Abstract
Within the last 60 years, the Earth’s atmosphere has experienced a steady and rapid increase in carbon dioxide (CO2) composition. Plants play a critical role in the carbon cycle as primary consumers of CO2 and the foundation of agricultural output. A timely and open question remains regarding how plants will acclimatize to increasing levels of CO2, a rate-limiting substrate in photosynthesis. While genetic traits alone provide robust currency for the selection of advantageous traits, genetic mutations and polymorphisms rarely revert, are slowly acquired, and can bottleneck breeding practices for crop resilience. Land plants are primarily sessile and among the array of multi-cellular organisms that have evolved epigenetic mechanisms to allow for rapid adaptations to occur in the face of turbulent environments. How can cells orchestrate these mechanisms with such sophistication? The interplay between epigenetic traits such as DNA methylation, histone modifications, and the 3D structure of chromatin underlie the plasticity of gene regulation, providing a molecular blueprint for retaining epigenetic "memories" of environmental conditions across generations via epigenetic reprogramming. In this dissertation, I investigate the hierarchical structure of epigenetic reprogramming that underlies the initiation of plant development at elevated CO2. First, I investigate the epigenetic properties of chromatin that re-wire transcription to support a heritable accelerated growth phenotype in Arabidopsis thaliana. Using high-resolution methylation-sensitive Chromatin Conformation Capture and sequencing (Hi-C), I reveal that CO2-dependent chromatin decondensation renders more accessible chromatin closer to the nuclear periphery and implicate interplay between key epigenetic mechanisms such as small RNA-directed DNA Methylation (RdDM), asymmetric maintenance methylation, and histone modifications involved in chromatin remodeling. This decondensation is supported by broad shifts in the genome activity of euchromatin and heterochromatin. At high resolution, I annotate Local Chromatin Domains (LCDs) and LCD Associated Loops (LALs) that connect specific genomic regions to macro-level changes in genome structure and transcriptional reprogramming at impacted loci. I identify trans acting factors that direct the formation of LCDs and LALs through the regulation of 5-methylcytosine (5mC) and H3K27me3 acting in cis. At sub-kilobase resolution, I define the reprogrammed transcriptional profile of wild-type (WT) and mutant plants responding to elevated CO2 and implicate epigenetic modifications such as 5mC and histone tail post-translational modifications, that are important in shaping the 3D structure of the genome, with the initiation of CO2-dependent epigenetic reprogramming. Together, my dissertation work reveals that the interface between epigenetic modifications and the 3D genome is critical for initiating and supporting the developmental program at elevated CO2.
Committee Chair
Blake Meyers
Committee Members
Douglas Chalker; Richard Slotkin; Robert Schmitz; Xuehua Zhong
Degree
Doctor of Philosophy (PhD)
Author's Department
Biology & Biomedical Sciences (Molecular Genetics & Genomics)
Document Type
Dissertation
Date of Award
8-13-2025
Language
English (en)
DOI
https://doi.org/10.7936/gp9w-xk85
Author's ORCID
https://orcid.org/0000-0002-0216-1030
Recommended Citation
Lewis, Scott, "The 3D Genome: Investigating CO2 Driven Chromatin Dynamics and Epigenetic Reprogramming in Arabidopsis thaliana" (2025). Arts & Sciences Theses and Dissertations. 3600.
The definitive version is available at https://doi.org/10.7936/gp9w-xk85