Systematic dissection of the evolutionarily conserved WetA developmental regulator across a genus of filamentous fungi

mBio

Volumn 9, Issue 4, 2018, Pages

  Wu, Ming Yueh ^a,f   Mead, Matthew E ^b   Lee, Mi Kyung ^c   Ostrem Loss, Erin M ^a   Kim, Sun Chang ^d   Rokas, Antonis ^b   Yu, Jae Hyuk ^a,e  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b VANDERBILT UNIVERSITY   (United States)

^c Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

^d Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

^e Konkuk University   (South Korea)

^f Ginkgo Bioworks   (United States)

Author keywords

Asexual development; Aspergillus; Gene regulatory network; Sporulation; WetA

Indexed keywords

REGULATOR PROTEIN; TRANSCRIPTOME; UNCLASSIFIED DRUG; WETA PROTEIN; DNA BINDING PROTEIN; FUNGAL PROTEIN;

ARTICLE; ASEXUAL SPORE; ASPERGILLUS FLAVUS; ASPERGILLUS FUMIGATUS; ASPERGILLUS NIDULANS; BRLA GENE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; FILAMENTOUS FUNGUS; FUNGAL GENE; GENE REGULATORY NETWORK; GENE REPRESSION; GENETIC CONSERVATION; MOLECULAR EVOLUTION; NEGATIVE FEEDBACK; NONHUMAN; PRIORITY JOURNAL; REGULATOR GENE; SPOROGENESIS; WETA GENE; ASPERGILLUS; FUNGUS SPORE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE KNOCKOUT; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM;

ASPERGILLUS; DNA-BINDING PROTEINS; EVOLUTION, MOLECULAR; FUNGAL PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, FUNGAL; GENE KNOCKOUT TECHNIQUES; GENE REGULATORY NETWORKS; SPORES, FUNGAL;

EID: 85055530331     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.01130-18     Document Type: Article

References (72)

