Plant-symbiotic fungi as chemical engineers: multi-genome analysis of the Clavicipitaceae reveals dynamics of alkaloid Loci

The fungal family Clavicipitaceae includes plant symbionts and parasites that produce several psychoactive and bioprotective alkaloids. The family includes grass symbionts in the epichloae clade (Epichloë and Neotyphodium species), which are extraordinarily diverse both in their host interactions and in their alkaloid profiles. Epichloae produce alkaloids of four distinct classes, all of which deter insects, and some—including the infamous ergot alkaloids—have potent effects on mammals. The exceptional chemotypic diversity of the epichloae may relate to their broad range of host interactions, whereby some are pathogenic and contagious, others are mutualistic and vertically transmitted (seed-borne), and still others vary in pathogenic or mutualistic behavior. We profiled the alkaloids and sequenced the genomes of 10 epichloae, three ergot fungi (Claviceps species), a morning-glory symbiont (Periglandula ipomoeae), and a bamboo pathogen (Aciculosporium take), and compared the gene clusters for four classes of alkaloids. Results indicated a strong tendency for alkaloid loci to have conserved cores that specify the skeleton structures and peripheral genes that determine chemical variations that are known to affect their pharmacological specificities. Generally, gene locations in cluster peripheries positioned them near to transposon-derived, AT-rich repeat blocks, which were probably involved in gene losses, duplications, and neofunctionalizations. The alkaloid loci in the epichloae had unusual structures riddled with large, complex, and dynamic repeat blocks. This feature was not reflective of overall differences in repeat contents in the genomes, nor was it characteristic of most other specialized metabolism loci. The organization and dynamics of alkaloid loci and abundant repeat blocks in the epichloae suggested that these fungi are under selection for alkaloid diversification. We suggest that such selection is related to the variable life histories of the epichloae, their protective roles as symbionts, and their associations with the highly speciose and ecologically diverse cool-season grasses

Impact of endophyte inoculation on the morphological identity of cultivars of Lolium perenne (L) and Festuca arundinacea (Schreb.)

Publication history: Accepted - 9 April 2020; Published online - 5 May 2020Grass endophytes have been shown to confer enhanced environmental resilience to symbiont cultivars with reports of modified growth. If inoculating with an endophyte (E+) made an accession morphologically distinct from its registered endophyte free (E−) accession, there could be protection and ownership issues for testing authorities and breeders. This study investigated if, in official Plant Breeders Rights (PBR) field trials, the morphological characteristics of E+and E− accessions of perennial ryegrass and tall fescue cultivars were sufficiently modified to designate them as mutually distinct and also distinct from their definitive accessions (Def), held by the testing authorities. Testing perennial ryegrass on 17 characters at 2 sites generated 48,960 observations and for tall fescue on 9 characters at 1 site, 12,960 observations (each for 3 accessions of 4 cultivars × 60 plants × 2 growing cycles). Distinctness required a p < 0.01 difference in a single character from the combined over years analysis (COYD). A few significant differences were recorded between E− and E+accessions. Cultivar Carn E+ was smaller than Carn E− for Infloresence Length (p < 0.01) in both years but COYD analysis (p < 0.05) was insufficient to declare distinctiveness. Overall, the number of observed differences between E−/E+ accessions was less or similar to the number expected purely by chance. In contrast, comparisons between Def and E− or E+ accessions showed a number of significant differences that were substantially more numerous than expected by chance. These results showed no conclusive evidence of endophyte inclusion creating false PBR distinctions but unexpectedly, several E− and E+ accessions were distinguished from their official definitive stock.This study was jointly funded by the EU Community Plant Variety Office, Angers, France and Euroseeds, Brussels, Belgium