Shifts in evolutionary lability underlie independent gains and losses of root-nodule symbiosis in a single clade of plants

Heather R. Kates (), Brian C. O’Meara, Raphael LaFrance, Gregory W. Stull, Euan K. James, Shui-Yin Liu, Qin Tian, Ting-Shuang Yi, Daniel Conde, Matias Kirst, Jean-Michel Ané, Douglas E. Soltis, Robert P. Guralnick, Pamela S. Soltis and Ryan A. Folk ()
Additional contact information
Heather R. Kates: University of Florida
Brian C. O’Meara: University of Tennessee
Raphael LaFrance: University of Florida
Gregory W. Stull: Chinese Academy of Sciences
Euan K. James: The James Hutton Institute
Shui-Yin Liu: Chinese Academy of Sciences
Qin Tian: Chinese Academy of Sciences
Ting-Shuang Yi: Chinese Academy of Sciences
Daniel Conde: Universidad Politécnica de Madrid (UPM)-Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA-CSIC), Campus de Montegancedo, Pozuelo de Alarcón
Matias Kirst: University of Florida
Jean-Michel Ané: University of Wisconsin-Madison
Douglas E. Soltis: University of Florida
Robert P. Guralnick: University of Florida
Pamela S. Soltis: University of Florida
Ryan A. Folk: Mississippi State University

Nature Communications, 2024, vol. 15, issue 1, 1-11

Abstract: Abstract Root nodule symbiosis (RNS) is a complex trait that enables plants to access atmospheric nitrogen converted into usable forms through a mutualistic relationship with soil bacteria. Pinpointing the evolutionary origins of RNS is critical for understanding its genetic basis, but building this evolutionary context is complicated by data limitations and the intermittent presence of RNS in a single clade of ca. 30,000 species of flowering plants, i.e., the nitrogen-fixing clade (NFC). We developed the most extensive de novo phylogeny for the NFC and an RNS trait database to reconstruct the evolution of RNS. Our analysis identifies evolutionary rate heterogeneity associated with a two-step process: An ancestral precursor state transitioned to a more labile state from which RNS was rapidly gained at multiple points in the NFC. We illustrate how a two-step process could explain multiple independent gains and losses of RNS, contrary to recent hypotheses suggesting one gain and numerous losses, and suggest a broader phylogenetic and genetic scope may be required for genome-phenome mapping.

Date: 2024
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DOI: 10.1038/s41467-024-48036-3

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