1. Ebbole DJ. 2010. The conidium, p 577–590. In Cellular and molecular biology of filamentous fungi. American Society of Microbiology, Washington, DC.
2. Calvo AM, Wilson RA, Bok JW, Keller NP. 2002. Relationship between secondary metabolism and fungal development. Microbiol Mol Biol Rev 66:447–459. https://doi.org/10.1128/MMBR.66.3.447-459.2002.
3. Yu JH, Keller NP. 2005. Regulation of secondary metabolism in filamentous fungi. Annu Rev Phytopathol 43:437–458. https://doi.org/10.1146/annurev.phyto.43.040204.140214.
4. Bennett JW, Klich MA. 1992, Aspergillus: biology and industrial applications. Butterworth-Heinemann, Boston, MA.
5. Alshannaq A, Yu JH. 2017. Occurrence, toxicity, and analysis of major mycotoxins in food. Int J Environ Res Public Health 14:632. https://doi.org/10.3390/ijerph14060632.
6. Fedorova ND, Khaldi N, Joardar VS, Maiti R, Amedeo P, Anderson MJ, Crabtree J, Silva JC, Badger JH, Albarraq A, Angiuoli S, Bussey H, Bowyer P, Cotty PJ, Dyer PS, Egan A, Galens K, Fraser-Liggett CM, Haas BJ, Inman JM, Kent R, Lemieux S, Malavazi I, Orvis J, Roemer T, Ronning CM, Sundaram JP, Sutton G, Turner G, Venter JC, White OR, Whitty BR, Youngman P, Wolfe KH, Goldman GH, Wortman JR, Jiang B, Denning DW, Nierman WC. 2008. Genomic islands in the pathogenic filamentous fungus Aspergillus fumigatus. PLoS Genet 4:e1000046. https://doi.org/10.1371/journal.pgen.1000046.
7. Timberlake WE, Boylan MT, Mirabito PM, Willett CE, Zimmerman CR. 1987. Isolation and physical characterization of three essential conidiation genes from Aspergillus nidulans. Antonie Van Leeuwenhoek 53:317. https://doi.org/10.1007/BF00400554.
8. Tao L, Yu JH. 2011. AbaA and WetA govern distinct stages of Aspergillus fumigatus development. Microbiology 157:313–326. https://doi.org/10.1099/mic.0.044271-0.
9. Desjardins CA, Champion MD, Holder JW, Muszewska A, Goldberg J, Bailão AM, Brigido MM, Ferreira ME, Garcia AM, Grynberg M, Gujja S, Heiman DI, Henn MR, Kodira CD, León-Narváez H, Longo LV, Ma LJ, Malavazi I, Matsuo AL, Morais FV, Pereira M, Rodríguez-Brito S, Sakthi-kumar S, Salem-Izacc SM, Sykes SM, Teixeira MM, Vallejo MC, Walter ME, Yandava C, Young S, Zeng Q, Zucker J, Felipe MS, Goldman GH, Haas BJ, McEwen JG, Nino-Vega G, Puccia R, San-Blas G, Soares CM, Birren BW, Cuomo CA. 2011. Comparative genomic analysis of human fungal pathogens causing paracoccidioidomycosis. PLoS Genet 7:e1002345. https://doi.org/10.1371/journal.pgen.1002345.
10. Martinelli SD, Clutterbuck AJ. 1971. A quantitative survey of conidiation mutants in Aspergillus nidulans. J Gen Microbiol 69:261–268. https://doi.org/10.1099/00221287-69-2-261.
11. Adams TH, Boylan MT, Timberlake WE. 1988. brlA is necessary and sufficient to direct conidiophore development in Aspergillus nidulans. Cell 54:353–362. https://doi.org/10.1016/0092-8674(88)90198-5.
12. Timberlake WE. 1993. Translational triggering and feedback fixation in the control of fungal development. Plant Cell 5:1453–1460. https://doi.org/10.1105/tpc.5.10.1453.
13. Sewall TC. 1994. Cellular effects of misscheduled brlA, abaA, and wetA expression in Aspergillus nidulans. Can J Microbiol 40:1035–1042. https://doi.org/10.1139/m94-164.
14. Clutterbuck AJ. 1969. A mutational analysis of conidial development in Aspergillus nidulans. Genetics 63:317–327.
15. Shin KS, Kim YH, Yu JH. 2015. Proteomic analyses reveal the key roles of BrlA and AbaA in biogenesis of gliotoxin in Aspergillus fumigatus. Biochem Biophys Res Commun 463:428–433. https://doi.org/10.1016/j.bbrc.2015.05.090.
16. Son H, Kim MG, Min K, Lim JY, Choi GJ, Kim JC, Chae SK, Lee YW. 2014. WetA is required for conidiogenesis and conidium maturation in the ascomycete fungus Fusarium graminearum. Eukaryot Cell 13:87–98. https://doi.org/10.1128/EC.00220-13.
17. Wang M, Sun X, Zhu C, Xu Q, Ruan R, Yu D, Li H. 2015. PdbrlA, PdabaA and PdwetA control distinct stages of conidiogenesis in Penicillium digi-digi-tatum. Res Microbiol 166:56–65. https://doi.org/10.1016/j.resmic.2014.12.003. tatum.
