Illumina identification of RsrA, a conserved C2H2 transcription factor coordinating the NapA mediated oxidative stress signaling pathway in Aspergillus

BMC Genomics

Volumn 15, Issue 1, 2014, Pages

  Bok, Woo ^a   Wiemann, Philipp ^a   Garvey, Graeme S ^a,b   Lim, Yun ^a   Haas, Brian ^c   Wortman, Jennifer ^c   Keller, Nancy P ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b Seminis Vegetable Seeds Inc   (United States)

^c BROAD INSTITUTE OF MIT AND HARVARD   (United States)

Author keywords

AP 1; Aspergillus; CCAAT; Mutagenesis; Next generation sequencing; Stress response

Indexed keywords

BASIC LEUCINE ZIPPER TRANSCRIPTION FACTOR; GLUTATHIONE; HYDROGEN PEROXIDE; PROTEIN ATFA; PROTEIN NAPA; PROTEIN RSRA; REACTIVE OXYGEN METABOLITE; STERIGMATOCYSTIN; THIOREDOXIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR YAP1; UNCLASSIFIED DRUG; FUNGAL PROTEIN;

ARTICLE; ASPERGILLUS; ASPERGILLUS FLAVUS; ASPERGILLUS FUMIGATUS; ASPERGILLUS NIDULANS; CONTROLLED STUDY; DELETION MUTANT; EXPOSURE; FUNGUS CULTURE; MUTAGENESIS; NONHUMAN; NUCLEIC ACID ANALYSIS; OXIDATIVE STRESS; PHENOTYPE; PROTEIN ANALYSIS; PROTEIN EXPRESSION; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; SPOROGENESIS; UPREGULATION; WILD TYPE; BIOLOGICAL MODEL; BIOSYNTHESIS; CYTOLOGY; DNA SEQUENCE; DRUG EFFECTS; FUNGUS SPORE; GENE DELETION; GENE EXPRESSION REGULATION; GENETIC COMPLEMENTATION; GENETIC TRANSCRIPTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MEIOSIS; METABOLISM; MITOSIS; NUCLEOTIDE SEQUENCE; REPRODUCTION; SOUTHERN BLOTTING; SYNTENY; THIN LAYER CHROMATOGRAPHY;

ASPERGILLUS; ASPERGILLUS FLAVUS; ASPERGILLUS FUMIGATUS; EMERICELLA NIDULANS; FUNGI;

ASPERGILLUS; BLOTTING, SOUTHERN; CHROMATOGRAPHY, THIN LAYER; CONSERVED SEQUENCE; FUNGAL PROTEINS; GENE DELETION; GENE EXPRESSION REGULATION, FUNGAL; GENETIC COMPLEMENTATION TEST; HYDROGEN PEROXIDE; MEIOSIS; MITOSIS; MODELS, BIOLOGICAL; OXIDATIVE STRESS; PHENOTYPE; REPRODUCTION; SEQUENCE ANALYSIS, DNA; SIGNAL TRANSDUCTION; SPORES, FUNGAL; STERIGMATOCYSTIN; SYNTENY; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84924336097     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-15-1011     Document Type: Article

References (71)

