Coevolutionary interactions between transposable elements and host silencing factors in genome gigantism of...

Caelifera (Insecta: Orthoptera) exhibits remarkable genome size variation (0.97-21.48 Gb), primarily driven by massive expansions of transposable elements (TEs), which contribute to genomic gigantism. Although TE insertions can enhance genome plasticity, they are generally deleterious, leading to a continuous coevolutionary arms race with host silencing mechanisms. Here, we analyzed the genomes of ten Caelifera species (0.97-9.08 Gb) and found that significant genome expansion in Acridoidea coincides with multiple waves of TE bursts and a slow rate of TE loss. In species with gigantized genomes, we observed a rapid reduction in the number of C2H2-ZNF domains (KRAB-ZFPs host silencing factors) accompanied by shifts in amino acid preferences at TE-targeting positions. For the PIWI-clade evolution, small genomes were subjected to stronger purifying selection compared to gigantized genomes. Notably, in gigantized genomes, extensive TE insertions resulted in ultra-long introns (> 200 kb) in PIWI-clade genes, with significantly reduced transcript abundance, which may represent a mechanism for TE anti-silencing. Moreover, Ago3 mRNA elongation in gigantized genomes (primarily 3' UTR-expansion driven) coincides with reduced transcript abundance. Importantly, the ping-pong cycle results in a simultaneous increase in both retrotransposon transcript abundance and piRNA abundance during genome gigantism. However, the increased piRNA abundance may not be sufficient to silence a larger proportion of retrotransposons, leading to a lower retrotransposon silencing ratio and a higher number of active retrotransposons. These results advance our understanding of how TE-host silencing coevolution shapes genome expansion and maintains genomic stability in gigantized genomes.