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Title: Evolutionary mechanisms involved in development of fungal secondary metabolite gene clusters

Author
item Moore, Geromy
item COLLEMARE, JEROME - Wageningen University
item LEBRUN, MARC-HENRI - Institut National De La Recherche Agronomique (INRA)
item BRADSHAW, ROSIE - Massey University

Submitted to: Book Chapter
Publication Type: Book / Chapter
Publication Acceptance Date: 5/31/2013
Publication Date: 5/21/2014
Citation: Moore, G.G., Collemare, J., Lebrun, M-H., Bradshaw, R.E. 2014. Evolutionary mechanisms involved in development of fungal secondary metabolite gene clusters. In: Osbourne, A., Goss, R.J., Carter, G.T., editors. Natural Products: Discourse, Diversity, and Design. Wiley-Blackwell Publishers, United Kingdom. p. 343-356.

Interpretive Summary:

Technical Abstract: There is extensive adaptability and diversity in fungi, even among closely related species, that enable them to occupy various ecological niches. Of particular importance for niche adaptation is the production of fungal secondary metabolites (SM) because they can offer a distinct selective advantage in specific environments. These metabolites may influence developmental processes such as sporulation, and biotic interactions such as competition with other microbes or virulence. The biosynthesis of fungal SMs requires a suite of genes that mostly occur in clusters. Analysis of the evolution of these clusters provides insights into the genetic processes that contribute to fungal evolution. Selective pressures can lead to changes in SM chemical structure and metabolic function through gene cluster modifications such as the duplication, loss, mutation, or reorganization of existing genes. A SM gene cluster may be also be acquired through horizontal gene transfer (HGT) from another species and subsequently modified by the above listed series of events. These genetic changes will become fixed in a given population when they confer a selective advantage and ultimately result in increased fitness for an organism, such as adaptation to a new ecological niche. Recombination involves the shuffling of genetic material between two individuals either from the same species or from closely related species, resulting in novel allele combinations in the offspring that may promote adaptation. Two main types of recombination occur in fungi: parasexual and sexual. Parasexual recombination is thought to occur rarely in natural populations and usually contributes little to population diversity because the exchanged genetic material is often similar between vegetatively compatible strains; hence it will not be discussed further here. The importance of sexuality in fungal natural populations is variable with many species showing a preference for asexual reproduction. However, evidence of sexuality is being uncovered in historically asexual species, suggesting that it is more common than initially expected. It is believed that sex in fungi must circumvent vegetative incompatibility, and occurs more frequently when ecological stressors or the accumulation of deleterious mutations require an adaptive shift in order to survive. Sexual recombination usually occurs between fungi with different mating type alleles, and involves hyphal anastomosis, nuclear fusion and meiotic recombination between homologous chromosomes. The resulting recombinant offspring may benefit from greater fitness and niche adaptation than the parental strains. Horizontal gene transfer involves the stable transmission of genetic material from one organism to another without karyogamy or sex. Historically, knowledge of HGT has been limited to prokaryotic organisms, but analyses of fungal genomes have provided increasing evidence of putative HGT in fungi. Successful HGT appears to offer a selective advantage in the recipient organism; however, the mechanisms of HGT between fungi are unclear since unquestionable evidence of fungal HGT is lacking. This chapter will explore two examples of SM clusters: aflatoxin-like gene clusters in fungi such as A. flavus and Ace1 gene clusters that were originally described in Magnaporthe oryzae. Both clusters occur in different classes of fungi, and a heterogeneous collection of gene clusters in related and more distant fungal taxa can help explain the evolutionary processes that led to their formation, maintenance, and inactivation/loss. Together, they illustrate the interplay of recombination and HGT, as well as other genomic modifications that can impact SM biosynthetic pathways in fungi.