Skip to main content
Log in

Aflatoxigenicity in Aspergillus: molecular genetics, phylogenetic relationships and evolutionary implications

  • Published:
Mycopathologia Aims and scope Submit manuscript

Abstract

Aflatoxins (AFs) are toxic and carcinogenic secondary metabolites produced by isolates of Aspergillus section Flavi as well as a number of Aspergillus isolates that are classified outside of section Flavi. Characterization of the AF and sterigmatocystin (ST) gene clusters and analysis of factors governing regulation of their biosynthesis has resulted in these two mycotoxins being the most extensively studied of fungal secondary metabolites. This wealth of information has allowed the determination of the molecular basis for non-production of AF in natural isolates of A. flavus and domesticated strains of A. oryzae. This review provides an overview of the molecular analysis of the AF and ST gene clusters as well as new information on an AF gene cluster identified in the non-section Flavi isolate, Aspergillus ochraceoroseus. Additionally, molecular phylogenetic analysis using AF biosynthetic gene sequences as well as ribosomal DNA internal transcribed spacer (ITS) sequences between various section Flavi and non-section Flavi species has enabled determination of the probable evolutionary history of the AF and ST gene clusters. A model for the evolution of the AF and ST gene clusters as well as possible biological roles for AF are discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. MA Klich JW Cary SB Beltz CA Bennett (2003) ArticleTitlePhylogenetic and morphological analysis of Aspergillus ochraceoroseus Mycologia 95 1252–1260 Occurrence Handle1:CAS:528:DC%2BD2cXitVCqsrw%3D

    CAS  Google Scholar 

  2. JC Frisvad RA Samson (2004) ArticleTitle Emericella venezuelensis, a new species with stellate ascospores producing sterigmatocystin and aflatoxin B1 Syst Appl Microbiol 27 672–680 Occurrence Handle15612624 Occurrence Handle1:CAS:528:DC%2BD2MXhtF2mtrc%3D Occurrence Handle10.1078/0723202042369910

    Article  PubMed  CAS  Google Scholar 

  3. JC Frisvad RA Samson J Smedsgaard (2004) ArticleTitle Emericella astellata, a new producer of aflatoxin B, B and sterigmatocystin Lett Appl Microbiol 38 440–445 Occurrence Handle15059218 Occurrence Handle1:CAS:528:DC%2BD2cXks1GrsLk%3D Occurrence Handle10.1111/j.1472-765X.2004.01520.x

    Article  PubMed  CAS  Google Scholar 

  4. JW Cary MA Klich SB Beltz (2005) ArticleTitleCharacterization of aflatoxin-producing fungi outside of Aspergillus section Flavi Mycologia 97 425–432 Occurrence Handle16396350 Occurrence Handle1:CAS:528:DC%2BD2MXmvF2ltr0%3D Occurrence Handle10.3852/mycologia.97.2.425

    Article  PubMed  CAS  Google Scholar 

  5. A Bartoli O Maggi (1978) ArticleTitleFour new species of Aspergillus from Ivory Coast soil Trans Br Mycol Soc 71 383–394 Occurrence Handle10.1016/S0007-1536(78)80064-3

    Article  Google Scholar 

  6. PJ Cotty DS Bayman DS Egel KS Elias (1994) Agriculture, aflatoxins and Aspergillus K Powell (Eds) The Genus Aspergillus Plenum Press New York 1–27

    Google Scholar 

  7. DM Geiser JW Dorner BW Horn JW Taylor (2000) ArticleTitleThe phylogenetics of mycotoxin and sclerotium production in Aspergillus flavus and Aspergillus oryzae Fungal Genet Biol 31 169–179 Occurrence Handle11273679 Occurrence Handle1:CAS:528:DC%2BD3MXitFylt78%3D Occurrence Handle10.1006/fgbi.2000.1215

    Article  PubMed  CAS  Google Scholar 

  8. PJ Cotty (1989) ArticleTitleVirulence and cultural characteristics of two Aspergillus flavus strains pathogenic on cotton Phytopathology 79 808–814

    Google Scholar 

  9. P Broek Particlevan den A Pittet H Hajjaj (2001) ArticleTitleAflatoxin genes and the aflatoxigenic potential of Koji moulds Appl Microbiol Biotechnol 57 192–199 Occurrence Handle11693919 Occurrence Handle10.1007/s002530100736

