Mining indole alkaloid synthesis gene clusters from genomes of 53 Claviceps strains revealed redundant gene copies and an approximate evolutionary hourglass model

Authors: LIU, MIAO - Agriculture And Agri-Food Canada; FINDLAY, WENDY - Agriculture And Agri-Food Canada; DETTMAN, JEREMY - Agriculture And Agri-Food Canada; WYKA, STEPHEN - Colorad0 State University; Broders, Kirk; SHOUKOUHI, PARIVASH - Agriculture And Agri-Food Canada; DADEJ, KASIA - Agriculture And Agri-Food Canada; KOLARIK, MIROSLAV - Czech Academy Of Sciences; BASNYAT, ARPEACE - Agriculture And Agri-Food Canada; MENZIES, JIM - Agriculture And Agri-Food Canada

Submitted to: Toxins
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/10/2021
Publication Date: 11/13/2021
Citation: Liu, M., Findlay, W., Dettman, J., Wyka, S.A., Broders, K., Shoukouhi, P., Dadej, K., Kolarik, M., Basnyat, A., Menzies, J.G. 2021. Mining indole alkaloid synthesis gene clusters from genomes of 53 Claviceps strains revealed redundant gene copies and an approximate evolutionary hourglass model. Toxins. 13(11). Article 799. https://doi.org/10.3390/toxins13110799.
DOI: https://doi.org/10.3390/toxins13110799

Interpretive Summary: Fungal pathogens in the genus Claviceps infect the grain of multiple crops including wheat, barley, rye, as well as forage and native grasses whereupon the fungus produces toxins, known as ergot alkaloids, that can be dangerous to both humans and livestock. The ergot alkaloids produced by different Claviceps species are numerous, diverse, and vary from beneficial to highly toxic to mammals. An ARS researcher at Peoria, Illinois, collaborated with researchers at Agriculture and Agri-Food Canada to examine 53 genomes of 19 Claviceps species to screen for these genes, aiming to understand the evolutionary patterns of these genes across the genus. Analysis of whole genome data found extensive duplication of genes in the ergot alkaloid pathway in the species, Claviceps purpurea that infects wheat and barley. These results support recent finding that individual strains of C. purpurea vary in the diversity of ergot alkaloid that they produce in infected grains. These finding will be of interest to those monitoring ergot alkaloid levels in grain crops as well as pharmaceutical scientist mining the diversity and function of individual ergot alkaloids for new drug development.

Technical Abstract: Ergot fungi (Claviceps spp.) are infamous for producing sclerotia containing a wide spectrum of ergot alkaloids (EA) toxic to humans and animals, making them nefarious villains in the agricultural and food industries, but also treasures for pharmaceuticals. In addition to three classes of EAs, several species also produce paspaline-derived indole diterpenes (IDT) that cause ataxia and staggers in livestock. Furthermore, two other types of alkaloids, i.e. loline (LOL) and peramine (PER), found in Epichloë spp., close relatives of Claviceps, have shown beneficial effects on host plants without evidence of toxicity to mammals. The gene clusters associated with the production of these alkaloids are known. We examined 53 genomes of 19 Claviceps spp. to screen for these genes, aiming to understand the evolutionary patterns of these genes across the genus through phylogenetic and DNA polymorphism analyses. Our results showed: 1) varied numbers of eas genes in C. sect. Claviceps and sect. Pusillae, none in sect. Citrinae, six idt/ltm genes in sect. Claviceps (except four in C. cyperi), zero to one partial (idtG) in sect. Pusillae, four in sect. Citrinae; 2) two to three copies of dmaW, easE, easF, idt/ltmB, itd/ltmQ in sect. Claviceps; 3) frequent gene gains and losses, and 4) an evolutionary hourglass pattern in the intra-specific eas gene diversity and divergence in C. purpurea.