Three-dimensional genome reorganization enables cytokinin-dependent activation of NODULE INCEPTION during symbiotic nodulation
Abstract
Legumes establish symbiotic interactions with soil-dwelling rhizobial bacteria, leading to the formation of nitrogen-fixing root nodules. This process requires extensive transcriptional reprogramming, which is associated with dynamic changes in DNA methylation and histone modifications. However, the role of three-dimensional (3D) genome architecture in symbiosis remains largely unexplored. Using high-throughput chromosome conformation capture, we reveal that the 3D chromatin landscape undergoes extensive reorganization in nitrogen-fixing symbiotic nodules compared with non-symbiotic roots and non-nitrogen-fixing nodules. These changes involve alterations in A/B compartmentalization and the establishment of enhancer-promoter loops linked to the symbiotic program. Strikingly, we identified a long-range chromatin loop that connects a 15-kb distal enhancer to the proximal promoter of the NODULE INCEPTION (NIN) gene, a master regulator of nodulation. This enhancer region contains multiple putative cytokinin (CK)-responsive elements, and CK-dependent induction of NIN in roots is associated with the formation of this enhancer-promoter interaction. Moreover, we demonstrate that the CK-signaling transcription factor RESPONSE REGULATOR B3 (RRB3) binds specifically to this distal enhancer region and contributes to the formation of the enhancer-promoter loop. Altogether, these results uncover a critical role for 3D chromatin reorganization in regulating gene expression during legume-rhizobium symbiosis and highlight a regulatory mechanism through which hormonal signaling shapes genome architecture and modulates NIN activation via long-range chromatin looping.
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BibTeX
@article{fonounifarde2026threedimensional,
title = {{Three-dimensional genome reorganization enables cytokinin-dependent activation of NODULE INCEPTION during symbiotic nodulation}},
author = {Camille Fonouni-Farde and Xing Ma and Francisco Sánchez-Rodríguez and David Latrasse and Rim Brik-Chaouche and Lucía Ferrero and Naïs Daviddi and Xiaoning He and Qingyi Wang and Mathias Brault and Sovanna Tan and Carole Laffont and Yonghua Tian and Charlotte Clappe and Xiaoyu Ma and Christine Lelandais and Federico Ariel and Martin Crespi and Moussa Benhamed and Florian Frugier},
journal = {Plant Communications},
year = {2026},
month = jul,
doi = {10.1016/j.xplc.2026.101986},
url = {https://hal.science/hal-05771822v1},
note = {CC BY 4.0},
}
RIS
TY - JOUR
TI - Three-dimensional genome reorganization enables cytokinin-dependent activation of NODULE INCEPTION during symbiotic nodulation
AU - Camille Fonouni-Farde
AU - Xing Ma
AU - Francisco Sánchez-Rodríguez
AU - David Latrasse
AU - Rim Brik-Chaouche
AU - Lucía Ferrero
AU - Naïs Daviddi
AU - Xiaoning He
AU - Qingyi Wang
AU - Mathias Brault
AU - Sovanna Tan
AU - Carole Laffont
AU - Yonghua Tian
AU - Charlotte Clappe
AU - Xiaoyu Ma
AU - Christine Lelandais
AU - Federico Ariel
AU - Martin Crespi
AU - Moussa Benhamed
AU - Florian Frugier
PY - 2026
DA - 2026/07/01
JO - Plant Communications
DO - 10.1016/j.xplc.2026.101986
UR - https://hal.science/hal-05771822v1
AB - Legumes establish symbiotic interactions with soil-dwelling rhizobial bacteria, leading to the formation of nitrogen-fixing root nodules. This process requires extensive transcriptional reprogramming, which is associated with dynamic changes in DNA methylation and histone modifications. However, the role of three-dimensional (3D) genome architecture in symbiosis remains largely unexplored. Using high-throughput chromosome conformation capture, we reveal that the 3D chromatin landscape undergoes extensive reorganization in nitrogen-fixing symbiotic nodules compared with non-symbiotic roots and non-nitrogen-fixing nodules. These changes involve alterations in A/B compartmentalization and the establishment of enhancer-promoter loops linked to the symbiotic program. Strikingly, we identified a long-range chromatin loop that connects a 15-kb distal enhancer to the proximal promoter of the NODULE INCEPTION (NIN) gene, a master regulator of nodulation. This enhancer region contains multiple putative cytokinin (CK)-responsive elements, and CK-dependent induction of NIN in roots is associated with the formation of this enhancer-promoter interaction. Moreover, we demonstrate that the CK-signaling transcription factor RESPONSE REGULATOR B3 (RRB3) binds specifically to this distal enhancer region and contributes to the formation of the enhancer-promoter loop. Altogether, these results uncover a critical role for 3D chromatin reorganization in regulating gene expression during legume-rhizobium symbiosis and highlight a regulatory mechanism through which hormonal signaling shapes genome architecture and modulates NIN activation via long-range chromatin looping.
SN - 2590-3462
SN - 2590-3462
ER -