Evolutionary Mechanisms Involved in Development of Fungal Secondary Metabolite Gene Clusters

Natural Products: Discourse, Diversity, and Design

Volumn , Issue , 2014, Pages 341-356

  Moore, Geromy G ^a   Collemare, Jérôme ^b   Lebrun, Marc Henri ^c   Bradshaw, Rosie E ^d  

^a SOUTHERN REGIONAL RESEARCH CENTER   (United States)

^b WAGENINGEN UNIVERSITY   (Netherlands)

^c INRA Institut National de la Recherche Agronomique   (France)

^d MASSEY UNIVERSITY   (New Zealand)

Author keywords

ACE1 gene clusters; Aspergillus flavus; Biosynthetic pathways; Evolutionary mechanisms; Fungal secondary metabolites (SM) gene clusters; Horizontal gene transfer (HGT)

Indexed keywords

EID: 84926432358     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1002/9781118794623.ch18     Document Type: Chapter

References (45)

1. Fox, E. M.; Howlett, B. J. Secondary metabolism: regulation and role in fungal biology. Curr. Opin. Microbiol. 2008, 11 (6), 481-487.
2. Keeling, P. J. Functional and ecological impacts of horizontal gene transfer in eukaryotes. Curr. Opin. Genet. Dev. 2009, 19 (6), 613-619.
3. Lee, S. C.; Ni, M.; Li, W.; Shertz, C.; Heitman, J. The evolution of sex: a perspective from the fungal kingdom. Microbiol. Mol. Biol. Rev. 2010, 74 (2), 298-340.
4. Fitzpatrick, D. A. Horizontal gene transfer in fungi. FEMS Microbiol. Lett. 2012, 329 (1), 1-8.
5. Milgroom, M. G. Recombination and the multilocus structure of fungal populations. Annu. Rev. Phytopathol. 1996, 34, 457-477.
6. Schoustra, S. E.; Debets, A. J. M.; Slakhorst, M.; Hoekstra, R. F. Mitotic recombination accelerates adaptation in the fungus Aspergillus nidulans. PLoS Genetics. 2007, 3 (4), 648-653.
7. Alexopoulos, C. J.; Mims, C. W.; Blackwell, M. Introductory Mycology. John Wiley and Sons: 1996; pp. 196-197.
8. Horn, B. W.; Moore, G. G.; Carbone, I. Sexual reproduction in Aspergillus flavus. Mycologia. 2009, 101 (3), 423-429.
9. O'Gorman, C. M.; Fuller, H. T.; Dyer, P. S. Discovery of a sexual cycle in the opportunistic fungal pathogen Aspergillus fumigatus. Nature. 2009, 457 (7228), 471-474.
10. Bruggeman, J.; Debets, A. J. M.; Swart, K.; Hoekstra, R. F. Male and female roles in crosses in Aspergillus nidulans as revealed by vegetatively incompatible parents. Fungal. Genet. Biol. 2003, 39 (2), 136-141.
11. Doolittle, W. F. Lateral genomics. Trends. Cell. Biol. 1999, 9, M5-M8.
12. Moore, G. G.; Singh, R.; Horn, B. W.; Carbone, I. Recombination and lineage-specific gene loss in the aflatoxin gene cluster of Aspergillus flavus. Mol. Ecol. 2009, 18 (23), 4870-4887.
13. Collemare, J.; Pianfetti, M.; Houlle, A-E.; et al. Magnaporthe grisea avirulence gene ACE1 belongs to an infection-specific gene cluster involved in secondary metabolism. New Phytol. 2008, 179 (1), 196-208.
14. Carbone, I.; Ramirez-Prado, J. H.; Jakobek, J. L.; Horn, B. W. Gene duplication, modularity and adaptation in the evolution of the aflatoxin gene cluster. BMC Evol. Biol. 2007, 7, 111.
15. Brown, D.W.; Yu, J-H.; Kelkar, H. S.; et al. Twenty-five coregulated transcripts define a sterigmatocystin gene cluster in Aspergillus nidulans. Proc. Natl. Acad. Sci. USA 1996, 93 (4), 1418-1422.
16. Bradshaw, R. E.; Ganley, R. J.; Jones,W. T.; Dyer, P. S. High levels of dothistromin toxin produced by the forest pathogen Dothistroma pini. Mycol. Res. 2000, 104 (3), 325-332.
17. Schwelm, A.; Bradshaw, R. E. Genetics of dothistromin biosynthesis of Dothistroma septosporum: An update. Toxins. 2010, 2 (11), 2680-2698.
18. Geiser, D. M.; Pitt, J. I.; Taylor, J. W. Cryptic speciation and recombination in the aflatoxinproducing fungus Aspergillus flavus. Proc. Natl. Acad. Sci. USA 1998, 95 (1), 388-393.
19. Carbone, I.; Jakobek, J. L.; Ramirez-Prado, J. H.; Horn, B.W. Recombination, balancing selection, and adaptive evolution in the aflatoxin gene cluster of Aspergillus parasiticus. Mol. Ecol. 2007, 16 (20), 4401-4417.
20. Moore, G. G.; Beltz, S. B.; Carbone, I.; et al. The population dynamics of aflatoxigenic aspergilli. In: Aflatoxins: Biochemistry and Molecular Biology; Guevara-González, R. G., Ed., InTech publishers; Croatia, 2011; pp. 347-366.
21. Ehrlich, K. C.; Cotty, P. J. An isolate of Aspergillus flavus used to reduce aflatoxin contamination in cottonseed has a defective polyketide synthase gene. Appl. Microbiol. Biotechnol. 2004, 65 (4), 473-478.
