Faruque Y, Alpi E, Antunes R, Arganiska J, Casanova EB, Bely B, Bingley M, Bonilla C, Britto R, Bursteinas B, Chan WM, Chavali G, Cibrian-Uhalte E, Da Silva A, De Giorgi M, Dimmer E, et al.: Update on activities at the Universal Protein Resource (UniProt) in 2013. Nucleic Acids Res 2013, 41(D1):D43-D47.
• [69]Dyer PS, O’Gorman CM: Sexual development and cryptic sexuality in fungi: insights from Aspergillus species. FEMS Microbiol Rev 2012, 36(1):165-192.
• [70]Krijgsheld P, Bleichrodt R, van Veluw GJ, Wang F, Müller WH, Dijksterhuis J, Wosten HAB: Development in Aspergillus. Stud Mycol 2013, 74(1):1-29.
• [71]Paoletti M, Seymour FA, Alcocer MJC, Kaur N, Caivo AM, Archer DB, Dyer PS: Mating type and the genetic basis of self-fertility in the model fungus Aspergillus nidulans. Curr Biol 2007, 17(16):1384-1389.
• [72]Bayram O, Braus GH: Coordination of secondary metabolism and development in fungi: the velvet family of regulatory proteins. FEMS Microbiol Rev 2012, 36(1):1-24.
• [73]Ariyo B, Tamerler C, Bucke C, Keshavarz T: Enhanced penicillin production by oligosaccharides from batch cultures of Penicillium chrysogenum in stirred-tank reactors. FEMS Microbiol Lett 1998, 166(1):165-170.
• [74]Yin W-B, Amaike S, Wohlbach DJ, Gasch AP, Chiang Y-M, Wang CCC, Bok JW, Rohlfs M, Keller NP: An Aspergillus nidulans bZIP response pathway hardwired for defensive secondary metabolism operates through aflR. Mol Microbiol 2012, 83(5):1024-1034.
• [75]Fisch KM, Gillaspy AF, Gipson M, Henrikson JC, Hoover AR, Jackson L, Najar FZ, Waegele H, Cichewicz RH: Chemical induction of silent biosynthetic pathway transcription in Aspergillus niger. J Ind Microbiol Biotechnol 2009, 36(9):1199-1213.
• [76]Lerat S, Forest M, Lauzier A, Grondin G, Lacelle S, Beaulieu C: Potato suberin induces differentiation and secondary metabolism in the genus Streptomyces. Microbes Environ 2012, 27(1):36-42.
• [77]Baker PJ, Poultney C, Liu Z, Gross R, Montclare JK: Identification and comparison of cutinases for synthetic polyester degradation. Appl Microbiol Biotechnol 2012, 93(1):229-240.
• [78]Gandini A, Pascoal Neto C, Silvestre AJD: Suberin: a promising renewable resource for novel macromolecular materials. Prog Polym Sci 2006, 31(10):878-892.
• [79]Salazar M, Vongsangnak W, Panagiotou G, Andersen MR, Nielsen J: Uncovering transcriptional regulation of glycerol metabolism in Aspergilli through genome-wide gene expression data analysis. Mol Genet Genomics 2009, 282(6):571-586.
• [80]Garrido SM, Kitamoto N, Watanabe A, Shintani T, Gomi K: Functional analysis of FarA transcription factor in the regulation of the genes encoding lipolytic enzymes and hydrophobic surface binding protein for the degradation of biodegradable plastics in Aspergillus oryzae. J Biosci Bioeng 2012, 113(5):549-555.
• [81]Rocha ALM, Di Pietro A, Ruiz-Roldan C, Roncero MIG: Ctf1, a transcriptional activator of cutinase and lipase genes in Fusarium oxysporum is dispensable for virulence. Mol Plant Pathol 2008, 9(3):293-304.
• [82]Bravo-Ruiz G, Ruiz-Roldan C, Roncero MIG: Lipolytic System of the Tomato Pathogen Fusarium oxysporum f. sp. lycopersici. Mol Plant Microbe In 2013, 26(9):1054-1067.
• [83]Kovalchuk A, Driessen AJM: Phylogenetic analysis of fungal ABC transporters. BMC Genomics 2010, 11(1):177.
• [84]Andrade AC, Van Nistelrooy JGM, Peery RB, Skatrud PL, De Waard MA: The role of ABC transporters from Aspergillus nidulans in protection against cytotoxic agents and in antibiotic production. Mol Gen Genet 2000, 263(6):966-977.
• [85]Holyoak CD, Bracey D, Piper PW, Kuchler K, Coote PJ: The Saccharomyces cerevisiae weak acid inducible ABC transporter Pdr12 transports fluorescein and preservative anions from the cytosol by an energy dependent mechanism. J Bacteriol 1999, 181(15):4644-4652.
