Genome sequence of an aflatoxigenic pathogen of Argentinian peanut, Aspergillus arachidicola

BMC Genomics

Volumn 19, Issue 1, 2018, Pages

  Moore, Geromy G ^a   Mack, Brian M ^a   Beltz, Shannon B ^a   Puel, Olivier ^b  

^a SOUTHERN REGIONAL RESEARCH CENTER   (United States)

^b TOXALIM RESEARCH CENTRE IN FOOD TOXICOLOGY   (France)

Author keywords

Aspergillus arachidicola; Gene ontology; Genome sequence; Mating type locus; Phylogenomics

Indexed keywords

ARGENTINIAN; ARTICLE; ASPERGILLUS; ASPERGILLUS ARACHIDICOLA; ASPERGILLUS FLAVUS; ASPERGILLUS PARASITICUS; FUNGAL GENOME; FUNGAL MATING TYPE GENE; FUNGAL STRAIN; GENE CLUSTER; GENE ONTOLOGY; GENE SEQUENCE; GENOME SIZE; NONHUMAN; PEANUT; PHYLOGENOMICS; SPECIES COMPARISON; SPECIES IDENTIFICATION; ARACHIS; GENE EXPRESSION PROFILING; GENETICS; HIGH THROUGHPUT SEQUENCING; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; PLANT DISEASE; PROCEDURES;

AFLATOXIN; FUNGAL PROTEIN; TRANSCRIPTOME;

AFLATOXINS; ARACHIS; ASPERGILLUS; FUNGAL PROTEINS; GENE EXPRESSION PROFILING; GENE ONTOLOGY; GENOME, FUNGAL; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; MOLECULAR SEQUENCE ANNOTATION; PLANT DISEASES; TRANSCRIPTOME;

EID: 85043472988     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/s12864-018-4576-2     Document Type: Article

References (62)

