Structure reveals that BAK1 as a co-receptor recognizes the BRI1-bound brassinolide
Open accessAbstract
In animals, steroid hormones play critical roles in many vital physiological processes. Brassinosteroids (BRs) produced by plants have similar structures to the animal steroid hormones and play indispensable roles in plant growth and development 1 . BRs have now acknowledgedly become a sixth class of plant hormones. In contrast to animal steroid hormones that bind to nuclear receptors, BRs are recognized by the cell surface receptor BRASSINOSTEROID-INSENSITIVE 1 (BRI1) 2 and its homologs 3 . BRI1 belongs to a large family of plant leucine-rich repeat (LRR) receptor kinases (RKs), characterized by an extracellular ligand-sensing domain and an intracellular kinase domain. The extracellular domain of BRI1 contains 25 LRRs (BRI1LRR) and an island domain. Recognition of brassinolide (BL), the most active BR identified thus far, by BRI1LRR is through a surface pocket embedded in a 70-aa island (residues 587-656) domain 4 , 5 . BR binding greatly enhances BRI1 heteromerization with a second RK, BRI1-associated kinase 1 (BAK1, also known as SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASE 3, SERK3) 6 , 7 . The BR-induced BRI1-BAK1 stable association initiates a phosphorylation-mediated cascade transducing the extracellular steroid signal to transcriptional programs 1 , 3 . This process is accompanied with dissociation of a BRI1 kinase inhibitor 1 (BKI1) from the intracellular domain of BRI1 3 . Several models on BR-induced BRI1 activation have been proposed 1 , 4 , 5 , 8 . However, whether BAK1 acts as a regulator or co-receptor of BRI1 and how BR binding promotes BRI1-BAK1 interaction are not well understood. To test whether the extracellular domains of BRI1 and BAK1 are sufficient to form a BL-induced complex, we expressed the LRR domains of Arabidopsis BRI1 (residues 24-784, BRI1LRR) and BAK1 (residues 1-220, BAK1LRR) in insect cells, purified the proteins to homogeneity, and tested their interaction using a gel filtration assay. Unexpectedly, when assayed with a buffer at pH 8.0, the BRI1LRR and BAK1LRR proteins did not form a stable complex ( Figure 1A ). As binding of BL to BRI1 occurs in the extracellular acidic space, we reasoned that lowering pH may favor formation of BL-induced BRI1LRR-BAK1LRR complexes. In complete agreement with the prediction, the two proteins strongly interacted with each other at pH 4.0 in the presence of BL, as indicated by co-migration of the two proteins in gel filtration, which was dependent on the existence of BL ( Figure 1A ). These results indicate that the extracellular domains of BRI1 and BAK1 interact with each other in a BL- and pH-dependent manner. The complex was eluted at the position corresponding to a monomeric BRI1LRR-BAK1LRR ( ∼ 100 kD), suggesting that BL binding induces no homodimerization of the BRI1LRR-BAK1LRR complex. Figure 1 BAK1LRR recognizes the BRI1LRR-bound BL to form a pH-dependent BRI1LRR-BAK1LRR heterodimer. (A) BL induces BRI1LRR-BAK1LRR heterodimerization in solution at an acidic pH. Top panel, gel filtration profiles of BRI1LRR and BAK1LRR in the presence (red at pH 4.0 and green at pH 8.0) and absence (purple) of BL. The vertical and horizontal axes represent ultraviolet absorbance (λ = 280 nm) and elution volume (ml), respectively. BL, brassinolide. The 2nd, 3rd and 4th panels are Coomassie blue staining of the peak fractions following SDS-PAGE. Frame colors indicate their corresponding gel filtration runs shown on the top. The numbers shown on top of the gels indicate elution volume (ml). MM: molecular weight maker; the five bands from top to bottom indicate 112 kD, 66 kD, 45 kD, 35 kD and 25 kD, respectively. (B) Overall structure of BRI1LRR-BL-BAK1LRR shown in cartoon. Color codes are indicated. “N” and “C” represent the N- and C-terminus, respectively. (C) BAK1LRR binding induces no striking conformational changes in BRI1LRR. Shown in the figure is structural comparison of the BAK1LRR-free and BAK1LRR-bound BL-BRI1LRR. BL in BRI1LRR and BRI1LRR-BL-BAK1LRR is shown in yellow and cyan, respectively. (D) BAK1LRR recognizes the BRI1LRR-bound BL. Detailed interactions of BL with the N-terminal side of BAK1LRR. The side chains from BAK1LRR and BRI1LRR are shown in cream white and purple, respectively. Dashed red lines indicate hydrogen bonds. Two of the carbon atoms in BL are labeled. (E) Direct interaction between BRI1LRR and BAK1LRR. Residues from BAK1LRR and BRI1LRR are labeled in black and purple, respectively. Full size image We then solved the crystal structure of the BRI1LRR-BL-BAK1LRR complex at a resolution of 3.6 Å ( Supplementary information, Table S1 ). The BRI1LRR-organized complex is assembled with a 1:1:1 stoichiometry ( Figure 1B ). Supporting the gel filtration data, no homodimeric complexes were formed in the structure. Structural comparison showed that the conformations of BRI1LRR in the BAK1LRR-free and BAK1LRR-bound forms are markedly similar ( Figure 1C ), indicating that BAK1LRR binding induces no striking conformational changes in
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Brassinosteroids are phytohormones that function as molecular glues by linking the membrane receptor kinase BRI1 to its coreceptors.
