Brassinosteroid-Promoted Growth

Abstract

Brassinosteroids (BRs) are highly potent growth-promoting sterol derivatives. BR-deficient or BR-insensitive mutants display dwarfism. Whole plants and excised tissues have been used to analyse the mechanisms involved in BR-promoted growth. BR stimulates cell elongation and cell division, and BR has specific effects on differentiation. Underlying physiological pathways include modification of cell wall properties, effects on carbohydrate assimilation and allocation, and control of aquaporin activities. BR apparently coordinates and integrates diverse processes required for growth, partly via interactions with other phytohormones setting the frame for BR responses. Ultimately, BR-promoted growth is mediated through genomic pathways. Positive regulators of the BR response (such as BZR1 and BES1) and putative downstream components (such as EXO) are involved in the regulation of BR-responsive genes and growth promotion. BR-responsive genes have been identified in several plant species. However, causal links between physiological effects and changes of transcript patterns, for the most part, are still unresolved. This review focuses on physiology and molecular mechanisms underlying BR-promoted growth in the different plant organs. Interactions with other phytohormones are discussed.

Brassinosteroid - cell division - cell elongation - growth

References

• 1 Altmann T.. Molecular physiology of brassinosteroids revealed by the analysis of mutants.  Planta. (1999);  208 1-11
• 2 Arteca J. M., Arteca R. N.. Brassinosteroid-induced exaggerated growth in hydroponically grown Arabidopsis plants.  Physiologia Plantarum. (2001);  112 104-112
• 3 Asami T., Min Y. K., Nagata N., Yamagishi K., Takatsuto S., Fujioka S., Murofushi N., Yamaguchi I., Yoshida S.. Characterization of brassinazole, a triazole-type brassinosteroid biosynthesis inhibitor.  Plant Physiology. (2000);  123 93-99
• 4 Azpiroz R., Wu Y. W., Locascio J. C., Feldmann K. A.. An Arabidopsis brassinosteroid-dependent mutant is blocked in cell elongation.  Plant Cell. (1998);  10 219-230
• 5 Bajguz A., Tretyn A.. The chemical characteristic and distribution of brassinosteroids in plants.  Phytochemistry. (2003);  62 1027-1046
• 6 Bancos S., Nomura T., Sato T., Molnar G., Bishop G.. J., Koncz C., Yokota T., Nagy F., Szekeres M.. Regulation of transcript levels of the Arabidopsis cytochrome P450 genes involved in brassinosteroid biosynthesis.  Plant Physiology. (2002);  130 504-513
• 7 Bishop G. J.. Brassinosteroid mutants of crops.  Journal of Plant Growth Regulation. (2003);  22 325-335
• 8 Bishop G. J., Harrison K., Jones J. D. G.. The tomato Dwarf gene isolated by heterologous transposon tagging encodes the first member of a new cytochrome P450 family.  Plant Cell. (1996);  8 959-969
• 9 Bishop G. J., Nomura T., Yokota T., Harrison K., Noguchi T., Fujioka S., Takatsuto S., Jones J. D. G., Kamiya Y.. The tomato DWARF enzyme catalyses C-6 oxidation in brassinosteroid biosynthesis.  Proceedings of the National Academy of Sciences of the USA. (1999);  96 1761-1766
• 10 Bouquin T., Meier C., Foster R., Nielsen M. E., Mundy J.. Control of specific gene expression by gibberellin and brassinosteroid.  Plant Physiology. (2001);  127 450-458
• 11 Braun P., Wild A.. The influence of brassinosteroid on growth and parameters of photosynthesis of wheat and mustard plants.  Journal of Plant Physiology. (1984);  116 189-196
