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Article

Mining Indole Alkaloid Synthesis Gene Clusters from Genomes of 53 Claviceps Strains Revealed Redundant Gene Copies and an Approximate Evolutionary Hourglass Model

by
Miao Liu
1,*,
Wendy Findlay
1,
Jeremy Dettman
1,
Stephen A. Wyka
2,
Kirk Broders
3,
Parivash Shoukouhi
1,
Kasia Dadej
1,
Miroslav Kolařík
4,
Arpeace Basnyat
1 and
Jim G. Menzies
5
1
Ottawa Research & Development Centre, Agriculture and Agri-Food Canada, Ottawa, ON K1A 0C6, Canada
2
Department of Agricultural Biology, Colorado State University, Fort Collins, CO 80523, USA
3
USDA, Agricultural Research Service, National Center for Agricultural Utilization Research, Mycotoxin Prevention and Applied Microbiology Research Unit, 1815 N. University St., Peoria, IL 61604, USA
4
Institute of Microbiology of the Czech Academy of Sciences CAS, 14220 Prague, Czech Republic
5
Morden Research and Development Centre, Agriculture and Agri-Food Canada, Morden, MB R6M 1Y5, Canada
*
Author to whom correspondence should be addressed.
Toxins 2021, 13(11), 799; https://doi.org/10.3390/toxins13110799
Submission received: 21 October 2021 / Revised: 9 November 2021 / Accepted: 10 November 2021 / Published: 13 November 2021
(This article belongs to the Special Issue Global Impact of Ergot Alkaloids)
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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 genomes of 53 strains 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, and 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.
Keywords: ergot alkaloids; ergot fungi; gene divergence; gene diversity; indole diterpenes; phylogeny; secondary metabolites ergot alkaloids; ergot fungi; gene divergence; gene diversity; indole diterpenes; phylogeny; secondary metabolites

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MDPI and ACS Style

Liu, M.; Findlay, W.; Dettman, J.; Wyka, S.A.; Broders, K.; Shoukouhi, P.; Dadej, K.; Kolařík, M.; Basnyat, A.; Menzies, J.G. Mining Indole Alkaloid Synthesis Gene Clusters from Genomes of 53 Claviceps Strains Revealed Redundant Gene Copies and an Approximate Evolutionary Hourglass Model. Toxins 2021, 13, 799. https://doi.org/10.3390/toxins13110799

AMA Style

Liu M, Findlay W, Dettman J, Wyka SA, Broders K, Shoukouhi P, Dadej K, Kolařík M, Basnyat A, Menzies JG. Mining Indole Alkaloid Synthesis Gene Clusters from Genomes of 53 Claviceps Strains Revealed Redundant Gene Copies and an Approximate Evolutionary Hourglass Model. Toxins. 2021; 13(11):799. https://doi.org/10.3390/toxins13110799

Chicago/Turabian Style

Liu, Miao, Wendy Findlay, Jeremy Dettman, Stephen A. Wyka, Kirk Broders, Parivash Shoukouhi, Kasia Dadej, Miroslav Kolařík, Arpeace Basnyat, and Jim G. Menzies. 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, no. 11: 799. https://doi.org/10.3390/toxins13110799

APA Style

Liu, M., Findlay, W., Dettman, J., Wyka, S. A., Broders, K., Shoukouhi, P., Dadej, K., Kolařík, 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), 799. https://doi.org/10.3390/toxins13110799

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