Folding features and dynamics of 3D genome architecture in plant fungal pathogens

Authors: XIA, CHONGJING - Institute Of Plant Protection - China; HUANG, LIANG - Institute Of Plant Protection - China; HUANG, JIE - Institute Of Plant Protection - China; ZHANG, HAO - Southwest University Of Science And Technology; HUANG, YING - University Of Paris; BENHAMED, MOUSSA - University Of Paris; WANG, MEINAN - Washington State University; Chen, Xianming; ZHANG, MIN - Sichuan Agricultural University; LIU, TAIGUO - Institute Of Plant Protection - China; CHEN, WANQUAN - Institute Of Plant Protection - China

Submitted to: Genome Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/18/2022
Publication Date: 10/17/2022
Citation: Xia, C., Huang, L., Huang, J., Zhang, H., Huang, Y., Benhamed, M., Wang, M., Chen, X., Zhang, M., Liu, T., Chen, W. 2022. Folding features and dynamics of 3D genome architecture in plant fungal pathogens. Genome Biology. 10(6). Article 02608-22. https://doi.org/10.1128/spectrum.02608-22.
DOI: https://doi.org/10.1128/spectrum.02608-22

Interpretive Summary: Folding and dynamics of three-dimensional (3D) genome organization are fundamental for eukaryotes executing genome functions, but have largely unexplored in non-model fungi. Here, we generate two chromosome-level assemblies for the wheat stripe rust fungus, using the Hi-C data for studying 3D genome architectures of plant pathogenic fungi. We observed the clustering of centromeres and telomeres on opposite sides of the nucleus for all plant pathogenic fungi examined in this study, in line with the canonical 'Rable' conformation in model fungi. Moreover, the chromatin organization of fungi followed a combination of the fractal globule model in short genomic distance and the equilibrium globule model in large distance. Surprisedly, chromosome compartmentalization was not detected in the examined plant fungal pathogens, suggesting distinct folding mechanisms of these fungi. We further analyzed the dynamics of 3D genome organization during two developmental stages of the stripe rust fungus, and the results indicated that regulation of gene activities might be independent of the changes of genome organization. In addition, comparison of genome organizations among fungal species indicated chromatin conformation conservation is independent of genome sequence synteny conservation in fungi. Our findings of the distinct features of 3D genome organization in plant pathogenic fungi will be an important step toward a comprehensive understanding of the principles of genome architecture and function in all eukaryotic kingdoms.

Technical Abstract: Background: Folding and dynamics of three-dimensional (3D) genome organization are fundamental for eukaryotes executing genome functions, but have largely unexplored in non-model fungi. Results: Here, we generate two chromosome-level assemblies for Puccinia striiformis f. sp. tritici (Pst), a fungus causing stripe rust disease on wheat, using the Hi-C data for studying 3D genome architectures of plant pathogenic fungi. We observed the clustering of centromeres and telomeres on opposite sides of the nucleus for all plant pathogenic fungi examined in this study, in line with the canonical 'Rable' conformation in model fungi. Moreover, the chromatin organization of fungi followed a combination of the fractal globule model in short genomic distance and the equilibrium globule model in large distance. Surprisedly, chromosome compartmentalization was not detected in the examined plant fungal pathogens, suggesting distinct folding mechanisms of these fungi. We further analyzed the dynamics of 3D genome organization during two developmental stages of Pst, and the results indicated that regulation of gene activities might be independent of the changes of genome organization. In addition, comparison of genome organizations among fungal species indicated chromatin conformation conservation is independent of genome sequence synteny conservation in fungi. Conclusions: Our findings of the distinct features of 3D genome organization in plant pathogenic fungi will be an important step toward a comprehensive understanding of the principles of genome architecture and function in all eukaryotic kingdoms.