Genotypic and Phenotypic Versatility of Aspergillus flavus during Maize Exploitation

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Reverberi, Massimo ^a   Punelli, Marta ^a   Scala, Valeria ^a   Scarpari, Marzia ^a   Uva, Paolo ^b   Mentzen, Wieslawa I ^b   Dolezal, Andrea L ^c   Woloshuk, Charles ^d   Pinzari, Flavia ^e   Fabbri, Anna A ^a   Fanelli, Corrado ^a   Payne, Gary A ^c  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b CENTER FOR ADVANCED STUDIES   (Italy)

^c NORTH CAROLINA STATE UNIVERSITY   (United States)

^d PURDUE UNIVERSITY   (United States)

^e CRA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ALKYL HYDROPEROXIDE REDUCTASE; FUNGAL ENZYME; SUPEROXIDE DISMUTASE; UNCLASSIFIED DRUG;

ADAPTIVE BEHAVIOR; ARTICLE; ASPERGILLUS FLAVUS; FUNGAL METABOLISM; FUNGUS GROWTH; GENE CLUSTER; GENE EXPRESSION; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; GENOTYPE ENVIRONMENT INTERACTION; GENOTYPE PHENOTYPE CORRELATION; MAIZE; METABOLITE; NONHUMAN; OXIDATIVE STRESS; PARASITISM; SAPROTROPH; TROPHIC LEVEL;

AFLATOXINS; ASPERGILLUS FLAVUS; CLUSTER ANALYSIS; ENERGY METABOLISM; GENE EXPRESSION REGULATION, FUNGAL; GENETIC ASSOCIATION STUDIES; GENOTYPE; METABOLOME; MOLECULAR SEQUENCE ANNOTATION; OXIDATIVE STRESS; PHENOTYPE; PROMOTER REGIONS, GENETIC; REPRODUCIBILITY OF RESULTS; SIGNAL TRANSDUCTION; TRANSCRIPTOME; ZEA MAYS;

EID: 84880402128     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0068735     Document Type: Article

References (70)

