Abstract
The ergot alkaloid biosynthesis system has become an excellent model to study evolutionary diversification of specialized (secondary) metabolites. This is a very diverse class of alkaloids with various neurotropic activities, produced by fungi in several orders of the phylum Ascomycota, including plant pathogens and protective plant symbionts in the family Clavicipitaceae. Results of comparative genomics and phylogenomic analyses reveal multiple examples of three evolutionary processes that have generated ergot-alkaloid diversity: gene gains, gene losses, and gene sequence changes that have led to altered substrates or product specificities of the enzymes that they encode (neofunctionalization). The chromosome ends appear to be particularly effective engines for gene gains, losses and rearrangements, but not necessarily for neofunctionalization. Changes in gene expression could lead to accumulation of various pathway intermediates and affect levels of different ergot alkaloids. Genetic alterations associated with interspecific hybrids of Epichloë species suggest that such variation is also selectively favored. The huge structural diversity of ergot alkaloids probably represents adaptations to a wide variety of ecological situations by affecting the biological spectra and mechanisms of defense against herbivores, as evidenced by the diverse pharmacological effects of ergot alkaloids used in medicine.
Highlights
The ergot alkaloid biosynthesis system has become an excellent model to study evolutionary diversification of specialized metabolites
The Ergot Alkaloid Biosynthesis (EAS) pathway specificity mentioned above is reflected in the structural content of EAS loci across the Clavicipitaceae, which varies based on presence or absence of genes that correspond to ergot alkaloid biosynthetic capability within a given strain
The presence of long transposon-derived repeat blocks seems consistent with the subterminal location of telomere-linked clusters like EAS and IDT/LTM, but the fact that they feature prominently in the Epichloë loline alkaloid (LOL) clusters, which are typically internal with extensive genic regions flanking both ends, suggests that this is a more general feature of alkaloid clusters [24]
Summary
The four conserved early pathway steps for all natural ergot alkaloids produce chanoclavine I (CC). (recently reviewed [20]), and are catalyzed by enzymes encoded in the four genes: dmaW, encoding dimethylallyltryptophan synthase, easF, encoding dimethylallyltryptophan N-methyltransferase, easC, encoding a catalase, and easE, encoding chanoclavine-I synthase. Some strains, such as E. elymi E56, produce CC as the pathway end-product because they contain functional copies only of these four genes in an EAS cluster, which we designate as EASCC (Figure 2; Table 1). Epichloëelymi a Pathway steps are color-coded based on the positions within the pathway as shown in Figure 1; b Specificity of encoded gene can vary. EasA functions as either an isomerase “+ iso” or reductase “+ red”; c Actual role not confirmed
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