Kinetic proofreading of lipochitooligosaccharides determines signal activation of symbiotic plant receptors
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Kinetic proofreading of lipochitooligosaccharides determines signal activation of symbiotic plant receptors. / Gysel, Kira; Laursen, Mette; Thygesen, Mikkel B.; Lironi, Damiano; Bozsóki, Zoltán; Hjuler, Christian T.; Maolanon, Nicolai N.; Cheng, Jeryl; Bjørk, Peter K.; Vinther, Maria; Madsen, Lene H.; Rübsam, Henriette; Muszyński, Artur; Ghodrati, Arshia; Azadi, Parastoo; Sullivan, John T.; Ronson, Clive W.; Jensen, Knud J.; Blaise, Mickaël; Radutoiu, Simona; Stougaard, Jens; Andersen, Kasper R.
I: Proceedings of the National Academy of Sciences of the United States of America, Bind 118, Nr. 44, e2111031118, 2021.Publikation: Bidrag til tidsskrift › Tidsskriftartikel › Forskning › fagfællebedømt
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TY - JOUR
T1 - Kinetic proofreading of lipochitooligosaccharides determines signal activation of symbiotic plant receptors
AU - Gysel, Kira
AU - Laursen, Mette
AU - Thygesen, Mikkel B.
AU - Lironi, Damiano
AU - Bozsóki, Zoltán
AU - Hjuler, Christian T.
AU - Maolanon, Nicolai N.
AU - Cheng, Jeryl
AU - Bjørk, Peter K.
AU - Vinther, Maria
AU - Madsen, Lene H.
AU - Rübsam, Henriette
AU - Muszyński, Artur
AU - Ghodrati, Arshia
AU - Azadi, Parastoo
AU - Sullivan, John T.
AU - Ronson, Clive W.
AU - Jensen, Knud J.
AU - Blaise, Mickaël
AU - Radutoiu, Simona
AU - Stougaard, Jens
AU - Andersen, Kasper R.
N1 - Publisher Copyright: © 2021 National Academy of Sciences. All rights reserved.
PY - 2021
Y1 - 2021
N2 - 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.
AB - 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.
KW - Kinetic proofreading
KW - Legume symbiosis
KW - Lipochitooligosaccharide signaling
KW - LysM receptors
KW - Receptor-ligand interaction
U2 - 10.1073/pnas.2111031118
DO - 10.1073/pnas.2111031118
M3 - Journal article
C2 - 34716271
AN - SCOPUS:85119274425
VL - 118
JO - Proceedings of the National Academy of Sciences of the United States of America
JF - Proceedings of the National Academy of Sciences of the United States of America
SN - 0027-8424
IS - 44
M1 - e2111031118
ER -
ID: 285715284