Transposon expansion is associated with reorganization of small RNA and DNA methylation landscapes in the morphologically minimal angiosperm Wolffia brasiliensis
Genome expansion in angiosperms is largely driven by transposable element (TE) proliferation, counteracted by epigenetic silencing. To investigate how TE amplification reshapes silencing landscapes, we compared two closely related, clonally propagating duckweeds, the TE-rich Wolffia brasiliensis, for which we report a draft genome assembly, and the TE-poor Spirodela polyrhiza, that share a broadly conserved silencing and methylation machinery. W. brasiliensis displays extensive and recent TE amplification with pervasive TE-gene interspersion, elevated genome-wide CG methylation, and high levels of both 22- and 24-nt siRNAs. Systematic cross-species comparison reveals that per-element silencing rules are conserved between the two duckweeds: TE length predicting siRNA-producing capacity, inverted-repeat-forming TEs as productive PTGS-associated loci, 24-nt siRNA production predicting non-CG methylation, and intragenic constraint on RdDM-associated methylation. What differs is the genome-wide deployment of these rules across dramatically different TE loads and genome architectures: some divergent outcomes, including elevated 24-nt siRNA abundance and pervasive TE-wide CG methylation, scale directly with TE content, whereas others: near-exclusive 22-nt processing of PTGS substrates, gene-proximity-dependent RdDM at intergenic TEs, and a strong correlation between gene body CG methylation and intragenic TE content that is not detectable in S. polyrhiza; require additional W. brasiliensis-specific contributions. These findings position TEs as central determinants of the epigenetic architecture that emerges from plant genome expansion, and reveal previously underappreciated plasticity in conserved silencing pathways. Significance statementComparing closely related duckweeds with contrasting TE loads but conserved silencing machinery, we show that per-element silencing rules are shared between the two species while the genome-wide outcomes those rules produce diverge profoundly with TE amplification and genome architecture. This reframes TE proliferation as a determinant not only of genome size but of the epigenetic architecture that emerges from it, uncovers a Wolffia-specific coupling between intragenic TE content and gene body CG methylation, and reveals unexpected plasticity in small RNA biogenesis pathways.