“brassinosteroids are phytohormones that function as MGs by linking the membrane receptor kinase BRI1 to its coreceptors (Fig. 3A and 4).71,88”
From Chasing molecular glue degraders: screening approaches (2022) · cites this paper as [88]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Plants have a sensitive perception system for the most conserved domain of bacterial flagellin
Felix, G., Duran, J. D., Volko, S. M., & Boller, T. (1999) · The Plant Journal · doi:10.1046/j.1365-313x.1999.00265.x · Cited by 1,719 · see citing works
A Putative Leucine-Rich Repeat Receptor Kinase Involved in Brassinosteroid Signal Transduction
Li, J., & Chory, J. (1997) · Cell · doi:10.1016/s0092-8674(00)80357-8 · Cited by 1,641 · see citing works
Li, J., Wen, J., Lease, K. A., Doke, J. T., Tax, F. E., & Walker, J. C. (2002) · Cell · doi:10.1016/s0092-8674(02)00812-7 · Cited by 1,450 · see citing works
BRI1/BAK1, a Receptor Kinase Pair Mediating Brassinosteroid Signaling
Nam, K. H., & Li, J. (2002) · Cell · doi:10.1016/s0092-8674(02)00814-0 · Cited by 1,217 · see citing works
The Acid Growth Theory of auxin-induced cell elongation is alive and well.
Rayle, D. L., & Cleland, R. E. (1992) · PLANT PHYSIOLOGY · doi:10.1104/pp.99.4.1271 · Cited by 868 · see citing works
Friedrichsen, D. M., Joazeiro, C. A. P., Li, J., Hunter, T. R., & Chory, J. (2000) · PLANT PHYSIOLOGY · doi:10.1104/pp.123.4.1247 · Cited by 474 · see citing works
Structural basis of steroid hormone perception by the receptor kinase BRI1
Hothorn, M., Belkhadir, Y., Dreux, M., Dabi, T., Noel, J. P., Wilson, I. A., & Chory, J. (2011) · Nature · doi:10.1038/nature10153 · Cited by 422 · see citing works
Structural insight into brassinosteroid perception by BRI1
She, J., Han, Z., Kim, T., Wang, J., Cheng, W., Chang, J., Shi, S., Wang, J., Yang, M., Wang, Z., et al. (2011) · Nature · doi:10.1038/nature10178 · Cited by 418 · see citing works
Self-citationSantiago, J., Henzler, C., & Hothorn, M. (2013) · Science · doi:10.1126/science.1242468 · Cited by 357 · see citing works
Wang, X., Li, X., Meisenhelder, J., Hunter, T. R., Yoshida, S., Asami, T., & Chory, J. (2005) · Developmental Cell · doi:10.1016/j.devcel.2005.05.001 · Cited by 302 · see citing works
Clouse, S. D. (2011) · The Arabidopsis Book · doi:10.1199/tab.0151 · Cited by 192 · see citing works
Sensing of microbial molecular patterns by Toll‐like receptors
Song, D. H., & Lee, J. (2012) · Immunological Reviews · doi:10.1111/j.1600-065x.2012.01167.x · Cited by 169 · see citing works
Extracellular leucine-rich repeats as a platform for receptor/coreceptor complex formation
Jaillais, Y., Belkhadir, Y., Balsemão-Pires, E., Dangl, J. L., & Chory, J. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1103556108 · Cited by 159 · see citing works
Brassinosteroid phytohormones: structure, bioactivity and applications
Zullo, M. A. T., & Adam, G. (2002) · Brazilian Journal of Plant Physiology · doi:10.1590/s1677-04202002000300001 · Cited by 133 · see citing works
Structural basis for differential recognition of brassinolide by its receptors
She, J., Han, Z., Zhou, B., & Chai, J. (2013) · Protein & Cell · doi:10.1007/s13238-013-3027-8 · Cited by 57 · see citing works
Self-citationJiang, J., Zhang, C., & Wang, X. (2013) · Journal of Integrative Plant Biology · doi:10.1111/jipb.12081 · Cited by 49 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Regulation of pattern recognition receptor signalling in plants
Couto, D., & Zipfel, C. (2016) · Nature reviews. Immunology · doi:10.1038/nri.2016.77 · Cited by 1,400 · see citing works
Brassinosteroids: Multidimensional Regulators of Plant Growth, Development, and Stress Responses
Nolan, T. M., Vukašinović, N., Liu, D., Russinova, E., & Yin, Y. (2019) · The Plant Cell · doi:10.1105/tpc.19.00335 · Cited by 1,106 · see citing works