    Article  PubMed  Google Scholar 

  10. CP Kurtzman BW Horn CW Hesseltine (1987) ArticleTitle Aspergillus nomius, a new aflatoxin-producing species related to Aspergillus flavus and Aspergillus tamarii Antonie Leeuwenhoek 53 147–158 Occurrence Handle3116923 Occurrence Handle1:STN:280:DyaL1c%2Fit1Knsw%3D%3D Occurrence Handle10.1007/BF00393843

    Article  PubMed  CAS  Google Scholar 

  11. T Goto DT Wicklow Y Ito (1996) ArticleTitleAflatoxin and cyclopiazonic acid production by a sclerotium-producing Aspergillus tamarii strain Appl Environ Microbiol 62 4036–4038 Occurrence Handle8899995 Occurrence Handle1:CAS:528:DyaK28Xms1Kiur8%3D

    PubMed  CAS  Google Scholar 

  12. PF Dowd (1998) Involvement of arthropods in the establishment of Mycotoxigenic fungi under field conditions KK Sinha D Bhatnagar (Eds) Mycotoxins in Agriculture and Food Safety Marcel Dekker New York 307–350

    Google Scholar 

  13. ML Boyd PJ Cotty (1997) ArticleTitle Aspergillus flavus and aflatoxin contamination of leguminous trees of the Sonoran Desert in Arizona Phytopathol 79 808–814

    Google Scholar 

  14. Bhatnagar D, Ehrlich KC, Chang P-K. Mycotoxins. In: Encyclopedia of Life Sciences, Vol. 12 London: Nature Publishing Company, 2000: 564–573

  15. EB Lillehoj (1991) Aflatoxin: an ecologically elicited genetic/activation signal JE Smith RS Henderson (Eds) Mycotoxins and Animal Foods CRC Press Boca Raton, FL 2–30

    Google Scholar 

  16. A Pringle J Taylor (2002) ArticleTitleThe fitness of filamentous fungi Trends Microbiol 10 474–481 Occurrence Handle12377558 Occurrence Handle1:CAS:528:DC%2BD38XnsF2ktLk%3D Occurrence Handle10.1016/S0966-842X(02)02447-2

    Article  PubMed  CAS  Google Scholar 

  17. H Wilkinson A Ramaswamy SC Sim NP Keller (2004) ArticleTitleIncreased conidiation associated with progression along the sterigmatocystin biosynthetic pathway Mycologia 96 1190–1198 Occurrence Handle1:CAS:528:DC%2BD2MXhsV2ltLc%3D

    CAS  Google Scholar 

  18. RH Proctor DW Brown RD Plattner AE Desjardins (2003) ArticleTitleCo-expression of 15 contiguous genes delineates a fumonisin biosynthetic gene cluster in Gibberella moniliformis Fungal Genet Biol 38 237–249 Occurrence Handle12620260 Occurrence Handle1:CAS:528:DC%2BD3sXhs1CgsL4%3D Occurrence Handle10.1016/S1087-1845(02)00525-X

    Article  PubMed  CAS  Google Scholar 

  19. J Yu P-K Chang KC Ehrlich JW Cary D Bhatnagar TE Cleveland GA Payne JE Linz CP Woloshuk JW Bennett (2004) ArticleTitleClustered pathway genes in aflatoxin biosynthesis Appl Environ Microbiol 70 1253–1262 Occurrence Handle15006741 Occurrence Handle1:CAS:528:DC%2BD2cXisVKjtLg%3D Occurrence Handle10.1128/AEM.70.3.1253-1262.2004

    Article  PubMed  CAS  Google Scholar 

  20. KC Ehrlich J Yu PJ Cotty (2005) ArticleTitleAflatoxin biosynthesis gene clusters and flanking regions J Appl Microbiol 99 518–527 Occurrence Handle16108793 Occurrence Handle1:CAS:528:DC%2BD2MXhtVyht7%2FF Occurrence Handle10.1111/j.1365-2672.2005.02637.x

    Article  PubMed  CAS  Google Scholar 

  21. J Yu P Chang D Bhatnagar TE Cleveland (2000) ArticleTitleCloning of a sugar utilization gene cluster in Aspergillus parasiticus Biochim Biophys Acta 1493 211–214 Occurrence Handle10978525 Occurrence Handle1:CAS:528:DC%2BD3cXmt1Snsb4%3D

