Marchantia TCP transcription factor activity correlates with three-dimensional chromatin structure

Information in the genome is not only encoded within sequence or epigenetic modifications, but is also found in how it folds in three-dimensional space. The formation of self-interacting genomic regions, named topologically associated domains (TADs), is known as a key feature of genome organization beyond the nucleosomal level. However, our understanding of the formation and function of TADs in plants is extremely limited. Here we show that the genome of Marchantia polymorpha, a member of a basal land plant lineage, exhibits TADs with epigenetic features similar to those of higher plants. By analysing various epigenetic marks across Marchantia TADs, we find that these regions generally represent interstitial heterochromatin and their borders are enriched with Marchantia transcription factor TCP1. We also identify a type of TAD that we name 'TCP1-rich TAD', in which genomic regions are highly accessible and are densely bound by TCP1 proteins. Transcription of TCP1 target genes differs on the basis gene location, and those in TCP1-rich TADs clearly show a lower expression level. In tcp1 mutant lines, neither TCP1-bound TAD borders nor TCP1-rich TADs display drastically altered chromatin organization patterns, suggesting that, in Marchantia, TCP1 is dispensable for TAD formation. However, we find that in tcp1 mutants, genes residing in TCP1-rich TADs have a greater extent of expression fold change as opposed to genes that do not belong to these TADs. Our results suggest that, besides standing as spatial chromatin-packing modules, plant TADs function as nuclear microcompartments associated with transcription factor activities.