TY - JOUR

T1 - Mechanistic basis for the activation of plant membrane receptor kinases by SERK-family coreceptors

AU - Hohmann, Ulrich

AU - Santiago, Julia

AU - Nicolet, Joël

AU - Olsson, Vilde

AU - Spiga, Fabio M.

AU - Hothorn, Ludwig A.

AU - Butenko, Melinka A.

AU - Hothorn, Michael

N1 - Funding Information: ACKNOWLEDGMENTS. We thank N. Geldner and Y. Jaillais for sharing Arabidopsis lines and plasmids; Y. Jaillais, R. Ulm, and C. S. Hardtke for commenting on the manuscript; and the staff at beam line PXIII of the Swiss Light Source (Villigen, Switzerland) for technical assistance during data collection. This work was supported by Swiss National Science Foundation Grant 31003A_156920, a Human Frontier Science Program Career Development Award (to M.H.), the European Molecular Biology Organization (EMBO) Young Investigator program (M.H.), and the Research Council of Norway Grant 230849/F20 (to M.A.B.). J.S. was supported by long-term fellowships from EMBO and the Federation of European Biochemical Societies.

PY - 2018/3/27

Y1 - 2018/3/27

N2 - Plant-unique membrane receptor kinases with leucine-rich repeat ectodomains (LRR-RKs) can sense small molecule, peptide, and protein ligands. Many LRR-RKs require SERK-family coreceptor kinases for high-affinity ligand binding and receptor activation. How one coreceptor can contribute to the specific binding of distinct ligands and activation of different LRR-RKs is poorly understood. Here we quantitatively analyze the contribution of SERK3 to ligand binding and activation of the brassinosteroid receptor BRI1 and the peptide hormone receptor HAESA. We show that while the isolated receptors sense their respective ligands with drastically different binding affinities, the SERK3 ectodomain binds the ligand-associated receptors with very similar binding kinetics. We identify residues in the SERK3 N-terminal capping domain, which allow for selective steroid and peptide hormone recognition. In contrast, residues in the SERK3 LRR core form a second, constitutive receptor-coreceptor interface. Genetic analyses of protein chimera between BRI1 and SERK3 define that signaling-competent complexes are formed by receptor-coreceptor heteromerization in planta. A functional BRI1-HAESA chimera suggests that the receptor activation mechanism is conserved among different LRR-RKs, and that their signaling specificity is encoded in the kinase domain of the receptor. Our work pinpoints the relative contributions of receptor, ligand, and coreceptor to the formation and activation of SERK-dependent LRR-RK signaling complexes regulating plant growth and development.

AB - Plant-unique membrane receptor kinases with leucine-rich repeat ectodomains (LRR-RKs) can sense small molecule, peptide, and protein ligands. Many LRR-RKs require SERK-family coreceptor kinases for high-affinity ligand binding and receptor activation. How one coreceptor can contribute to the specific binding of distinct ligands and activation of different LRR-RKs is poorly understood. Here we quantitatively analyze the contribution of SERK3 to ligand binding and activation of the brassinosteroid receptor BRI1 and the peptide hormone receptor HAESA. We show that while the isolated receptors sense their respective ligands with drastically different binding affinities, the SERK3 ectodomain binds the ligand-associated receptors with very similar binding kinetics. We identify residues in the SERK3 N-terminal capping domain, which allow for selective steroid and peptide hormone recognition. In contrast, residues in the SERK3 LRR core form a second, constitutive receptor-coreceptor interface. Genetic analyses of protein chimera between BRI1 and SERK3 define that signaling-competent complexes are formed by receptor-coreceptor heteromerization in planta. A functional BRI1-HAESA chimera suggests that the receptor activation mechanism is conserved among different LRR-RKs, and that their signaling specificity is encoded in the kinase domain of the receptor. Our work pinpoints the relative contributions of receptor, ligand, and coreceptor to the formation and activation of SERK-dependent LRR-RK signaling complexes regulating plant growth and development.

KW - Brassinosteroid signaling

KW - Floral abscission

KW - Leucine-rich repeat domain

KW - Membrane receptor kinase

KW - Receptor activation

UR - http://www.scopus.com/inward/record.url?scp=85044527914&partnerID=8YFLogxK

U2 - 10.1073/pnas.1714972115

DO - 10.1073/pnas.1714972115

M3 - Article

C2 - 29531026

AN - SCOPUS:85044527914

VL - 115

SP - 3488

EP - 3493

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 - 13

ER -