• [86]Vangelatos I, Roumelioti K, Gournas C, Suarez T, Scazzocchio C, Sophianopoulou V: Eisosome organization in the filamentous ascomycete Aspergillus nidulans. Eukaryot Cell 2010, 9(10):1441-1454.
• [87]Kelly DE, Kraševec N, Mullins J, Nelson DR: The CYPome (cytochrome P450 complement) of Aspergillus nidulans. Fungal Genet Biol 2009, 46:S53-S61.
• [88]Kitazume T, Takaya N, Nakayama N, Shoun H: Fusarium oxysporum fatty-acid subterminal hydroxylase (CYP505) is a membrane-bound eukaryotic counterpart of Bacillus megaterium cytochrome P450BM3. J Biol Chem 2000, 275(50):39734-39740.
• [89]Vanhanen S, West M, Kroon JTM, Lindner N, Casey J, Cheng Q, Elborough KM, Slabas AR: A consensus sequence for long-chain fatty-acid alcohol oxidases from Candida identifies a family of genes involved in lipid omega-oxidation in yeast with homologues in plants and bacteria. J Biol Chem 2000, 275(6):4445-4452.
• [90]Hynes MJ, Murray SL, Khew GS, Davis MA: Genetic analysis of the role of peroxisomes in the utilization of acetate and fatty acids in Aspergillus nidulans. Genetics 2008, 178(3):1355-1369.
• [91]Reiser K, Davis MA, Hynes MJ: Aspergillus nidulans contains six possible fatty acyl-CoA synthetases with FaaB being the major synthetase for fatty acid degradation. Arch Microbiol 2010, 192(5):373-382.
• [92]Reiser K, Davis MA, Hynes MJ: AoxA is a major peroxisomal long chain fatty acyl-CoA oxidase required for beta-oxidation in A. nidulans. Curr Genet 2010, 56(2):139-150.
• [93]De Cremer K, Mathys J, Vos C, Froenicke L, Michelmore RW, Cammue BPA, De Coninck B: RNAseq-based transcriptome analysis of Lactuca sativa infected by the fungal necrotroph Botrytis cinerea. Plant Cell Environ 2013, 36(11):1992-2007.
• [94]Maggio-Hall LA, Lyne P, Wolff JA, Keller NP: A single acyl-CoA dehydrogenase is required for catabolism of isoleucine, valine and short-chain fatty acids in Aspergillus nidulans. Fungal Genet Biol 2008, 45(3):180-189.
• [95]Pusztahelyi T, Klement É, Szajli E, Klem J, Miskei M, Karányi Z, Emri T, Kóvacs S, Orosz G, Kóvacs KL, Medzihradszky KF, Prade RA, Pócsi I: Comparison of transcriptional and translational changes caused by long-term menadione exposure in Aspergillus nidulans. Fungal Genet Biol 2011, 48(2):92-103.
• [96]Mathew S, Abraham TE: Bioconversions of ferulic acid, an hydroxycinnamic acid. Crit Rev Microbiol 2006, 32(3):115-125.
• [97]Caspi R, Altman T, Dreher K, Fulcher CA, Subhraveti P, Keseler IM, Kothari A, Krummenacker M, Latendresse M, Mueller LA, Ong Q, Paley S, Pujar A, Shearer AG, Travers M, Weerasinghe D, Zhang PF, Karp PD: The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of pathway/genome databases. Nucleic Acids Res 2012, 40(D1):D742-D753.
• [98]Tamayo EN, Villanueva A, Hasper AA, de Graaff LH, Ramón D, Orejas M: CreA mediates repression of the regulatory gene xlnR which controls the production of xylanolytic enzymes in Aspergillus nidulans. Fungal Genet Biol 2008, 45(6):984-993.
• [99]Gygi SP, Rist B, Gerber SA, Turecek F, Gelb MH, Aebersold R: Quantitative analysis of complex protein mixtures using isotope-coded affinity tags. Nat Biotechnol 1999, 17(10):994-999.
• [100]Hinnebusch AG: Translational regulation of GCN4 and the general amino acid control of yeast. Annu Rev Microbiol 2005, 59:407-450.
• [101]Beyer A, Hollunder J, Nasheuer HP, Wilhelm T: Post-transcriptional expression regulation in the yeast Saccharomyces cerevisiae on a genomic scale. Mol Cell Proteomics 2004, 3(11):1083-1092.
• [102]Laloo B, Simon D, Veilla V, Lauzel D, Guyonnet-Duperat V, Moreau-Gaudry F, Sagliocco F, Grosset C: Analysis of post-transcriptional regulations by a functional, integrated, and quantitative method. Mol Cell Proteomics 2009, 8(8):1777-1788.
• [103]Martins I, Garcia H, Varela A, Núñez O, Planchon S, Galceran MT, Renaut J, Rebelo LPN, Silva Pereira C: Investigating Aspergillus nidulans secretome during colonisation of cork cell walls. J Proteomics 2014, 26(98):175-188.