• 12 Cerana R., Bonetti A., Marre M. T., Romani G., Lado P., Marre E.. Effects of a brassinosteroid on growth and electrogenic proton extrusion in Azuki bean epicotyls.  Physiologia Plantarum. (1983);  59 23-27
• 13 Choe S., Fujioka S., Noguchi T., Takatsuto S., Yoshida S., Feldmann K. A.. Overexpression of DWARF4 in the brassinosteroid biosynthetic pathway results in increased vegetative growth and seed yield in Arabidopsis. .  The Plant Journal. (2001);  26 573-582
• 14 Choe S., Schmitz R. J., Fujioka S., Takatsuto S., Lee M. O., Yoshida S., Feldmann K. A., Tax F. E.. Arabidopsis brassinosteroid-insensitive dwarf12 mutants are semidominant and defective in a glycogen synthase kinase 3b-like kinase.  Plant Physiology. (2002);  130 1506-1515
• 15 Chono M., Honda I., Zeniya H., Yoneyama K., Saisho D., Takeda K., Takatsuto S., Hoshino T., Watanabe Y.. A semidwarf phenotype of barley uzu results from a nucleotide substitution in the gene encoding a putative brassinosteroid receptor.  Plant Physiology. (2003);  133 1209-1219
• 16 Clouse S. D.. Brassinosteroid signal transduction: clarifying the pathway from ligand perception to gene expression.  Molecular Cell. (2002 a);  10 973-982
• 17 Clouse S. D.. Arabidopsis mutants reveal multiple roles for sterols in plant development.  Plant Cell. (2002 b);  14 1995-2000
• 18 Clouse S. D., Langford M., McMorris T. C.. A brassinosteroid-insensitive mutant in Arabidopsis thaliana exhibits multiple defects in growth and development.  Plant Physiology. (1996);  111 671-678
• 19 Clouse S. D., Hall A. F., Langford M., McMorris T. C., Baker M. E.. Physiological and molecular effects of brassinosteroids on Arabidopsis thaliana. .  Journal of Plant Growth Regulation. (1993);  12 61-66
• 20 Coll-Garcia D., Mazuch J., Altmann T., Müssig C.. EXORDIUM regulates brassinosteroid-responsive genes.  FEBS Letters. (2004);  563 82-86
• 21 De Michelis M. I., Lado P.. Effects of a brassinosteroid on growth and on H⁺ extrusion in isolated radish cotyledons: comparison with the effects of benzyladenine.  Physiologia Plantarum. (1986);  68 603-607
• 22 Friedrichsen D. M., Joazeiro C. A. P., Li J. M., Hunter T., Chory J.. Brassinosteroid-insensitive-1 is a ubiquitously expressed leucine-rich repeat receptor serine/threonine kinase.  Plant Physiology. (2000);  123 1247-1255
• 23 Friedrichsen D. M., Nemhauser J., Muramitsu T., Maloof J. N., Alonso J., Ecker J. R., Furuya M., Chory J.. Three redundant brassinosteroid early response genes encode putative bHLH transcription factors required for normal growth.  Genetics. (2002);  162 1445-1456
• 24 Fujioka S.. Natural occurrence of brassinosteroids in the plant kingdom. Sakurai, A., Yokota, T., and Clouse, S. D., eds. Brassinosteroids: Steroidal Plant Hormones. Berlin, New York; Springer (1999): 21-45
• 25 Goda H., Sawa S., Asami T., Fujioka S., Shimada Y., Yoshida S.. Comprehensive comparison of auxin-regulated and brassinosteroid-regulated genes in Arabidopsis. .  Plant Physiology. (2004);  134 1555-1573
• 26 Goetz M., Godt D. E., Roitsch T.. Tissue-specific induction of the mRNA for an extracellular invertase isoenzyme of tomato by brassinosteroids suggests a role for steroid hormones in assimilate partitioning.  The Plant Journal. (2000);  22 515-522
• 27 Gregory L. E.. Acceleration of plant growth through seed treatment with brassins.  American Journal of Botany. (1981);  68 586-588
• 28 Gregory L. E., Mandava N. B.. The activity and interaction of brassinolide and gibberellic-acid in mung bean epicotyls.  Physiologia Plantarum. (1982);  54 239-243
