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 mainly determined by proliferation of transposable elements (TEs) whose activity is counteracted by epigenetic silencing mechanisms. However, the diversity in genome size as well as different composition and specificity of silencing components among species suggest a complex interplay during genome evolution. To investigate this relationship, we compare two closely related, clonally propagating duckweed species: Wolffia brasiliensis with a TE-rich genome and TE-poor Spirodela polyrhiza. Despite a similar and conserved epigenetic toolbox, W. brasiliensis is characterized by extensive TE amplification, pervasive TE-gene interspersion, elevated global CG methylation, and high levels of both 22- and 24-nt siRNAs. Pattern, abundance, and origin of small RNAs reveal plasticity in conserved post-transcriptional silencing (PTGS) pathways as well as selective RNA-directed DNA methylation engagement. Strikingly, intragenic TEs frequently produce siRNAs yet fail to acquire stable non-CG methylation, while their presence correlates strongly with the emergence of gene body CG methylation extending beyond TE sequences. These results indicate that structural consequences of TE expansion--length, configuration, and genomic context--can reshape small RNA deployment and methylation landscapes without major alteration of core silencing pathways composition and expression. These findings in duckweeds highlight the central role of TEs in structuring plant (epi-)genomes and illustrate their role for evolution of genome architecture even in predominantly clonally reproducing plants.