Plant PRRs and the Activation of Innate Immune Signaling
Macho, A. P., & Zipfel, C. (2014) · Molecular Cell · doi:10.1016/j.molcel.2014.03.028 · Cited by 992 · see citing works
The FERONIA Receptor Kinase Maintains Cell-Wall Integrity during Salt Stress through Ca2+ Signaling
Feng, W., Kita, D., Peaucelle, A., Cartwright, H. N., Doan, V., Duan, Q., Liu, M.-C. J., Maman, J., Steinhorst, L., Schmitz-Thom, I., et al. (2018) · Current Biology · doi:10.1016/j.cub.2018.01.023 · Cited by 770 · see citing works
Cao, Y., Liang, Y., Tanaka, K., Nguyen, C. T., Jedrzejczak, R. P., Joachimiak, A., & Stacey, G. S. (2014) · eLife · doi:10.7554/elife.03766 · Cited by 681 · see citing works
Brassinosteroid signaling in plant development and adaptation to stress
Planas‐Riverola, A., Gupta, A., Betegón‐Putze, I., Bosch, N., Ibañes, M., & Caño‐Delgado, A. I. (2019) · Development · doi:10.1242/dev.151894 · Cited by 520 · see citing works
Receptor-Like Cytoplasmic Kinases: Central Players in Plant Receptor Kinase–Mediated Signaling
Liang, X., & Zhou, J. (2018) · Annual Review of Plant Biology · doi:10.1146/annurev-arplant-042817-040540 · Cited by 505 · see citing works
Two for all: receptor-associated kinases SOBIR1 and BAK1
Liebrand, T. W. H., van den Burg, H. A., & JOOSTEN, M. H. A. J. (2013) · Trends in Plant Science · doi:10.1016/j.tplants.2013.10.003 · Cited by 339 · see citing works
Brassinosteroids Regulate Root Growth, Development, and Symbiosis
Wei, Z., & Li, J. (2015) · Molecular Plant · doi:10.1016/j.molp.2015.12.003 · Cited by 320 · see citing works
The Structural Basis of Ligand Perception and Signal Activation by Receptor Kinases
Hohmann, U., Lau, K., & Hothorn, M. (2017) · Annual Review of Plant Biology · doi:10.1146/annurev-arplant-042916-040957 · Cited by 302 · see citing works
An extracellular network of Arabidopsis leucine-rich repeat receptor kinases
Smakowska‐Luzan, E., Mott, G. A., Parys, K., Stegmann, M., Howton, T. C., Layeghifard, M., Neuhold, J., Lehner, A., Kong, J., Grünwald, K., et al. (2018) · Nature · doi:10.1038/nature25184 · Cited by 307 · see citing works
The Leucine-Rich Repeat Receptor Kinase BIR2 Is a Negative Regulator of BAK1 in Plant Immunity
Halter, T., Imkampe, J., Mazzotta, S., Wierzba, M., Postel, S., Bücherl, C. A., Kiefer, C. S., Stahl, M., Chinchilla, D., Wang, X., et al. (2014) · Current Biology · doi:10.1016/j.cub.2013.11.047 · Cited by 286 · see citing works
Mechanistic insight into a peptide hormone signaling complex mediating floral organ abscission
Santiago, J., Brandt, B., Wildhagen, M., Hohmann, U., Hothorn, L. A., Butenko, M. A., & Hothorn, M. (2016) · eLife · doi:10.7554/elife.15075 · Cited by 267 · see citing works
SERKing Coreceptors for Receptors
Ma, X., Xu, G., He, P., & Shan, L. (2016) · Trends in Plant Science · doi:10.1016/j.tplants.2016.08.014 · Cited by 267 · see citing works
Differential Function of Arabidopsis SERK Family Receptor-like Kinases in Stomatal Patterning
Meng, X., Chen, X., Mang, H., Liu, C., Yu, X., Gao, X., Torii, K. U., He, P., & Shan, L. (2015) · Current Biology · doi:10.1016/j.cub.2015.07.068 · Cited by 266 · see citing works
Trade-off between growth and immunity: role of brassinosteroids
Lozano‐Durán, R., & Zipfel, C. (2014) · Trends in Plant Science · doi:10.1016/j.tplants.2014.09.003 · Cited by 266 · see citing works
Brassinosteroids (BRs) Role in Plant Development and Coping with Different Stresses
Manghwar, H., Hussain, A., Ali, Q., & Liu, F. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23031012 · Cited by 266 · see citing works
The molecular circuitry of brassinosteroid signaling
Belkhadir, Y., & Jaillais, Y. (2015) · New Phytologist · doi:10.1111/nph.13269 · Cited by 253 · see citing works