18. 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. https://doi.org/10.1016/j.fgb.2009.10.004.
19. Li F, Shi HQ, Ying SH, Feng MG. 2015. WetA and VosA are distinct regulators of conidiation capacity, conidial quality, and biological control potential of a fungal insect pathogen. Appl Microbiol Biotechnol 99:10069–10081. https://doi.org/10.1007/s00253-015-6823-7.
20. Marshall MA, Timberlake WE. 1991. Aspergillus nidulans wetA activates spore-specific gene expression. Mol Cell Biol 11:55–62. https://doi.org/10.1128/MCB.11.1.55.
21. Sewall TC, Mims CW, Timberlake WE. 1990. Conidium differentiation in Aspergillus nidulans wild-type and wet-white (wetA) mutant strains. Dev Biol 138:499–508. https://doi.org/10.1016/0012-1606(90)90215-5.
22. Mirabito PM, Adams TH, Timberlake WE. 1989. Interactions of three sequentially expressed genes control temporal and spatial specificity in Aspergillus development. Cell 57:859–868. https://doi.org/10.1016/0092-8674(89)90800-3.
23. Prade RA, Timberlake WE. 1994. The Penicillium chrysogenum and Aspergillus nidulans wetA developmental regulatory genes are functionally equivalent. Mol Gen Genet 244:539–547. https://doi.org/10.1007/BF00 583905.
24. de Vries RP, Riley R, Wiebenga A, Aguilar-Osorio G, Amillis S, Uchima CA, Anderluh G, Asadollahi M, Askin M, Barry K, Battaglia E, Bayram Ö, Benocci T, Braus-Stromeyer SA, Caldana C, Cánovas D, Cerqueira GC, Chen F, Chen W, Choi C, Clum A, Dos Santos RA, Damásio AR, Diallinas G, Emri T, Fekete E, Flipphi M, Freyberg S, Gallo A, Gournas C, Habgood R, Hainaut M, Harispe ML, Henrissat B, Hildén KS, Hope R, Hossain A, Karabika E, Karaffa L, Karányi Z, Kraševec N, Kuo A, Kusch H, LaButti K, Lagendijk EL, Lapidus A, Levasseur A, Lindquist E, Lipzen A, et al. 2017. Comparative genomics reveals high biological diversity and specific adaptations in the industrially and medically important fungal genus Aspergillus. Genome Biol 18:28. https://doi.org/10.1186/s13059-017-1151-0.
25. Park HS, Yu JH. 2012. Genetic control of asexual sporulation in filamentous fungi. Curr Opin Microbiol 15:669–677. https://doi.org/10.1016/j.mib.2012.09.006.
26. Boylan MT, Mirabito PM, Willett CE, Zimmerman CR, Timberlake WE. 1987. Isolation and physical characterization of three essential conidiation genes from Aspergillus nidulans. Mol Cell Biol 7:3113–3118. https://doi.org/10.1128/MCB.7.9.3113.
27. Chang YC, Timberlake WE. 1993. Identification of Aspergillus brlA response elements (BREs) by genetic selection in yeast. Genetics 133: 29–38.
28. Adams TH, Timberlake WE. 1990. Upstream elements repress premature expression of an Aspergillus developmental regulatory gene. Mol Cell Biol 10:4912–4919. https://doi.org/10.1128/MCB.10.9.4912.
29. Andrianopoulos A, Timberlake WE. 1994. The Aspergillus nidulans abaA gene encodes a transcriptional activator that acts as a genetic switch to control development. Mol Cell Biol 14:2503–2515. https://doi.org/10.1128/MCB.14.4.2503.
30. Wu MY, Mead ME, Kim SC, Rokas A, Yu JH. 2017. WetA bridges cellular and chemical development in Aspergillus flavus. PLoS One 12:e0179571. https://doi.org/10.1371/journal.pone.0179571.
31. Piskacek S, Gregor M, Nemethova M, Grabner M, Kovarik P, Piskacek M. 2007. Nine-amino-acid transactivation domain: establishment and prediction utilities. Genomics 89:756–768. https://doi.org/10.1016/j.ygeno.2007.02.003.
32. Nguyen Ba AN, Pogoutse A, Provart N, Moses AM. 2009. NLStradamus: a simple Hidden Markov Model for nuclear localization signal prediction. BMC Bioinformatics 10:202. https://doi.org/10.1186/1471-2105-10-202.
33. Horton P, Park KJ, Obayashi T, Fujita N, Harada H, Adams-Collier CJ, Nakai K. 2007. WoLF PSORT: protein localization predictor. Nucleic Acids Res 35:W585–W587. https://doi.org/10.1093/nar/gkm259.
34. Mi H, Dong Q, Muruganujan A, Gaudet P, Lewis S, Thomas PD. 2010. PANTHER version 7: improved phylogenetic trees, orthologs and collaboration with the Gene Ontology Consortium. Nucleic Acids Res 38: D204–D210. https://doi.org/10.1093/nar/gkp1019.
