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Plant Carnivory and the Evolution of Novelty in Sarracenia alata

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2018, Doctor of Philosophy, Ohio State University, Evolution, Ecology and Organismal Biology.
Most broadly, this study aimed to develop a better understanding of how organisms evolve novel functions and traits, and examine how seemingly complex adaptive trait syndromes can convergently evolve. As an ideal example of this, the carnivorous plants were chosen. This polyphyletic grouping contains taxa derived from multiple independent evolutionary origins, in at least five plant orders, and has resulted in striking convergence of niche and morphology. First, a database study was performed, with the goal of understanding the evolutionary trends that impact carnivorous plants as a whole. Using carnivorous and non-carnivorous plant genomes available from GenBank. An a priori list of Gene Ontology-coded functions implicated in plant carnivory by earlier studies was constructed via literature review. Experimental and control samples were tested for statistical overrepresentation of these functions. It was found that, while some functions were significant in some taxa, there was no overall shared signal of plant carnivory, with each taxon presumably having selected for a different subset of these functions. Next, analyses were performed that targeted Sarracenia alata specifically. A reference genome for S. alata was assembled using PacBio, Illumina, and BioNano data and annotated using MAKER-P with additional preliminary database filtration. From these, it was found that Sarracenia alata possesses significant and substantial overrepresentation of genes with functions associated with plant carnivory, at odds with the hypothesis that the plant primarily relies on symbioses. Finally, pitcher fluid was collected from S. alata in the field. RNA was extracted from the fluid, sequenced via Illumina, and assembled with Trinity. Sequences were sorted into host plant and microbiome based on BLAST match to the S. alata reference genome. It was found that, while S. alata contributes two-thirds of the transcripts, these encode no digestive enzymes and a very limited set of transport channel proteins; however, these functions were identified in microbe-originated transcripts. A large portion of S. alata’s transcripts were instead found to encode anti-microbial peptides (AMPs). These short proteins are known to play a role in modulating gut microflora in animals, and while they are documented in plants, their role had never been addressed in carnivorous plants. From these findings, I have concluded that there are a large number of evolutionary paths that lead to highly similar adaptive strategies; specific relevant functions may be identified, but the subset of these used by a given lineage will vary greatly. In Sarracenia alata specifically, it appears that at one point in time there was strong selection favoring the retention of genes associated with prey digestion. However, at present these do not appear to be expressed, with microbial symbioses instead responsible for the bulk of the digestive process. Instead, the plant has likely evolved to specialize in a regulatory role, modulating the microbial composition of its fluid via the production of AMPs. This shows that not only do lineages evolve via different pathways, but that the same lineage may change its adaptive specialization at different points in its history.
Bryan Carstens, Ph.D. (Advisor)
Marymegan Daly, Ph.D. (Committee Member)
Zakee Sabree, Ph.D. (Committee Member)
Andrea Wolfe, Ph.D. (Committee Member)
148 p.

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Citations

  • Wheeler, G. L. (2018). Plant Carnivory and the Evolution of Novelty in Sarracenia alata [Doctoral dissertation, Ohio State University]. OhioLINK Electronic Theses and Dissertations Center. http://rave.ohiolink.edu/etdc/view?acc_num=osu1531948732481904

    APA Style (7th edition)

  • Wheeler, Gregory. Plant Carnivory and the Evolution of Novelty in Sarracenia alata. 2018. Ohio State University, Doctoral dissertation. OhioLINK Electronic Theses and Dissertations Center, http://rave.ohiolink.edu/etdc/view?acc_num=osu1531948732481904.

    MLA Style (8th edition)

  • Wheeler, Gregory. "Plant Carnivory and the Evolution of Novelty in Sarracenia alata." Doctoral dissertation, Ohio State University, 2018. http://rave.ohiolink.edu/etdc/view?acc_num=osu1531948732481904

    Chicago Manual of Style (17th edition)