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Lotus japonicus karrikin receptors display divergent ligand-binding specificities and organ-dependent redundancy

View ORCID ProfileSamy Carbonnel, Salar Torabi, View ORCID ProfileMaximilian Griesmann, Elias Bleek, View ORCID ProfileYuhong Tang, Stefan Buchka, View ORCID ProfileVeronica Basso, View ORCID ProfileMitsuru Shindo, View ORCID ProfileFrançois-Didier Boyer, View ORCID ProfileTrevor L. Wang, View ORCID ProfileMichael Udvardi, View ORCID ProfileMark Waters, View ORCID ProfileCaroline Gutjahr
doi: https://doi.org/10.1101/754937
Samy Carbonnel
1LMU Munich, Faculty of Biology, Genetics, Biocenter Martinsried, Großhaderner Str. 2-4, 82152 Martinsried, Germany
2Technical University of Munich (TUM), School of Life Sciences Weihenstephan, Plant Genetics, Emil Ramann Str. 4, 85354 Freising, Germany
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Salar Torabi
1LMU Munich, Faculty of Biology, Genetics, Biocenter Martinsried, Großhaderner Str. 2-4, 82152 Martinsried, Germany
2Technical University of Munich (TUM), School of Life Sciences Weihenstephan, Plant Genetics, Emil Ramann Str. 4, 85354 Freising, Germany
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Maximilian Griesmann
1LMU Munich, Faculty of Biology, Genetics, Biocenter Martinsried, Großhaderner Str. 2-4, 82152 Martinsried, Germany
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Elias Bleek
1LMU Munich, Faculty of Biology, Genetics, Biocenter Martinsried, Großhaderner Str. 2-4, 82152 Martinsried, Germany
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Yuhong Tang
3Noble Research Institute, Ardmore, Oklahoma 73401 USA
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Stefan Buchka
1LMU Munich, Faculty of Biology, Genetics, Biocenter Martinsried, Großhaderner Str. 2-4, 82152 Martinsried, Germany
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Veronica Basso
1LMU Munich, Faculty of Biology, Genetics, Biocenter Martinsried, Großhaderner Str. 2-4, 82152 Martinsried, Germany
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Mitsuru Shindo
4Institute for Materials Chemistry and Engineering, Kyushu University, Kasugakoen-6, Kasuga, Fukuoka, 816-8580, Japan
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François-Didier Boyer
5Université Paris-Saclay, CNRS, Institut de Chimie des Substances Naturelles, UPR 2301, 91198, Gif-sur-Yvette, France
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Trevor L. Wang
6John Innes Centre, Norwich Research Park, Norwich NR4 7UH, UK
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Michael Udvardi
3Noble Research Institute, Ardmore, Oklahoma 73401 USA
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Mark Waters
7School of Molecular Sciences, The University of Western Australia, 35 Stirling Hwy, Perth, WA 6009, Australia
8Australian Research Council Centre of Excellence in Plant Energy Biology, The University of Western Australia, 35 Stirling Hwy, Perth, WA 6009, Australia
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Caroline Gutjahr
1LMU Munich, Faculty of Biology, Genetics, Biocenter Martinsried, Großhaderner Str. 2-4, 82152 Martinsried, Germany
2Technical University of Munich (TUM), School of Life Sciences Weihenstephan, Plant Genetics, Emil Ramann Str. 4, 85354 Freising, Germany
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  • For correspondence: caroline.gutjahr@tum.de
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Abstract

Karrikins (KARs), smoke-derived butenolides, are perceived by the α/β-fold hydrolase KARRIKIN INSENSITIVE2 (KAI2) and are thought to mimic endogenous, yet elusive plant hormones tentatively called KAI2-ligands (KLs). The sensitivity to different karrikin types as well as the number of KAI2 paralogs varies among plant species, suggesting diversification and co-evolution of ligand-receptor relationships. In legumes, which comprise a number of important crops with protein-rich, nutritious seed, KAI2 has duplicated. We report sub-functionalization of KAI2a and KAI2b in the model legume Lotus japonicus and demonstrate that their ability to bind the synthetic ligand GR24ent-5DS differs in vitro as well as in genetic assays in Lotus japonicus and in the heterologous Arabidopsis thaliana background. These differences can be explained by the exchange of a widely conserved phenylalanine in the binding pocket of KAI2a with a tryptophan in KAI2b, which occured independently in KAI2 proteins of several unrelated angiosperms. Furthermore, two polymorphic residues in the binding pocket are conserved across a number of legumes and may contribute to ligand binding preferences. Unexpectedly, L. japonicus responds to diverse synthetic KAI2-ligands in an organ-specific manner. Hypocotyl development responds to KAR1, KAR2 and rac-GR24, while root system development responds only to KAR1. This organ-specificity cannot be explained by receptor-ligand preferences alone, because LjKAI2a is sufficient for karrikin responses in the hypocotyl, while LjKAI2a and LjKAI2b operate redundantly in roots. Our findings open novel research avenues into the evolution and diversity of butenolide ligand-receptor relationships, their ecological significance and the mechanisms controlling diverse developmental responses to different KAI2 ligands.

Competing Interest Statement

The authors have declared no competing interest.

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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-NC 4.0 International license.
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Posted September 02, 2020.
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Lotus japonicus karrikin receptors display divergent ligand-binding specificities and organ-dependent redundancy
Samy Carbonnel, Salar Torabi, Maximilian Griesmann, Elias Bleek, Yuhong Tang, Stefan Buchka, Veronica Basso, Mitsuru Shindo, François-Didier Boyer, Trevor L. Wang, Michael Udvardi, Mark Waters, Caroline Gutjahr
bioRxiv 754937; doi: https://doi.org/10.1101/754937
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Lotus japonicus karrikin receptors display divergent ligand-binding specificities and organ-dependent redundancy
Samy Carbonnel, Salar Torabi, Maximilian Griesmann, Elias Bleek, Yuhong Tang, Stefan Buchka, Veronica Basso, Mitsuru Shindo, François-Didier Boyer, Trevor L. Wang, Michael Udvardi, Mark Waters, Caroline Gutjahr
bioRxiv 754937; doi: https://doi.org/10.1101/754937

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