    PubMed  CAS  Google Scholar 

  22. P Bucher (1990) ArticleTitleWeight matrix descriptions of four eukaryotic RNA polymerase II promoter elements derived from 502 unrelated promoters J Mol Biol 212 563–578 Occurrence Handle2329577 Occurrence Handle1:CAS:528:DyaK3cXktFyrsr8%3D Occurrence Handle10.1016/0022-2836(90)90223-9

    Article  PubMed  CAS  Google Scholar 

  23. FM Narendja MA Davis MJ Hynes M Kato A Aoyama F Naruse T Kobayashi N Tsukagoshi R Heeswijck Particlevan D Gomez I Garcia C Scazzocchio B Cubero R Kucharski E Bartnik (1999) ArticleTitleAnCF, the CCAAT binding complex of Aspergillus nidulans, is essential for the formation of a DNase I-hypersensitive site in the 5′ region of the amdS gene Mol Cell Biol 19 6523–6531 Occurrence Handle10490592 Occurrence Handle1:CAS:528:DyaK1MXmtlamtbo%3D

    PubMed  CAS  Google Scholar 

  24. S Steidl MJ Hynes AA Brakhage (2001) ArticleTitleThe Aspergillus nidulans multimeric CCAAT binding complex AnCF is negatively autoregulated via its hapB subunit gene J Mol Biol 306 643–653 Occurrence Handle11243777 Occurrence Handle1:CAS:528:DC%2BD3MXhslSnsr4%3D Occurrence Handle10.1006/jmbi.2001.4412

    Article  PubMed  CAS  Google Scholar 

  25. J Tilburn S Sarkar DA Widdick EA Espeso M Orejas J Mungroo MA Penalva HN Arst SuffixJr (1995) ArticleTitleThe Aspergillus PacC zinc finger transcription factor mediates regulation of both acid- and alkaline expressed genes by ambient pH EMBO J 14 779–790 Occurrence Handle7882981 Occurrence Handle1:CAS:528:DyaK2MXktF2msL4%3D

    PubMed  CAS  Google Scholar 

  26. K Then Bergh AA Brakhage (1998) ArticleTitleRegulation of the Aspergillus nidulans penicillin biosynthesis gene acvA (pcbAB) by amino acids: implication for involvement of the transcription factor PACC Appl Environ Microbiol 64 843–849 Occurrence Handle9501424 Occurrence Handle1:STN:280:DyaK1c7mt1Sntw%3D%3D

    PubMed  CAS  Google Scholar 

  27. A Andrianopoulos WE Timberlake (1994) ArticleTitleThe Aspergillus nidulans abaA gene encodes a transcriptional activator that acts as a genetic switch to control development Mol Cell Biol 14 2503–2515 Occurrence Handle8139553 Occurrence Handle1:CAS:528:DyaK2cXktVagur0%3D

    PubMed  CAS  Google Scholar 

  28. S Han J Navarro RA Greve TH Adams (1993) ArticleTitleTranslational repression of brlA expression prevents premature development in Aspergillus Embo J 12 2449–2457 Occurrence Handle8508770 Occurrence Handle1:CAS:528:DyaK3sXks1Gku7s%3D

    PubMed  CAS  Google Scholar 

  29. MI Muro-Pasteur R Gonzalez J Strauss F Narendja C Scazzocchio (1999) ArticleTitleThe GATA factor AreA is essential for chromatin remodelling in a eukaryotic bidirectional promoter EMBO J 18 1584–1597 Occurrence Handle10.1093/emboj/18.6.1584

    Article  Google Scholar 

  30. ML Berbee JW Taylor (2001) Fungal molecular evolution: gene trees and geologic time DJ McLaughlin E McLaughlin PA Lemke (Eds) The Mycota Springer Berlin 229–246

    Google Scholar 

  31. DS Heckman DM Geiser BR Eidell RL Stauffer NL Kardos SB Hedges (2001) ArticleTitleMolecular evidence for the early colonization of land by fungi and plants Science 293 1129–1133 Occurrence Handle11498589 Occurrence Handle1:CAS:528:DC%2BD3MXmtVWrtLk%3D Occurrence Handle10.1126/science.1061457