1. Calvo AM, Wilson RA, Bok JW, Keller NP: Relationship between secondary metabolism and fungal development. Microbiol Mol Biol Rev 2002, 66:447-459. 10.1128/MMBR.66.3.447-459.2002
2. Hong SY, Roze LV, Wee J, Linz JE: Evidence that a transcription factor regulatory network coordinates oxidative stress response and secondary metabolism in aspergilli. Microbiologyopen 2013, 2:144-160. 10.1002/mbo3.63
3. Montibus M, Pinson-Gadais L, Richard-Forget F, Barreau C, Ponts N: Coupling of transcriptional response to oxidative stress and secondary metabolism regulation in filamentous fungi. Crit Rev Microbiol 2013. doi:10.3109/1040841X.2013.829416
4. Grintzalis K, Vernardis SI, Klapa MI, Georgiou CD: Role of oxidative stress in Sclerotial differentiation and aflatoxin B1 biosynthesis in Aspergillus flavus. Appl Environ Microbiol 2014, 80:5561-5571. 10.1128/AEM.01282-14
5. Wu D, Oide S, Zhang N, Choi MY, Turgeon BG: ChLae1 and ChVel1 regulate T-toxin production, virulence, oxidative stress response, and development of the maize pathogen Cochliobolus heterostrophus. PLoS Pathog 2012, 8:e1002542. 10.1371/journal.ppat.1002542
6. Hong SY, Roze LV, Linz JE: Oxidative stress-related transcription factors in the regulation of secondary metabolism. Toxins (Basel) 2013, 5:683-702. 10.3390/toxins5040683
7. Kim HJ: Exploitation of reactive oxygen species by fungi: roles in host-fungus interaction and fungal development. J Microbiol Biotechnol 2014, 24:1455-1463.
8. Bayram O, Krappmann S, Ni M, Bok JW, Helmstaedt K, Valerius O, Braus-Stromeyer S, Kwon NJ, Keller NP, Yu JH, Braus GH: VelB/VeA/LaeA complex coordinates light signal with fungal development and secondary metabolism. Science 2008, 320:1504-1506. 10.1126/science.1155888
9. Baidya S, Duran RM, Lohmar JM, Harris-Coward PY, Cary JW, Hong S-Y, Roze LV, Linz JE, Calvo AM: VeA is associated with the response to oxidative stress in the aflatoxin producer aspergillus flavus. Eukaryot Cell 2014, 13:1095-1103. 10.1128/EC.00099-14
10. Jain S, Keller NP: Insights to fungal biology through LaeA sleuthing. Fungal Biol Rev 2013, 27:51-59. 10.1016/j.fbr.2013.05.004
11. Calvo AM: The VeA regulatory system and its role in morphological and chemical development in fungi. Fungal Genet Biol 2008, 45:1053-1061. 10.1016/j.fgb.2008.03.014
12. Cary JW, Obrian GR, Nielsen DM, Nierman WC, Harris-Coward P, Yu JH, Bhatnagar D, Cleveland TE, Payne GA, Calvo AM: Elucidation of veA-dependent genes associated with aflatoxin and sclerotial production in Aspergillus flavus by functional genomics. Appl Environ Microbiol 2007, 76:1107-1118.
13. Georgianna DR, Fedorova ND, Burroughs JL, Dolezal AL, Bok JW, Horowitz-Brown S, Woloshuk CP, Yu J, Keller NP, Payne GA: Beyond aflatoxin: four distinct expression patterns and functional roles associated with Aspergillus flavus secondary metabolism gene clusters. Mol Plant Pathol 2010, 11:213-226. 10.1111/j.1364-3703.2009.00594.x
14. Perrin RM, Fedorova ND, Bok JW, Cramer RA, Wortman JR, Kim HS, Nierman WC, Keller NP: Transcriptional regulation of chemical diversity in Aspergillus fumigatus by LaeA. PLoS Pathog 2007, 3:e50. 10.1371/journal.ppat.0030050
15. Kamerewerd J, Zadra I, Kurnsteiner H, Kuck U: PcchiB1, encoding a class V chitinase, is affected by PcVelA and PcLaeA, and is responsible for cell wall integrity in Penicillium chrysogenum. Microbiology 2011, 157:3036-3048. 10.1099/mic.0.051896-0
16. Karimi Aghcheh R, Druzhinina IS, Kubicek CP: The putative protein methyltransferase LAE1 of Trichoderma atroviride is a key regulator of asexual development and mycoparasitism. PLoS One 2013, 8:e67144. 10.1371/journal.pone.0067144
17. Seiboth B, Karimi RA, Phatale PA, Linke R, Hartl L, Sauer DG, Smith KM, Baker SE, Freitag M, Kubicek CP: The putative protein methyltransferase LAE1 controls cellulase gene expression in Trichoderma reesei. Mol Microbiol 2012, 84:1150-1164. 10.1111/j.1365-2958.2012.08083.x
