Brassinosteroids and Plant Steroid Hormone Signaling

Bishop, Gerard J.; Koncz, Csaba

doi:10.1105/tpc.001461

Cited by 270Plant Molecular Biology ResearchPlant biochemistry and biosynthesisLight effects on plants

Brassinosteroids and Plant Steroid Hormone Signaling

Open access

Bishop, Gerard J., Koncz, Csaba·2002·The Plant Cell

DOI 10.1105/tpc.001461PMC PMC151250

Open this paper in CoChat — free account

Abstract

Structures of Steroid Hormones. Chemical structure of brassinolide and castasterone plant steroid hormones, in comparison with the mammalian sex steroid hormones testosterone and oestradiol, and the insect steroid hormone ecdysone. Highlighted are carbon numbers of BL having oxygen moieties that are important for BR activity. BR Biosynthesis Pathway. A simplified scheme of the BR biosynthesis pathway including steps of early and late C-6 oxidation that lead to the synthesis of BL (Noguchi et al., 2000; Shimada et al., 2001). Mutations in genes coding for key biosynthetic enzymes are in bold. det-2, DEETIOLATED-2, steroid 5α reductase (Li et al., 1996); dwf4, DWARF4 cytochrome P450 CYP90B, C-22 hydroxylase (Choe et al., 1998); cpd, CONSTITUTIVE PHOTOMORPHOGENIC and DWARFISM cytochrome P450 CYP90A, C-23 hydroxylase (Szekeres et al., 1996); dx, DWARF cytochrome P450 CYP85, C-6 oxidase (Bishop et al., 1996, 1999; Shimada et al., 2001); DDWF, DARK-INDUCED dwf-LIKE-1, cytochrome P450 CYP92A6, C-2 hydroxylase (Kang et al., 2001). In animal cells, steroid hormones are perceived by binding to their cognate nuclear steroid receptors, which are present in the cytoplasm. Once activated, the receptor complex is transferred to the nucleus to promote or repress transcription of hormone-responsive genes (Beato et al., 1995). This is called genomic signaling because it involves the genome in generating a physiological response. Steroid hormones can also elicit cellular responses in the presence of inhibitors of transcription or protein synthesis, and in enucleated cells. This mechanism is often referred to as nongenomic steroid signaling because it is not mediated by the genome. Some of the nongenomic signaling mechanisms imply a direct interaction between nuclear steroid receptors and other signaling molecules. Nongenomic steroid signaling pathways can also stimulate alterations in second messenger levels, ion fluxes, and protein kinase activities via as-yet uncharacterized steroid carrier proteins and plasma membrane–associated receptors (for reviews, see Wehling, 1997; Falkenstein et al., 2000). The annotation of the Arabidopsis genome sequence (Arabidopsis Genome Initiative, 2000) has confirmed the previous notion (Li and Chory, 1997; McCarty and Chory, 2000) that plants lack close homologs of animal nuclear steroid receptors. Steroid signaling in plants that also leads to alteration in transcription or a physiological response is therefore probably mediated by alternative mechanisms that may be similar to nongenomic steroid signaling in animals. This review highlights the characterization of genes and mutations that is beginning to reveal the mode of steroid hormone action in plants, but at the same time is mindful that this was preceded by the characterization of BR's effects on plant growth and development. To identify regulatory functions in plant steroid signaling, a genetic approach was exploited that aimed at the isolation of brassinosteroid insensitive (bri) Arabidopsis mutants (Clouse et al., 1996). Intriguingly, initial characterization of these bri mutants led only to the identification of multiple mutant alleles of the BRI1 gene, which was subsequently cloned by chromosome walking (Li and Chory, 1997). BRI1 encodes a leucine-rich repeat receptor-like kinase (LRR-RLK) that provides an important key to deciphering primary events in BR signaling. In addition to summarizing our current knowledge on the regulatory role of BRI1, this review provides a brief look at the characterization of further genes that is beginning to provide an insight into some intricate signaling functions controlling steroid hormone action in plants. The leaf bending caused by extracts from Distylium racemosum in the rice lamina inclination assay (Marumo et al., 1968) is one of the earliest reports of BR activity in plants. In this assay, BRs caused dose-dependent swelling of the adaxial cells in the joint between the leaf blade and sheath of etiolated rice seedlings. The angle of the leaf bending caused by the swelling is used as a sensitive bioassay during BR isolation and quantification procedures (Crozier et al. 2000). An early report on growth-promoting activity of “brassin,” from which BL was isolated, was based on BL-mediated stimulation of elongation of bean 2nd and 3rd internode, with higher concentrations causing splitting of the stem (Mitchell et al., 1970; Grove et al., 1979). BL and synthetic analogs were subsequently used in various bioassays, which indicated that in addition to leaf bending, cell elongation, and cell division, BL also effects source/sink relationships (Krizek and Mandava, 1983b), proton pumping and membrane polarization (Cerana et al., 1983; Romani et al., 1983), photosynthesis (Braun and Wild, 1984), and stress responses including thermotolerance (Wilen et al., 1995; Dhaubhadel et al., 1999) and senescence (Mandava et al., 1981). In addition to these effects, BRs promote vascular differentiation (Iwasaki a

Integrity signals

Registry

Crossref · 10.1105/tpc.001461

Cites

109 of 109 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

We couldn’t retrieve this paper’s full text, so its claims and self-check weren’t run. The registry and citation checks still apply.

