Characterization of natural antisense transcript, sclerotia development and secondary metabolism by strand-specific RNA sequencing of Aspergillus flavus

PLoS ONE

Volumn 9, Issue 5, 2014, Pages

  Wu, Xinliang ^a   Zhou, Bin ^a   Yin, Chao ^a   Guo, Yong ^a   Lin, Ying ^a   Pan, Li ^a   Wang, Bin ^a  

^a SOUTH CHINA UNIVERSITY OF TECHNOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

SODIUM; TRANSCRIPTOME; COMPLEMENTARY RNA; FUNGAL PROTEIN; MESSENGER RNA;

ALTERNATIVE RNA SPLICING; ARTICLE; ASPERGILLUS FLAVUS; BIOSYNTHESIS; CONTROLLED STUDY; FUNGAL DEVELOPMENT; FUNGAL STRAIN; FUNGAL STRUCTURES; FUNGUS IDENTIFICATION; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE IDENTIFICATION; GENETIC TRANSCRIPTION; GENOME ANALYSIS; MOLECULAR DYNAMICS; MYCELIUM; NONHUMAN; QUANTITATIVE ANALYSIS; RNA SEQUENCE; SCLEROTIUM (ASCOMYCOTA); SECONDARY METABOLISM; SEQUENCE ANALYSIS; VIRUS GENOME; AGRICULTURE; AMINO ACID SEQUENCE; CHEMICAL STRUCTURE; CHEMISTRY; GENE EXPRESSION PROFILING; GENETICS; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY; PROTEIN CONFORMATION; REPRODUCTION;

AGRICULTURE; AMINO ACID SEQUENCE; ASPERGILLUS FLAVUS; FUNGAL PROTEINS; GENE EXPRESSION PROFILING; MODELS, MOLECULAR; MOLECULAR SEQUENCE ANNOTATION; MOLECULAR SEQUENCE DATA; MYCELIUM; PROTEIN CONFORMATION; REPRODUCTION; RNA, ANTISENSE; RNA, MESSENGER; SEQUENCE ANALYSIS, RNA;

EID: 84901370151     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0097814     Document Type: Article

References (81)