22. Chang, P-K.; Horn, B. W.; Dorner, J. W. Sequence breakpoints in the aflatoxin biosynthesis gene cluster and flanking regions in nonaflatoxigenic Aspergillus flavus isolates. Fungal Genet. Biol. 2005, 42 (11), 914-923.
23. Ehrlich, K. C.; Chang, P-K.; Yu, J.; Cotty, P. J. Aflatoxin biosynthesis cluster gene cypA is required for G aflatoxin formation. Appl. Environ. Microbiol. 2004, 70 (11), 6518-6524.
24. Cary, J. W.; Harris-Coward, P. Y.; Ehrlich, K. C.; et al. Functional and phylogenetic analysis of the Aspergillus ochraceoroseus aflQ (ordA) gene ortholog. Mycologia. 2012, 104 (4), 857-864.
25. Slot, J. C.; Rokas, A. Horizontal transfer of a large and highly toxic secondary metabolite gene cluster between fungi. Curr. Biol. 2011, 21 (2), 134-139.
26. Böhnert, H. U.; Fudal, I.; Dioh,W.; et al. A putative polyketide synthase/peptide synthetase from Magnaporthe grisea signals pathogen attack to resistant rice. Plant Cell. 2004, 16 (9), 2499-2513.
27. Khaldi, N.; Collemare, J.; Lebrun, M-H.; Wolfe, K. H. Evidence for horizontal transfer of a secondary metabolite gene cluster between fungi. Genome Biol. 2008, 9 (1), R18.
28. Qiao, K.; Chooi, Y. H.; Tang, Y. Identification and engineering of the cytochalasin gene cluster from Aspergillus clavatus NRRL 1. Metab. Eng. 2011, 13 (6), 723-732.
29. Notredame, C.; Higgins, D. G.; Heringa, J. T-Coffee:Anovel method for fast and accurate multiple sequence alignment. J. Mol. Biol. 2000, 302 (1), 205-217.
30. Tamura, K.; Peterson, D.; Peterson, N.; et al. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 2011, 28 (10), 2731-2739.
31. O'Connell, R. J.; Thon, M. R.; Hacquard, S.; et al. Lifestyle transitions in plant pathogenic Colletotrichum fungi deciphered by genome and transcriptome analyses. Nat. Genet. 2012, 44 (9), 1060-1065.
32. Wang, H.; Xu, Z.; Gao, L.; Hao, B. A fungal phylogeny based on 82 complete genomes using the composition vector method. BMC Evol. Biol. 2009, 9, 195.
33. Berka, R. M.; Grigoriev, I. V.; Otillar, R.; et al. Comparative genomic analysis of the thermophilic biomass-degrading fungi Myceliophthora thermophila and Thielavia terrestris. Nat. Biotechnol. 2011, 29 (10), 922-927.
34. Patron, N. J.; Waller, R. F.; Cozijnsen, A. J.; et al. Origin and distribution of epipolythiodioxopiperazine (ETP) gene clusters in filamentous ascomycetes. BMC Evol. Biol. 2007, 7, 174.
35. Saikia, S.; Nicholson, M. J.; Young, C.; et al. The genetic basis for indole-diterpene chemical diversity in filamentous fungi. Mycol. Res. 2008, 112 (2), 184-199.
36. Spröte, P.; Hynes, M. J.; Hortschansky, P.; et al. Identification of the novel penicillin biosynthesis gene aatB of Aspergillus nidulans and its putative evolutionary relationship to this fungal secondary metabolism gene cluster. Mol. Microbiol. 2008, 70 (2), 445-461.
37. Proctor, R. H.; McCormick, S. P.; Alexander, N. J.; Desjardins, A. E. Evidence that a secondary metabolic biosynthetic gene cluster has grown by gene relocation during evolution of the filamentous fungus Fusarium. Mol. Microbiol. 2009, 74 (5), 1128-1142.
38. Wong, S.; Wolfe, K. H. Birth of a metabolic gene cluster in yeast by adaptive gene relocation. Nat. Genet. 2005, 37 (7), 777-782.
39. Khaldi, N.;Wolfe, K. H. Evolutionary origins of the fumonisin secondary metabolite gene cluster in Fusarium verticillioides and Aspergillus niger. Int. J. Evol. Biol. 2011, 2011, 423821, 7 pages.
40. Campbell, M. A.; Rokas, A.; Slot, J. C. Horizontal transfer and death of a fungal secondary metabolic gene cluster. Genome Biol. Evol. 2012, 4 (3), 289-293.
41. Stajich, J. E.; Wilke, S. K.; Ahrén, D.; et al. (Insights into evolution of multicellular fungi from the assembled chromosomes of the mushroom Coprinopsis cinerea (Coprinus cinereus). Proc. Natl. Acad. Sci. USA 2010, 107 (26), 11889-11894.
42. Brakhage, A. A.; Al-Abdallah, Q.; Tüncher, A.; Spröte, P. Evolution of β-lactam biosynthesis genes and recruitment of trans-acting factors. Phytochemistry. 2005, 66 (11), 1200-1210.
43. Akagi, Y.; Akamatsu, H.; Otani, H.; Kodama, M. Horizontal chromosome transfer, a mechanism for the evolution and differentiation of a plant-pathogenic fungus. Eukaryot. Cell. 2009, 8 (11), 1732-1738.
44. Ma, L. J.; van derDoes, H. C.; Borkovich, K. A.; et al. Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature. 2010, 464 (7287), 367-373.
45. Cary, J. W.; Ehrlich, K. C. Aflatoxigenicity in Aspergillus: molecular genetics, phylogenetic relationships and evolutionary implications. Mycopathologia. 2006, 162 (3), 167-177.