1. Pildain MB, Frisvad JC, Vaamonde G, Cabral D, Varga J, Samson RA. Two novel aflatoxin-producing Aspergillus species from Argentinean peanuts. Int J Syst Evol Microbiol. 2008;58:725-35.
2. Varga J, Frisvad JC, Samson RA. Two new aflatoxin producing species, and an overview of Aspergillus section Flavi. Stud Mycol. 2011;69:57-80.
3. Gonçalves SS, Stchigel AM, Cano JF, Godoy-Martinez PC, Colombo AL, Guarro J. Aspergillus novoparasiticus: a new clinical species of the section Flavi. Med Mycol. 2012;50:152-60.
4. Soares C, Rodrigues P, Peterson SW, Lima N, Venâncio A. Three new species of Aspergillus section Flavi isolated from almonds and maize in Portugal. Mycologia. 2012;104:682-97.
5. Santini A, Ritieni A. Aflatoxins: risk, exposure and remediation. In: Razzaghi-Abyaneh M, editor. Rijeka: Aflatoxins - recent advances and future prospects: InTech; 2013. https://doi.org/10.5772/52866.
6. Gonçalves JS, Ferracin LM, Carneiro Vieira ML, Iamanaka BT, Taniwaki MH, Pelegrinelli Fungaro MH. Molecular analysis of Aspergillus section Flavi isolated from Brazil nuts. World J Microbiol Biotechnol. 2012;28:1817-25.
7. Negri CE, Gonçalves SS, Xafranski H, Bergamasco MD, Aquinob VR, Castroc PTO, Colomboa AL. Cryptic and rare Aspergillus species in Brazil: prevalence in clinical samples and in vitro susceptibility to triazoles. J Clin Microbiol. 2014;52:3633-40.
8. Viaro HP, da Silva JJ, de Souza Ferranti L, Bordini JG, Massi FP, Pelegrinelli Fungaro MH. The first report of A. novoparasiticus, A. arachidicola and A. pseudocaelatus in Brazilian corn kernels. Int J Food Microbiol. 2017;243:46-51.
9. Olarte RA, Worthington CJ, Horn BW, Moore GG, Singh R, Monacell JT, Dorner JW, Stone EA, Xie D-Y, Carbone I. Enhanced diversity and aflatoxigenicity in interspecific hybrids of Aspergillus flavus and Aspergillus parasiticus. Mol Ecol. 2015;24:1889-909.
10. Frisvad JC, Skouboe P, Samson RA. Taxonomic comparison of three different groups of aflatoxin producers and a new efficient producer of aflatoxin B1, sterigmatocystin and 3-O-methylsterigmatocystin, Aspergillus rambellii sp. nov. Syst Appl Microbiol. 2005;28:442-53.
11. Simão FA, Waterhouse RM, Ioannidis P, Kriventseva EV, Zdobnov EM. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics. 2015;31:3210-2.
12. Linz JE, Wee J, Roze LV. Aspergillus parasiticus SU-1 genome sequence, predicted chromosome structure, and comparative gene expression under aflatoxin-inducing conditions: evidence that differential expression contributes to species phenotype. Eukaryot Cell. 2014;13:1113-23.
13. Machida M, Asai K, Sano M, Tanaka T, Kumagai T, Terai G, Kusumoto K-I, Arima T, Akita O, Kashiwagi Y, Abe K, Gomi K, Horiuchi H, Kitamoto K, Kobayashi T, Takeuchi M, Denning DW, Galagan JE, Nierman WC, Yu J, Archer DB, Bennett JW, Bhatnagar D, Cleveland TE, Fedorova ND, Gotoh O, Horikawa H, Hosoyama A, Ichinomiya M, Igarashi R, et al. Genome sequencing and analysis of Aspergillus oryzae. Nature. 2005;438:1157-61.
14. Payne GA, Nierman WC, Wortman JR, Pritchard BL, Brown D, Dean RA, Bhatnagar D, Cleveland TE, Machida M, Yu J. Whole genome comparison of Aspergillus flavus and A. oryzae. Med Mycol. 2006;44:9-11.
15. Moore GG, Mack BM, Beltz SB. Genomic sequence of the aflatoxigenic filamentous fungus Aspergillus nomius. BMC Genomics. 2015;16:551.
16. Moore GG, Mack BM, Beltz SB, Gilbert MK. Draft genome sequence of an aflatoxigenic Aspergillus species, A. bombycis. Genome Biol Evol. 2016;8:3297-300.
17. Hua ST, Mcalpin CE, Chang P-K, Sarreal SL. Characterization of toxigenic and atoxigenic Aspergillus flavus isolates from pistachio. Mycotoxin Res. 2012;28:67-75.
18. Klich MA. Identification of common aspergillus species. Centraalbureau voor Shimmelcultures: Utrecht; 2002.
19. Li M, Rollins JA. The development-specific protein (Ssp1) from Sclerotinia sclerotiorum is encoded by a novel gene expressed exclusively in sclerotium tissues. Mycologia. 2009;101:34-43.
20. Rollins JA. The Sclerotinia sclerotiorum pac1 gene is required for sclerotial development and virulence. Mol Plant-Microbe Interact. 2003;16:785-95.