Ligand-Induced Receptor-like Kinase Complex Regulates Floral Organ Abscission in Arabidopsis
Meng, X., Zhou, J., Tang, J., Li, B., de Oliveira, M. V. V., Chai, J., He, P., & Shan, L. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.01.023 · Cited by 208 · see citing works
Self-citationOu, Y., Lu, X., Zi, Q., Xun, Q., Zhang, J., Wu, Y., Shi, H., Wei, Z., Zhao, B., Zhang, X., et al. (2016) · Cell Research · doi:10.1038/cr.2016.63 · Cited by 193 · see citing works
Chasing molecular glue degraders: screening approaches
Domostegui, A., Nieto-Barrado, L., Perez-Lopez, C., & Mayor-Ruiz, C. (2022) · Chemical Society Reviews · doi:10.1039/d2cs00197g · Cited by 200 · see citing works
Structural basis for recognition of an endogenous peptide by the plant receptor kinase PEPR1
Tang, J., Han, Z., Sun, Y., Zhang, H., Gong, X., & Chai, J. (2014) · Cell Research · doi:10.1038/cr.2014.161 · Cited by 196 · see citing works
Self-citationSaini, S., Sharma, I., & Pati, P. K. (2015) · Frontiers in Plant Science · doi:10.3389/fpls.2015.00950 · Cited by 193 · see citing works
Transcription Factor OsWRKY53 Positively Regulates Brassinosteroid Signaling and Plant Architecture
Tian, X., Li, X., Zhou, W., Ren, Y., Wang, Z., Liu, Z., Tang, J., Tong, H., Fang, J., & Bu, Q. (2017) · PLANT PHYSIOLOGY · doi:10.1104/pp.17.00946 · Cited by 192 · see citing works
Self-citationNegative control of BAK1 by protein phosphatase 2A during plant innate immunity
Segonzac, C., Macho, A. P., Sanmartín, M., Ntoukakis, V. E., Sánchez‐Serrano, J. J., & Zipfel, C. (2014) · The EMBO Journal · doi:10.15252/embj.201488698 · Cited by 183 · see citing works
Plant cell surface receptor-mediated signaling – a common theme amid diversity
He, Y., Zhou, J., Shan, L., & Meng, X. (2018) · Journal of Cell Science · doi:10.1242/jcs.209353 · Cited by 169 · see citing works
Genome-Wide Expression Pattern Analyses of the Arabidopsis Leucine-Rich Repeat Receptor-Like Kinases
Wu, Y., Xun, Q., Guo, Y., Zhang, J., Cheng, K., Shi, T., He, K., Hou, S., Gou, X., & Li, J. (2015) · Molecular Plant · doi:10.1016/j.molp.2015.12.011 · Cited by 168 · see citing works
Bojar, D., Martinez, J., Santiago, J., Rybin, V., Bayliss, R. W., & Hothorn, M. (2014) · The Plant Journal · doi:10.1111/tpj.12445 · Cited by 161 · see citing works
Tian, X., He, M., Mei, E., Zhang, B., Tang, J., Xu, M., Liu, J., Li, X., Wang, Z., Tang, W., et al. (2021) · The Plant Cell · doi:10.1093/plcell/koab137 · Cited by 165 · see citing works
Self-citationLi, Q., Lü, J., Yu, J., Zhang, C., He, J., & Liu, Q. (2018) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2018.04.003 · Cited by 163 · see citing works
The growth–defense pivot: crisis management in plants mediated by LRR-RK surface receptors
Belkhadir, Y., Yang, L., Hetzel, J., Dangl, J. L., & Chory, J. (2014) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2014.06.006 · Cited by 162 · see citing works
The brassinosteroid signaling network—a paradigm of signal integration
Wang, W., Bai, M., & Wang, Z. (2014) · Current Opinion in Plant Biology · doi:10.1016/j.pbi.2014.07.012 · Cited by 155 · see citing works
Gui, J., Zheng, S., Liu, C., Shen, J., Li, J., & Li, L. (2016) · Developmental Cell · doi:10.1016/j.devcel.2016.06.011 · Cited by 154 · see citing works
Plant cell wall signalling and receptor-like kinases
Wolf, S. (2017) · Biochemical Journal · doi:10.1042/bcj20160238 · Cited by 152 · see citing works
V-ATPase activity in the TGN/EE is required for exocytosis and recycling in Arabidopsis
Luo, Y., Scholl, S., Doering, A., Zhang, Y., Irani, N. G., Rubbo, S. D., Neumetzler, L., Krishnamoorthy, P., van Houtte, I., Mylle, E., et al. (2015) · Nature Plants · doi:10.1038/nplants.2015.94 · Cited by 150 · see citing works
Plant cell wall-mediated disease resistance: Current understanding and future perspectives
