Comparative Genome Analyses Highlight Transposon-Mediated Genome Expansion and the Evolutionary Architecture of 3D Genomic Folding in Cotton

Transposable element (TE) amplification has been recognized as a driving force mediating genome size expansion and evolution, but the consequences for shaping 3D genomic architecture remains largely unknown in plants. Here, we report reference-grade genome assemblies for three species of cotton ranging 3-fold in genome size, namely Gossypium rotundifolium (K-2), G. arboreum (A(2)), and G. raimondii (D-5), using Oxford Nanopore Technologies. Comparative genome analyses document the details of lineage-specific TE amplification contributing to the large genome size differences (K-2, 2.44 Gb; A(2), 1.62 Gb; D-5, 750.19 Mb) and indicate relatively conserved gene content and synteny relationships among genomes. We found that approximately 17% of syntenic genes exhibit chromatin status change between active (A) and inactive (B) compartments, and TE amplification was associated with the increase of the proportion of A compartment in gene regions (similar to 7,000 genes) in K-2 and A(2) relative to D-5. Only 42% of topologically associating domain (TAD) boundaries were conserved among the three genomes. Our data implicate recent amplification of TEs following the formation of lineage-specific TAD boundaries. This study sheds light on the role of transposon-mediated genome expansion in the evolution of higher-order chromatin structure in plants.

Automated summary

Transposable element (TE) amplification plays a crucial role in mediating genome size expansion and evolution, with lineage-specific TE amplification contributing to large genome size differences in cotton species. The study also reveals changes in chromatin status in gene regions due to TE amplification and highlights the recent amplification of TEs affecting the formation of lineage-specific TAD boundaries in plants.