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ETD Abstract Container

Abstract Header

Computational, Evolutionary and Functional Genetic Characterization of Fungal Gene Clusters Adapted to Degrade Plant Defense Chemicals

Gluck Thaler, Emile

Abstract Details

2019, Doctor of Philosophy, Ohio State University, Plant Pathology.
Fungal interactions with plants pose both significant risks and benefits to global economies and ecosystems. As pathogens, fungi consume crops at our expense, and as mutualists and decayers, they maintain the health of fields, forests and soils. A key trait underlying these varied lifestyles is the ability to degrade toxic chemicals produced by plants to defend themselves from fungal attack. However, little is known about the genetic bases of these degradative (i.e., catabolic) mechanisms, or the evolutionary processes that give rise to adaptive catabolism, which has resulted in a fundamental gap in our understanding of how fungi adapt to their plant hosts. One promising approach to address these gaps in our knowledge is the study of metabolic gene clusters (MGCs), which are groups of neighboring genes that encode enzymatic, transporter and regulatory proteins participating in the same or related metabolic pathway. The self-contained nature of MGCs facilitates the discovery of genes encoding adaptive pathways, as well as investigations into the mechanisms shaping their evolution. Yet the extent to which catabolic genes form MGCs is unknown, largely due to a lack of tools suitable for their identification. The primary research objectives of this dissertation are thus twofold: to first develop computational tools for the identification of MGCs encoding the degradation of plant defense chemicals, and to then characterize the MGCs identified by these tools using phylogenetic and functional genetic analyses in order to elucidate the evolutionary processes driving fungal catabolic adaptation to plant tissues. In Chapter 1, I synthesize what is currently known about catabolic MGCs and their contributions to fungal ecological adaptation, with a focus on the evolutionary forces driving their assembly, maintenance and dispersal in fungal populations. In Chapter 2, I review the impact of one of these forces, horizontal gene transfer, on the evolution of eukaryotic microbial pathogens, including fungi. In Chapter 3, by developing a novel computer program that models how gene order is typically conserved in fungal genomes, I show that genes involved in the degradation of plant defenses form unexpectedly conserved clusters with biased ecological distributions, and identify gene families that are repeatedly incorporated into different types of clusters, which suggests they encode critical enzymatic functions for plant defense degradation. In Chapter 4, I characterize the function and evolution of three MGCs identified in Chapter 3 that contain a gene involved in the degradation of stilbenoid plant defense compounds, stilbene cleavage oxygenase (SCO). Using heterologous gene expression and liquid chromatography to conduct in vitro enzymatic assays, we found that SCOs located in different MGCs have similar substrate specificities, indicating that there has been little evolution at the level of enzymatic function. In contrast, phylogenetic analyses suggest multiple independent origins of SCO’s association with different cluster types, consistent with recurrent selection for specific gene combinations that are generated through combinatorial evolution. Together, the work presented in this dissertation demonstrates that catabolic MGCs are more prevalent than previously thought, and suggests that combinatorial evolution, especially as it manifests at the level of genome organization, is an important force shaping fungal adaptation in plant-associated niches.
Jason Slot (Advisor)
Ana Alonso (Committee Member)
Pierluigi Bonello (Committee Member)
Laura Kubatko (Committee Member)
219 p.

Recommended Citations

Citations

  • Gluck Thaler, E. (2019). Computational, Evolutionary and Functional Genetic Characterization of Fungal Gene Clusters Adapted to Degrade Plant Defense Chemicals [Doctoral dissertation, Ohio State University]. OhioLINK Electronic Theses and Dissertations Center. http://rave.ohiolink.edu/etdc/view?acc_num=osu1555406081422532

    APA Style (7th edition)

  • Gluck Thaler, Emile. Computational, Evolutionary and Functional Genetic Characterization of Fungal Gene Clusters Adapted to Degrade Plant Defense Chemicals. 2019. Ohio State University, Doctoral dissertation. OhioLINK Electronic Theses and Dissertations Center, http://rave.ohiolink.edu/etdc/view?acc_num=osu1555406081422532.

    MLA Style (8th edition)

  • Gluck Thaler, Emile. "Computational, Evolutionary and Functional Genetic Characterization of Fungal Gene Clusters Adapted to Degrade Plant Defense Chemicals." Doctoral dissertation, Ohio State University, 2019. http://rave.ohiolink.edu/etdc/view?acc_num=osu1555406081422532

    Chicago Manual of Style (17th edition)