Genetics, Genomics and Evolution of Ergot Alkaloid Diversity

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.

Evolution of Chemical Diversity in Echinocandin Lipopeptide Antifungal Metabolites

“…Experimental evidence and mechanistic studies for such claims are still lacking. Other studies of disjunct distributions of fungal secondary-metabolite gene clusters have explained these dispersed distributions by normal genomic processes, including gene duplications and losses (4,82). Therefore, the phylogenetic pattern underlying echinocandin distribution exhibits hallmarks of incomplete lineage sorting and multiple pathway losses driven by strong selection pressure (34), including environmental factors and interactions with other organisms that have acted on individuals to maintain or degrade the gene cluster (Fig.…”

Phylogenomics and evolution of secondary metabolism in plant-associated fungi

“…It is assumed to involve fusion of hyphae or spores between distinct species and the genetic transfer of secondary metabolite gene clusters, most likely through some form of mitotic recombination [49,50 ]. Other mechanisms that likely explain the distribution of some fungal secondary metabolite genes and gene clusters are complex patterns of gene gains and losses, neofunctionalization, incomplete lineage sorting and trans-species polymorphisms [51,52 ], all of which can also lead to incongruent gene-species evolutionary histories. The current sampling of fungal genomes is still …”

“…NRPSs contain a basic modular structure that comprises an adenylation (=AMPylation [52 ]) domain (A), which recognizes and activates an amino acid residue (often nonproteinogenic amino acid and occasionally hydroxy acid), a thiolation domain (T), which covalently binds the residue to the NRPS enzyme via a thioester linkage, and a condensation domain (C), which grows the peptide by adding residue 'n' to residue 'n + 1'. NRPS A-domains show varying levels of specificity with some A-domains activating a single residue, whereas others are less discriminating and may activate multiple residues.…”

Plant-Microbe Interactions: A Molecular Approach

“…Conversely, microbial diseases in plants have been associated with famine and poverty over the past several decades. In extreme cases, for instance, in the case of ergot poisoning caused by the fungus Claviceps purpurea , humans and animals present with neurological and metabolic symptoms, leading even to death (Young et al 2015 ). However, with modern agricultural practices and increased awareness about these interactions, various aspects of the plant-microbe interactions are well understood.…”