1. Richard JL, Payne GA (2003) Editors. Mycotoxins: Risks in Plant, Animal, and Human Systems. Task Force Report 139. Council for Agricultural Science and Technology. Ames, Iowa. 199.
2. Diener UL, Cole RJ, Sanders TH, Payne GA, Lee LJ, et al. (1987) Epidemiology of aflatoxin formation by Aspergillus flavus. Ann Rev Phytopathol 25: 249-270.
3. Munkvold GP, (2003) Cultural and genetic approaches to managing mycotoxins in maize. Annu Rev Phytopathol 41: 99-116.
4. Payne GA, Nystrom GJ, Bhatnagar D, Cleveland TE, Woloshuk CP, (1993) Cloning of the af-2 Gene Involved in Aflatoxin Biosynthesis from Aspergillus flavus. Appl Environ Microbiol 59(1): 156-162.
5. Scheidegger KA, Payne GA, (2003) Unlocking the secrets behind secondary metabolism: a review of Aspergillus flavus from pathogenicity to functional genomics. J Toxicol 22: 423-459.
6. Wicklow DT, Horn BW, (1982) Sclerotium production by Aspergillus flavus on corn kernels. Mycologia 74(3): 398-403.
7. Calvo AM, Wilson RA, Bok JW, Keller NP, (2002) Relationship between secondary metabolism and fungal development. Microbiol Mol Biol Rev 66: 447-459.
8. Noverr MC, Huffnagle GB, (2004) Regulation of Candida albicans morphogenesis by fatty acid metabolites. Infect Immun 72(11): 6206-6210.
9. Desmond OJ, Manners JM, Stephens AE, Maclean DJ, Schenk PM, et al. (2008) The Fusarium mycotoxin deoxynivalenol elicits hydrogen peroxide production, programmed cell death and defense responses in wheat. Mol Plant Pathol 9(4): 435-445.
10. Lillehoj EB (1991) Aflatoxin: an ecologically elicited genetic activation signal. In: Smith JE, Henderson RS editors. Mycotoxins and animal foods. CRC Press, Boca Raton, Fla, 2-30.
11. Georgianna DR, Fedorova ND, Burroughs JL, Dolezal AL, Bok JW, et al. (2010) Beyond aflatoxin: four distinct expression patterns and functional roles associated with Aspergillus flavus secondary metabolism gene clusters. Mol Plant Pathol 11(2): 213-226.
12. Bayram O, Krappmann S, Ni M, Bok JW, Helmstaedt K, et al. (2008) VelB/VeA/LaeA complex coordinates light signal with fungal development and secondary metabolism. Science 320: 1504-1506.
13. Chandler D, Crowe LM, Chapman D, (1984) A population based threshold model to demonstrate that physiological manipulation of endogenous reserves can increase the virulence of insect pathogenic fungi. BCPC Crop Sci Technol 4B: 309-314.
14. Nesci A, Etcheverry M, Magan N, (2004) Osmotic and matric potential effects on growth, sugar alcohol and sugar accumulation by Aspergillus section Flavi strains from Argentina. J Appl Microbiol 96: 965-972.
15. Amaike S, Keller NP, (2011) Aspergillus flavus. Ann Rev Phytopathol 49: 107-133.
16. Reese BN, Payne GA, Nielsen DM, Woloshuk CP, (2011) Gene expression profile and response to maize kernels by Aspergillus flavus. Phytopathol 101(7): 797-804.
17. Wang Z, Yan S, Liu C, Chen F, Wang T, (2012) Proteomic analysis reveals an aflatoxin-triggered immune response in cotyledons of Arachis hypogaea infected with Aspergillus flavus. J Proteome 11: 2739-2753.
18. Woloshuk CP, Cavaletto JR, Cleveland TE, (1997) Inducers of aflatoxin biosynthesis from colonized maize kernels are generated by an amylase activity from Aspergillus flavus. Phytopathol 87: 164-169.
19. Cleveland TE, Carter-Wientjes CH, De Lucca AJ, Boué SM, (2009) Effect of soybean volatile compounds on Aspergillus flavus growth and aflatoxin production. J Food Sci. 74(2): H83-87.
20. Hountondji FC, Hanna R, Sabelis MW, (2006) Does methyl salicylate, a component of herbivore-induced plant odor, promote sporulation of the mite-pathogenic fungus Neozygites tanajoae? Exp Appl Acarol 39(1): 63-74.
21. Gao XQ, Kolomiets MV, (2009) Host-derived lipids and oxylipins are crucial signals in modulating mycotoxin production by fungi. Toxic Rev 28: 79-88.
22. Mita G, Fasano P, De Domenico S, Perrone G, Epifani F, et al. (2007) 9-Lipoxygenase metabolism is involved in the almond/Aspergillus carbonarius interaction. J Exp Bot 58(7): 1803-1811.
