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

Knaack, Sara A.; Conde, Daniel; Chakraborty, Sanhita; Balmant, Kelly M.; Irving, Thomas B.; Maia, Lucas Silva; Triozzi, Paolo M.; Dervinis, Christopher; Pereira, Wendell J.; Maeda, Junko; Schmidt, Henry W.; Ané, Jean-Michel; Kirst, Matias; Roy, Sushmita

doi:10.1186/s12915-022-01450-9

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

Journal Article · Wed Nov 09 00:00:00 EST 2022 · BMC Biology

DOI:https://doi.org/10.1186/s12915-022-01450-9· OSTI ID:1975673

Knaack, Sara A. ^[1]; Conde, Daniel ^[2]; Chakraborty, Sanhita ^[1]; Balmant, Kelly M. ^[2]; Irving, Thomas B. ^[1]; Maia, Lucas Silva ^[1]; Triozzi, Paolo M. ^[2]; Dervinis, Christopher ^[2]; Pereira, Wendell J. ^[2]; Maeda, Junko ^[1]; Schmidt, Henry W. ^[2]; Ané, Jean-Michel ^[1]; Kirst, Matias ^[2];

^[1]

University of Wisconsin, Madison, WI (United States)
University of Florida, Gainesville, FL (United States)

Symbiotic associations between bacteria and leguminous plants lead to the formation of root nodules that fix nitrogen needed for sustainable agricultural systems. Symbiosis triggers extensive genome and transcriptome remodeling in the plant, yet an integrated understanding of the extent of chromatin changes and transcriptional networks that functionally regulate gene expression associated with symbiosis remains poorly understood. In particular, analyses of early temporal events driving this symbiosis have only captured correlative relationships between regulators and targets at mRNA level. Here, we characterize changes in transcriptome and chromatin accessibility in the model legume Medicago truncatula, in response to rhizobial signals that trigger the formation of root nodules. We profiled the temporal chromatin accessibility (ATAC-seq) and transcriptome (RNA-seq) dynamics of M. truncatula roots treated with bacterial small molecules called lipo-chitooligosaccharides that trigger host symbiotic pathways of nodule development. Using a novel approach, dynamic regulatory module networks, we integrated ATAC-seq and RNA-seq time courses to predict cis-regulatory elements and transcription factors that most significantly contribute to transcriptomic changes associated with symbiosis. 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. Our transcriptomic and chromatin accessibility datasets provide a valuable resource to understand the gene regulatory programs controlling the early stages of the dynamic process of symbiosis. The regulators identified provide potential targets for future experimental validation, and the engineering of nodulation in species is unable to establish that symbiosis naturally.

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Research Organization:: Univ. of Florida, Gainesville, FL (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: SC0018247

OSTI ID:: 1975673

Journal Information:: BMC Biology, Vol. 20, Issue 1; Related Information: Data is deposited in NCBI/GEO under accession GSE154845; ISSN 1741-7007

Publisher:: BioMed CentralCopyright Statement

Country of Publication:: United States

Language:: English

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59 BASIC BIOLOGICAL SCIENCES
Nitrogen fixation
Nodulation
Symbiosis
Chromatin accessibility
Transcriptome and chromatin dynamics
Gene regulatory network
Cis-regulatory elements
Machine learning
Medicago

Additional file 1 of Temporal change in chromatin accessibility predicts regulators of nodulation in Medicago truncatula Knaack, Sara A.; Conde, Daniel; Chakraborty, Sanhita https://doi.org/10.6084/m9.figshare.21532836 The current record is supplemented by this text	text	January 2022
Additional file 2 of Temporal change in chromatin accessibility predicts regulators of nodulation in Medicago truncatula Knaack, Sara A.; Conde, Daniel; Chakraborty, Sanhita https://doi.org/10.6084/m9.figshare.21532839 The current record is supplemented by this dataset	dataset	January 2022

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

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