Kinetic proofreading of lipochitooligosaccharides determines signal activation of symbiotic plant receptors

Kira Gysel, Mette Laursen, Mikkel B. Thygesen, Damiano Lironi, Zoltán Bozsóki, Christian T. Hjuler, Nicolai N. Maolanon, Jeryl Cheng, Peter K. Bjørk, Maria Vinther, Lene H. Madsen, Henriette Rübsam, Artur Muszyński, Arshia Ghodrati, Parastoo Azadi, John T. Sullivan, Clive W. Ronson, Knud J. Jensen, Mickaël Blaise, Simona RadutoiuJens Stougaard, Kasper R. Andersen*

*Corresponding author for this work

Research output: Contribution to journalJournal articleResearchpeer-review

30 Citations (Scopus)
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Abstract

Plants and animals use cell surface receptors to sense and interpret environmental signals. In legume symbiosis with nitrogen-fixing bacteria, the specific recognition of bacterial lipochitooligosaccharide (LCO) signals by single-pass transmembrane receptor kinases determines compatibility. Here, we determine the structural basis for LCO perception from the crystal structures of two lysin motif receptor ectodomains and identify a hydrophobic patch in the binding site essential for LCO recognition and symbiotic function. We show that the receptor monitors the composition of the amphiphilic LCO molecules and uses kinetic proofreading to control receptor activation and signaling specificity. We demonstrate engineering of the LCO binding site to fine-tune ligand selectivity and correct binding kinetics required for activation of symbiotic signaling in plants. Finally, the hydrophobic patch is found to be a conserved structural signature in this class of LCO receptors across legumes that can be used for in silico predictions. Our results provide insights into the mechanism of cell-surface receptor activation by kinetic proofreading of ligands and highlight the potential in receptor engineering to capture benefits in plant-microbe interactions.

Original languageEnglish
Article numbere2111031118
JournalProceedings of the National Academy of Sciences of the United States of America
Volume118
Issue number44
Number of pages10
ISSN0027-8424
DOIs
Publication statusPublished - 2021

Bibliographical note

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© 2021 National Academy of Sciences. All rights reserved.

Keywords

  • Kinetic proofreading
  • Legume symbiosis
  • Lipochitooligosaccharide signaling
  • LysM receptors
  • Receptor-ligand interaction

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