21. Jin FJ, Takahashi T, Matsushima K-I, Hara S, Shinohara Y, Maruyama J, Kitamoto K, Koyama Y. SclR, a basic helix-loop-helix transcription factor, regulates hyphal morphology and promotes sclerotial formation in Aspergillus oryzae. Eukaryot Cell. 2011;10:945-55.
22. Chang P-K, Scharfenstein LL, Ehrlich KC, Diana Di Mavungu J. The Aspergillus flavus fluP-associated metabolite promotes sclerotial production. Fungal Biol. 2016;120:1258-68.
23. Chang P-K, Scharfenstein LL, Li RW, Arroyo-Manzanares N, De Saeger S, Di Mavungu JD. Aspergillus flavus aswA, a gene homolog of Aspergillus nidulans oefC, regulates sclerotial development and biosynthesis of sclerotium-associated secondary metabolites. Fungal Genet Biol. 2017;104:29-37.
24. Calvo AM, Bok J, Brooks W, Keller NP. veA is required for toxin and sclerotial production in Aspergillus parasiticus. Appl Environ Microbiol. 2004;70:4733-9.
25. Medema MH, Blin K, Cimermancic P, de Jager V, Zakrzewski P, Michael A, Fischbach MA, Weber T, Takano E, Breitling R. antiSMASH: rapid identification, annotation and analysis of secondary metabolite biosynthesis gene clusters in bacterial and fungal genome sequences. Nucleic Acids Res. 2011;39:W339-46.
26. Khaldi N, Seifuddin FT, Turner G, Haft D, Nierman WC, Wolfe KH, Fedorova ND. SMURF: genomic mapping of fungal secondary metabolite clusters. Fungal Genet Biol. 2010;47:736-41.
27. Chang P-K, Ehrlich KC. Cyclopiazonic acid biosynthesis by Aspergillus flavus. Toxin Rev. 2011;30:79-89.
28. Holzapfel CW. The isolation and structure of cyclopiazonic acid, a toxic metabolite of Penicillium cyclopium Westling. Tetrahedron. 1968;24:2101-19.
29. Chang P-K, Horn BW, Dorner JW. Clustered genes involved in cyclopiazonic acid production are next to the aflatoxin biosynthesis gene cluster in Aspergillus flavus. Fungal Genet Biol. 2009;46:176-82.
30. Chang PK, Abbas HK, Weaver MA, Ehrlich KC, Scharfenstein LL, Cotty PJ. Identification of genetic defects in the atoxigenic biocontrol strain Aspergillus flavus K49 reveals the presence of a competitive recombinant group in field populations. Int J Food Microbiol. 2012;154:192-6.
31. Wollenberg RD, Saei W, Westphal KR, Klitgaard CS, Nielsen KL, Lysøe E, Gardiner DM, Wimmer R, Sondergaard TE, Sørensen JL. Chrysogine biosynthesis is mediated by a two-module nonribosomal peptide synthetase. J Nat Prod. 2017;80:2131-5.
32. Shah AJ, Tilburn J, Adlard MW, Arst Jr HN. pH regulation of penicillin production in Aspergillus nidulans. FEMS Microbiol Lett. 1991;77:209-12.
33. Lopez-Diam TM, Flannigan B. Production of patulin and cytochalasin E by Aspergillus clavatus during malting of barley and wheat. Int J Food Microbiol. 1997;35:129-36.
34. Zargar S. Inhibitory effect of various aqueous medicinal plant extracts on citrinin production a fungal biomass by Penicillium notatum and Aspergillus niger. IAIM. 2014;1:1-8.
35. Wang X, Wang J, Lai D, Wang W, Dai J, Zhou L, Liu Y. Ustiloxin G, a new cyclopeptide mycotoxin from rice false smut balls. Toxins. 2017;9:54.
36. Umemura M, Nagano N, Koike H, Kawano J, Ishii T, Miyamura Y, Kikuchi M, Tamano K, Yu J, Shin-ya K, Machida M. Characterization of the biosynthetic gene cluster for the ribosomally synthesized cyclic peptide ustiloxin B in Aspergillus flavus. Fungal Genet Biol. 2014;68:23-30.
37. Ha GT, Wong RK, Zhang Y. Huperzine a as potential treatment of Alzheimer's disease: an assessment on chemistry, pharmacology, and clinical studies. Chem Biodivers. 2011;8:1189-204.
38. Holm DK, Peterson LM, Klitgaard A, Knudsen PB, Jarczynska ZD, Nielsen KF, Gotfredsen CH, Larsen TO, Mortensen UH. Molecular and chemical characterization of the biosynthesis of the 6-MSA-derived meroterpenoid Yanuthone D in Aspergillus niger. Chem Biol. 2014;21:519-29.
39. Sunderhaus JD, Sherman DH, Williams RM. Studies on the biosynthesis of the stephacidin and notoamide natural products: a stereochemical and genetic conundrum. Israel J Chem. 2011;51:442-52.
