Three-Dimensional Genome Architecture of Pathogenic Oomycete Provides Insights into Chromatin Architecture and Regulatory Complexity

Chromosomes are folded hierarchically into compartments, domains, and chromatin loops within the three-dimensional (3D) nuclear space. Despite their relevance for agriculture, little is known about the 3D genome architecture of the plant pathogenic oomycetes and their potential influence on gene regulation and pathogenicity. To address this, we generated a chromosome-scale reference genome and elucidated the 3D genome organization of the multi-host phytopathogenic oomycete Phytophthora capsici for the first time. The P. capsici genome has 17 chromosomes with Rabl configuration, with non-random inter-chromosomal interactions. Each chromosome separates into a core, gene-rich, transcriptionally active ‘A’ compartment and a repeat-rich, pathogenic ‘B’ compartment with a higher evolutionary rate. Topologically associated domains (TADs) are prominent with transcriptionally active, gene-rich boundaries that coincide with accessible open chromatin regions. Genes within each TAD exhibit stage-specific co-expression, indicating these motifs serve as functional regulatory units. P. capsici harbors chromatin loops similar to those in mammals. However, no CTCF binding sites are present. Instead, a strong over-representation of intergenic zf-C2H2 binding regions at loop anchors, a pattern consistent with observations in microbial eukaryotes, is revealed. Altogether, these findings provide a comprehensive view of the three-dimensional genome architecture of oomycetes, advancing our understanding of the underlying mechanistic insights.