Ergot Claviceps purpurea (fries) Tulasne alkaloid diversity and virulence: evolution, genetic diversification, and metabolic engineering (review)

Claviceps purpurea (Fries) Tulasne is a valuable source of many bioactive metabolites (alkaloids) for pharmaceutical industry and a unique plant-parasite model but also a serious adversary for plant growing, feed and livestock industries causing significant economic damage in different countries. Ergot appeared in South America in the Paleocene, the age of the genus Claviceps is 20.4 million years (K. Píchová et al., 2018). Intraspecific diversity and divergence of indole alkaloid production gene cluster occurred in accordance with the evolutionary “hourglass model” (M. Liu et al., 2021). Ergometrine, ergosine, ergotamine, a-ergocryptine, ergocornine, ergocristine and 8-S(-inine-) epimers are the major identified ergoalkaloids which account for approximately 50 % of the ergot alkaloid metabolome. Claviceps alkaloid gene clusters consist of varying numbers of genes, posses two or three copies of dmaW , easE , easF genes, and there are many facts of frequent gene loss and acquisition (M. Liu et al., 2021). Differences in metabolomic profiles of C. purpurea indole alkaloids correlate with the lpsA gene variability. Diversity of the ergot alkaloids is a result of sequence diversity in the easH / lpsA tandem-duplicated region (C. Hicks et al., 2021). The lpsA1 and lpsA2 genes derived from recombination events (S. Wyka et al., 2022), i.e., the lpsA genes are supposed to be due to reshuffling (C. Hicks et al., 2021). C . purpurea has a relatively large accessory genome (~ 38 %), high recombination rates (ρ = 0.044), and transposon-mediated gene duplication (S. Wyka et al., 2022). A transgenic yeast line is capable of producing enantiopure D-lysergic acid up to a level of 1.7 mg/l (G. Wong et al., 2022). Genetically engineered cultures of Metarhizium brunneum can produce 86.9 % lysergic acid and 72.8% dihydrolysirgic acid (K. Davis et al., 2020). Expression of the trpE and dmaW genes is quantitatively related to intensity of alkaloid synthesis in saprophytic Claviceps cultures (M. Králová et al., 2021). Pectin is the main target of CAZymes proteins responsible for cell wall degradation during C. purpurea and C. paspali infection (B. Oeser et al., 2017; H. Oberti et al., 2021). Polygalacturonase, MAP kinase, transcription factor CPTF1 ( Cptf1 gene), GTPase ( Cdc42 gene) make the main contribution to Claviceps virulence (B. Oeser et al., 2017; E. Tente et al., 2021). Ergot affects the auxin, ethylene, and cytokinin pathways in plants, with varying effects depending on tissue type and time after inoculation (E. Tente, 2020; Tente et al., 2021). Wheat resistance is due to mutations in DELLA proteins (E. Tente, 2020; A. Gordon et al., 2020) while rye resistance is due to pectinesterase activity, cell wall modification, and modulation of pollen tube growth (COBRA-like protein and pectinesterase inhibitor) (K. Mahmood et al., 2020).