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?

Plant steroid hormones, brassinosteroids, initiate signaling by combining with plasma membrane receptors.
“However, the plant steroid hormones, brassinosteroids, initiate signaling by combining with plasma membrane receptors [11].”
From G protein-coupled receptors function as cell membrane receptors for the steroid hormone 20-hydroxyecdysone (2020) · cites this paper as [11]
Plant steroid hormones, such as brassinosteroids, employ a nongenomic pathway to initiate signaling by combining with plasma membrane receptor kinases for gene transactivation.
“However, plant steroid hormones, such as brassinosteroids, employ a nongenomic pathway to initiate signaling by combining with plasma membrane receptor kinases for gene transactivation [8].”
From G-protein-coupled receptor participates in 20-hydroxyecdysone signaling on the plasma membrane (2014) · cites this paper as [8]

1 retracted

CLAVATA3, a Multimeric Ligand for the CLAVATA1 Receptor-Kinase
Trotochaud, A. E., Jeong, S., & Clark, S. E. (2000) · Science · doi:10.1126/science.289.5479.613 · Cited by 185 · see citing works
Retracted
Analysis of the genome sequence of the flowering plant Arabidopsis thaliana
Initiative, T. A. G. (2000) · Nature · doi:10.1038/35048692 · Cited by 9,301 · see citing works
Biochemistry & molecular biology of plants
(2001) · Choice Reviews Online · doi:10.5860/choice.38-3895 · Cited by 2,980 · see citing works
FLS2
Gómez‐Gómez, L., & Boller, T. (2000) · Molecular Cell · doi:10.1016/s1097-2765(00)80265-8 · Cited by 2,350 · see citing works
A Receptor Kinase-Like Protein Encoded by the Rice Disease Resistance Gene, Xa21
Song, W.-Y., Wang, G., Chen, L.-L., Kim, H.-S., Pi, L.-Y., Holsten, T., Gardner, J., Wang, B., Zhai, W.-X., Zhu, L.-H., et al. (1995) · Science · doi:10.1126/science.270.5243.1804 · Cited by 2,274 · see citing works
Steroid hormone receptors: Many Actors in search of a plot
Beato, M., Herrlich, P. A., & Schütz, G. (1995) · Cell · doi:10.1016/0092-8674(95)90201-5 · Cited by 1,806 · 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
Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases
Shiu, S., & Bleecker, A. B. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.181141598 · Cited by 1,472 · see citing works
BRASSINOSTEROIDS: Essential Regulators of Plant Growth and Development
Clouse, S. D., & Sasse, J. M. (1998) · Annual Review of Plant Physiology and Plant Molecular Biology · doi:10.1146/annurev.arplant.49.1.427 · Cited by 1,462 · see citing works
The CLAVATA1Gene Encodes a Putative Receptor Kinase That Controls Shoot and Floral Meristem Size in Arabidopsis
Clark, S. E., Williams, R. W., & Meyerowitz, E. M. (1997) · Cell · doi:10.1016/s0092-8674(00)80239-1 · Cited by 1,373 · see citing works
Cholesterol Modification of Hedgehog Signaling Proteins in Animal Development
Porter, J. A., Young, K. E., & Beachy, P. A. (1996) · Science · doi:10.1126/science.274.5285.255 · Cited by 1,360 · see citing works
Signaling of Cell Fate Decisions by CLAVATA3 in Arabidopsis Shoot Meristems
Fletcher, J. C., Brand, U., Running, M., Simon, R. G., & Meyerowitz, E. M. (1999) · Science · doi:10.1126/science.283.5409.1911 · Cited by 1,359 · see citing works
The leucine-rich repeat: a versatile binding motif
Kobe, B., & Deisenhofer, J. (1994) · Trends in Biochemical Sciences · doi:10.1016/0968-0004(94)90090-6 · Cited by 1,212 · see citing works
Dependence of Stem Cell Fate in Arabidopsis on a Feedback Loop Regulated by CLV3 Activity
Brand, U., Fletcher, J. C., Hobe, M., Meyerowitz, E. M., & Simon, R. G. (2000) · Science · doi:10.1126/science.289.5479.617 · Cited by 1,123 · see citing works
The Toll gene of drosophila, required for dorsal-ventral embryonic polarity, appears to encode a transmembrane protein
Hashimoto, C., Hudson, K., & Anderson, K. V. (1988) · Cell · doi:10.1016/0092-8674(88)90516-8 · Cited by 1,097 · see citing works
Brassinolide, a plant growth-promoting steroid isolated from Brassica napus pollen
Grove, M. D., Spencer, G. F., Rohwedder, W. K., Mandava, N. B., Worley, J. F., Warthen, J. D., Steffens, G. L., Flippen-Anderson, J. L., & Cook, J. C. (1979) · Nature · doi:10.1038/281216a0 · Cited by 1,024 · see citing works
Brassinosteroids Rescue the Deficiency of CYP90, a Cytochrome P450, Controlling Cell Elongation and De-etiolation in Arabidopsis