Molina, A., Jordá, L., Torres, M. Á. M., Martín‐Dacal, M., Berlanga, D. J., Fernández‐Calvo, P., Gómez-Rubio, E., & Martín‐Santamaría, S. (2024) · Molecular Plant · doi:10.1016/j.molp.2024.04.003 · Cited by 150 · see citing works
Phosphocode-dependent functional dichotomy of a common co-receptor in plant signalling
Perraki, A., DeFalco, T. A., Derbyshire, P., Ávila-Pacheco, J., Séré, D., Sklenář, J., Qi, X., Stransfeld, L., Schwessinger, B., Kadota, Y., et al. (2018) · Nature · doi:10.1038/s41586-018-0471-x · Cited by 148 · see citing works
Extracellular pH sensing by plant cell-surface peptide-receptor complexes
Liu, L., Song, W., Huang, S., Jiang, K., Moriwaki, Y., Wang, Y., Men, Y., Zhang, D., Wen, X., Han, Z., et al. (2022) · Cell · doi:10.1016/j.cell.2022.07.012 · Cited by 146 · see citing works
Self-citationReceptor kinase‐mediated control of primary active proton pumping at the plasma membrane
Fuglsang, A. T., Kristensen, A., Cuin, T. A., Schulze, W. X., Persson, J., Thuesen, K. H., Ytting, C. K., Oehlenschlæger, C. B., Mahmood, K., Søndergaard, T. E., et al. (2014) · The Plant Journal · doi:10.1111/tpj.12680 · Cited by 145 · see citing works
Dockter, C., Gruszka, D., Braumann, I., Druka, A., Druka, I., Franckowiak, J. D., Gough, S. P., Janeczko, A., Kurowska, M. M., Lundqvist, J., et al. (2014) · PLANT PHYSIOLOGY · doi:10.1104/pp.114.250738 · Cited by 141 · see citing works
SERK Family Receptor-like Kinases Function as Co-receptors with PXY for Plant Vascular Development
Zhang, H., Lin, X., Han, Z., Wang, J., Qu, L., & Chai, J. (2016) · Molecular Plant · doi:10.1016/j.molp.2016.07.004 · Cited by 134 · see citing works
Self-citationImkampe, J., Halter, T., Huang, S., Schulze, S., Mazzotta, S., Schmidt, N., Manstretta, R., Postel, S., Wierzba, M., Yang, Y., et al. (2017) · The Plant Cell · doi:10.1105/tpc.17.00376 · Cited by 133 · see citing works
Growth control: brassinosteroid activity gets context
Singh, A. P., & Savaldi‐Goldstein, S. (2015) · Journal of Experimental Botany · doi:10.1093/jxb/erv026 · Cited by 131 · see citing works
Zhang, B., Wang, X., Zhao, Z., Wang, R., Huang, X., Zhu, Y., Li, Y., Wang, Y., Xu, X., Burlingame, A. L., et al. (2015) · PLANT PHYSIOLOGY · doi:10.1104/pp.15.01668 · Cited by 124 · see citing works
Self-citationLi, Z., Ou, Y., Zhang, Z., Li, J., & He, Y. (2018) · Molecular Plant · doi:10.1016/j.molp.2018.06.007 · Cited by 124 · see citing works
Holton, N. J., Nekrasov, V., Ronald, P. C., & Zipfel, C. (2015) · PLoS Pathogens · doi:10.1371/journal.ppat.1004602 · Cited by 122 · see citing works
Spontaneous symbiotic reprogramming of plant roots triggered by receptor-like kinases
Ried, M. K., Antolín‐Llovera, M., & Parniske, M. (2014) · eLife · doi:10.7554/elife.03891 · Cited by 118 · see citing works
Molecular control of stomatal development
Zoulias, N., Harrison, E. L., Casson, S. A., & Gray, J. E. (2018) · Biochemical Journal · doi:10.1042/bcj20170413 · Cited by 116 · see citing works
Jiang, J., Zhang, C., & Wang, X. (2015) · The Plant Cell · doi:10.1105/tpc.114.133678 · Cited by 115 · see citing works
Ren, H. Y., Willige, B. C., Jaillais, Y., Geng, S., Park, M. Y., Gray, W. M., & Chory, J. (2019) · PLoS Genetics · doi:10.1371/journal.pgen.1007904 · Cited by 115 · see citing works
Kinase activity of SOBIR1 and BAK1 is required for immune signalling
van der Burgh, A. M., Postma, J., Robatzek, S., & JOOSTEN, M. H. A. J. (2018) · Molecular Plant Pathology · doi:10.1111/mpp.12767 · Cited by 114 · see citing works
Catanzariti, A., Do, H. T. T., Bru, P., de Sain, M., Thatcher, L. F., Rep, M., & Jones, D. A. (2016) · The Plant Journal · doi:10.1111/tpj.13458 · Cited by 115 · see citing works
Cytokinin signaling: from the ER or from the PM? That is the question!
