TOPLESS are tetrameric plant corepressors of the conserved Tup1/Groucho/TLE (transducin-like enhancer of split) family. We show that they interact through their TOPLESS domains (TPDs) with two functionally important ethylene response factor–associated amphiphilic repression (EAR) motifs of the rice strigolactone signaling repressor D53: the universally conserved EAR-3 and the monocot-specific EAR-2.We present the crystal structure of the monocot-specific EAR-2 peptide in complexwith the TOPLESS-related protein 2 (TPR2) TPD, inwhich the EAR-2motif binds the same TPD groove as jasmonate and auxin signaling repressors butmakes additional contacts with a second TPD site tomediate TPD tetramer-tetramer interaction.Wevalidated the functional relevance of the two TPD binding sites in reporter gene assays and in transgenic rice and demonstrate that EAR-2 binding induces TPD oligomerization. Moreover, we demonstrate that the TPD directly binds nucleosomes and the tails of histones H3 and H4. Higher-order assembly of TPD complexes induced by EAR-2 binding markedly stabilizes the nucleosome-TPD interaction. These results establish a newTPD-repressor bindingmode that promotes TPDoligomerization and TPD-nucleosome interaction, thus illustrating the initial assembly of a repressor-corepressor-nucleosome complex.