Szekeres, M., Németh, K., Koncz–Kálmán, Z., Mathur, J., Kauschmann, A., Altmann, T., Rédei, G. P., Nagy, F., Schell, J., & Koncz, C. (1996) · Cell · doi:10.1016/s0092-8674(00)81094-6 · Cited by 998 · see citing works
Self-citation
Multiple Actions of Steroid Hormones—A Focus on Rapid, Nongenomic Effects
Falkenstein, E., Tillmann, H.-C., Christ, M., Feuring, M., & Wehling, M. (2000) · Pharmacological Reviews · doi:10.1016/s0031-6997(24)01468-6 · Cited by 986 · see citing works
Isolation of the Tomato Cf-9 Gene for Resistance to Cladosporium fulvum by Transposon Tagging
Jones, D. A., Thomas, C. M., Hammond-Kosack, K. E., Balint-Kurti, P. J., & Jones, J. D. G. (1994) · Science · doi:10.1126/science.7973631 · Cited by 912 · see citing works
A Role for Brassinosteroids in Light-Dependent Development of Arabidopsis
Li, J., Nagpal, P., Vitart, V., McMorris, T. C., & Chory, J. (1996) · Science · doi:10.1126/science.272.5260.398 · Cited by 856 · see citing works
BRI1 is a critical component of a plasma-membrane receptor for plant steroids
Wang, Z.-Y., Seto, H., Fujioka, S., Yoshida, S., & Chory, J. (2001) · Nature · doi:10.1038/35066597 · Cited by 846 · see citing works
Drosophila Toll is activated by Gram-positive bacteria through a circulating peptidoglycan recognition protein
Michel, T., Reichhart, J., Hoffmann, J., & Royet, J. (2001) · Nature · doi:10.1038/414756a · Cited by 829 · see citing works
A Brassinosteroid-Insensitive Mutant in Arabidopsis thaliana Exhibits Multiple Defects in Growth and Development
Clouse, S. D., Langford, M., & McMorris, T. C. (1996) · PLANT PHYSIOLOGY · doi:10.1104/pp.111.3.671 · Cited by 819 · see citing works
Loss of Function of a Rice brassinosteroid insensitive1 Homolog Prevents Internode Elongation and Bending of the Lamina Joint
Yamamuro, C., Ihara, Y., Wu, X., Noguchi, T., Fujioka, S., Takatsuto, S., Ashikari, M., Kitano, H., & Matsuoka, M. (2000) · The Plant Cell · doi:10.1105/tpc.12.9.1591 · Cited by 758 · see citing works
A structural basis of the interactions between leucine-rich repeats and protein ligands
Kobe, B., & Deisenhofer, J. (1995) · Nature · doi:10.1038/374183a0 · Cited by 729 · see citing works
The Arabidopsis ERECTA gene encodes a putative receptor protein kinase with extracellular leucine-rich repeats.
Torii, K. U., Mitsukawa, N., Oosumi, T., et al. (1996) · The Plant Cell · doi:10.1105/tpc.8.4.735 · Cited by 716 · see citing works
Regulation of Brassinosteroid Signaling by a GSK3/SHAGGY-Like Kinase
Li, J., & Nam, K. H. (2002) · Science · doi:10.1126/science.1065769 · Cited by 668 · see citing works
SPECIFIC, NONGENOMIC ACTIONS OF STEROID HORMONES
Wehling, M. (1997) · Annual Review of Physiology · doi:10.1146/annurev.physiol.59.1.365 · Cited by 657 · see citing works
The Arabidopsis CLAVATA2 Gene Encodes a Receptor-Like Protein Required for the Stability of the CLAVATA1 Receptor-Like Kinase
Jeong, S., Trotochaud, A. E., & Clark, S. E. (1999) · The Plant Cell · doi:10.1105/tpc.11.10.1925 · Cited by 648 · see citing works
Cholesterol Modification of Sonic Hedgehog Is Required for Long-Range Signaling Activity and Effective Modulation of Signaling by Ptc1
Lewis, P. M., Dunn, M., McMahon, J. A., Logan, M. P. O., Martin, J. F., St‐Jacques, B., & McMahon, A. P. (2001) · Cell · doi:10.1016/s0092-8674(01)00369-5 · Cited by 513 · see citing works
Perception of Brassinosteroids by the Extracellular Domain of the Receptor Kinase BRI1
He, Z., Wang, Z., Li, J., Zhu, Q., Lamb, C. J., Ronald, P. C., & Chory, J. (2000) · Science · doi:10.1126/science.288.5475.2360 · Cited by 492 · see citing works
The DWF4 Gene of Arabidopsis Encodes a Cytochrome P450 That Mediates Multiple 22α-Hydroxylation Steps in Brassinosteroid Biosynthesis
Choe, S., Dilkes, B. P., Fujioka, S., Takatsuto, S., Sakurai, A., & Feldmann, K. A. (1998) · The Plant Cell · doi:10.1105/tpc.10.2.231 · Cited by 484 · see citing works
BIN2 , a New Brassinosteroid-Insensitive Locus in Arabidopsis
Li, J., Nam, K. H., Vafeados, D. K., et al. (2001) · PLANT PHYSIOLOGY · doi:10.1104/pp.127.1.14 · Cited by 475 · see citing works
Toll receptors in innate immunity.
Imler, J., & Hoffmann, J. (2001) · Trends in Cell Biology · doi:10.1016/s0962-8924(01)02004-9 · Cited by 474 · see citing works
Brassinosteroid-Insensitive-1 Is a Ubiquitously Expressed Leucine-Rich Repeat Receptor Serine/Threonine Kinase
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
Brassinosteroid-Insensitive Dwarf Mutants of Arabidopsis Accumulate Brassinosteroids