1. Yu J, Cleveland TE, Wilkinson JR, Campbell BC, Kim JH, et al. (2006) Aspergillus flavus expressed sequence tags and microarray as tools in understanding aflatoxin biosynthesis. Mycotoxin Res 22: 16-21.
2. Yu J, Whitelaw CA, Nierman WC, Bhatnagar D, Cleveland TE (2004) Aspergillus flavus expressed sequence tags for identification of genes with putative roles in aflatoxin contamination of crops. FEMS Microbiol Lett 237: 333-340. (Pubitemid 39091969)
3. Chang PK, Wilkinson JR, Horn BW, Yu J, Bhatnagar D, et al. (2007) Genes differentially expressed by Aspergillus flavus strains after loss of aflatoxin production by serial transfers. Appl Microbiol Biotechnol 77: 917-925. (Pubitemid 350159871)
4. Yu J, Fedorova ND, Montalbano BG, Bhatnagar D, Cleveland TE, et al. (2011) Tight control of mycotoxin biosynthesis gene expression in Aspergillus flavus by temperature as revealed by RNA-Seq. FEMS Microbiol Lett 322: 145-149.
5. Wilkinson JR, Yu J, Bland JM, Nierman WC, Bhatnagar D, et al. (2007) Amino acid supplementation reveals differential regulation of aflatoxin biosynthesis in Aspergillus flavus NRRL 3357 and Aspergillus parasiticus SRRC 143. Appl Microbiol Biotechnol 74: 1308-1319. (Pubitemid 46674063)
6. Chang PK, Bennett JW, Cotty PJ (2002) Association of aflatoxin biosynthesis and sclerotial development in Aspergillus parasiticus. Mycopathologia 153: 41-48. (Pubitemid 34209393)
7. Cotty PJ (1988) Aflatoxin and sclerotical production by Aspergillus flavus: influence of pH. Phytopathology 78: 1250-1253.
8. Geiser DM, Timberlake WE, Arnold ML (1996) Loss of meiosis in Aspergillus. Mol Biol Evol 13: 809-817. (Pubitemid 26240085)
9. Khaldi N, Seifuddin FT, Turner G, Haft D, Nierman WC, et al. (2010) SMURF: Genomic mapping of fungal secondary metabolite clusters. Fungal Genet Biol 47: 736-741.
10. Payne GA, Nierman WC, Wortman JR, Pritchard BL, Brown D, et al. (2006) Whole genome comparison of Aspergillus flavus and A. oryzae. Med Mycol 44: 9-11. (Pubitemid 44524078)
11. Horn BW, Dorner JW (1999) Regional differences in production of aflatoxin B1 and cyclopiazonic acid by soil isolates of Aspergillus flavus along a transect within the United States. Appl Environ Microbiol 65: 1444-1449. (Pubitemid 29173668)
12. Cotty P (1989) Virulence and cultural characteristics of two Aspergillus flavus strains pathogenic on cotton. Phytopathology 79: 808-814.
13. Bayman P, Cotty PJ (1993) Genetic diversity in Aspergillus flavus: association with aflatoxin production and morphology. Can J Bot 71: 23-31.
14. Bennett J, Fernholz F, Lee L (1978) Effect of light on aflatoxins, anthraquinones, and sclerotia in Aspergillus flavus and A. parasiticus. Mycologia 70: 104-116.
15. Littley E, Rahe J (1992) Sclerotial morphogenesis in Sclerotium cepivorum in vitro. Can J Bot 70: 772-778.
16. Willetts H, Bullock S (1992) Developmental biology of sclerotia. Mycol Res 96: 801-816.
17. Rollins JA, Dickman MB (1998) Increase in endogenous and exogenous cyclic AMP levels inhibits sclerotial development in Sclerotinia sclerotiorum. Appl Environ Microbiol 64: 2539-2544. (Pubitemid 28303297)
18. Georgiou CD, Patsoukis N, Papapostolou I, Zervoudakis G (2006) Sclerotial metamorphosis in filamentous fungi is induced by oxidative stress. Integr Comp Biol 46: 691-712. (Pubitemid 44736411)
19. Chang P-K, Hua S (2007) Molasses supplementation promotes conidiation but suppresses aflatoxin production by small sclerotial Aspergillus flavus. Lett Appl Microbiol 44: 131-137. (Pubitemid 46146581)
20. Calvo AM, Bok J, Brooks W, Keller NP (2004) veA is required for toxin and sclerotial production in Aspergillus parasiticus. Appl Environ Microbiol 70: 4733-4739. (Pubitemid 39095499)
21. Amaike S, Keller NP (2009) Distinct roles for VeA and LaeA in development and pathogenesis of Aspergillus flavus. Eukaryot Cell 8: 1051-1060.
22. Cary J, OBrian G, Nielsen D, Nierman W, Harris-Coward P, et al. (2007) Elucidation of veA-dependent genes associated with aflatoxin and sclerotial production in Aspergillus flavus by functional genomics. Appl Microbiol Biotechnol 76: 1107-1118.
23. Katayama S, Tomaru Y, Kasukawa T, Waki K, Nakanishi M, et al. (2005) Antisense transcription in the mammalian transcriptome. Science 309: 1564-1566.
24. Zhoug S, Wen SM, Zhang DF, Wang QL, Wang SQ, et al. (1998) Sequencing of PCR amplified HBV DNA pre-c and c regions in the 2.2.15 cells and antiviral action by targeted antisense oligonucleotide directed against sequence. World J Gastroenterol 4: 434-436. (Pubitemid 128620208)
25. Smith CA, Robertson D, Yates B, Nielsen DM, Brown D, et al. (2008) The effect of temperature on Natural Antisense Transcript (NAT) expression in Aspergillus flavus. Curr Genet 54: 241-269.
