3D Genome Organization in Brown Algae

Abstract

The three-dimensional (3D) organization of the genome plays a crucial role in gene regulation and epigenetic states. In animal genomes, core 3D genome features like topologically associated domains (TADs) and chromatin loops have been extensively characterized, whereas in plants such higher order structures are less pronounced. Beyond animals and plants, however, relatively little is known about the 3D genome organization evolution. This thesis explores the evolution of 3D genome organization in brown algae by comparing species differing in genome size, sexual systems (dioicous and monoicous), and morphological complexity. By substantially improving chromosomal-level assemblies, I demonstrated that brown algal genomes exhibit a high degree of linear conservation relative to the outgroup species, with only moderate rates of interchromosomal rearrangement. Examining interspecies variations in 3D chromatin organization revealed distinct patterns of nuclear architecture in brown algae shaped by evolutionary history. Comparative analysis suggests that 3D genome architecture is broadly conserved over approximately 11 million years of brown algae evolution. Notably, sex chromosomes and sex homologs display divergent interactions profiles distinct from autosomes. Consistent non-Rabl chromosome folding patterns were identified, which enabled the characterization of “centromere interaction clusters” and “telomere interaction clusters”. Identification of the centromeric regions revealed longterm co-evolution with a specific lineage of “centrophilic” LTR retrotransposons, which are uniquely present at the centromeres in most brown algal species and likely constitute the centromeric repeat. This study presents the first comparative analysis of 3D chromatin organization across six phylogenetically diverse brown algal species and one outgroup, offering new insights into 3D genome architecture within the eukaryotic lineage through the integration of high-resolution Hi-C data, gene expression profiling, centromere characterization, and ancestral genome reconstruction.