The three-dimensional genome architecture drives symbiotic nodulation in legumes [DAP]

Among the detected novel chromatin loops, we identified one connecting a 15kb distal region with the proximal promoter of the TF NODULE INCEPTION (NIN), a major regulator of the developmental transition required for symbiosome development and N2-fixation. Interestingly, the NIN gene displays a complex spatiotemporal regulation governed by distinct cis-regulatory sequences including this conserved distal -15 kb region. Furthermore, NIN distal promoter region contains several putative cytokinin (CK) response elements (CE) and we showed that NIN transcriptional induction by CKs likely depends on the formation of an enhancer-promoter loop bringing the -15 kb conserved distal CE element close to the -5 kb proximal promoter region of NIN.

To gain further insight, we showed that NIN transcriptional induction by CKs depends on the TYPE-B RESPONSE REGULATOR 3 (RRB3) TF, which only binds to the distal NIN promoter region. These results suggest that a TF complex involving type-B RRs deposited on NIN distal region controls the formation of a chromatin loop responsible for NIN spatiotemporal regulation and subsequently coordinates nodulation developmental programs.

More generally, the reorganization of the linear genome in this symbiotic plant-bacteria interaction reveals a new regulatory level where cell-cell communication of bacterial symbionts impacts 3D genome organization and transcription reprograming of the host eukaryote.