26. Faghihi MA, Wahlestedt C (2009) Regulatory roles of natural antisense transcripts. Nat Rev Mol Cell Biol 10: 637-643.
27. Ambros V (2004) The functions of animal microRNAs. Nature 431: 350-355.
28. Donaldson ME, Saville BJ (2012) Natural antisense transcripts in fungi. Mol Microbiol 85: 405-417.
29. Matzke MA, Birchler JA (2005) RNAi-mediated pathways in the nucleus. Nat Rev Genet 6: 24-35. (Pubitemid 39657895)
30. Kawasaki H, Taira K (2004) Induction of DNA methylation and gene silencing by short interfering RNAs in human cells. Nature 431: 211-217. (Pubitemid 39243476)
31. Morris KV, Chan SW, Jacobsen SE, Looney DJ (2004) Small interfering RNA-induced transcriptional gene silencing in human cells. Science 305: 1289-1292. (Pubitemid 39129233)
32. Fukagawa T, Nogami M, Yoshikawa M, Ikeno M, Okazaki T, et al. (2004) Dicer is essential for formation of the heterochromatin structure in vertebrate cells. Nat Cell Biol 6: 784-791. (Pubitemid 39144485)
33. Imamura T, Yamamoto S, Ohgane J, Hattori N, Tanaka S, et al. (2004) Non-coding RNA directed DNA demethylation of Sphk1 CpG island. Biochem Biophys Res Commun 322: 593-600. (Pubitemid 39490344)
34. Murrell A, Heeson S, Reik W (2004) Interaction between differentially methylated regions partitions the imprinted genes Igf2 and H19 into parent-specific chromatin loops. Nat Genet 36: 889-893. (Pubitemid 39014109)
35. Andersen AA, Panning B (2003) Epigenetic gene regulation by noncoding RNAs. Curr Opin Cell Biol 15: 281-289. (Pubitemid 36638645)
36. Misra S, Crosby MA, Mungall CJ, Matthews BB, Campbell KS, et al. (2002) Annotation of the Drosophila melanogaster euchromatic genome: a systematic review. Genome Biol 3: RESEARCH0083.
37. Chen N, Stein LD (2006) Conservation and functional significance of gene topology in the genome of Caenorhabditis elegans. Genome Res 16: 606-617.
38. Osato N, Yamada H, Satoh K, Ooka H, Yamamoto M, et al. (2003) Antisense transcripts with rice full-length cDNAs. Genome Biol 5: R5.
39. Wang XJ, Gaasterland T, Chua NH (2005) Genome-wide prediction and identification of cis-natural antisense transcripts in Arabidopsis thaliana. Genome Biol 6: R30.
40. Chen J, Sun M, Kent WJ, Huang X, Xie H, et al. (2004) Over 20% of human transcripts might form sense-antisense pairs. Nucleic Acids Res 32: 4812-4820. (Pubitemid 39429685)
41. Carninci P, Kasukawa T, Katayama S, Gough J, Frith MC, et al. (2005) The transcriptional landscape of the mammalian genome. Science 309: 1559-1563.
42. Yu J, Nierman WC, Fedorova ND, Bhatnagar D, Cleveland TE, et al. (2011) What can the Aspergillus flavus genome offer to mycotoxin research. Mycology 2 218-236.
43. Wang B, Guo G, Wang C, Lin Y, Wang X, et al. (2010) Survey of the transcriptome of Aspergillus oryzae via massively parallel mRNA sequencing. Nucleic Acids Res 38: 5075-5087.
44. Zhong S, Joung JG, Zheng Y, Chen YR, Liu B, et al. (2011) High-throughput illumina strand-specific RNA sequencing library preparation. Cold Spring Harb Protoc 2011: 940-949.
45. Mamanova L, Turner DJ (2011) Low-bias, strand-specific transcriptome Illumina sequencing by on-flowcell reverse transcription (FRT-seq). Nat Protoc 6: 1736-1747.
46. Yassour M, Pfiffner J, Levin JZ, Adiconis X, Gnirke A, et al. (2010) Strand-specific RNA sequencing reveals extensive regulated long antisense transcripts that are conserved across yeast species. Genome Biol 11: R87.
47. Vivancos AP, Guell M, Dohm JC, Serrano L, Himmelbauer H (2010) Strand-specific deep sequencing of the transcriptome. Genome Res 20: 989-999.
48. Wang L, Si Y, Dedow LK, Shao Y, Liu P, et al. (2011) A low-cost library construction protocol and data analysis pipeline for Illumina-based strand-specific multiplex RNA-seq. PLoS One 6: e26426.
49. Parkhomchuk D, Borodina T, Amstislavskiy V, Banaru M, Hallen L, et al. (2009) Transcriptome analysis by strand-specific sequencing of complementary DNA. Nucleic Acids Res 37: e123.
50. Li R, Yu C, Li Y, Lam TW, Yiu SM, et al. (2009) SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 25: 1966-1967.
51. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5: 621-628. (Pubitemid 351911867)
52. Dillies MA, Rau A, Aubert J, Hennequet-Antier C, Jeanmougin M, et al. (2012) A comprehensive evaluation of normalization methods for Illumina high-throughput RNA sequencing data analysis. Brief Bioinform. doi: 10.1093/bib/bbs046.
53. Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, et al. (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21: 3674-3676. (Pubitemid 41264107)
54. Ye J, Fang L, Zheng H, Zhang Y, Chen J, et al. (2006) WEGO: a web tool for plotting GO annotations. Nucleic Acids Res 34: W293-297. (Pubitemid 44529781)