Noguchi, T., Fujioka, S., Choe, S., Takatsuto, S., Yoshida, S., Yuan, H., Feldmann, K. A., & Tax, F. E. (1999) · PLANT PHYSIOLOGY · doi:10.1104/pp.121.3.743 · Cited by 473 · see citing works
A Role for Brassinosteroids in Germination in Arabidopsis
Steber, C. M., & McCourt, P. (2001) · PLANT PHYSIOLOGY · doi:10.1104/pp.125.2.763 · Cited by 463 · see citing works
The CLAVATA1 Receptor-like Kinase Requires CLAVATA3 for Its Assembly into a Signaling Complex That Includes KAPP and a Rho-Related Protein
Trotochaud, A. E., Hao, T., Wu, G., Yang, Z., & Clark, S. E. (1999) · The Plant Cell · doi:10.1105/tpc.11.3.393 · Cited by 417 · see citing works
Brassins—a New Family of Plant Hormones from Rape Pollen
Mitchell, J. W., Mandava, N. B., Worley, J. F., Plimmer, J. R., & Smith, M. V. (1970) · Nature · doi:10.1038/2251065a0 · Cited by 401 · see citing works
Characterization of Brassinazole, a Triazole-Type Brassinosteroid Biosynthesis Inhibitor
Asami, T., Min, Y. K., Nagata, N., Yamagishi, K., Takatsuto, S., Fujioka, S., Murofushi, N., Yamaguchi, I., & Yoshida, S. (2000) · PLANT PHYSIOLOGY · doi:10.1104/pp.123.1.93 · Cited by 398 · see citing works
HAESA, an Arabidopsis leucine-rich repeat receptor kinase, controls floral organ abscissionPreprint
Jinn, T.-L., Stone, J. M., & Walker, J. C. (2000) · Genes & Development · doi:10.1101/gad.14.1.108 · Cited by 389 · see citing works
Promotive effect of brassinosteroids on cell division involves a distinct CycD3‐induction pathway in Arabidopsis
Hu, Y., Bao, F., & Li, J. (2000) · The Plant Journal · doi:10.1046/j.1365-313x.2000.00915.x · Cited by 372 · see citing works
Genetic evidence for an essential role of brassinosteroids in plant development
Kauschmann, A., Jessop, A. C., Koncz, C., Szekeres, M., Willmitzer, L., & Altmann, T. (1996) · The Plant Journal · doi:10.1046/j.1365-313x.1996.9050701.x · Cited by 353 · see citing works
Self-citation
SIGNALING PATHWAYS THAT ESTABLISH THE DORSAL-VENTRAL PATTERN OF THE DROSOPHILA EMBRYO
Morisalo, D., & Anderson, K. V. (1995) · Annual Review of Genetics · doi:10.1146/annurev.ge.29.120195.002103 · Cited by 351 · see citing works
Overexpression of DWARF4 in the brassinosteroid biosynthetic pathway results in increased vegetative growth and seed yield in Arabidopsis
Choe, S., Fujioka, S., Noguchi, T., Takatsuto, S., Yoshida, S., & Feldmann, K. A. (2001) · The Plant Journal · doi:10.1046/j.1365-313x.2001.01055.x · Cited by 340 · see citing works
The tomato DWARF enzyme catalyses C-6 oxidation in brassinosteroid biosynthesis
Bishop, G. J., Nomura, T., Yokota, T., Harrison, K., Noguchi, T., Fujioka, S., Takatsuto, S., Jones, J. D. G., & Kamiya, Y. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.4.1761 · Cited by 332 · see citing works
Self-citation
The Arabidopsis DIMINUTO/DWARF1 Gene Encodes a Protein Involved in Steroid Synthesis
Klahre, U., Noguchi, T., Fujioka, S., Takatsuto, S., Yokota, T., Nomura, T., Yoshida, S., & Chua, N. (1998) · The Plant Cell · doi:10.1105/tpc.10.10.1677 · Cited by 290 · see citing works
The structure, biosynthesis and function of brassinosteroids
Yokota, T. (1997) · Trends in Plant Science · doi:10.1016/s1360-1385(97)01017-0 · Cited by 262 · see citing works
Plants Steroid Hormones, Brassinosteroids: Current Highlights of Molecular Aspects on their Synthesis/Metabolism, Transport, Perception and Response
Bishop, G. J., & Yokota, T. (2001) · Plant and Cell Physiology · doi:10.1093/pcp/pce018 · Cited by 260 · see citing works
Self-citation
Brassinosteroids : steroidal plant hormones
Sakurai, A., 横田, 孝., & Clouse, S. D. (1999) · Springer eBooks · Cited by 247 · see citing works
Treatment with 24-epibrassinolide, a brassinosteroid, increases the basic thermotolerance of Brassica napus and tomato seedlings
Dhaubhadel, S., Chaudhary, S., Dobinson, K. F., & Krishna, P. (1999) · Plant Molecular Biology · doi:10.1023/a:1006283015582 · Cited by 239 · see citing works
Control of Meristem Development by CLAVATA1 Receptor Kinase and Kinase-Associated Protein Phosphatase Interactions1
Stone, J. M., Trotochaud, A. E., Walker, J. C., & Clark, S. E. (1998) · PLANT PHYSIOLOGY · doi:10.1104/pp.117.4.1217 · Cited by 237 · see citing works
A possible role for kinase-associated protein phosphatase in the Arabidopsis CLAVATA1 signaling pathway
Williams, R. W., Wilson, J. M., & Meyerowitz, E. M. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.19.10467 · Cited by 236 · see citing works