18. Yang Q, Chen Y, Ma Z: Involvement of BcVeA and BcVelB in regulating conidiation, pigmentation and virulence in Botrytis cinerea. Fungal Genet Biol 2012, 50:63-71.
19. Shaaban MI, Bok JW, Lauer C, Keller NP: Suppressor mutagenesis identifies a velvet complex remediator of Aspergillus nidulans secondary metabolism. Eukaryot Cell 2010, 9:1816-1824. 10.1128/EC.00189-10
20. Soukup AA, Chiang YM, Bok JW, Reyes-Dominguez Y, Oakley BR, Wang CC, Strauss J, Keller NP: Overexpression of the Aspergillus nidulans histone 4 acetyltransferase EsaA increases activation of secondary metabolite production. Mol Microbiol 2012, 86:314-330. 10.1111/j.1365-2958.2012.08195.x
21. Blumenstiel JP, Noll AC, Griffiths JA, Perera AG, Walton KN, Gilliland WD, Hawley RS, Staehling-Hampton K: Identification of EMS-induced mutations in Drosophila melanogaster by whole-genome sequencing. Genetics 2009, 182:25-32. 10.1534/genetics.109.101998
22. Doitsidou M, Poole RJ, Sarin S, Bigelow H, Hobert O: C. elegans mutant identification with a one-step whole-genome-sequencing and SNP mapping strategy. PLoS One 2010, 5:e15435. 10.1371/journal.pone.0015435
23. Nowrousian M, Teichert I, Masloff S, Kuck U: Whole-genome sequencing of Sordaria macrospora mutants identifies developmental genes. G3 (Bbethesda) 2012, 2:261-270. 2012
24. Uchida N, Sakamoto T, Kurata T, Tasaka M: Identification of EMS-induced causal mutations in a non-reference Arabidopsis thaliana accession by whole genome sequencing. Plant Cell Physiol 2011, 52:716-722. 10.1093/pcp/pcr029
25. Butchko RA, Adams TH, Keller NP: Aspergillus nidulans mutants defective in stc gene cluster regulation. Genetics 1999, 153:715-720.
26. Horn BW, Moore GG, Carbone I: Sexual reproduction in Aspergillus flavus. Mycologia 2009, 101:423-429. 10.3852/09-011
27. O'Gorman CM, Fuller HT, Dyer PS: Discovery of a sexual cycle in the opportunistic fungal pathogen Aspergillus fumigatus. Nature 2009, 457:471-474. 10.1038/nature07528
28. Malavazi I, Savoldi M, Di Mauro SM, Menck CF, Harris SD, Goldman MH, Goldman GH: Transcriptome analysis of Aspergillus nidulans exposed to camptothecin-induced DNA damage. Eukaryot Cell 2006, 5:1688-1704. 10.1128/EC.00167-06
29. Hansberg W, Salas-Lizana R, Dominguez L: Fungal catalases: function, phylogenetic origin and structure. Arch Biochem Biophys 2012, 525:170-180. 10.1016/j.abb.2012.05.014
30. Yin W-B, Reinke AW, Szilágyi M, Emri T, Chiang Y-M, Keating AE, Pócsi I, Wang CCC, Keller NP: bZIP transcription factors affecting secondary metabolism, sexual development and stress responses in Aspergillus nidulans. Microbiology 2013, 159:77-88. 10.1099/mic.0.063370-0
31. Asano Y, Hagiwara D, Yamashino T, Mizuno T: Characterization of the bZip-type transcription factor NapA with reference to oxidative stress response in Aspergillus nidulans. Biosci Biotechnol Biochem 2007, 71:1800-1803. 10.1271/bbb.70133
32. Thon M, Al Abdallah Q, Hortschansky P, Scharf DH, Eisendle M, Haas H, Brakhage AA: The CCAAT-binding complex coordinates the oxidative stress response in eukaryotes. Nucleic Acids Res 2010, 38:1098-1113. 10.1093/nar/gkp1091
33. Lara-Rojas F, Sanchez O, Kawasaki L, Aguirre J: Aspergillus nidulans transcription factor AtfA interacts with the MAPK SakA to regulate general stress responses, development and spore functions. Mol Microbiol 2011, 80:436-454. 10.1111/j.1365-2958.2011.07581.x
34. Kato M: An overview of the CCAAT-box binding factor in filamentous fungi: assembly, nuclear translocation, and transcriptional enhancement. Biosci Biotechnol Biochem 2005, 69:663-672. 10.1271/bbb.69.663
35. Lessing F, Kniemeyer O, Wozniok I, Loeffler J, Kurzai O, Haertl A, Brakhage AA: The Aspergillus fumigatus transcriptional regulator AfYap1 represents the major regulator for defense against reactive oxygen intermediates but is dispensable for pathogenicity in an intranasal mouse infection model. Eukaryot Cell 2007, 6:2290-2302. 10.1128/EC.00267-07