Romanov, G. A., Lomin, S. N., & Schmülling, T. (2018) · New Phytologist · doi:10.1111/nph.14991 · Cited by 112 · see citing works
ABLs and TMKs are co-receptors for extracellular auxin
(2023) · doi:10.1016/j.cell.2023.10.017 · Cited by 112 · see citing works
Designed abscisic acid analogs as antagonists of PYL-PP2C receptor interactions
Takeuchi, J., Okamoto, M., Akiyama, T., Muto, T., Yajima, S., Sue, M., Seo, M., Kanno, Y., Kamo, T., Endo, A., et al. (2014) · Nature Chemical Biology · doi:10.1038/nchembio.1524 · Cited by 111 · see citing works
Yang, X., Bai, Y., Shang, J., Xin, R., & Tang, W. (2016) · Plant Cell & Environment · doi:10.1111/pce.12763 · Cited by 108 · see citing works
Signaling Peptides and Receptors Coordinating Plant Root Development
Oh, E., Seo, P. J., & Kim, J. (2018) · Trends in Plant Science · doi:10.1016/j.tplants.2017.12.007 · Cited by 107 · see citing works
Structure and function of the Arabidopsis ABC transporter ABCB19 in brassinosteroid export
Ying, W., Wang, Y., Wei, H., Luo, Y., Ma, Q., Zhu, H., Janssens, H., Vukašinović, N., Kvasnica, M., Winne, J. M., et al. (2024) · Science · doi:10.1126/science.adj4591 · Cited by 107 · see citing works
Cui, Y., Hu, C., Zhu, Y., Cheng, K., Li, X., Wei, Z., Xue, L., Lin, F., Shi, H., Yi, J., et al. (2018) · The Plant Cell · doi:10.1105/tpc.17.00586 · Cited by 106 · see citing works
Liu, Y., Huang, X., Li, M., He, P., & Zhang, Y. (2016) · New Phytologist · doi:10.1111/nph.14072 · Cited by 103 · see citing works
Mechanistic basis for the activation of plant membrane receptor kinases by SERK-family coreceptors
Hohmann, U., Santiago, J., Nicolet, J., Lalun, V. O., Spiga, F. M., Hothorn, L. A., Butenko, M. A., & Hothorn, M. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1714972115 · Cited by 103 · see citing works
Paradigms of receptor kinase signaling in plants
Bender, K. W., & Zipfel, C. (2023) · Biochemical Journal · doi:10.1042/bcj20220372 · Cited by 64 · see citing works
Yaqoob, U., Jan, N., Prabhavathi, V., Siddique, K. H. M., & John, R. (2022) · Plant Stress · doi:10.1016/j.stress.2022.100075 · Cited by 97 · see citing works
Chakraborty, S., Nguyen, B., Wasti, S. D., & Xu, G. (2019) · Molecules · doi:10.3390/molecules24173081 · Cited by 93 · see citing works
Crystal structure of the plant receptor-like kinase TDR in complex with the TDIF peptide
Morita, J., Kato, K., Nakane, T., Kondo, Y., Fukuda, H., Nishimasu, H., Ishitani, R., & Nureki, O. (2016) · Nature Communications · doi:10.1038/ncomms12383 · Cited by 92 · see citing works
Regulation of Brassinosteroid Homeostasis in Higher Plants
Wei, Z., & Li, J. (2020) · Frontiers in Plant Science · doi:10.3389/fpls.2020.583622 · Cited by 92 · see citing works
Interdependent Nutrient Availability and Steroid Hormone Signals Facilitate Root Growth Plasticity
Singh, A. P., Fridman, Y., Holland, N., Ackerman-Lavert, M., Zananiri, R., Jaillais, Y., Henn, A., & Savaldi‐Goldstein, S. (2018) · Developmental Cell · doi:10.1016/j.devcel.2018.06.002 · Cited by 88 · see citing works
Kim, E., Lee, S., Park, C. H., Kim, S., Hsu, C., Xu, S., Wang, Z., Kim, S., & Kim, T. (2019) · The Plant Cell · doi:10.1105/tpc.18.00941 · Cited by 85 · see citing works
Brassinosteroid Biosynthesis Is Modulated via a Transcription Factor Cascade of COG1, PIF4, and PIF5
Wei, Z., Yuan, T., Tarkowská, D., Kim, J., Nam, H. G., Novák, O., He, K., Gou, X., & Li, J. (2017) · PLANT PHYSIOLOGY · doi:10.1104/pp.16.01778 · Cited by 84 · see citing works
New Insights on Leucine-Rich Repeats Receptor-Like Kinase Orthologous Relationships in Angiosperms
Dufayard, J.-F., Bettembourg, M., Fischer, I., Droc, G., Guiderdoni, E., Périn, C., Chantret, N., & Diévart, A. (2017) · Frontiers in Plant Science · doi:10.3389/fpls.2017.00381 · Cited by 83 · see citing works
Shouting out loud: signaling modules in the regulation of stomatal development
Herrmann, A., & Torii, K. U. (2020) · PLANT PHYSIOLOGY · doi:10.1093/plphys/kiaa061 · Cited by 81 · see citing works
Plant pattern-recognition receptors controlling innate immunity
Li, L., Yu, Y., Zhou, Z., & Zhou, J. (2016) · Science China Life Sciences · doi:10.1007/s11427-016-0115-2 · Cited by 81 · see citing works
Q&A: what are brassinosteroids and how do they act in plants?
