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Hehmeyer, Jenks 2020 Biology Thesis Title Hehmeyer, Jenks 2020 Biology Thesis Title: Evolution of a transcriptional regulator of cup cell differentiation in Dictyostelium discoideum: Advisor: Robert Savage Advisor is Co-author/Adviser Restricted Data Used: None of the above Second Advisor: Release: release now Authenticated User Access (does not apply to released theses): Contains Copyrighted Material: No EVOLUTION OF A TRANSCRIPTIONAL REGULATOR OF CUP CELL DIFFERENTIATION IN DICTYOSTELIUM DISCOIDEUM by JENKS HEHMEYER Robert Savage, Advisor A thesis submitted in partial fulfillment of the requirements for the Degree of Bachelor of Arts with Honors in Biology WILLIAMS COLLEGE Williamstown, Massachusetts May 31, 2020 2 Abstract The evolution of novel cell types contributed extensively to the emergence of new organismal functions in animals, plants, and other multicellular lineages. However, very little is currently understood about cell type evolution. A major challenge is understanding how transcription factor evolution contributes to the origination of new cell types. I characterized the developmental roles of two paralogous transcription factor genes, fasA and fasB, in the slime mold Dictyostelium discoideum, a Eukaryote that forms simple multicellular fruiting bodies consisting of only three terminal cell types. fasA is essential for the generation of the cups, structures that play critical somatic roles in Dictyostelium discoideum fruiting bodies. Specifically, fasA initiates the sorting of precup cells to their ultimate locations, a process that seems to occur upon cup cell differentiation. fasB plays a minor role in the formation of the stalk. The cup cell is a genus-specific cell type that evolved from the stalk cell, and the segmental duplication that gave rise to fasA and fasB also took place at the base of Dictyostelium. However, sequence and expression pattern analyses demonstrate that the evolution of fasA is unlikely to have contributed to the origination of cup cells. 3 Introduction Cell differentiation is a critical process in unicellular and multicellular organisms alike. During differentiation, a cell changes from one stable state to another. These states, or cell types, differ in form and function, a reflection of differences in the underlying patterns of gene expression. Specifically, the enactment of differentiation involves suppression of the one gene expression program and activation of another, through changes in the set of transcription factors (TFs) interacting with the chromatin. Often, this transition involves multiple signaling and TF cascades, resulting in the passage through transient cell states before the activation of a battery of TFs that is able to maintain its own expression—the “core regulatory complex” of “terminal selectors” [1-3]. In unicellular organisms, differentiation generally occurs in response to changes in environmental conditions. In multicellular organisms, differentiation may be induced by extracellular molecules, physical cell-cell or cell-surface interactions, or asymmetric cell division. The spatiotemporal patterning of these signals ensures the correct arrangement of cells and tissues. Generally, multicellular organisms have highly proliferative stem cells that are specifically responsible for differentiation; the “terminal cell types” that constitute the majority of a mature organism and carry out its metabolic, structural, and behavioral functions, have very limited capacity for differentiation. The evolution of certain multicellular lineages has involved great increases in the number of terminal cell types. For example, histological and transcriptomic data indicate that adult mammals possess hundreds of cell types [4, 5]; however, the earliest branching metazoans, the sponges, ctenophores, placozoans, and cnidarians, have far fewer cell types [6-10], indicating that, similarly, the common ancestor of all metazoans had relatively little cell specialization. The 4 diversification of cell types over the course of metazoan evolution had critical functional ramifications. For example, the origination of neurons likely had significant consequences for the coordination of movement [11]. The current paradigm for cell type origination is the “sister cell type hypothesis” [1]. According to this hypothesis, the evolution of a new cell type is most likely to occur through the divergence of an existing cell type into two distinct “sister” cell types. This cell type duplication involves maintenance of the parent cell type’s function by one daughter cell type and adoption of a slightly distinct function by the other. Such “cell type neofunctionalization” requires differentiation of the cell type to occur by its own independent process—individualization—so that a change in the gene expression