35. Sewall TC, Mims CW, Timberlake WE. 1990. abaA controls phialide differentiation in Aspergillus nidulans. Plant Cell 2:731–739. https://doi.org/10.1105/tpc.2.8.731.
36. Inglis DO, Binkley J, Skrzypek MS, Arnaud MB, Cerqueira GC, Shah P, Wymore F, Wortman JR, Sherlock G. 2013. Comprehensive annotation of secondary metabolite biosynthetic genes and gene clusters of Aspergillus nidulans, A. fumigatus, A. niger and A. oryzae. BMC Microbiol 13:91. https://doi.org/10.1186/1471-2180-13-91.
37. Lind AL, Wisecaver JH, Lameiras C, Wiemann P, Palmer JM, Keller NP, Rodrigues F, Goldman GH, Rokas A. 2017. Drivers of genetic diversity in secondary metabolic gene clusters within a fungal species. PLoS Biol 15:e2003583. https://doi.org/10.1371/journal.pbio.2003583.
38. Mayorga ME, Timberlake WE. 1992. The developmentally regulated Aspergillus nidulans wA gene encodes a polypeptide homologous to polyketide and fatty acid synthases. Mol Gen Genet 235:205–212. https://doi.org/10.1007/BF00279362.
39. Machanick P, Bailey TL. 2011. MEME-ChIP: motif analysis of large DNA datasets. Bioinformatics 27:1696–1697. https://doi.org/10.1093/bioinformatics/btr189.
40. Grant CE, Bailey TL, Noble WS. 2011. FIMO: scanning for occurrences of a given motif. Bioinformatics 27:1017–1018. https://doi.org/10.1093/bioinformatics/btr064.
41. Timberlake WE. 1990. Molecular genetics of Aspergillus development. Annu Rev Genet 24:5–36. https://doi.org/10.1146/annurev.ge.24.120190.000253.
42. Bayry J, Beaussar TA, Dufrene YF, Sharma M, Bansal K, Kniemeyer O, Aimanianda V, Brakhage AA, Kaveri SV, Kwon-Chung KJ, Latge J-P, Beauvais A. 2014. Surface structure characterization of Aspergillus fumigatus conidia mutated in the melanin synthesis pathway and their human cellular immune response. Infect Immun 82:3141–3153.
43. Tsai HF, Wheeler MH, Chang YC, Kwon-Chung KJ. 1999. A developmentally regulated gene cluster involved in conidial pigment biosynthesis in Aspergillus fumigatus. J Bacteriol 181:6469–6477.
44. Brown SJ, Kellett PJ, Lippard SJ. 1993. Ixr1, a yeast protein that binds to platinated DNA and confers sensitivity to cisplatin. Science 261:603–605. https://doi.org/10.1126/science.8342024.
45. Coornaert D, Vissers S, André B. 1991. The pleiotropic UGA35(DURL) regulatory gene of Saccharomyces cerevisiae: cloning, sequence and identity with the DAL81 gene. Gene 97:163–171. https://doi.org/10.1016/0378-1119(91)90048-G.
46. Friden P, Schimmel P. 1987. LEU3 of Saccharomyces cerevisiae encodes a factor for control of RNA levels of a group of leucine-specific genes. Mol Cell Biol 7:2708–2717. https://doi.org/10.1128/MCB.7.8.2708.
47. Ahmed YL, Gerke J, Park HS, Bayram Ö, Neumann P, Ni M, Dickmanns A, Kim SC, Yu JH, Braus GH, Ficner R. 2013. The Velvet family of fungal regulators contains a DNA-binding domain structurally similar to NF-κB. PLoS Biol 11:e1001750. https://doi.org/10.1371/journal.pbio.1001750.
48. Park HS, Ni M, Jeong KC, Kim YH, Yu JH. 2012. The role, interaction and regulation of the Velvet regulator VelB in Aspergillus nidulans. PLoS One 7:e45935. https://doi.org/10.1371/journal.pone.0045935.
49. Sarikaya Bayram O, Bayram O, Valerius O, Park HS, Irniger S, Gerke J, Ni M, Han KH, Yu JH, Braus GH. 2010. LaeA control of Velvet family regulatory proteins for light-dependent development and fungal cell-type specificity. PLoS Genet 6:e1001226. https://doi.org/10.1371/journal.pgen.1001226.
50. Park HS, Yu YM, Lee MK, Maeng PJ, Kim SC, Yu JH. 2015. Velvet-mediated repression of β-glucan synthesis in Aspergillus nidulans spores. Sci Rep 5:10199. https://doi.org/10.1038/srep10199.
51. Ni M, Yu JH. 2007. A novel regulator couples sporogenesis and trehalose biogenesis in Aspergillus nidulans. PLoS One 2:e970. https://doi.org/10.1371/journal.pone.0000970.
52. Käfer E. 1977. Meiotic and mitotic recombination in Aspergillus and its chromosomal aberrations. Adv Genet 19:33–131. https://doi.org/10.1016/S0065-2660(08)60245-X.
53. Shaaban MI, Bok JW, Lauer C, Keller NP. 2010. Suppressor mutagenesis identifies a velvet complex remediator of Aspergillus nidulans secondary metabolism. Eukaryot Cell 9:1816–1824. https://doi.org/10.1128/EC.00189-10.