36. Thön M, Al-Abdallah Q, Hortschansky P, Brakhage AA: The thioredoxin system of the filamentous fungus Aspergillus nidulans: impact on development and oxidative stress response. J Biol Chem 2007, 282:27259-27269. 10.1074/jbc.M704298200
37. Burns C, Geraghty R, Neville C, Murphy A, Kavanagh K, Doyle S: Identification, cloning, and functional expression of three glutathione transferase genes from Aspergillus fumigatus. Fungal Genet Biol 2005, 42:319-327. 10.1016/j.fgb.2005.01.001
38. Sato I, Shimizu M, Hoshino T, Takaya N: The glutathione system of Aspergillus nidulans involves a fungus-specific glutathione S -transferase. J Biol Chem 2009, 284:8042-8053. 10.1074/jbc.M807771200
39. Kawasaki L, Wysong D, Diamond R, Aguirre J: Two divergent catalase genes are differentially regulated during Aspergillus nidulans development and oxidative stress. J Bacteriol 1997, 179:3284-3292.
40. Oberegger H, Zadra I, Schoeser M, Haas H: Iron starvation leads to increased expression of Cu/Zn-superoxide dismutase in Aspergillus. FEBS Lett 2000, 485:113-116. 10.1016/S0014-5793(00)02206-7
41. DePristo MA, Banks E, Poplin R, Garimella KV, Maguire JR, Hartl C, Philippakis AA, del Angel G, Rivas MA, Hanna M, McKenna A, Fennell TJ, Kernytsky AM, Sivachenko AY, Cibulskis K, Gabriel SB, Altshuler D, Daly MJ: A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet 2011, 43:491-498. 10.1038/ng.806
42. Zuryn S, Le Gras S, Jamet K, Jarriault S: A strategy for direct mapping and identification of mutations by whole-genome sequencing. Genetics 2010, 186:427-430. 10.1534/genetics.110.119230
43. Bok JW, Keller NP: LaeA, a regulator of secondary metabolism in Aspergillus spp. Eukaryot Cell 2004, 3:527-535. 10.1128/EC.3.2.527-535.2004
44. Seetharam A, Stuart GW: A study on the distribution of 37 well conserved families of C2H2 zinc finger genes in eukaryotes. BMC Genomics 2013, 14:420. 10.1186/1471-2164-14-420
45. Nierman WC, Pain A, Anderson MJ, Wortman JR, Kim HS, Arroyo J, Berriman M, Abe K, Archer DB, Bermejo C, Bennett J, Bowyer P, Chen D, Collins M, Coulsen R, Davies R, Dyer PS, Farman M, Fedorova N, Fedorova N, Feldblyum TV, Fischer R, Fosker N, Fraser A, García JL, García MJ, Goble A, Goldman GH, Gomi K, Griffith-Jones S, et al.: Genomic sequence of the pathogenic and allergenic filamentous fungus Aspergillus fumigatus. Nature 2005, 438:1151-1156. 10.1038/nature04332
46. Lara-Ortiz T, Riveros-Rosas H, Aguirre J: Reactive oxygen species generated by microbial NADPH oxidase NoxA regulate sexual development in Aspergillus nidulans. Mol Microbiol 2003, 50:1241-1255. 10.1046/j.1365-2958.2003.03800.x
47. Hernandez-Onate MA, Esquivel-Naranjo EU, Mendoza-Mendoza A, Stewart A, Herrera-Estrella AH: An injury-response mechanism conserved across kingdoms determines entry of the fungus Trichoderma atroviride into development. Proc Natl Acad Sci U S A 2012, 109:14918-14923. 10.1073/pnas.1209396109
48. Sato I, Shimatani K, Fujita K, Abe T, Shimizu M, Fujii T, Hoshino T, Takaya N: Glutathione reductase/glutathione is responsible for cytotoxic elemental sulfur tolerance via polysulfide shuttle in fungi. J Biol Chem 2011, 286:20283-20291. 10.1074/jbc.M111.225979
49. Atkinson HJ, Babbitt PC: Glutathione transferases are structural and functional outliers in the thioredoxin fold. Biochemistry 2009, 48:11108-11116. 10.1021/bi901180v
50. Shimizu K, Keller NP: Genetic involvement of a cAMP-dependent protein kinase in a G protein signaling pathway regulating morphological and chemical transitions in Aspergillus nidulans. Genetics 2001, 157:591-600.
51. Tsitsigiannis DI, Kowieski TM, Zarnowski R, Keller NP: Endogenous lipogenic regulators of spore balance in Aspergillus nidulans. Eukaryot Cell 2004, 3:1398-1411. 10.1128/EC.3.6.1398-1411.2004
52. Shaaban M, Palmer JM, El-Naggar WA, El-Sokkary MA, el SE H, Keller NP: Involvement of transposon-like elements in penicillin gene cluster regulation. Fungal Genet Biol 2010, 47:423-432. 10.1016/j.fgb.2010.02.006
