Graduation Year

2021

Document Type

Dissertation

Degree

Ph.D.

Degree Name

Doctor of Philosophy (Ph.D.)

Degree Granting Department

Biology (Integrative Biology)

Major Professor

Christina L. Richards, Ph.D.

Committee Member

Kathleen M. Scott, Ph.D.

Committee Member

David B. Lewis, Ph.D.

Committee Member

A. Randall Hughes, Ph.D.

Keywords

salt marsh, epigenomics, foundation species, gene expression, non-genetic inheritance, plant-fungal interactions, mangrove

Abstract

I was born and raised in rural Florida on a tributary of the Withlacoochee River. “Withlacoochee” comes from a series of Muscogee Creek words that together mean “big little water,” possibly owing to the seasonal fluctuations in the breadth and flow of the river or to the chain of lakes that in part form it. The name contains within it an understanding of the capacity of land and water to undergo great shifts. It conjures images of mutable boundaries, of water covering and receding across the landscape over and over again. Many of my clearest memories from childhood are related to observing and interacting with the expansive natural world around me: dissecting a cottonmouth with my dad on the dining room table; watching gopher tortoises hatch from their eggs and tumble out of their sandy nest behind my Mama Jean’s double-wide trailer; seeing a hawk catch a siren in the backyard creek and eat it on a nearby fence post; the El Niño that brought the freshwater ‘jubilee,’ a rare phenomenon that results in the congregation of thousands of fish, amphibians, crayfish, turtles, and other aquatic organisms, to our backdoor. As I collected the names of each animal I encountered, my favorite books became field guides, and I would pore over them for hours memorizing the shapes and colors that made each species distinct. It was, I think, driven not just by fascination, but by a kind of deep familial love for the incredible biodiversity that inhabits Earth and the joy it brought me to be surrounded by it.

As I grew into young adulthood, I was sensitive to the changes I saw in the world around me. The cyclical fluctuations of the ecosystems I knew so well were becoming increasingly unpredictable and the effects of resource overconsumption were coming increasingly into focus—from climate change to chemical spills to habitat loss to the spread of invasive species. I watched thousands of acres of longleaf pine forests and scrub get ground up and converted into expanses of sterile stucco suburban homes. To my horror, blissful summers spent snorkeling and diving the Florida Reef Tract entranced by this ‘rainforest of the sea’ transformed into bearing witness to its swift collapse from a combination of overfishing, disease linked to sewage effluents, and the impacts of climate change-related ocean acidification and warming sea surface temperatures. I spent a year with AmeriCorps removing acres of invasive exotic plants from Florida State Parks, then moved to New Orleans just in time to volunteer with the Audubon Society transporting seabirds injured by the Deepwater Horizon disaster to Louisiana State University’s School of Veterinary Medicine for rehabilitation. It became impossible to ignore the scale of ecological devastation around me. I returned to Florida and re-enrolled in school, determined to devote my life to the field of ecology in the hopes that I might contribute to efforts to understand and protect biodiversity.

During my dissertation work, I learned about the power of incorporating genomics approaches to explore how foundation plants of coastal ecosystems respond to natural environmental challenges. Coastal ecosystems such as mangrove forests and Spartina alterniflora-dominated salt marshes are exceptional systems within which to explore mechanisms of molecular response due in part to the pronounced natural stress conditions these plant species must cope with. These ecosystems are also particularly vulnerable to the effects of anthropogenic activities such as climate change and habitat fragmentation. Evidence has accumulated that shows that molecular mechanisms of organismal response to environmental conditions extend beyond the genome and these nongenetic sources of variation can be heritable. These epigenetic sources of variation may be particularly important for genetically depauperate and non-sexually reproducing plant populations.

I had the great fortune of developing my understanding of the field of ecological epigenetics while becoming part of a network of researchers from around the globe during my dissertation work. These interactions provided new insight into my understanding of the natural world as well as critical training. I was sponsored by the Chateaubriand Fellowship to work with the Aïnouche group in Rennes, France who are among the world’s experts in genomics of complex polyploid plants. While I was in the Aïnouche lab in Rennes, France, I learned valuable skills that enhanced my dissertation work. I was also able to work with the Aïnouche group and other collaborators of an international team associated with the Make Our Planet Great Again project led by my advisor, Christina Richards, to publish a manuscript in Philosophical Transactions of the Royal Society B. We reviewed the literature that applied genomics approaches, specifically focused on understanding how epigenetic mechanisms contribute to the processes of plant invasions (see Appendix 1). This massive literature review provided a rich background for much of my dissertation work.

One of the outstanding questions in ecological epigenetics is whether epigenetic differences can be inherited independently of genetic variation. In chapter one, I used epiGBS to investigate inheritance patterns of DNA methylation between natural maternal and experimental offspring populations of the red mangrove, Rhizophora mangle. This was a good system to investigate the importance of epigenetic differences because previous work reported low genetic diversity and high levels of inbreeding. Still, work done by Master’s student Kristen Langanke showed that differences among maternal families and among populations were the most consistent predictor of putatively adaptive traits like height growth, succulence, leaf mass ratio, root to shoot biomass allocation and total biomass. I found low genetic diversity but high epigenetic diversity in natural maternal populations, and that a considerable portion of epigenetic differences uncovered from offspring populations was explained by maternal family. With this work, I have shown that epigenetic variation could be an important component of diversity in genetically depauperate populations of this species of conservation concern. Epigenetic diversity could be particularly important in mangroves since they face myriad environmental challenges from natural and anthropogenic stressors.

In chapter two, I used the genomics approach of epigenotyping-by-sequencing (epiGBS) to investigate genomic and epigenomic diversity in natural populations of Spartina alterniflora near Charleston, South Carolina to examine how different genetic variants of this foundation salt marsh plant react to environmental variation. The genome of this species is large and complex and unlike in red mangrove, several studies have reported high levels of genetic diversity. In addition, pronounced differences in traits are observed in tandem with a narrow intertidal gradient, but much remains to be understood about environmental conditions that shape this phenotypic variation. My results showed that genomic sequence variation explained most of the variation in DNA methylation; however, this study provided evidence that DNA methylation distinctly contributes to plant responses to environmental variation.

Gene expression variation is also a critical component of plant response and it is known to be influenced by biotic interactions. In chapter three, I used RNA-seq to examine gene expression in experimental populations of S. alterniflora to determine how response to stress may be facilitated by interactions with non-mycorrhizal, root-endophytic marine fungi, Lulworthia spp. I found that gene expression was chiefly explained by population and habitat, but that fungal inoculum treatments explained a small but notable portion of the variation. These endophytes are thought to play a functionally similar role to mycorrhizal fungi by providing plants with increased macronutrients, and thereby potentially mediating the degree of abiotic stress experienced by plants. However, genes that were highly enriched in response to fungi appears to be related to the decomposition of plant lignocellulose, which indicates that this plant-fungal symbiosis may not always be mutualistic

While there are plenty of new questions that arise from my dissertation research, this work contributions to our understanding of how plants respond to environmental challenges and variability at the level of the genome, epigenome, and the transcriptome. The continued application of these methods in ecological contexts could help us better anticipate plant response to climate change, and their further integration into the study of both species of conservation concern and invasive species could provide us with more nuanced understandings of how to successfully manage outcomes for plant populations in rapidly changing ecosystems. I hope to be a part of these future pursuits and solutions.

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