23. Reverberi M, Ricelli A, Zjalic S, Fabbri AA, Fanelli C, (2010) Natural functions of mycotoxins and control of their biosynthesis in fungi. Appl Microbiol Biotechnol 87: 899-911.
24. Tsitsigiannis DI, Keller NP, (2007) Oxylipins as developmental and host-fungal communication signals. Trends Microbiol 15: 109-118.
25. Burow GB, Nesbitt TC, Dunlap J, Keller NP, (1997) Seed lipoxygenase products modulate Aspergillus mycotoxin biosynthesis. Mol Plant Microbe Interact 10: 380-387.
26. Georgianna DR, Payne GA, (2009) Genetic regulation of aflatoxin biosynthesis: from gene to genome. Fungal Genet Biol 46: 113-125.
27. Fisch KM, Gillaspy AF, Gipson M, Henrikson JC, Hoover AR, et al. (2009) Chemical induction of silent biosynthetic pathway transcription in Aspergillus niger. J Ind Microbiol Biotechnol 36: 1199-1213.
28. Dantigny P, Nanguy SPM, (2009) Review: Significance of the physiological state of fungal spores. Int J Food Microbiol 134: 16-20.
29. Jablonka E, Oborny B, Molnar I, Kisdi E, Hofbauer J, et al. (1995) The adaptive advantage of phenotypic memory in changing environments. Philos T R Soc B 350(1332): 133-141.
30. Yang YH, Xiao Y, Segal M, (2005) Identifying differentially expressed genes from microarray experiments via statistic synthesis. Bioinformatics 21: 1084-1093.
31. Wahl R, Wippel K, Goos S, Kämper J, Sauer N, (2010) A novel high-affinity sucrose transporter is required for virulence of the plant pathogen Ustilago maydis. PLoS Biol 98(2): e1000303.
32. Kulkarni RD, Thon MR, Pan H, Dean RA, (2005) Novel G-protein-coupled receptor-like proteins in the plant pathogenic fungus Magnaporthe grisea. Genome Biol 6(3): R24.
33. Christensen SA, Kolomiets MV, (2011) The lipid language of plant-fungal interactions. Fungal Genet Biol 48(1): 4-14.
34. Affeldt KJ, Brodhagen M, Keller NP, (2012) Aspergillus oxylipin signaling and quorum sensing pathways depend on g protein-coupled receptors. Toxins (Basel) 4(9): 695-717.
35. Jablonka E, Lamb MJ, (1989) The inheritance of acquired epigenetic variations. J Theor Biol 139(1): 69-83.
36. Jablonka E, Lamb MJ (1995) Epigenetic Inheritance and Evolution: The Lamarckian Dimension. Oxford (UK): Oxford University Press. P250.
37. Jablonka E, Raz G, (2009) Epigenetic inheritance: prevalence, mechanisms, and implications for the study of heredity and evolution. Q Rev Biol 84(2): 131-176.
38. Atanasova L, Druzhinina IS, (2010) Global nutrient profiling by Phenotype MicroArrays: a tool complementing genomic and proteomic studies in conidial fungi. J Zhejiang Univ-Sci B (Biomed & Biotechnol) 11(3): 151-168.
39. Reverberi M, Zjalic S, Ricelli A, Punelli F, Camera E, et al. (2008) Modulation of antioxidant defense in Aspergillus parasiticus is involved in aflatoxin biosynthesis: a role for the ApyapA gene. Eukariot Cell 7(6): 988-1000.
40. Roze LV, Chanda A, Wee J, Awad D, Linz JE, (2011) Stress-related transcription factor Atfb integrates secondary metabolism with oxidative stress response in Aspergilli. J Biol Chem 286(40): 35137-35148.
41. Reverberi M, Gazzetti K, Punelli F, Scarpari M, Zjalic S, et al. (2012) Aoyap1 regulates OTA synthesis by controlling cell redox balance in Aspergillus ochraceus. Appl Microbiol Biotechnol. 95(5): 1293-304.
42. Fanelli C, Fabbri AA, Pieretti S, Finotti E, Passi S, (1985) Effect of different antioxidants and free radical scavengers on aflatoxin production. Mycol Res 1: 65-69.
43. Hong SY, Roze LV, Linz JE, (2013) Oxidative stress-related transcription factors in the regulation of secondary metabolism. Toxins (Basel) 5(4): 683-702.
44. Hong SY, Roze LV, Wee J, Linz JE, (2013) Evidence that a transcription factor regulatory network coordinates oxidative stress response and secondary metabolism in aspergilli. Microbiology open. 2(1): 144-160.
45. Jingtao S, Folk D, Bradley TJ, Tower J, (2002) Induced overexpression of mitochondrial Mn-superoxide dismutase extends the life span of adult Drosophila melanogaster. Genetics 161(2): 661-672.