BRS1, a serine carboxypeptidase, regulates BRI1 signaling in Arabidopsis thaliana
Li, J., Lease, K. A., Tax, F. E., et al. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.091065998 · Cited by 229 · see citing works
Brassinosteroid-6-Oxidases from Arabidopsis and Tomato Catalyze Multiple C-6 Oxidations in Brassinosteroid Biosynthesis
Shimada, Y., Fujioka, S., Miyauchi, N., Kushiro, M., Takatsuto, S., Nomura, T., Yokota, T., Kamiya, Y., Bishop, G. J., & Yoshida, S. (2001) · PLANT PHYSIOLOGY · doi:10.1104/pp.126.2.770 · Cited by 227 · see citing works
Self-citation
Transcription of the Arabidopsis CPD gene, encoding a steroidogenic cytochrome P450, is negatively controlled by brassinosteroids
Mathur, J., Molnár, G., Fujioka, S., Takatsuto, S., Sakurai, A., Yokota, T., Adam, G., Voigt, B., Nagy, F., Maas, C., et al. (1998) · The Plant Journal · doi:10.1046/j.1365-313x.1998.00158.x · Cited by 225 · see citing works
Self-citation
The Arabidopsis XET‐related gene family: environmental and hormonal regulation of expression
Xu, W. M., Campbell, P. H., Vargheese, A. K., et al. (1996) · The Plant Journal · doi:10.1046/j.1365-313x.1996.9060879.x · Cited by 225 · see citing works
Molecular Cloning and Characterization of a Brassinosteroid-Regulated Gene from Elongating Soybean (Glycine max L.) Epicotyls
Zurek, D. M., & Clouse, S. D. (1994) · PLANT PHYSIOLOGY · doi:10.1104/pp.104.1.161 · Cited by 218 · see citing works
Cell signalling at the shoot meristem
Clark, S. E. (2001) · Nature Reviews Molecular Cell Biology · doi:10.1038/35067079 · Cited by 217 · see citing works
A Putative Role for the Tomato Genes DUMPY and CURL-3 in Brassinosteroid Biosynthesis and Response
Koka, C. R., Cerny, R. E., Gardner, R. G., Noguchi, T., Fujioka, S., Takatsuto, S., Yoshida, S., & Clouse, S. D. (2000) · PLANT PHYSIOLOGY · doi:10.1104/pp.122.1.85 · Cited by 215 · see citing works
The tomato Dwarf gene isolated by heterologous transposon tagging encodes the first member of a new cytochrome P450 family.
Bishop, G. J., Harrison, K., & Jones, J. D. G. (1996) · The Plant Cell · doi:10.1105/tpc.8.6.959 · Cited by 206 · see citing works
Self-citation
Blockage of Brassinosteroid Biosynthesis and Sensitivity Causes Dwarfism in Garden Pea
Nomura, T., Nakayama, M., Reid, J. B., et al. (1997) · PLANT PHYSIOLOGY · doi:10.1104/pp.113.1.31 · Cited by 202 · see citing works
Brassinosteroids Induce Entry into the Final Stage of Tracheary Element Differentiation in Cultured Zinnia Cells
Yamamoto, R., Demura, T., & Fukuda, H. (1997) · Plant and Cell Physiology · doi:10.1093/oxfordjournals.pcp.a029262 · Cited by 191 · see citing works
Recombinant Brassinosteroid Insensitive 1 Receptor-Like Kinase Autophosphorylates on Serine and Threonine Residues and Phosphorylates a Conserved Peptide Motif in Vitro
Oh, M., Ray, W. K., Huber, S. C., Asara, J. M., Gage, D. A., & Clouse, S. D. (2000) · PLANT PHYSIOLOGY · doi:10.1104/pp.124.2.751 · Cited by 190 · see citing works
The UCU1 Arabidopsis Gene Encodes a SHAGGY/GSK3-like Kinase Required for Cell Expansion along the Proximodistal Axis
Pérez‐Pérez, J. M., Ponce, M. R., & Micol, J. L. (2002) · Developmental Biology · doi:10.1006/dbio.2001.0543 · Cited by 177 · see citing works
Light and Brassinosteroid Signals Are Integrated via a Dark-Induced Small G Protein in Etiolated Seedling Growth
Kang, J., Yun, J., Kim, D., Chung, K.-S., Fujioka, S., Kim, J., Dae, H.-W., Yoshida, S., Takatsuto, S., Song, P., et al. (2001) · Cell · doi:10.1016/s0092-8674(01)00370-1 · Cited by 176 · see citing works
Steroid hormones and plant growth and development
Geuns, J. M. C. (1978) · Phytochemistry · doi:10.1016/s0031-9422(00)89671-5 · Cited by 169 · see citing works
Biosynthetic Pathways of Brassinolide in Arabidopsis
Noguchi, T., Fujioka, S., Choe, S., Takatsuto, S., Tax, F. E., Yoshida, S., & Feldmann, K. A. (2000) · PLANT PHYSIOLOGY · doi:10.1104/pp.124.1.201 · Cited by 168 · see citing works
Control of Specific Gene Expression by Gibberellin and Brassinosteroid
Bouquin, T., Meier, C., Foster, R., et al. (2001) · PLANT PHYSIOLOGY · doi:10.1104/pp.010173 · Cited by 162 · see citing works
Brassinolide, a growth‐promoting steroidal lactone
Yopp, J. H., Mandava, N. B., & Sasse, J. M. (1981) · Physiologia Plantarum · doi:10.1111/j.1399-3054.1981.tb02729.x · Cited by 159 · see citing works