55. Kent WJ (2002) BLAT - the BLAST-like alignment tool. Genome Res 12: 656-664.
56. Yavatkar AS, Lin Y, Ross J, Fann Y, Brody T, et al. (2008) Rapid detection and curation of conserved DNA via enhanced-BLAT and EvoPrinterHD analysis. BMC Genomics 9: 106.
57. Trapnell C, Pachter L, Salzberg SL (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25: 1105-1111.
58. Wang ET, Sandberg R, Luo S, Khrebtukova I, Zhang L, et al. (2008) Alternative isoform regulation in human tissue transcriptomes. Nature 456: 470-476. (Pubitemid 352759009)
59. Wang L, Feng Z, Wang X, Zhang X (2010) DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 26: 136-138.
60. Arentshorst M, Ram AF, Meyer V (2012) Using non-homologous end-joining-deficient strains for functional gene analyses in filamentous fungi. Methods Mol Biol 835: 133-150.
61. Machida M, Yamada O, Gomi K (2008) Genomics of Aspergillus oryzae: learning from the history of Koji mold and exploration of its future. DNA Res 15: 173-183.
62. Mignone F, Gissi C, Liuni S, Pesole G (2002) Untranslated regions of mRNAs. Genome Biol 3: REVIEWS0004.
63. Wilhelm BT, Marguerat S, Watt S, Schubert F, Wood V, et al. (2008) Dynamic repertoire of a eukaryotic transcriptome surveyed at single-nucleotide resolution. Nature 453: 1239-1243. (Pubitemid 351913597)
64. Lackner DH, Beilharz TH, Marguerat S, Mata J, Watt S, et al. (2007) A network of multiple regulatory layers shapes gene expression in fission yeast. Mol Cell 26: 145-155. (Pubitemid 46550937)
65. Ruiz-Echevarria MJ, Peltz SW (2000) The RNA binding protein Pub1 modulates the stability of transcripts containing upstream open reading frames. Cell 101: 741-751.
66. Vilela C, McCarthy JE (2003) Regulation of fungal gene expression via short open reading frames in the mRNA 5′ untranslated region. Mol Microbiol 49: 859-867. (Pubitemid 36981334)
67. Nagalakshmi U, Wang Z, Waern K, Shou C, Raha D, et al. (2008) The transcriptional landscape of the yeast genome defined by RNA sequencing. Science 320: 1344-1349. (Pubitemid 351929471)
68. Liang S, Wang B, Pan L, Ye Y, He M, et al. (2012) Comprehensive structural annotation of Pichia pastoris transcriptome and the response to various carbon sources using deep paired-end RNA sequencing. BMC Genomics 13: 738.
69. McGuire AM, Pearson MD, Neafsey DE, Galagan JE (2008) Cross-kingdom patterns of alternative splicing and splice recognition. Genome Biol 9: R50.
70. Arnold K, Bordoli L, Kopp J, Schwede T (2006) The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22: 195-201. (Pubitemid 43205406)
71. Schwede T, Kopp J, Guex N, Peitsch MC (2003) SWISS-MODEL: An automated protein homology-modeling server. Nucleic Acids Res 31: 3381-3385. (Pubitemid 37442164)
72. Sibthorp C, Wu H, Cowley G, Wong PW, Palaima P, et al. (2013) Transcriptome analysis of the filamentous fungus Aspergillus nidulans directed to the global identification of promoters. BMC Genomics 14: 847.
73. Neil H, Malabat C, d'Aubenton-Carafa Y, Xu Z, Steinmetz LM, et al. (2009) Widespread bidirectional promoters are the major source of cryptic transcripts in yeast. Nature 457: 1038-1042.
74. Pel HJ, de Winde JH, Archer DB, Dyer PS, Hofmann G, et al. (2007) Genome sequencing and analysis of the versatile cell factory Aspergillus niger CBS 513.88. Nat Biotechnol 25: 221-231. (Pubitemid 46227122)
75. Galagan JE, Calvo SE, Cuomo C, Ma LJ, Wortman JR, et al. (2005) Sequencing of Aspergillus nidulans and comparative analysis with A. fumigatus and A. oryzae. Nature 438: 1105-1115. (Pubitemid 41831674)
76. Jorgensen TR, Nielsen KF, Arentshorst M, Park J, van den Hondel CA, et al. (2011) Submerged conidiation and product formation by Aspergillus niger at low specific growth rates are affected in aerial developmental mutants. Appl Environ Microbiol 77: 5270-5277.
77. Yamada O, Lee BR, Gomi K, Iimura Y (1999) Cloning and functional analysis of the Aspergillus oryzae conidiation regulator gene brlA by its disruption and misscheduled expression. J Biosci Bioeng 87: 424-429. (Pubitemid 29239002)
78. Wieser J, Adams TH (1995) flbD encodes a Myb-like DNA-binding protein that coordinates initiation of Aspergillus nidulans conidiophore development. Genes Dev 9: 491-502.
79. Yu J, Cleveland TE, Nierman WC, Bennett JW (2005) Aspergillus flavus genomics: gateway to human and animal health, food safety, and crop resistance to diseases. Rev Iberoam Micol 22: 194-202. (Pubitemid 43241079)
80. Calvo AM (2008) The VeA regulatory system and its role in morphological and chemical development in fungi. Fungal Genet Biol 45: 1053-1061.
81. Georgianna DR, Payne GA (2009) Genetic regulation of aflatoxin biosynthesis: from gene to genome. Fungal Genet Biol 46: 113-125.