46. Gardner PR, Fridovich I, (1991) Superoxide sensitivity of the Escherichia coli aconitase. J Biol Chem 266(29): 19328-19333.
47. Bernardi P, (1999) Mitochondrial transport of cations: channels, exchangers and permeability transition. Physiol. Rev.79 (4):: 1127-55.
48. Horiguchi H, Yurimoto H, Kato N, Sakai Y, (2001) Antioxidant system within yeast peroxisome: Biochemical and physiological characterization of cbpmp20 in the methylotrophic yeast Candida boidinii. J Biol Chem 276(17): 14279-14288.
49. Lee J, Spector D, Godon C, Labarre J, Toledano MB, (1998) A new antioxidant with alkyl hydroperoxide defense properties in yeast. J Biol Chem 274: 4537-4544.
50. 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(9): 736-741.
51. Marui J, Yamane N, Ohashi-Kunihiro S, Ando T, Terabayashi Y, et al. (2011) Kojic acid biosynthesis in Aspergillus oryzae is regulated by a Zn(II)(2)Cys(6) transcriptional activator and induced by kojic acid at the transcriptional level. Biosci Bioeng. 112(1): 40-43.
52. Forseth RR, Amaike S, Schwenk D, Affeldt KJ, Hoffmeister D, et al. (2013) Homologous NRPS-like gene clusters mediate redundant small-molecule biosynthesis in Aspergillus flavus. Angew Chem Int Ed Engl. 52(5): 1590-1594.
53. Gijzen M, Nürnberger T, (2006) "Nep1-like proteins from plant pathogens: Recruitment and diversification of the NPP1 domain across taxa. Phytochem. 67: 1800-1807.
54. Denning DW, (1998) Invasive Aspergillosis. Clin Infect Dis 26: 781-805.
55. Santhanam P, van Esse HP, Albert I, Faino L, Nürnberger T, et al. (2013) Evidence for Functional Diversification Within a Fungal NEP1-Like Protein Family. MPMI 26(3): 278-286.
56. Reverberi M, Fabbri AA, Fanelli C (2012) Oxidative stress and oxylipins in plant-fungus interaction. In: Witzany, Guenther editors. Biocommunication of Fungi. Springer ISBN 978-94-007-4263-5.
57. Reverberi M, Zjalic S, Punelli F, Ricelli A, Fabbri AA, et al. (2007) Apyap1 affects aflatoxin biosynthesis during Aspergillus parasiticus growth in maize seeds. Food Addit Contam 24(10): 1070-1075.
58. Mittler R, Vanderauwera S, Gollery M, Van Breusegem F, (2004) The reactive oxygen gene network of plants; Trends Plant Sci. 9: 490-498.
59. Torres MA, (2010) ROS in biotic interactions. Physiol Plantarum 138: 414-429.
60. He Z-M, Price MS, O'Brian GR, Georgianna DR, Payne GA, (2007) Improved protocols for functional analysis in the pathogenic fungus Aspergillus flavus. BMC Microbiol 7: 104-116.
61. Färber P, Geisen R, Holzapfel WH, (1997) Detection of aflatoxinogenic fungi in figs by a PCR reaction. Int J Food Microbiol 36(2-3): 215-20.
62. Irizarry RA, Bolstad BM, Collin F, Cope LM, Hobbs B, et al. (2003) Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res 31(4): e15.
63. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, et al. (2003) Exploration, Normalization, and Summaries of High Density Oligonucleotide Array Probe Level Data. Biostatistics 4(2): 249-264.
64. R Development Core Team. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria, 2011.
65. Levine DM, Haynor DR, Castle JC, Stepaniants SB, Pellegrini M, et al. (2006) Pathway and gene-set activation measurement from mRNA expression data: the tissue distribution of human pathways. Genome Biol 7(10): R93.
66. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, et al. (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 25(1): 25-29.
67. Mulder NJ, Apweiler R, Attwood TK, Bairoch A, Bateman A, et al. (2007) New developments in the InterPro database. Nucleic Acids Res Database issue 35: D224-228.
68. Zhan S, Horrocks J, Lukens LN, (2006) Islands of co-expressed neighbouring genes in Arabidopsis thaliana suggest higher-order chromosome domains. Plant J 45: 347-357.
69. Thomas-Chollier M, Defrance M, Medina-Rivera A, Sand O, Herrmann C, et al. (2011) RSAT 2011: regulatory sequence analysis tools. Nucleic Acids Res Web Server issue 39: W86-91.
70. Legendre P, Legendre L (1998) Numerical Ecology. Second English Edition. Elsevier, Amsterdam, 406 p.