NSF-BSF: Collaborative Research: Developmental genetics of host invasion initiated by fungal spores

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Fungi interact with their environments and with human life in various ways. Fungal adaptation to their environments has resulted in diverse fungal lifestyles. Just within the fungal class Sordariomycetes, there are examples of mutualistic symbionts living harmoniously with plants; pathogens that damage and kill plants or mammals; fungi that decompose organic matter; fungi that attack other fungi; zombie fungi that parasitize, manipulate, and kill insects. The life history of each of these fungi begins with a simple spore called a conidium. Conidia can be produced rapidly and in huge numbers, and provide the primary means for dispersal to new hosts. This research program will examine changes in gene expression among species during conidium germination and growth on different hosts. This will reveal the evolved features that enable spore germination and host colonization under different conditions to better understand fungus ecology and evolution. The diversity of fungi also renders them an exciting and tractable teaching platform; broader impacts include a fungal ecology education project in which students at Celentano Biotechnology, Health and Medical Magnet School 6th grade students collect, identify, and isolate fungi commonly found on plants and insects. This collaborative research will elucidate the genetic basis of sporulation and evolution of fungal parasitism in Sordariomycetes. This class of fungi contain members that have evolved the capability and specificity to attack plants, insects, fish, mammals, and fungi via in situ spore germination. Seven Sordariomycetes will be studied: two entomopathogens (Metarhizium anisopliae and Cordyceps militaris), a plant pathogen (Fusarium graminearum), a plant endophyte (Epichloe festucae), two mycoparasites (Tolypocladium ophioglossoides and Trichoderma asperellum), and the saprotrophic model Neurospora crassa (with endophytic capabilities). Asexual spores (conidia) of these fungi will be germinated to initiate colonies in medium and on host plants. Comparative genomics and transcriptomics will be performed on the resulting cultures. This will provide insights into their shared genetic programming and into the evolved basis of their divergent host preferences. Evolutionary ancestral expression inference will be used to identify genes responsible for pathogenicity. This approach will identify genes that have undergone recent shifts in gene expression during spore germination-in particular, shifts that occurred along the shared ancestral lineages where key traits (such as host specificity or pathogenic morphogenesis) have evolved. Genes that are substantially upregulated, downregulated, or conserved in level of expression during the recent evolution of each of these seven species and their ancestors will be determined. These genes will be genetically perturbed and the resulting phenotypes will be investigated to determine their function in pathogenesis, potentially leading to new technologies for the control of fungal infections in diverse contexts.This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.