The single-cell transcriptome program of nodule development cellular lineages in Medicago truncatula
Wendell J. Pereira,
Jade Boyd,
Daniel Conde,
Paolo M. Triozzi,
Kelly M. Balmant,
Christopher Dervinis,
Henry W. Schmidt,
Carolina Boaventura-Novaes,
Sanhita Chakraborty,
Sara A. Knaack,
Yueyao Gao,
Frank Alexander Feltus,
Sushmita Roy,
Jean-Michel Ané,
Julia Frugoli,
Matias Kirst
Affiliations
Wendell J. Pereira
School of Forest, Fisheries, and Geomatics Sciences, University of Florida, Gainesville, FL 32611, USA
Jade Boyd
School of Forest, Fisheries, and Geomatics Sciences, University of Florida, Gainesville, FL 32611, USA
Daniel Conde
School of Forest, Fisheries, and Geomatics Sciences, University of Florida, Gainesville, FL 32611, USA; Centro de Biotecnología y Genómica de Plantas, Universidad Politécnica de Madrid – Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria, 28223 Madrid, Spain
Paolo M. Triozzi
School of Forest, Fisheries, and Geomatics Sciences, University of Florida, Gainesville, FL 32611, USA; PlantLab, Center of Plant Sciences, Sant’Anna School of Advanced Studies, 56010 Pisa, Italy
Kelly M. Balmant
School of Forest, Fisheries, and Geomatics Sciences, University of Florida, Gainesville, FL 32611, USA; Horticultural Sciences Department, University of Florida, Gainesville, FL 32611, USA
Christopher Dervinis
School of Forest, Fisheries, and Geomatics Sciences, University of Florida, Gainesville, FL 32611, USA
Henry W. Schmidt
School of Forest, Fisheries, and Geomatics Sciences, University of Florida, Gainesville, FL 32611, USA
Carolina Boaventura-Novaes
School of Forest, Fisheries, and Geomatics Sciences, University of Florida, Gainesville, FL 32611, USA
Sanhita Chakraborty
Department of Bacteriology, University of Wisconsin – Madison, Madison, WI 53706, USA
Sara A. Knaack
Wisconsin Institute for Discovery, University of Wisconsin, Madison, WI 53715, USA
Yueyao Gao
Department of Genetics & Biochemistry, Clemson University, Clemson, SC 29634, USA; Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA
Frank Alexander Feltus
Department of Genetics & Biochemistry, Clemson University, Clemson, SC 29634, USA; Biomedical Data Science and Informatics Program, Clemson University, Clemson, SC, USA; Clemson Center for Human Genetics, Clemson University, Greenwood, SC 29646, USA
Sushmita Roy
Wisconsin Institute for Discovery, University of Wisconsin, Madison, WI 53715, USA; Department of Biostatistics and Medical Informatics, University of Wisconsin, Madison, WI 53726, USA; Department of Computer Sciences, University of Wisconsin, Madison, WI 53706, USA
Jean-Michel Ané
Department of Bacteriology, University of Wisconsin – Madison, Madison, WI 53706, USA
Julia Frugoli
Department of Genetics & Biochemistry, Clemson University, Clemson, SC 29634, USA
Matias Kirst
School of Forest, Fisheries, and Geomatics Sciences, University of Florida, Gainesville, FL 32611, USA; Corresponding author
Summary: Legumes establish a symbiotic relationship with nitrogen-fixing rhizobia by developing nodules. Nodules are modified lateral roots that undergo changes in their cellular development in response to bacteria, but the transcriptional reprogramming that occurs in these root cells remains largely uncharacterized. Here, we describe the cell-type-specific transcriptome response of Medicago truncatula roots to rhizobia during early nodule development in the wild-type genotype Jemalong A17, complemented with a hypernodulating mutant (sunn-4) to expand the cell population responding to infection and subsequent biological inferences. The analysis identifies epidermal root hair and stele sub-cell types associated with a symbiotic response to infection and regulation of nodule proliferation. Trajectory inference shows cortex-derived cell lineages differentiating to form the nodule primordia and, posteriorly, its meristem, while modulating the regulation of phytohormone-related genes. Gene regulatory analysis of the cell transcriptomes identifies new regulators of nodulation, including STYLISH 4, for which the function is validated.