    Article  PubMed  CAS  Google Scholar 

  32. T Kasuga TJ White JW Taylor (2002) ArticleTitleEstimation of nucleotide substitution rates in eurotiomycete fungi Mol Biol Evol 19 2318–2324 Occurrence Handle12446823 Occurrence Handle1:CAS:528:DC%2BD38Xps12hsb4%3D

    PubMed  CAS  Google Scholar 

  33. S Kroken NL Glass JW Taylor OC Yoder BG Turgeon (2003) ArticleTitlePhylogenomic analysis of type I polyketide synthase genes in pathogenic and saprobic ascomycetes Proc Natl Acad Sci USA 100 15670–15675 Occurrence Handle14676319 Occurrence Handle1:CAS:528:DC%2BD2cXhtVCgtw%3D%3D Occurrence Handle10.1073/pnas.2532165100

    Article  PubMed  CAS  Google Scholar 

  34. L Bardi C Cocito M Marzona (1999) ArticleTitle Saccharomyces cerevisiae cell fatty acid composition and release during fermentation without aeration and in absence of exogenous lipids Int J Food Microbiol 47 133–140 Occurrence Handle10357281 Occurrence Handle1:CAS:528:DyaK1MXjs1ejtLY%3D Occurrence Handle10.1016/S0168-1605(98)00203-7

    Article  PubMed  CAS  Google Scholar 

  35. I Fujii ZG Chen Y Ebizuka U Sankawa (1991) ArticleTitleIdentification of emodinanthrone oxygenase in fungus Aspergillus terreus Biochem Int 25 1043–1049 Occurrence Handle1810248 Occurrence Handle1:CAS:528:DyaK38XitlWns7g%3D

    PubMed  CAS  Google Scholar 

  36. PL Foster (2000) ArticleTitleAdaptive mutation: implications for evolution Bioessays 22 1067–1074 Occurrence Handle11084622 Occurrence Handle1:CAS:528:DC%2BD3MXmslWmtbo%3D Occurrence Handle10.1002/1521-1878(200012)22:12<1067::AID-BIES4>3.0.CO;2-Q

    Article  PubMed  CAS  Google Scholar 

  37. MJ Dunham H Badrane T Ferea J Adams PO Brown F Rosenzweig D Botstein (2002) ArticleTitleCharacteristic genome rearrangements in experimental evolution of Saccharomyces cerevisiae Proc Natl Acad Sci USA 99 16144–16149 Occurrence Handle12446845 Occurrence Handle1:CAS:528:DC%2BD38Xps1ensL0%3D Occurrence Handle10.1073/pnas.242624799

    Article  PubMed  CAS  Google Scholar 

  38. S Schmidt S Sunyaev P Bork T Dandekar (2003) ArticleTitleMetabolites: a helping hand for pathway evolution? Trends Biochem Sci 28 336–341 Occurrence Handle12826406 Occurrence Handle1:CAS:528:DC%2BD3sXkvVCmsr0%3D Occurrence Handle10.1016/S0968-0004(03)00114-2

    Article  PubMed  CAS  Google Scholar 

  39. M Zuniga G Perez F Gonzalez-Candelas (2002) ArticleTitleEvolution of arginine deiminase (ADI) pathway genes Mol Phylogenet Evol 25 429–444 Occurrence Handle12450748 Occurrence Handle1:CAS:528:DC%2BD38Xosl2gtL0%3D Occurrence Handle10.1016/S1055-7903(02)00277-4

    Article  PubMed  CAS  Google Scholar 

  40. PJ Cotty (1997) ArticleTitleAflatoxin-producing potential of communities of Aspergillus section Flavi from cotton producing areas in the United States Mycol Res 101 698–704 Occurrence Handle10.1017/S0953756296003139

    Article  Google Scholar 

  41. M Lynch JS Conery (2000) ArticleTitleThe evolutionary fate and consequences of duplicate genes Science 290 1151–1155 Occurrence Handle11073452 Occurrence Handle1:CAS:528:DC%2BD3cXotVChsb8%3D Occurrence Handle10.1126/science.290.5494.1151

    Article  PubMed  CAS  Google Scholar 

  42. D Ober T Hartmann (2000) ArticleTitlePhylogenetic origin of a secondary pathway: the case of pyrrolizidine alkaloids Plant Mol Biol 44 445–450 Occurrence Handle11197320 Occurrence Handle1:CAS:528:DC%2BD3MXmtFWrtw%3D%3D Occurrence Handle10.1023/A:1026597621646

