Comparative genomics and transcriptomics during sexual development gives insight into the life history of the cosmopolitan fungus Fusarium neocosmosporiellum

Authors: KIM, WONYONG - Michigan State University; CAVINDER, BRAD - Michigan State University; Proctor, Robert; O Donnell, Kerry; TOWNSEND, JEFFREY - Yale University; TRAIL, FRANCES - Michigan State University

Submitted to: Frontiers in Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/20/2019
Publication Date: 6/7/2019
Citation: Kim, W., Cavinder, B., Proctor, R.H., O'Donnell, K., Townsend, J.P., Trail, F. 2019. Comparative genomics and transcriptomics during sexual development gives insight into the life history of the cosmopolitan fungus Fusarium neocosmosporiellum. Frontiers in Microbiology. https://doi.org/10.3389/fmicb.2019.01247.
DOI: https://doi.org/10.3389/fmicb.2019.01247

Interpretive Summary: The fungus Fusarium includes species that cause severe diseases on economically important crops and/or that produce toxins (mycotoxins) that pose health risks to humans and livestock. The species Fusarium graminearum and Fusarium neocosmosporiellum differ in many respects. For example, F. graminearum causes wheat head blight, which can severely reduce yield and contaminate grain with mycotoxins; whereas, F. neocosmosporiellum causes fruit- and root-rot diseases on numerous field crops, but it is not considered a wheat pathogen or mycotoxin producer. Despite these and other differences, both species employ a similar mechanism to produce large numbers sexual spores (ascospores) that disperse the fungi in the environment and allow them to infect crops. To identify factors that could be used to block ascospore production, we investigated genetic changes that occur in the two fungi during sexual development. The results indicate that similar sets of genes were turned on and off in both fungi. A prominent difference was that more genes involved in movement of nutrients from the environment into fungal cells were turned on to a higher level in F. neocosmosporiellum than in F. graminearum. One gene (PKS7) that was turned on in both fungi is involved in production of a molecule that belongs to a class of metabolites known as polyketides. Inactivation of the PKS7 gene in F. neocosmosporiellum blocked ascospore production. Thus, PKS7 could serve as a target to reduce ascospore-mediated spread of some Fusarium species. These research results have potential to contribute to strategies that reduce diseases and mycotoxins problems caused by Fusarium, and thereby improve the safety of crops used for production of food and feed.

Technical Abstract: Fusarium neocosmosporiellum (formerly Neocosmospora vasinfecta) is a cosmopolitan fungus that has been reported from soil, herbivore dung, and as a fruit- and root-rot pathogen of numerous field crops, although it is not known to cause significant losses on any crop. Taking advantage of the fact that this species produces prolific numbers of perithecia in culture, the genome of F. neocosmosporiellum was sequenced and transcriptomic analysis across five stages of perithecium development was performed to better understand the metabolic potential for sexual development and gain insight into its life history. Perithecium morphology together with the genome and transcriptome were compared with those of the plant pathogen F. graminearum, a model for studying perithecium development. Larger ascospores of F. neocosmosporiellum and their tendency to discharge as a cluster demonstrated a duality of dispersal: the majority are passively dispersed through the formation of cirrhi, while a minority of spores are shot longer distances than those of F. graminearum. The predicted gene number in the F. neocosmosporiellum genome was similar to that in F. graminearum, but F. neocosmosporiellum had more carbohydrate metabolism-related and transmembrane transport genes. Many transporter genes were differentially expressed during perithecium development in F. neocosmosporiellum, which may account for its larger perithecia. Comparative analysis of the secondary metabolite gene clusters identified several polyketide synthase genes that were induced during later stages of perithecium development. Deletion of a polyketide synthase gene in F. neocosmosporiellum resulted in a defective perithecium phenotype, suggesting an important role of the corresponding metabolite, which has yet to be identified, in perithecium development. Results of this study have provided novel insights into the genomic underpinning of development in F. neocosmosporiellum, which may help elucidate its ability to occupy diverse ecological niches.