program—specialization—may occur. While individualization may occur by multiple mechanisms, specialization necessarily involves change in the core regulatory complex. Recruitment of an existent TF to the core regulatory complex could suffice for specialization (Figure 1A). This could occur, for example, if extracellular conditions change in a particular tissue of an organism, causing some, but not all, cells of one type to express a general reaction TF [12]. The duplication and neofunctionalization of a terminal selector is another likely mechanism for cell type neofuntionalization, as mutations in the DNA-binding domain and promoter of the neofunctionalized terminal selector could cause both cell type specialization and individualization, respectively (Figure 1B). Such a TF duplication event was responsible for the evolution of the vertebrate hair cell from an axoned mechanosensory cell [1]. 5 A. B. Transcription factor introduction Transcription factor duplication Ancestral cell type Ancestral cell type TS-A TS-A tf-c TS-B TS-B TS-C TS-C TS-D tf-c duplication to tf-c1 and tf-c2 Expression of tf-d in subset of cells Change in TF-C2 regulation Integration of TF-D into state regulation Change in TF-C2 binding site preference Novel cell type Ancestral-like cell type Ancestral-like cell type Novel cell type TS-A TS-A TS-A TS-A TS-B TS-B TS-B TS-B TS-C TS-C TS-C1 TS-C1 TS-D TS-D TS-C2 TS-C2 tf-c1 tf-c2 Further changes Further changes Figure 1: Two mechanisms of cell type origination. TS stands for “terminal selector”; TS-A through D represent transcription factors regulating cell state. A. The expression of a preexisting transcription factor in a subset of cells of one type causes these cells to adopt a distinct identity. B. Duplication of a terminal selector, followed by neofunctionalization through both DNA- binding domain amino acid sequence change and change in expression regulation, causes a new cell type to evolve. This example, however, represents one of very few cell type origination events for which the molecular changes responsible have been inferred [1, 12, 13]. Indeed, the evolutionary relationships between the cell types of different species are poorly understood. While recent advances in single cell RNA sequencing and the interspecific analysis of this data mean that we could be entering an era of “cell type phylogenetics” soon [11, 14], understanding cell type evolution will likely still require biochemical and genetic experiments to identify the genes responsible for regulating differentiation of each cell type in each species. 6 One group of protistan Eukaryotes, the dictyostelids, show promise as a simple “model clade” for studying the mechanisms of cell type evolution. The dictyostelids—also referred to as the “social amoebae”—are in the class Eumycetozoa (the true slime molds) of the supergroup Amoebozoa, the sister clade to the Animals and Fungi (Figure 2A) [15]. Dictyostelids are free- living amoeboid organisms that inhabit forest soils worldwide. They are generally found as mitotically-dividing populations of single cells that feed on bacteria. Under conditions of starvation, these amoebae localize and aggregate into a multicellular unit. This multicellular unit adopts an elongated form, the sorogen, that ultimately develops into a fruiting body, or sorocarp, consisting of a stalk bearing a round mass of spores. Fruiting body formation—sorocarpy—is largely independent of cell division, instead requiring organized movement of amoebae followed by their differentiation into terminal cell types [16]. Dictyostelid sorocarpic development is best known in the model species Dictyostelium discoideum (Figure 2B). In this species, the sorogen may migrate freely prior to fruiting body formation, a process that, in nature, allows cells to reach the surface of the soil. The migrating sorogen, or slug, is made up of several precursor cell populations (Figure 2C) [17, 18]. The anterior of the slug consists of the prestalk A (“PstA”) cells at the tip and the prestalk O (“PstO”) cells just behind them. The posterior two-thirds of the slug consists primarily of the prespore cells. Scattered amongst the prespore cells are the anterior-like cells (ALCs), so called because they, like the PstA and PstO cells, possess large lysosomal vacuoles; in addition, many ALCs express either ecmA or ecmB—extracellular matrix protein genes associated with the PstA and PstO lineages—though some express neither. Several extracellular signals contribute to this precursor patterning [19]. Extracellular cAMP is critical for prespore differentiation [20], while 7 the polyketide DIF-1 is responsible for the differentiation of the PstO cells and some, but not all, of the ALCs [18, 21]. Another polyketide or polyketides contribute to PstA differentiation
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