In a breakthrough paper, Schardl’s group and collaborators have published 15 genomes of diverse species of Clavicipitaceae plant endophytes and parasites in the last issue of PloS Genetics. The Clavicipitaceae (Pezizomycotina, Sordariomycetes, Hypocreales) includes “ergot” fungi that parasitize ears of cereals and produce the toxic ergoline derivatives; ergot fungi have historically caused epidemics of gangrenous poisonings, the ergotism, also known as the Saint Anthony’s Fire. The ascomycetous family also includes plant endophytic symbionts 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. They synthesize alkaloids with chemical similarities to biogenic amines that deter insects, livestock, and wildlife from feeding on the fungus or plant. Thanks to this chemical warfare, Epichloae protect their hosts from cattle grazing. The lysergic acid diethylamide (LSD), a semisynthetic ergot alkaloid originally developed as an antidepressant, is the most potent known hallucinogen.
In this study, they sequenced the genomes of 10 epichloae, three ergot fungi (Claviceps species), a morning-glory symbiont (Periglandula ipomoeae), and the bamboo witch’s broom pathogen (Aciculosporium take), profiled the alkaloids in these species and compared the gene clusters for four classes of alkaloids. The genomes were primarily sequenced by shotgun 454 pyrosequencing, but paired-end and mate-pair reads were used to scaffold several assemblies. Size of the assembled genome among the sequenced strains varied 2-fold from 29.2 to 58.7 Mb, with wide ranges even within the genera Claviceps (31–52.3 Mb) and Epichloë (29.2–49.3 Mb). This genome size variation is mainly resulting from the abundance of repeated elements, which ranged from 4.7 to 56.9%. Annotated genome sequences have been posted at www.endophyte.uky.edu.
In the epichloae, the clusters of genes coding for enzymes of alkaloid biosynthesis contain very large blocks of repetitive elements which promote gene losses, mutations, and even the evolution of new genes. Two striking features emerged from the detailed analysis of alkaloid biosynthesis gene clusters. Firstly, in most alkaloid loci in most species, the periphery of each cluster was enriched in genes that by virtue of their presence, absence, or sequence variations determined the diversity of alkaloids within the respective chemical class. Second, alkaloid gene loci of the epichloae had extraordinarily large and pervasive blocks of AT- rich repeats derived from retroelements, DNA transposons, and MITEs. This finding suggests that these plant-interacting fungi are under selection for alkaloid diversification.
In their conclusions, the authors suggest that this selection of chemotypes is related to the variable life histories of the epichloae, their protective roles as symbionts, and their associations with the ecologically diverse cool-season grasses.
Schardl CL, Young CA, Hesse U, Amyotte SG, Andreeva K, et al. (2013) Plant-Symbiotic Fungi as Chemical Engineers: Multi-Genome Analysis of the Clavicipitaceae Reveals Dynamics of Alkaloid Loci. PLoS Genet 9(2): e1003323. doi:10.1371/journal.pgen.1003323