Currencies of Mutualisms: Sources of Alkaloid Genes in Vertically Transmitted Epichloae

Abstract

The epichloae (Epichloë and Neotyphodium species), a monophyletic group of fungi in the family Clavicipitaceae, are systemic symbionts of cool-season grasses (Poaceae subfamily Poöideae). Most epichloae are vertically transmitted in seeds (endophytes), and most produce alkaloids that attack nervous systems of potential herbivores. These protective metabolites include ergot alkaloids and indole-diterpenes (tremorgens), which are active in vertebrate systems, and lolines and peramine, which are more specific against invertebrates. Several Epichloë species have been described which are sexual and capable of horizontal transmission, and most are vertically transmissible also. Asexual epichloae are mainly or exclusively vertically transmitted, and many are interspecific hybrids with genomic contributions from two or three ancestral Epichloë species. Here we employ genome-scale analyses to investigate the origins of biosynthesis gene clusters for ergot alkaloids (EAS), indole-diterpenes (IDT), and lolines (LOL) in 12 hybrid species. In each hybrid, the alkaloid-gene and housekeeping-gene relationships were congruent. Interestingly, hybrids frequently had alkaloid clusters that were rare in their sexual ancestors. Also, in those hybrids that had multiple EAS, IDT or LOL clusters, one cluster lacked some genes, usually for late pathway steps. Possible implications of these findings for the alkaloid profiles and endophyte ecology are discussed.

Epichloë hybrida, sp. nov., an emerging model system for investigating fungal allopolyploidy

“…All genomic and transcriptomic data described below have been deposited in publicly accessible databases (see SUPPLEMENTARY TABLE 1 for full access details). A fragmentary genome assembly was reported by Schardl et al (2013b).…”

“…; see also Christensen et al 2012). The strain has also been referenced under the identifier e144 (Schardl et al 2013b). Because E. hybrida makes several classes of secondary metabolites that deter insect feeding (Christensen et al 1993), perennial ryegrass cultivars carrying E. hybrida were advanced for commercialization in 1990.…”

“…Assembled genes have been deposited in GenBank (SUPPLEMENTARY TABLE 1; see also Schardl et al 2013b for additional accessions of these genes).…”

“…Furthermore, asexual propagation (vertical transmission) is theorized to be selected for in mutualistic relationships (Ewald 1987). Two or more subgenomes can often produce a more diverse range of alkaloids than one haploid genome as well, thus potentially increasing host fitness (Schardl et al 2013b).…”

Breaking through the feed barrier: options for improving forage genetics

“…The Epichloë forms endo-symbioses with grasses in the subfamily Pooideae, including important forage species such as perennial ryegrass, tall fescue (Festuca arundinacea) and meadow fescue (F. pratensis). It plays a key role in pasture, primarily through the production of secondary metabolites, including alkaloids that protect the host plant from biotic and abiotic stress (Johnson et al 2013;Schardl et al 2013).…”