Brassinosteroids and gibberellins promote tobacco seed germination by distinct pathways
Leubner‐Metzger, G. (2001) · Planta · doi:10.1007/s004250100542 · Cited by 155 · see citing works
Brassinosteroids Act as Regulators of Tracheary-Element Differentiation in Isolated Zinnia Mesophyll Cells
Iwasaki, T., & Shibaoka, H. (1991) · Plant and Cell Physiology · doi:10.1093/oxfordjournals.pcp.a078163 · Cited by 152 · see citing works
Brassinosteroid actions in plants
Li, J., & Chory, J. (1999) · Journal of Experimental Botany · doi:10.1093/jxb/50.332.275 · Cited by 151 · see citing works
The sax1 dwarf mutant of Arabidopsis thaliana shows altered sensitivity of growth responses to abscisic acid, auxin, gibberellins and ethylene and is partially rescued by exogenous brassinosteroid
Ephritikhine, G., Fellner, M., Vannini, C., Lapous, D., & Barbier‐Brygoo, H. (1999) · The Plant Journal · doi:10.1046/j.1365-313x.1999.00454.x · Cited by 150 · see citing works
Receptor kinase activation and signal transduction in plants: an emerging picture
Torii, K. U. (2000) · Current Opinion in Plant Biology · doi:10.1016/s1369-5266(00)00097-2 · Cited by 139 · see citing works
Conservation and Innovation in Plant Signaling Pathways
McCarty, D. R., & Chory, J. (2000) · Cell · doi:10.1016/s0092-8674(00)00113-6 · Cited by 137 · see citing works
Recent progress in brassinosteroid research
Sasse, J. M. (1997) · Physiologia Plantarum · doi:10.1111/j.1399-3054.1997.tb03076.x · Cited by 136 · see citing works
Characterization of XET-Related Genes of Rice
Uozu, S., Miyako, T.-U., Kitano, H., et al. (2000) · PLANT PHYSIOLOGY · doi:10.1104/pp.122.3.853 · Cited by 135 · see citing works
The current status of physiology and biochemistry of brassinosteroids
Sakurai, A., & Fujioka, S. (1993) · Plant Growth Regulation · doi:10.1007/bf00024257 · Cited by 134 · see citing works
Molecular physiology of brassinosteroids revealed by the analysis of mutants
Altmann, T. (1999) · Planta · doi:10.1007/s004250050528 · Cited by 127 · see citing works
Brassinosteroid/Sterol Synthesis and Plant Growth as Affected bylka and lkb Mutations of Pea1
Nomura, T., Kitasaka, Y., Takatsuto, S., et al. (1999) · PLANT PHYSIOLOGY · doi:10.1104/pp.119.4.1517 · Cited by 124 · see citing works
Brassinolide, a growth‐promoting steroidal lactone
Mandava, N. B., Sasse, J. M., & Yopp, J. H. (1981) · Physiologia Plantarum · doi:10.1111/j.1399-3054.1981.tb02730.x · Cited by 124 · see citing works
Brassinosteroid signal transduction: still casting the actors
Schumacher, K., & Chory, J. (2000) · Current Opinion in Plant Biology · doi:10.1016/s1369-5266(99)00038-2 · Cited by 123 · see citing works
Effects of 24‐epibrassinolide on freezing and thermotolerance of bromegrass (Bromus inermis) cell cultures
Wilen, R. W., Sacco, M. A., Gusta, L. V., et al. (1995) · Physiologia Plantarum · doi:10.1111/j.1399-3054.1995.tb00827.x · Cited by 99 · see citing works
The Influence of Brassinosteroid on Growth and Parameters of Photosynthesis of Wheat and Mustard Plants
Braun, P., & Wild, A. (1984) · Journal of Plant Physiology · doi:10.1016/s0176-1617(84)80088-7 · Cited by 99 · see citing works
Brassinazole, an Inhibitor of Brassinosteroid Biosynthesis, Inhibits Development of Secondary Xylem in Cress Plants (Lepidium sativum)
Nagata, N., Asami, T., & Yoshida, S. (2001) · Plant and Cell Physiology · doi:10.1093/pcp/pce122 · Cited by 97 · see citing works
The effect of brassinosteroid on auxin‐induced ethylene production by etiolated mung bean segments
Arteca, R. N., Tsai, D., Schlagnhaufer, C. D., et al. (1983) · Physiologia Plantarum · doi:10.1111/j.1399-3054.1983.tb06277.x · Cited by 83 · see citing works
Steroid signaling in plants: from the cell surface to the nucleus
Friedrichsen, D. M., & Chory, J. (2001) · BioEssays · doi:10.1002/bies.1148 · Cited by 83 · see citing works
A Possible Double Role for Brassinolide in the Reorientation of Cortical Microtubules in the Epidermal Cells of Azuki Bean Epicotyls
Mayumi, K., & Shibaoka, H. (1995) · Plant and Cell Physiology · doi:10.1093/oxfordjournals.pcp.a078734 · Cited by 79 · see citing works
Receptor serine/threonine protein kinases in signalling: analysis of the erecta receptor‐like kinase of Arabidopsis thaliana
Lease, K. A., Lau, N. Y., Schuster, R. A., et al. (2001) · New Phytologist · doi:10.1046/j.1469-8137.2001.00150.x · Cited by 75 · see citing works
