Kinetic proofreading of lipochitooligosaccharides determines signal activation of symbiotic plant receptors
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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.
| Originalsprog | Engelsk |
|---|---|
| Artikelnummer | e2111031118 |
| Tidsskrift | Proceedings of the National Academy of Sciences of the United States of America |
| Vol/bind | 118 |
| Udgave nummer | 44 |
| Antal sider | 10 |
| ISSN | 0027-8424 |
| DOI | |
| Status | Udgivet - 2021 |
Bibliografisk note
Funding Information:
We thank Theis Brock-Nannestad and Kasper K. S?rensen for HR-MS data, Ola Blixt and Simon B. Hansen for helpful discussions, Angelique Jakobsen and Lene Krusell for the full-length NFP receptor expression construct, and Leila Kathleen Walker for manuscript editing. We thankMarjolein Thunnissen, Thomas Ursby, and Jie Nan for beamline support during synchrotron data collection at beamlines I911-3 (MAX-lab II) and Bio- MAX at the MAX IV Laboratory and Cy Jeffries for the assistance during synchrotron SAXS data collection at beamline P12 operated by EMBL Hamburg at the PETRA III storage ring (Deutsches Elektronen-Synchrotron). This work was funded by the project Engineering Nitrogen Symbiosis for Africa currently supported through a grant to the University of Cambridge by the Bill and Melinda Gates Foundation and the UK Government's Department for International Development and the Danish National Research Foundation (DNRF79) and in part by the US Department of Energy grant (Grant No. DE-SC0015662).
Funding Information:
ACKNOWLEDGMENTS. We thank Theis Brock-Nannestad and Kasper K. Sørensen for HR-MS data, Ola Blixt and Simon B. Hansen for helpful discussions, Angelique Jakobsen and Lene Krusell for the full-length NFP receptor expression construct, and Leila Kathleen Walker for manuscript editing. We thank Marjolein Thunnissen, Thomas Ursby, and Jie Nan for beamline support during synchrotron data collection at beamlines I911-3 (MAX-lab II) and Bio-MAX at the MAX IV Laboratory and Cy Jeffries for the assistance during synchrotron SAXS data collection at beamline P12 operated by EMBL Hamburg at the PETRA III storage ring (Deutsches Elektronen-Synchrotron). This work was funded by the project Engineering Nitrogen Symbiosis for Africa currently supported through a grant to the University of Cambridge by the Bill and Melinda Gates Foundation and the UK Government’s Department for International Development and the Danish National Research Foundation (DNRF79) and in part by the US Department of Energy grant (Grant No. DE-SC0015662).
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