Temporal change in chromatin accessibility predicts regulators of nodulation in Medicago truncatula

Abstract

Rhizobia can establish symbiotic associations with legumes to provide plants with nitrogen needed in agricultural systems. Symbiosis triggers extensive genome and transcriptome remodeling in the plant, yet the extent of chromatin changes and impact on gene expression is unknown. We profiled the temporal chromatin accessibility (ATAC-seq) and transcriptome (RNA-seq) dynamics of M. truncatula roots treated with rhizobia lipo-chitooligosaccharides. Using a novel approach, Dynamic Regulatory Module Networks, we predicted gene expression as a function of chromatin accessibility and accessible cis-regulatory elements. This approach identified the cis-regulatory elements and associated transcription factors that most significantly contribute to transcriptomic changes triggered by lipo-chitooligosaccharides. Regulators involved in auxin (IAA4-5,SHY2), ethylene (EIN3, ERF1) and abscisic acid (ABI5) hormone response, as well as histone and DNA methylation (IBM1), emerged among those most predictive of transcriptome dynamics. RNAi-based knockdown of EIN3 and ERF1 reduced nodule number in M. truncatula validating the role of these predicted regulators in symbiosis between legumes and rhizobia. Significance StatementLegumes can fix nitrogen through symbiosis with rhizobia in root nodules, a critical mutualistic relationship for crop productivity and agricultural sustainability. Introducing this symbiotic relationship into non-legume crops is of great interest, but limited knowledge of host genome modifications induced by rhizobia has hampered such efforts. We applied time-course analysis of chromatin accessibility and gene expression of M. truncatula roots treated with rhizobia lipochitooligosaccharides. We show that extensive remodeling of genome accessibility drives a large component of the temporal transcriptome dynamics. By predicting gene expression as a function of accessibility of regulatory features, we identified known and novel regulators that are associated with early nodule development, which may be critical for its engineering into crops.