Expression of a plant gene with sequence similarity to animal TGF‐β receptor interacting protein is regulated by brassinosteroids and required for normal plant development
Jiang, J., & Clouse, S. D. (2001) · The Plant Journal · doi:10.1046/j.1365-313x.2001.01007.x · Cited by 74 · see citing works
Tissue‐specific induction of the mRNA for an extracellular invertase isoenzyme of tomato by brassinosteroids suggests a role for steroid hormones in assimilate partitioning
Goetz, M., Godt, D. E., & Roitsch, T. G. (2000) · The Plant Journal · doi:10.1046/j.1365-313x.2000.00766.x · Cited by 74 · see citing works
An Arabidopsis Cell Cycle–Dependent Kinase-Related Gene, CDC2b, Plays a Role in Regulating Seedling Growth in Darkness
Yoshizumi, T., Nagata, N., Shimada, H., & Matsui, M. (1999) · The Plant Cell · doi:10.1105/tpc.11.10.1883 · Cited by 73 · see citing works
Effects of a brassinosteroid on growth and electrogenic proton extrusion in Azuki bean epicotyls
Cerana, R., Bonetti, A., Marrè, M. T., et al. (1983) · Physiologia Plantarum · doi:10.1111/j.1399-3054.1983.tb06565.x · Cited by 70 · see citing works
Molecular genetic analysis of brassinosteroid action
Clouse, S. D. (1997) · Physiologia Plantarum · doi:10.1111/j.1399-3054.1997.tb03077.x · Cited by 56 · see citing works
Review article. Brassinosteroid actions in plants
Li, J. (1999) · Journal of Experimental Botany · doi:10.1093/jexbot/50.332.275 · Cited by 53 · see citing works
Effects of a brassinosteroid on growth and electrogenic proton extrusion in maize root segments
Romani, G., Marriè, M. T., Bonetti, A., Cerana, R., LADO, P., & Marrè, E. (1983) · Physiologia Plantarum · doi:10.1111/j.1399-3054.1983.tb06275.x · Cited by 52 · see citing works
Brassinosteroid signaling in plants
Müssig, C., & Altmann, T. (2001) · Trends in Endocrinology and Metabolism · doi:10.1016/s1043-2760(01)00477-5 · Cited by 37 · see citing works
Biochemical and genetic analysis of brassinosteroid metabolism and function in Arabidopsis
Szekeres, M., & Koncz, C. (1998) · Plant Physiology and Biochemistry · doi:10.1016/s0981-9428(98)80099-5 · Cited by 36 · see citing works
Self-citation
Receptor-like kinases in plant development
Torii, K. U., & Clark, S. E. (2000) · Advances in botanical research · doi:10.1016/s0065-2296(00)32026-2 · Cited by 34 · see citing works
Epibrassinolide‐inhibition of development of excised, adventitious and intact roots of tomato (Lycopersicon esculentum): comparison with the effects of steroidal estrogens
Guan, M., & Roddick, J. G. (1988) · Physiologia Plantarum · doi:10.1111/j.1399-3054.1988.tb02043.x · Cited by 34 · see citing works
Steroidal Estrogens and Androgens in Relation to Reproductive Development in Higher Plants
Jones, J. L., & Roddick, J. G. (1988) · Journal of Plant Physiology · doi:10.1016/s0176-1617(88)80047-6 · Cited by 32 · see citing works
Influence of spectral quality on the growth response of intact bean plants to brassinosteroid, a growth‐promoting steroidal lactone. I. Stem elongation and morphogenesis
Krizek, D. T., & Mandava, N. B. (1983) · Physiologia Plantarum · doi:10.1111/j.1399-3054.1983.tb02294.x · Cited by 31 · see citing works
Comparison of the effects of epibrassinolide and steroidal estrogens on adventitious root growth and early shoot development in mung bean cuttings
Guan, M., & Roddick, J. G. (1988) · Physiologia Plantarum · doi:10.1111/j.1399-3054.1988.tb00621.x · Cited by 30 · see citing works
Influence of spectral quality on the growth response of intact bean plants to brassinosteroid, a growth‐promoting steroidal lactone. II. Chlorophyll content and partitioning of assimilate
Krizek, D. T., & Mandava, N. B. (1983) · Physiologia Plantarum · doi:10.1111/j.1399-3054.1983.tb02295.x · Cited by 26 · see citing works
Light Inhibition of Brassinosteroid-Induced Ethylene Production
Arteca, R. N., & Bachman, J. M. (1987) · Journal of Plant Physiology · doi:10.1016/s0176-1617(87)80097-4 · Cited by 25 · see citing works
The Presence of Novel Plant Growth Regulators in Leaves of Distylium racemosum Sied et Zucc
Marumo, S., Hattori, H., Abe, H., et al. (1968) · Agricultural and Biological Chemistry · doi:10.1271/bbb1961.32.528 · Cited by 23 · see citing works
Arabidopsis research 2001.
Eckardt, N. A., Araki, T., Benning, C., et al. (2001) · PubMed · doi:10.1105/tpc.130920 · Cited by 10 · see citing works
Conservation and Innovation.
Rivers, W. M. (1972) · Cited by 8 · see citing works