Tang, J., Han, Z., & Chai, J. (2016) · BMC Biology · doi:10.1186/s12915-016-0340-8 · Cited by 81 · see citing works
Self-citationPaired Receptor and Coreceptor Kinases Perceive Extracellular Signals to Control Plant Development
Gou, X., & Li, J. (2020) · PLANT PHYSIOLOGY · doi:10.1104/pp.19.01343 · Cited by 80 · see citing works
ERECTA and BAK1 Receptor Like Kinases Interact to Regulate Immune Responses in Arabidopsis
Jordá, L., Sopeña‐Torres, S., Escudero, V., Núñez-Corcuera, B., Delgado-Cerezo, M., Torii, K. U., & Molina, A. (2016) · Frontiers in Plant Science · doi:10.3389/fpls.2016.00897 · Cited by 79 · see citing works
Wang, R., Liu, M., Yuan, M., Osés-Prieto, J. A., Cai, X., Sun, Y., Burlingame, A. L., Wang, Z., & Tang, W. (2015) · Molecular Plant · doi:10.1016/j.molp.2015.10.007 · Cited by 79 · see citing works
Self-citationStructural insight into the activation of plant receptor kinases
Han, Z., Sun, Y., & Chai, J. (2014) · Current Opinion in Plant Biology · doi:10.1016/j.pbi.2014.04.008 · Cited by 77 · see citing works
Self-citationAntagonistic Regulation of Arabidopsis Growth by Brassinosteroids and Abiotic Stresses
Chung, Y., Kwon, S. I., & Choe, S. (2014) · Molecules and Cells · doi:10.14348/molcells.2014.0127 · Cited by 75 · see citing works
Proteolytic Processing of SERK3/BAK1 Regulates Plant Immunity, Development, and Cell Death
Zhou, J., Wang, P., Claus, L. A. N., Savatin, D. V., Xu, G., Wu, S.-J., Meng, X., Russinova, E., He, P., & Shan, L. (2019) · PLANT PHYSIOLOGY · doi:10.1104/pp.18.01503 · Cited by 72 · see citing works
Importance of tyrosine phosphorylation in receptor kinase complexes
Macho, A. P., Lozano‐Durán, R., & Zipfel, C. (2015) · Trends in Plant Science · doi:10.1016/j.tplants.2015.02.005 · Cited by 70 · see citing works
Structural insights into ligand recognition and activation of plant receptor kinases
Song, W., Han, Z., Wang, J., Lin, G., & Chai, J. (2016) · Current Opinion in Structural Biology · doi:10.1016/j.sbi.2016.09.012 · Cited by 69 · see citing works
Self-citationShi, H., Li, X. S., Lv, M., & Li, J. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms231710149 · Cited by 67 · see citing works
DROOPY LEAF1 controls leaf architecture by orchestrating early brassinosteroid signaling
Zhao, M., Tang, S., Zhang, H., He, M., Liu, J., Zhi, H., Sui, Y., Liu, X., Jia, G., Zhao, Z., et al. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2002278117 · Cited by 66 · see citing works
Ligand–receptor interactions in plant hormone signaling
Takeuchi, J., Fukui, K., Seto, Y., Takaoka, Y., & Okamoto, M. (2020) · The Plant Journal · doi:10.1111/tpj.15115 · Cited by 65 · see citing works
The SERK3 elongated allele defines a role for BIR ectodomains in brassinosteroid signalling
Hohmann, U., Nicolet, J., Moretti, A., Hothorn, L. A., & Hothorn, M. (2018) · Nature Plants · doi:10.1038/s41477-018-0150-9 · Cited by 64 · see citing works
Xi, L., Wu, X., Gilbert, M., & Schulze, W. X. (2019) · Frontiers in Plant Science · doi:10.3389/fpls.2019.00472 · Cited by 62 · see citing works
Structural Insight into Recognition of Plant Peptide Hormones by Receptors
Zhang, H., Han, Z., Song, W., & Chai, J. (2016) · Molecular Plant · doi:10.1016/j.molp.2016.10.002 · Cited by 61 · see citing works
Self-citationRegulation of Three Key Kinases of Brassinosteroid Signaling Pathway
Mao, J., & Li, J. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21124340 · Cited by 60 · see citing works
BAK1 is involved in AtRALF1-induced inhibition of root cell expansion