53. Hammond TM, Andrewski MD, Roossinck MJ, Keller NP: Aspergillus mycoviruses are targets and suppressors of RNA silencing. Eukaryot Cell 2008, 7:350-357. 10.1128/EC.00356-07
54. Nayak T, Szewczyk E, Oakley CE, Osmani A, Ukil L, Murray SL, Hynes MJ, Osmani SA, Oakley BR: A versatile and efficient gene-targeting system for Aspergillus nidulans. Genetics 2006, 172:1557-1566.
55. Balazs A, Pocsi I, Hamari Z, Leiter E, Emri T, Miskei M, Olah J, Toth V, Hegedus N, Prade RA, Molnár M, Pócsi I: AtfA bZIP-type transcription factor regulates oxidative and osmotic stress responses in Aspergillus nidulans. Mol Genet Genomics 2010, 283:289-303. 10.1007/s00438-010-0513-z
56. He ZM, Price MS, Obrian GR, Georgianna DR, Payne GA: Improved protocols for functional analysis in the pathogenic fungus Aspergillus flavus. BMC Microbiol 2007, 7:104. 10.1186/1471-2180-7-104
57. da Silva Ferreira ME, Kress MR, Savoldi M, Goldman MH, Hartl A, Heinekamp T, Brakhage AA, Goldman GH: The akuB(KU80) mutant deficient for nonhomologous end joining is a powerful tool for analyzing pathogenicity in Aspergillus fumigatus. Eukaryot Cell 2006, 5:207-211. 10.1128/EC.5.1.207-211.2006
58. Xue T, Nguyen CK, Romans A, Kontoyiannis DP, May GS: Isogenic auxotrophic mutant strains in the Aspergillus fumigatus genome reference strain AF293. Arch Microbiol 2004, 182:346-353. 10.1007/s00203-004-0707-z
59. Bok JW, Balajee SA, Marr KA, Andes D, Nielsen KF, Frisvad JC, Keller NP: LaeA, a regulator of morphogenetic fungal virulence factors. Eukaryot Cell 2005, 4:1574-1582. 10.1128/EC.4.9.1574-1582.2005
60. Wieser J, Lee BN, Fondon J 3rd, Adams TH: Genetic requirements for initiating asexual development in Aspergillus nidulans. Curr Genet 1994, 27:62-69. 10.1007/BF00326580
61. Li H: A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data. Bioinformatics 2011, 27:2987-2993. 10.1093/bioinformatics/btr509
62. McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altshuler D, Gabriel S, Daly M, DePristo MA: The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 2010, 20:1297-1303. 10.1101/gr.107524.110
63. Abeel T, Van Parys T, Saeys Y, Galagan J, Van de Peer Y: GenomeView: a next-generation genome browser. Nucleic Acids Res 2012, 40:e12. 10.1093/nar/gkr995
64. Bok JW, Soukup AA, Chadwick E, Chiang YM, Wang CC, Keller NP: VeA and MvlA repression of the cryptic orsellinic acid gene cluster in Aspergillus nidulans involves histone 3 acetylation. Mol Microbiol 2013, 89:963-974. 10.1111/mmi.12326
65. Calvo AM, Bok J, Brooks W, Keller NP: veA is required for toxin and sclerotial production in Aspergillus parasiticus. Appl Environ Microbiol 2004, 70:4733-4739. 10.1128/AEM.70.8.4733-4739.2004
66. Mooney JL, Yager LN: Light is required for conidiation in Aspergillus nidulans. Genes Dev 1990, 4:1473-1482. 10.1101/gad.4.9.1473
67. da Silva Ferreira ME, Heinekamp T, Härtl A, Brakhage AA, Semighini CP, Harris SD, Savoldi M, de Gouvêa PF, de Souza Goldman MH, Goldman GH: Functional characterization of the Aspergillus fumigatus calcineurin. Fungal Genet Biol 2007, 44:219-230. 10.1016/j.fgb.2006.08.004
68. Szewczyk E, Nayak T, Oakley CE, Edgerton H, Xiong Y, Taheri-Talesh N, Osmani SA, Oakley BR: Fusion PCR and gene targeting in Aspergillus nidulans. Nat Protoc 2006, 1:3111-3120.
69. Sambrook J, Russell DW: Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press. 2001.
70. Amaike S, Keller NP: Distinct roles for VeA and LaeA in development and pathogenesis of Aspergillus flavus. Eukaryot Cell 2009, 8:1051-1060. 10.1128/EC.00088-09
71. Cerqueira GC, Arnaud MB, Inglis DO, Skrzypek MS, Binkley G, Simison M, Miyasato SR, Binkley J, Orvis J, Shah P, Wymore F, Sherlock G, Wortman JR: The Aspergillus Genome Database: multispecies curation and incorporation of RNA-Seq data to improve structural gene annotations. Nucleic Acids Res 2014,42(Database issue):D705-D710.