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1. Structural and functional analyses explain Pea KAI2 receptor diversity and reveal stereoselective catalysis during signal perception

Author

Angelica M. Guercio, Salar Torabi, David Cornu, Marion Dalmais, Abdelhafid Bendahmane, Christine Le Signor, Jean-Paul Pillot, Philippe Le Bris, François-Didier Boyer, Catherine Rameau, Caroline Gutjahr, Alexandre de Saint Germain, and Nitzan Shabek

Subjects
Biology (General), QH301-705.5
Abstract

Guercio et al., combine structural biology, biochemistry, and plant biology to reveal the dual functions of evolutionarily diverged Pisum KAI2A and KAI2B as both receptors and enzymes with distinct ligand selectivity, and propose adaptive sensitivity to strigolactone phytohormones by KAI2B. They reported the structures of KAI2 in apo and ligand intermediate -bound states that further illuminate KAI2s catalysis mechanism.

Published
2022
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2. Structural and functional analyses explain Pea KAI2 receptor diversity and reveal stereoselective catalysis during signal perception

Author

David Cornu, François-Didier Boyer, Angelica M. Guercio, Nitzan Shabek, Alexandre de Saint Germain, Philippe Le Bris, Abdelhafid Bendahmane, Caroline Gutjahr, Salar Torabi, Catherine Rameau, Christine Le Signor, Marion Dalmais, Jean-Paul Pillot, Institut de Chimie des Substances Naturelles (ICSN), Institut de Chimie du CNRS (INC)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS), University of California [Davis] (UC Davis), University of California (UC), Technische Universität Munchen - Université Technique de Munich [Munich, Allemagne] (TUM), Institut de Biologie Intégrative de la Cellule (I2BC), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS), Institut des Sciences des Plantes de Paris-Saclay (IPS2 (UMR_9213 / UMR_1403)), Université d'Évry-Val-d'Essonne (UEVE)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS)-Université Paris Cité (UPCité)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Agroécologie [Dijon], Université de Bourgogne (UB)-AgroSup Dijon - Institut National Supérieur des Sciences Agronomiques, de l'Alimentation et de l'Environnement-Université Bourgogne Franche-Comté [COMUE] (UBFC)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Institut Jean-Pierre Bourgin (IJPB), AgroParisTech-Université Paris-Saclay-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), and 2047396/National Science Foundation (NSF)2028283/National Science Foundation (NSF)

Subjects
0106 biological sciences, QH301-705.5, [SDV]Life Sciences [q-bio], Arabidopsis, Strigolactone, Medicine (miscellaneous), 01 natural sciences, General Biochemistry, Genetics and Molecular Biology, Catalysis, Serine, 03 medical and health sciences, Plant Growth Regulators, Hydrolase, [SDV.BV]Life Sciences [q-bio]/Vegetal Biology, [SDV.BBM.BC]Life Sciences [q-bio]/Biochemistry, Molecular Biology/Biochemistry [q-bio.BM], Biology (General), Receptor, Histidine, 030304 developmental biology, Butenolide, 0303 health sciences, [SDV.BBM.BS]Life Sciences [q-bio]/Biochemistry, Molecular Biology/Structural Biology [q-bio.BM], Chemistry, Arabidopsis Proteins, Peas, food and beverages, [SDV.BV.BOT]Life Sciences [q-bio]/Vegetal Biology/Botanics, Ligand (biochemistry), Biochemistry, Perception, Signal transduction, General Agricultural and Biological Sciences, 010606 plant biology & botany
Abstract

KAI2 are plant α/β hydrolase receptors, which perceive smoke-derived butenolide signals (karrikins) and putative endogenous, yet unidentified phytohormones (KAI2-ligands, KLs). The number of functional KAI2 receptors varies among plant species. It has been suggested that KAI2 gene duplication and sub-functionalization plays an adaptative role for diverse environments or ligand diversification by altering the receptor responsiveness to specific KLs. Legumes represent one of the largest families of flowering plants and contain many essential agronomic crops. Prior to legume diversification, KAI2 underwent duplication, resulting in KAI2A and KAI2B. Integrating plant genetics, ligand perception and enzymatic assays, and protein crystallography, we demonstrate that Pisum sativum KAI2A and KAI2B act as receptors and enzymes with divergent ligand stereoselectivity. KAI2B has a stronger affinity than KAI2A towards the KAI2-ligand (-)-GR24 and remarkably hydrolyses a broader range of substrates including the strigolactone-like isomer (+)-GR24. We determine the crystal structures of PsKAI2B in apo and butenolide-bound states. The biochemical and structural analyses as well as recorded mass spectra of KAI2s reveal a transient intermediate on the catalytic serine and a stable adduct on the catalytic histidine, further illuminating the role of KAI2 not only as receptors but also as bona fide enzymes. Our work uncovers the stereoselectivity of ligand perception and catalysis by evolutionarily diverged KAI2 receptors in KAR/KL signaling pathways and proposes adaptive sensitivity to KAR/KL and strigolactone phytohormones by KAI2B.

Published
2022

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