Dressano, K., Ceciliato, P. H. O., da Silva, A. L., Guerrero‐Abad, J. C., Bergonci, T., Ortiz‐Morea, F. A., Bürger, M., Silva-Filho, M. C., & de Moura, D. S. (2017) · PLoS Genetics · doi:10.1371/journal.pgen.1007053 · Cited by 59 · see citing works
Receptor‐Like Kinases: Key Regulators of Plant Development and Defense
Li, J., & Tax, F. E. (2013) · Journal of Integrative Plant Biology · doi:10.1111/jipb.12129 · Cited by 56 · see citing works
Bender, K. W., Wang, X., Cheng, G. B., Kim, H. S., Zielinski, R. E., & Huber, S. C. (2015) · Biochemical Journal · doi:10.1042/bj20141403 · Cited by 56 · see citing works
Huang, L., Zhang, L., Zeng, R., Wang, X., Zhang, H., Wang, L., Liu, S., Wang, X., & Chen, T. (2020) · Genes · doi:10.3390/genes11080919 · Cited by 56 · see citing works
Nucleocytoplasmic trafficking is essential for BAK 1‐ and BKK 1‐mediated cell‐death control
Du, J., Gao, Y., Zhan, Y., Zhang, S., Wu, Y., Xiao, Y., Zou, B., He, K., Gou, X., Li, G., et al. (2016) · The Plant Journal · doi:10.1111/tpj.13125 · Cited by 55 · see citing works
Protein Phosphorylation Response to Abiotic Stress in Plants
Damaris, R. N., & Yang, P. (2021) · Methods in molecular biology · doi:10.1007/978-1-0716-1625-3_2 · Cited by 49 · see citing works
BAK 1 Directly Regulates Brassinosteroid Perception and BRI 1 Activation
He, K., Xu, S., & Li, J. (2013) · Journal of Integrative Plant Biology · doi:10.1111/jipb.12122 · Cited by 52 · see citing works
Moffett, A. S., Bender, K. W., Huber, S. C., & Shukla, D. (2017) · Journal of Biological Chemistry · doi:10.1074/jbc.m117.792762 · Cited by 51 · see citing works
Guo, F., Lv, M., Zhang, J., & Li, J. (2024) · Plant and Cell Physiology · doi:10.1093/pcp/pcae047 · Cited by 50 · see citing works
The brassinosteroid receptor BRI 1 can generate cGMP enabling cGMP ‐dependent downstream signaling
Wheeler, J. I., Wong, A., Marondedze, C., Groen, A. J., Kwezi, L., Freihat, L., Vyas, J., Raji, M. A., Irving, H. R., & Gehring, C. (2017) · The Plant Journal · doi:10.1111/tpj.13589 · Cited by 49 · see citing works
Moonlighting Proteins Shine New Light on Molecular Signaling Niches
Turek, I., & Irving, H. R. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22031367 · Cited by 48 · see citing works
- Authors
- Sun, Y., Han, Z., Tang, J., Hu, Z., Chai, C., Zhou, B., & Chai, J.
- Affiliations
- Center for Life Sciences (CN)
- Corresponding author
- Chai, Jijie
- Venue
- Cell Research
- Published
- 2013-10-15
- Volume
- 23
- Issue
- 11
- Pages
- 1326-1329
- ISSN
- 1001-0602 (ISSN-L)
- 1748-7838
- PMC
- PMC3817550
- OpenAlex
- W1997054375
- Cited by
- 264
- References
- 16
- Citations by year
- 2026: 12 · 2025: 18 · 2024: 23 · 2023: 15 · 2022: 16 · 2021: 15 · 2020: 21 · 2019: 18 · 2018: 29 · 2017: 23 · 2016: 27 · 2015: 20 · 2014: 23 · 2013: 4
- FWCI
- 29.73
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Cell Research (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion, cc-by-nc-sa)
- PubMed (publishedVersion)
- Funders
- Salt Science Research Foundation
- Topics
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Molecular Biology Research
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant-Microbe Interactions and Immunity
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Plant Reproductive Biology
- Keywords
- BAK1, BRI1, brassinosteroids, brassinolide, co-receptors, leucine-rich repeat receptor-like kinases, receptor complex structure, receptor activation, Arabidopsis thaliana, plant hormone signaling, receptor dimerization, ligand binding
- MeSH terms
- Models, Molecular, Protein Conformation, Protein Kinases, Steroids, Heterocyclic, Protein Serine-Threonine Kinases, Arabidopsis Proteins, Brassinosteroids
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