54. Seo JA, Guan Y, Yu JH. 2003. Suppressor mutations bypass the requirement of fluG for asexual sporulation and sterigmatocystin production in Aspergillus nidulans. Genetics 165:1083–1093.
55. Yu JH, Hamari Z, Han KH, Seo JA, Reyes-Domínguez Y, Scazzocchio C. 2004. Double-joint PCR: a PCR-based molecular tool for gene manipulations in filamentous fungi. Fungal Genet Biol 41:973–981. https://doi.org/10.1016/j.fgb.2004.08.001.
56. Han KH, Seo JA, Yu JH. 2004. Regulators of G-protein signalling in Aspergillus nidulans: RgsA downregulates stress response and stimulates asexual sporulation through attenuation of GanB (Galpha) signalling. Mol Microbiol 53:529–540. https://doi.org/10.1111/j.1365-2958.2004.04163.x.
57. Andrews S. 2010. FastQC: a quality control tool for high throughput sequence data. http://www.bioinformatics.babraham.ac.uk/projects/fastqc/.
58. Stajich JE, Harris T, Brunk BP, Brestelli J, Fischer S, Harb OS, Kissinger JC, Li W, Nayak V, Pinney DF, Stoeckert CJ, Roos DS. 2012. FungiDB: an integrated functional genomics database for fungi. Nucleic Acids Res 40:D675–D681. https://doi.org/10.1093/nar/gkr918.
59. Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL. 2013. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 14:R36. https://doi.org/10.1186/gb-2013-14-4-r36.
60. Anders S, Pyl PT, Huber W. 2015. HTSeq—a python framework to work with high-throughput sequencing data. Bioinformatics 31:166–169. https://doi.org/10.1093/bioinformatics/btu638.
61. Love MI, Huber W, Anders S. 2014. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15:550. https://doi.org/10.1186/s13059-014-0550-8.
62. Supek F, Bošnjak M, Škunca N, Šmuc T. 2011. REVIGO summarizes and visualizes long lists of Gene Ontology terms. PLoS One 6:e21800. https://doi.org/10.1371/journal.pone.0021800.
63. Park HS, Yuj H. 2012. Multi-copy genetic screen in Aspergillus nidulans, p 183–190. In Keller NP, Turner G (ed), Fungal secondary metabolism. Humana Press, Totowa, NJ.
64. Bolger AM, Lohse M, Usadel B. 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120. https://doi.org/10.1093/bioinformatics/btu170.
65. Li H. 2013. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv https://arxiv.org/abs/1303.3997.
66. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R; 1000 Genome Project Data Processing Subgroup. 2009. The Sequence Alignment Map Format and SAMtools. Bioinformatics 25:2078–2079.
67. Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, Nusbaum C, Myers RM, Brown M, Li W, Liu XS. 2008. Model-based analysis of ChIP-seq (MACS). Genome Biol 9:R137. https://doi.org/10.1186/gb-2008-9-9-r137.
68. Landt SG, Marinov GK, Kundaje A, Kheradpour P, Pauli F, Batzoglou S, Bernstein BE, Bickel P, Brown JB, Cayting P, Chen Y, DeSalvo G, Epstein C, Fisher-Aylor KI, Euskirchen G, Gerstein M, Gertz J, Hartemink AJ, Hoffman MM, Iyer VR, Jung YL, Karmakar S, Kellis M, Kharchenko PV, Li Q, Liu T, Liu XS, Ma L, Milosavljevic A, Myers RM, Park PJ, Pazin MJ, Perry MD, Raha D, Reddy TE, Rozowsky J, Shoresh N, Sidow A, Slattery M, Stamatoyannopoulos JA, Tolstorukov MY, White KP, Xi S, Farnham PJ, Lieb JD, Wold BJ, Snyder M. 2012. ChIP-seq guidelines and practices of the ENCODE and modENCODE consortia. Genome Res 22:1813–1831. https://doi.org/10.1101/gr.136184.111.
69. Kharchenko PV, Tolstorukov MY, Park PJ. 2008. Design and analysis of ChIP-seq experiments for DNA-binding proteins. Nat Biotechnol 26: 1351–1359. https://doi.org/10.1038/nbt.1508.
70. Quinlan AR, Hall IM. 2010. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26:841–842. https://doi.org/10.1093/bioinformatics/btq033.
71. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402. https://doi.org/10.1093/nar/25.17.3389.
72. Thomas PD, Campbell MJ, Kejariwal A, Mi H, Karlak B, Daverman R, Diemer K, Muruganujan A, Narechania A. 2003. PANTHER: a library of protein families and subfamilies indexed by function. Genome Res 13:2129–2141. https://doi.org/10.1101/gr.772403.