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Molecular mechanism for the recognition of sequence-divergent CIF peptides by the plant receptor kinases GSO1/SGN3 and GSO2

View ORCID ProfileSatohiro Okuda, View ORCID ProfileSatoshi Fujita, View ORCID ProfileAndrea Moretti, View ORCID ProfileUlrich Hohmann, View ORCID ProfileVerónica G. Doblas, Yan Ma, Alexandre Pfister, View ORCID ProfileBenjamin Brandt, View ORCID ProfileNiko Geldner, View ORCID ProfileMichael Hothorn
doi: https://doi.org/10.1101/692228
Satohiro Okuda
1Structural Plant Biology Laboratory, Department of Botany and Plant Biology, University of Geneva, 1211 Geneva, Switzerland
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Satoshi Fujita
2Department of Plant Molecular Biology, University of Lausanne, 1015 Lausanne, Switzerland
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Andrea Moretti
1Structural Plant Biology Laboratory, Department of Botany and Plant Biology, University of Geneva, 1211 Geneva, Switzerland
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Ulrich Hohmann
1Structural Plant Biology Laboratory, Department of Botany and Plant Biology, University of Geneva, 1211 Geneva, Switzerland
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Verónica G. Doblas
2Department of Plant Molecular Biology, University of Lausanne, 1015 Lausanne, Switzerland
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Yan Ma
2Department of Plant Molecular Biology, University of Lausanne, 1015 Lausanne, Switzerland
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Alexandre Pfister
2Department of Plant Molecular Biology, University of Lausanne, 1015 Lausanne, Switzerland
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Benjamin Brandt
1Structural Plant Biology Laboratory, Department of Botany and Plant Biology, University of Geneva, 1211 Geneva, Switzerland
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Niko Geldner
2Department of Plant Molecular Biology, University of Lausanne, 1015 Lausanne, Switzerland
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  • For correspondence: niko.geldner@unil.ch michael.hothorn@unige.ch
Michael Hothorn
1Structural Plant Biology Laboratory, Department of Botany and Plant Biology, University of Geneva, 1211 Geneva, Switzerland
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  • ORCID record for Michael Hothorn
  • For correspondence: niko.geldner@unil.ch michael.hothorn@unige.ch
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Abstract

Plants use leucine-rich repeat receptor kinases (LRR-RKs) to sense sequence diverse peptide hormones at the cell surface. A 3.0 Å crystal structure of the LRR-RK GSO1/SGN3 regulating Casparian strip formation in the endodermis reveals a large spiral-shaped ectodomain. The domain provides a binding platform for 21 amino-acid CIF peptide ligands, which are tyrosine sulfated by the tyrosylprotein sulfotransferase TPST/SGN2. GSO1/SGN3 harbors a binding pocket for sulfotyrosine and makes extended backbone interactions with CIF2. Quantitative biochemical comparisons reveal that GSO1/SGN3 – CIF2 represents one of the strongest receptor-ligand pairs known in plants. Multiple missense mutations are required to block CIF2 binding in vitro, and GSO1/SGN3 function in vivo. Using structure-guided sequence analysis we uncover novel CIF peptides conserved among higher plants. Quantitative binding assays with known and novel CIFs suggest that the homologous LRR-RKs GSO1/SGN3 and GSO2 have evolved unique peptide binding properties to control different developmental processes. A quantitative biochemical interaction screen, a CIF peptide antagonist and genetic analyses together implicate SERK LRR-RKs as essential co-receptor kinases required for GSO1/SGN3 and GSO2 receptor activation. 0ur work provides a mechanistic framework for the recognition of sequence-divergent peptide hormones in plants.

Significance Statement Two sequence-related plant membrane receptor kinases and their shape-complementary co-receptors are shown to selectively sense members of a small family of secreted peptide hormones to control formation of an important diffusion barrier in the plant root.

Footnotes

  • Discussion updated, figure conversion errors fixed.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-ND 4.0 International license.
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Posted July 05, 2019.
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Molecular mechanism for the recognition of sequence-divergent CIF peptides by the plant receptor kinases GSO1/SGN3 and GSO2
Satohiro Okuda, Satoshi Fujita, Andrea Moretti, Ulrich Hohmann, Verónica G. Doblas, Yan Ma, Alexandre Pfister, Benjamin Brandt, Niko Geldner, Michael Hothorn
bioRxiv 692228; doi: https://doi.org/10.1101/692228
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Molecular mechanism for the recognition of sequence-divergent CIF peptides by the plant receptor kinases GSO1/SGN3 and GSO2
Satohiro Okuda, Satoshi Fujita, Andrea Moretti, Ulrich Hohmann, Verónica G. Doblas, Yan Ma, Alexandre Pfister, Benjamin Brandt, Niko Geldner, Michael Hothorn
bioRxiv 692228; doi: https://doi.org/10.1101/692228

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