    Article  PubMed  CAS  Google Scholar 

  43. D Wheeler R Hope SB Cooper G Dolman GC Webb CD Bottema AA Gooley M Goodman RA Holland (2001) ArticleTitleAn orphaned mammalian beta-globin gene of ancient evolutionary origin Proc Natl Acad Sci USA 98 1101–1106 Occurrence Handle11158601 Occurrence Handle1:CAS:528:DC%2BD3MXht1Smsbg%3D Occurrence Handle10.1073/pnas.98.3.1101

    Article  PubMed  CAS  Google Scholar 

  44. A Vidal-Cros F Viviani G Labesse M Boccara M Gaudry (1994) ArticleTitlePolyhydroxynaphthalene reductase involved in melanin biosynthesis in Magnaporthe grisea. Purification, cDNA cloning and sequencing Eur J Biochem 219 985–992 Occurrence Handle8112349 Occurrence Handle1:CAS:528:DyaK2cXhvVKrtb0%3D Occurrence Handle10.1111/j.1432-1033.1994.tb18581.x

    Article  PubMed  CAS  Google Scholar 

  45. BL Gomez JD Nosanchuk (2003) ArticleTitleMelanin and fungi Curr Opin Infect Dis 16 91–96 Occurrence Handle12734441 Occurrence Handle1:CAS:528:DC%2BD3sXitF2htL8%3D

    PubMed  CAS  Google Scholar 

  46. RE Bradshaw D Bhatnagar RJ Ganley CJ Gillman BJ Monahan JM Seconi (2002) ArticleTitle Dothistroma pini, a forest pathogen, contains homologs of aflatoxin biosynthetic pathway genes Appl Environ Microbiol 68 2885–2892 Occurrence Handle12039746 Occurrence Handle1:CAS:528:DC%2BD38XksVWqsbY%3D Occurrence Handle10.1128/AEM.68.6.2885-2892.2002

    Article  PubMed  CAS  Google Scholar 

  47. PF Dowd (1992) Insect interaction with mycotoxin-producing fungi and their hosts D Bhatnagar EB Lillehoj DK Arora (Eds) Mycotoxins in Ecological Systems NumberInSeriesVol. 5 Marcel Dekker New York 137–155

    Google Scholar 

  48. GC Llewellyn CL Gee PC Sherertz (1988) ArticleTitleToxic responses of developing fifth instar milkweed bugs, Oncopeltus fasciatus (Hemiptera), to aflatoxin B1 Bull Environ Contam Toxicol 40 332–338 Occurrence Handle3130911 Occurrence Handle1:CAS:528:DyaL1cXhs1ejs78%3D Occurrence Handle10.1007/BF01689088

    Article  PubMed  CAS  Google Scholar 

  49. SW Peterson Y Ito BW Horn T Goto (2001) ArticleTitle Aspergillus bombycis, a new aflatoxigenic species and genetic variation in its sibling species, A. nomius Mycologia 93 689–703 Occurrence Handle1:CAS:528:DC%2BD3MXlvFKks7o%3D

    CAS  Google Scholar 

  50. JM Henson MJ Butler AW Day (1999) ArticleTitleThe dark side of the mycelium: melanins of phytopathogenic fungi Annu Rev Phytopathol 37 447–471 Occurrence Handle11701831 Occurrence Handle1:CAS:528:DyaK1MXnt1WntL4%3D Occurrence Handle10.1146/annurev.phyto.37.1.447

    Article  PubMed  CAS  Google Scholar 

  51. A Inagaki Y Takano Y Kubo K Mise I Furusawa (2000) ArticleTitleConstruction of an equalized cDNA library from Colletotrichum lagenarium and its application to the isolation of differentially expressed genes Can J Microbiol 46 150–158 Occurrence Handle10721483 Occurrence Handle1:CAS:528:DC%2BD3cXhtlSqs74%3D Occurrence Handle10.1139/cjm-46-2-150

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jeffrey W. Cary.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cary, J.W., Ehrlich, K.C. Aflatoxigenicity in Aspergillus: molecular genetics, phylogenetic relationships and evolutionary implications. Mycopathologia 162, 167–177 (2006). https://doi.org/10.1007/s11046-006-0051-8

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11046-006-0051-8

Keywords

Navigation