Kinetic proofreading of lipochitooligosaccharides determines signal activation of symbiotic plant receptors

Publikation: Bidrag til tidsskrift › Tidsskriftartikel › Forskning › fagfællebedømt

Standard

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

Harvard

Gysel, K, Laursen, M, Thygesen, MB, Lironi, D, Bozsóki, Z, Hjuler, CT, Maolanon, NN, Cheng, J, Bjørk, PK, Vinther, M, Madsen, LH, Rübsam, H, Muszyński, A, Ghodrati, A, Azadi, P, Sullivan, JT, Ronson, CW, Jensen, KJ, Blaise, M, Radutoiu, S, Stougaard, J & Andersen, KR 2021, 'Kinetic proofreading of lipochitooligosaccharides determines signal activation of symbiotic plant receptors', Proceedings of the National Academy of Sciences of the United States of America, bind 118, nr. 44, e2111031118. https://doi.org/10.1073/pnas.2111031118

APA

Gysel, K., Laursen, M., Thygesen, M. B., Lironi, D., Bozsóki, Z., Hjuler, C. T., Maolanon, N. N., Cheng, J., Bjørk, P. K., Vinther, M., Madsen, L. H., Rübsam, H., Muszyński, A., Ghodrati, A., Azadi, P., Sullivan, J. T., Ronson, C. W., Jensen, K. J., Blaise, M., ... Andersen, K. R. (2021). Kinetic proofreading of lipochitooligosaccharides determines signal activation of symbiotic plant receptors. Proceedings of the National Academy of Sciences of the United States of America, 118(44), [e2111031118]. https://doi.org/10.1073/pnas.2111031118

Vancouver

Gysel K, Laursen M, Thygesen MB, Lironi D, Bozsóki Z, Hjuler CT o.a. Kinetic proofreading of lipochitooligosaccharides determines signal activation of symbiotic plant receptors. Proceedings of the National Academy of Sciences of the United States of America. 2021;118(44). e2111031118. https://doi.org/10.1073/pnas.2111031118

Author

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. / Kinetic proofreading of lipochitooligosaccharides determines signal activation of symbiotic plant receptors. I: Proceedings of the National Academy of Sciences of the United States of America. 2021 ; Bind 118, Nr. 44.

Bibtex

@article{93dd0350305f491399d3b6f78bfdaf24,

title = "Kinetic proofreading of lipochitooligosaccharides determines signal activation of symbiotic plant receptors",

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.",

keywords = "Kinetic proofreading, Legume symbiosis, Lipochitooligosaccharide signaling, LysM receptors, Receptor-ligand interaction",

author = "Kira Gysel and Mette Laursen and Thygesen, {Mikkel B.} and Damiano Lironi and Zolt{\'a}n Bozs{\'o}ki and Hjuler, {Christian T.} and Maolanon, {Nicolai N.} and Jeryl Cheng and Bj{\o}rk, {Peter K.} and Maria Vinther and Madsen, {Lene H.} and Henriette R{\"u}bsam and Artur Muszy{\'n}ski and Arshia Ghodrati and Parastoo Azadi and Sullivan, {John T.} and Ronson, {Clive W.} and Jensen, {Knud J.} and Micka{\"e}l Blaise and Simona Radutoiu and Jens Stougaard and Andersen, {Kasper R.}",

year = "2021",

doi = "10.1073/pnas.2111031118",

language = "English",

volume = "118",

journal = "Proceedings of the National Academy of Sciences of the United States of America",

issn = "0027-8424",

publisher = "The National Academy of Sciences of the United States of America",

number = "44",

}

RIS

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.

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

Kemisk Institut