Conformational Changes in Three-Dimensional Chromatin Structure in Paulownia fortunei After Phytoplasma Infection

Higher-order chromatin structures play important roles in regulating multiple biological processes such as growth and development as well as biotic and abiotic stress response. However, little is known about three-dimensional chromatin structures in Paulownia or about whole-genome chromatin conformational changes that occur in response to Paulownia witches' broom (PaWB) disease. We used high-throughput chromosome conformation capture (Hi-C) to obtain genome-wide profiles of chromatin conformation in both healthy and phytoplasma-infected Paulownia fortunei genome. The heat map results indicated that the strongest interactions between chromosomes were in the telomeres. We confirmed that the main structural characteristics of A/B compartments, topologically associated domains, and chromatin loops were prominent in the Paulownia genome and were clearly altered in phytoplasma-infected plants. By combining chromatin immunoprecipitation sequencing, Hi-C signals, and RNA sequencing data, we inferred that the chromatin structure changed and the modification levels of three histones (H3K4me3/K9ac/K36me3) increased in phytoplasma-infected P. fortunei, which was associated with changes of transcriptional activity. We concluded that for epigenetic modifications, transcriptional activity might function in combination to shape chromatin packing in healthy and phytoplasm-infected Paulownia. Finally, 11 genes (e.g., RPN6, Sec61 subunit-a) that were commonly located at specific topologically associated domain boundaries, A/B compartment switching and specific loops, and had been associated with histone marks were identified and considered as closely related to PaWB stress. Our results provide new insights into the nexus between gene regulation and chromatin conformational alterations in nonmodel plants upon phytopathogen infection and plant disease resistance.

Automated summary

This study investigated the chromatin structure and its changes in Paulownia under phytoplasma infection using Hi-C technology. The strongest interactions between chromosomes were found in the telomeres. Combined analysis of other data indicated that the chromatin structure changed and the modification levels of certain histones increased in phytoplasma-infected Paulownia. Additionally, several genes associated with phytoplasma stress were identified.