Transposon Dynamics Drive Genome Evolution and Regulate Genetic Mechanisms of Agronomic Traits in Cotton

Transposable elements (TEs) serve as important drivers mediating polyploidization events and phenotypic diversification in plant genomes. However, the dynamic changes in various TE subclasses post-polyploidization and their mechanisms of influencing phenotypic variation require further investigation. The allopolyploid <i>Gossypium</i> species, originating from two diploid progenitors, provide an ideal model for studying TE dynamics following polyploidization. This study investigated TE dynamics post-polyploidization based on 21 diploid and 7 polyploid cotton genomes. The Tekay subclass of the Gypsy serves as a major driver of <i>Gossypium</i> genome evolution, as it underwent two burst events in the At-subgenome and its progenitor, exhibiting the highest abundance, longest length, and largest proportion among all TE subclasses. In contrast, the Gopia superfamily Tork subclass has lower abundance but greater genic association, facilitating environmental adaptation and phenotypic variation. Additionally, a pan-TE-related structural variation, the pan-TRV map, was constructed by integrating resequencing data from 256 accessions. Genome-wide analysis of 28 cotton genomes identified 142,802 TRVs, among which 72,116 showed polymorphisms in the 256 <i>G. hirsutum</i> accessions. The Gypsy superfamily, particularly the Tekay subclass, has been identified as a major source of TRVs, while Copia-type elements demonstrate significantly greater enrichment in gene-proximal genomic regions. A total of 334 TRVs exhibiting statistically significant associations with 10 key phenotypic traits, including 164 TRVs affecting yield components and 170 TRVs determining fiber quality. This investigation delineates the evolutionary significance of transposable elements in <i>Gossypium</i> genome diversification while simultaneously providing novel functional markers and potential editing targets for genetic dissection and molecular breeding of key agronomic traits in cotton.