Folding Features and Dynamics of 3D Genome Architecture in Plant Fungal Pathogens

ABSTRACT The folding and dynamics of three-dimensional (3D) genome organization are fundamental for eukaryotes executing genome functions but have been largely unexplored in nonmodel fungi. Using high-throughput sequencing coupled with chromosome conformation capture (Hi-C) data, we generated two chromosome-level assemblies for Puccinia striiformis f. sp. tritici, a fungus causing stripe rust disease on wheat, for studying 3D genome architectures of plant pathogenic fungi. The chromatin organization of the fungus followed a combination of the fractal globule model and the equilibrium globule model. Surprisingly, chromosome compartmentalization was not detected. Dynamics of 3D genome organization during two developmental stages of P. striiformis f. sp. tritici indicated that regulation of gene activities might be independent of the changes of genome organization. In addition, chromatin conformation conservation was found to be independent of genome sequence synteny conservation among different fungi. These results highlighted the distinct folding principles of fungal 3D genomes. Our findings should be an important step toward a holistic understanding of the principles and functions of genome architecture across different eukaryotic kingdoms. IMPORTANCE Previously, our understanding of 3D genome architecture has mainly come from model mammals, insects, and plants. However, the organization and regulatory functions of 3D genomes in fungi are largely unknown. In this study, we comprehensively investigated P. striiformis f. sp. tritici, a plant fungal pathogen, and revealed distinct features of the 3D genome, comparing it with the universal folding feature of 3D genomes in higher eukaryotic organisms. We further suggested that there might be distinct regulatory mechanisms of gene expression that are independent of chromatin organization changes during the developmental stages of this rust fungus. Moreover, we showed that the evolutionary pattern of 3D genomes in this fungus is also different from the cases in mammalian genomes. In addition, the genome assembly pipeline and the generated two chromosome-level genomes will be valuable resources. These results highlighted the unexplored distinct features of 3D genome organization in fungi. Therefore, our study provided complementary knowledge to holistically understand the organization and functions of 3D genomes across different eukaryotes.