40. TePaske MR, Gloer JB, Wicklow DT, Dowd PF. Aflavarin and β-Aflatrem: new anti-insectan metabolites from the sclerotia of Aspergillus flavus. J Nat Prod. 1992;55:1080-6.
41. Cary JW, Han Z, Yin Y, Lohmar JM, Shantappa S, Harris-Coward PY, Mack B, Ehrlich KC, Wei Q, Arroyo-Manzanares N, Uka V, Vanhaecke L, Bhatnagar D, Yu J, Nierman WC, Johns MA, Sorensen D, Shen H, De Saeger S, Diana Di Mavungu J, Calvo AM. Transcriptome analysis of Aspergillus flavus reveals veA-dependent regulation of secondary metabolite gene clusters, including the novel aflavarin cluster. Eukaryot Cell. 2015;14:983-97.
42. Ramirez-Prado JH, Moore GG, Horn BW, Carbone I. Characterization and population analysis of the mating-type genes in Aspergillus flavus and Aspergillus parasiticus. Fungal Genet Biol. 2008;45:1292-9.
43. Tsui CK-M, DiGuistini S, Wang Y, Feau N, Dhillon B, Bohlmann J, Hamelin RC. Unequal recombination and evolution of the mating-type (MAT) loci in the pathogenic fungus Grosmannia clavigera and relatives. G3-Genes Genom Genet. 2013;3:465-80.
44. Metzenberg RL, Glass NL. Mating type and mating strategies in Neurospora. BioEssays. 1990;12:53-9.
45. Chang P-K, Ehrlich KC. What does genetic diversity of Aspergillus flavus tell us about Aspergillus oryzae? Int J Food Microbiol. 2010;138:189-99.
46. Ehrlich KC, Chang P-K, Yu J, Cotty PJ. Aflatoxin biosynthesis cluster gene cypA is required for G aflatoxin formation. Appl Environ Microb. 2004;70:6518-24.
47. Breitenbach M, Weber M, Rinnerthaler M, Karl T, Breitenbach-Koller L. Oxidative stress in fungi: its function in signal transduction, interaction with plant hosts, and lignocellulose degradation. Biomol Ther. 2015;5:318-42.
48. Ichinose H, Wariishi H. Heterologous expression and mechanistic investigation of a fungal cytochrome P450 (CYP5150A2): involvement of alternative redox partners. Arch Biochem Biophys. 2012;518:8-15.
49. Caza M, Kronstad JW. Shared and distinct mechanisms of iron acquisition by bacterial and fungal pathogens of humans. Front Cell Infect Microbiol. 2013;3:80.
50. Horn BW, Gell RM, Singh R, Sorensen RB, Carbone I. Sexual reproduction in Aspergillus flavus sclerotia: acquisition of novel alleles from soil populations and uniparental mitochondrial inheritance. PLoS One. 2016; https://doi.org/10.1371/journal.pone.0146169.
51. Garbelotto M, Gonthier P, Nicolotti G. Ecological constraints limit the fitness of fungal hybrids in the Heterobasidion annosum species complex. Appl Environ Microbiol. 2007;73:6106-11.
52. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin LV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol. 2012;19:455-77.
53. Cantarel BL, Korf I, Robb SMC, Parra G, Ross E, Moore B, Holt C, Sánchez Alvarado A, Yandell M. MAKER: an easy-to-use annotation pipeline designed for emerging model organism genomes. Genome Res. 2008;18:188-96.
54. Lomsadze A, Ter-Hovhannisyan V, Chernoff YO, Borodovsky M. Gene identification in novel eukaryotic genomes by self-training algorithm. Nucleic Acids Res. 2005;33:6494-506.
55. Stanke M, Waack S. Gene prediction with a hidden Markov model and a new intron submodel. Bioinformatics. 2003;19-Suppl 2:215-25.
56. Lechner M, Findeiss S, Steiner L, Marz M, Stadler PF, Prohaska SJ. Proteinortho: detection of (co-) orthologs in large-scale analysis. BMC Bioinformatics. 2011;12:124.
57. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32:1792-7.
58. Castresana J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol. 2000;17:540-52.
59. Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics. 2006;22:2688-90.
60. Young MD, Wakefield MJ, Smyth GK, Oshlack A. Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol. 2010;11:R14.
61. Tarailo-Graovac M, Chen N. Using RepeatMasker to identify repetitive elements in genomic sequences. Curr Protoc Bioinform. 2009;25:4.10.1-4.10.14.
62. Jurka J, Kapitonov VV, Pavlicek A, Klonowski P, Kohany O, Walichiewicz J. Repbase update, a database of eukaryotic repetitive elements. Cytogenet Genome Res. 2005;110:462-7.