Flagged first, then by citations

Sorted by citations

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
Anticancer and antiproliferative activity of natural brassinosteroids
Malíková, J., Swaczynová, J., Kolář, Z., & Strnad, M. (2008) · Phytochemistry · doi:10.1016/j.phytochem.2007.07.028 · Cited by 170 · see citing works
Steroid signaling in plants and insects—common themes, different pathways
Thummel, C. S., & Chory, J. (2002) · Genes & Development · doi:10.1101/gad.1042102 · Cited by 161 · see citing works
G protein-coupled receptors function as cell membrane receptors for the steroid hormone 20-hydroxyecdysone
Zhao, X.-F. (2020) · Cell Communication and Signaling · doi:10.1186/s12964-020-00620-y · Cited by 60 · see citing works
G-protein-coupled receptor participates in 20-hydroxyecdysone signaling on the plasma membrane
Cai, M.-J., Dong, D.-J., Wang, Y., Liu, P.-C., Liu, W., Wang, J.-X., & Zhao, X.-F. (2014) · Cell Communication and Signaling · doi:10.1186/1478-811x-12-9 · Cited by 44 · see citing works

Authors: Bishop, G. J., & Koncz, C.
Affiliations: Max Planck Society (DE)
ORCID: Bishop, Gerard J.
Koncz, Csaba
Venue: The Plant Cell
Publisher: Oxford University Press (OUP)
Published: 2002-05
Volume: 14
Issue: suppl 1
Pages: S97-S110
ISSN: 1040-4651 (ISSN-L)
1532-298X
DOI: 10.1105/tpc.001461
PMC: PMC151250
OpenAlex: W1749881282
Cited by: 270
References: 109
Citations by year: 2026: 5 · 2025: 10 · 2024: 8 · 2023: 11 · 2022: 9 · 2021: 12 · 2020: 13 · 2019: 10 · 2018: 9 · 2017: 10 · 2016: 9 · 2015: 9 · 2014: 17 · 2013: 6 · 2012: 15
FWCI: 22.38
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: aspb.org/publications/aspb-journals/open-articles (vor, 365 d)
Locations: The Plant Cell (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Max Planck Institute for Plasma Physics (submittedVersion)
Max Planck Digital Library (submittedVersion)
MPG.PuRe (Max Planck Society) (submittedVersion)
Topics: Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Molecular Biology Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Plant biochemistry and biosynthesis
Life Sciences › Agricultural and Biological Sciences › Plant Science › Light effects on plants
Keywords: brassinosteroids, brassinolide, castasterone, plant steroid hormones, steroidogenesis, cytochrome P450, non-genomic steroid action, nuclear steroid receptors, plant growth and development, plant hormones, ecdysone, testosterone, estradiol
MeSH terms: Cell Membrane, Cholestanols, Membrane Proteins, Mutation, Plant Growth Regulators, Protein Kinases, Steroids, Heterocyclic, Signal Transduction, Protein Serine-Threonine Kinases, Arabidopsis, Receptor Protein-Tyrosine 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

Brassinosteroids and Plant Steroid Hormone Signaling

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Cites

Cited by

Related

Record

About these checks