• 29 Grove M. D., Spencer G. F., Rohwedder W. K., Mandava N., Worley J. F., Warthen J. D. J. R., Steffens G. L., Flippen-Anderson J. L., Cook J. C. J. R.. Brassinolide, a plant growth promoting steroid isolated from Brassica napus pollen.  Nature. (1979);  281 216-217
• 30 Guan M., Roddick J. G.. Epibrassinolide inhibition of development of excised, adventitious and intact roots of tomato (Lycopersicon esculentum): comparison with the effects of steroidal estrogens.  Physiologia Plantarum. (1988);  74 720-726
• 31 Halliday K. J., Fankhauser C.. Phytochrome-hormonal signalling networks.  The New Phytologist. (2003);  157 449-463
• 32 He J. X., Gendron J. M., Yang Y. L., Li J. M., Wang Z. Y.. The GSK3-like kinase BIN2 phosphorylates and destabilizes BZR1, a positive regulator of the brassinosteroid signaling pathway in Arabidopsis. .  Proceedings of the National Academy of Sciences of the USA. (2002);  99 10185-10190
• 33 Hong Z., Ueguchi-Tanaka M., Shimizu-Sato S., Inukai Y., Fujioka S., Shimada Y., Takatsuto S., Agetsuma M., Yoshida S., Watanabe Y., Uozu S., Kitano H., Ashikari M., Matsuoka M.. Loss-of-function of a rice brassinosteroid biosynthetic enzyme, C-6 oxidase, prevents the organized arrangement and polar elongation of cells in the leaves and stem.  The Plant Journal. (2002);  32 495-508
• 34 Hong Z., Ueguchi-Tanaka M., Umemura K., Uozu S., Fujioka S., Takatsuto S., Yoshida S., Ashikari M., Kitano H., Matsuoka M.. A rice brassinosteroid-deficient mutant, ebisu dwarf (d2), is caused by a loss of function of a new member of cytochrome P450.  Plant Cell. (2003);  15 2900-2910
• 35 Ikekawa N., Zhao Y. J.. Application of 24-epibrassinolide in agriculture. Cutler, H. G., Yokota, T., and Adam, G., eds. Brassinosteroids: Chemistry, Bioactivity, and Applications. Washington, D.C.; American Chemical Society (1991): 280-291
• 36 Jiang J. R., Clouse S. D.. 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.  The Plant Journal. (2001);  26 35-45
• 37 Kamuro Y., Takatsuto S.. Capability for and problems of practical uses of brassinosteroids. Cutler, H. G., Yokota, T., and Adam, G., ed. Brassinosteroids: Chemistry, Bioactivity, and Applications. Washington, D.C.; American Chemical Society (1991): 292-297
• 38 Kamuro Y., Takatsuto S.. Practical application of brassinosteroids in agricultural fields. Sakurai, A., Yokota, T., and Clouse, S. D., eds. Brassinosteroids: Steroidal Plant Hormones. Berlin, New York; Springer (1999): 223-241
• 39 Kang J. G., Yun J., Kim D. H., Chung K. S., Fujioka S., Kim J. I., Dae H. W., Yoshida S., Takatsuto S., Song P. S., Park C. M.. Light and brassinosteroid signals are integrated via a dark-induced small G protein in etiolated seedling growth.  Cell. (2001);  105 625-636
• 40 Katsumi M.. Interaction of a brassinosteroid with IAA and GA3 in the elongation of cucumber hypocotyl sections.  Plant and Cell Physiology. (1985);  26 615-626
• 41 Kauschmann A., Jessop A., Koncz C., Szekeres M., Willmitzer L., Altmann T.. Genetic evidence for an essential role of brassinosteroids in plant development.  The Plant Journal. (1996);  9 701-713
• 42 Khripach V., Zhabinskii V., De Groot A.. Twenty years of brassinosteroids: steroidal plant hormones warrant better crops for the XXI century.  Annals of Botany. (2000);  86 441-447
• 43 Kim S. K., Chang S. C., Lee E. J., Chung W. S., Kim Y. S., Hwang S., Lee J. S.. Involvement of brassinosteroids in the gravitropic response of primary root of maize.  Plant Physiology. (2000);  123 997-1004
