Production of the antibiotic secondary metabolite solanapyrone A by the fungal plant pathogen Ascochyta rabiei during fruiting body formation in saprobic growth

Abstract

Fungi are noted producers of a diverse array of secondary metabolites, many of which are of pharmacological importance. However, the biological roles of the vast majority of these molecules during the fungal life cycle in nature remain elusive. Solanapyrones are polyketide-derived secondary metabolites produced by diverse fungal species including the plant pathogen Ascochyta rabiei. This molecule was originally thought to function as a phytotoxin facilitating pathogenesis of A. rabiei. Chemical profiling and gene expression studies showed that solanapyrone A was specifically produced during saprobic, but not parasitic growth of A. rabiei. Expression of the gene encoding the final enzymatic step in solanapyrone biosynthesis was specifically associated with development of the asexual fruiting bodies of the fungus on certain substrates. In confrontation assays with saprobic fungi that were commonly found in chickpea debris in fields, A. rabiei effectively suppressed the growth of all competing fungi, such as Alternaria, Epicoccum and Ulocladium species. Solanapyrone A was directly detected in the inhibitory zone using a MALDI-imaging mass spectrometry, and the purified compound showed significant antifungal activities against the potential saprobic competitors. These results suggest that solanapyrone A plays an important role for competition and presumably the survival of the fungus.

Phytotoxic Metabolites Produced by Legume-Associated Ascochyta and Its Related Genera in the Dothideomycetes

“…The phenylpropanoid pathway of higher plants comprises the two main branches leading to the biosynthesis of lignin and flavonoids including many phytoalexins that play roles in defense against microbial and animal parasites. Pinolidoxin was detected using MALDI imaging mass spectrometry in hyphae on the growing front of the A. pinodies colony [47]. The available evidence of in situ localization, the broad spectrum of phytotoxicity and the mode of action suggest that pinolidoxin plays a role during hyphal invasion likely by modulating plant defense responses.…”

Identification of a Polyketide Synthase Gene Responsible for Ascochitine Biosynthesis in Ascochyta fabae and Its Abrogation in Sister Taxa

“…As with solanapyrone, ascochitine was produced during sporulation, while another polyketide, pinolidoxin, produced by A. pinodes, was detected mainly in young, advanced hyphae (52). Together with the reported antifungal activities, these observations suggest that ascochitine may play a role in competition with other fungi during saprobic growth stages in nature (2, 52).…”

“…pinodes, was detected mainly in young, advanced hyphae (52). Together with the reported antifungal activities, these observations suggest that ascochitine may play a role in competition with other fungi during saprobic growth stages in nature (2, 52). Genes involved in secondary metabolite production are generally believed to confer a fitness advantage to the producing organism (51, 53).…”

De novo assembly and comparative transcriptome analysis of Monilinia fructicola, Monilinia laxa and Monilinia fructigena, the causal agents of brown rot on stone fruits

“…Bifunctional solanapyrone synthases, over-expressed in both MFRC and MFRG, are involved in the biosynthesis of the polyketide-derived phytotoxins solanapyrones in Alternaria solani , Ascochyta rabiei and other fungi. Their phytotoxicity is well documented but their contribution to the pathogenicity has been questioned, while antifungal activity against microorganic competitors has been reported during saprotrophic but not parasitic growth [ 65 ]. β-lactamase transcripts were reconstructed in MFRC.…”