• 44 Kohout L., Strnad M., Kaminek M.. Types of Brassinosteroids and Their Bioassays. Cutler, H. G., Yokota, T., and Adam, G., eds. Brassinosteroids: Chemistry, Bioactivity, and Applications. Washington, D.C.; American Chemical Society (1991): 56-73
• 45 Koka C. V., Cerny R. E., Gardner R. G., Noguchi T., Fujioka S., Takatsuto S., Yoshida S., Clouse S. D.. A putative role for the tomato genes DUMPY and CURL-3 in brassinosteroid biosynthesis and response.  Plant Physiology. (2000);  122 85-98
• 46 Li J., Wen J. Q., Lease K. A., Doke J. T., Tax F. E., Walker J. C.. BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling.  Cell. (2002);  110 213-222
• 47 Li J. M., Chory J.. A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction.  Cell. (1997);  90 929-938
• 48 Li J. M., Nagpal P., Vitart V., McMorris T. C., Chory J.. A role for brassinosteroids in light-dependent development of Arabidopsis. .  Science. (1996);  272 398-401
• 49 Li J. M., Nam K. H., Vafeados D., Chory J.. BIN2, a new brassinosteroid-insensitive locus in Arabidopsis. .  Plant Physiology. (2001);  127 14-22
• 50 Lösel R., Wehling M.. Nongenomic actions of steroid hormones.  Nature Reviews Molecular Cell Biology. (2003);  4 46-56
• 51 Mandava N. B.. Plant growth-promoting brassinosteroids.  Annual Review of Plant Physiology and Plant Molecular Biology. (1988);  39 23-52
• 52 Mandava N. B., Sasse J. M., Yopp J. H.. Brassinolide, a growth promoting steroidal lactone II. Activity in selected gibberellin and cytokinin bioassays.  Physiologia Plantarum. (1981);  53 453-461
• 53 Mandava N. B., Thompson M. J., Yopp J. H.. Effects of selected inhibitors of RNA and protein synthesis on brassinosteroid-induced responses in mung bean epicotyls.  Journal of Plant Physiology. (1987);  128 53-66
• 54 Montoya T., Nomura T., Farrar K., Kaneta T., Yokota T., Bishop G. J.. Cloning the tomato Curl3 gene highlights the putative dual role of the leucine-rich repeat receptor kinase tBRI1/SR160 in plant steroid hormone and peptide hormone signaling.  Plant Cell. (2002);  14 3163-3176
• 55 Mora-Garcia S., Vert G., Yin Y., Cano-Delgado A., Cheong H., Chory J.. Nuclear protein phosphatases with Kelch-repeat domains modulate the response to brassinosteroids in Arabidopsis. .  Genes & Development. (2004);  18 448-460
• 56 Mori M., Nomura T., Ooka H., Ishizaka M., Yokota T., Sugimoto K., Okabe K., Kajiwara H., Satoh K., Yamamoto K., Hirochika H., Kikuchi S.. Isolation and characterization of a rice dwarf mutant with a defect in brassinosteroid biosynthesis.  Plant Physiology. (2002);  130 1152-1161
• 57 Morillon R., Catterou M., Sangwan R. S., Sangwan B. S., Lassalles J. P.. Brassinolide may control aquaporin activities in Arabidopsis thaliana. .  Planta. (2001);  212 199-204
• 58 Müssig C., Altmann T.. Genomic brassinosteroid effects.  Journal of Plant Growth Regulation. (2003);  22 313-324
• 59 Müssig C., Shin G. H., Altmann T.. Brassinosteroids promote root growth in Arabidopsis. .  Plant Physiology. (2003);  133 1261-1271
• 60 Nakaya M., Tsukaya H., Murakami N., Kato M.. Brassinosteroids control the proliferation of leaf cells of Arabidopsis thaliana. .  Plant and Cell Physiology. (2002);  43 239-244
• 61 Nam K. H., Li J. M.. BRI1/BAK1, a receptor kinase pair mediating brassinosteroid signaling.  Cell. (2002);  110 203-212
• 62 Nomura T., Bishop G. J., Kaneta T., Reid J. B., Chory J., Yokota T.. The LKA gene is a BRASSINOSTEROID INSENSITIVE 1 homolog of pea.  The Plant Journal. (2003);  36 291-300
• 63 Nomura T., Jager C. E., Kitasaka Y., Takeuchi K., Fukami M., Yoneyama K., Matsushita Y., Nyunoya H., Takatsuto S., Fujioka S., Smith J. J., Kerckhoffs L. H. J., Reid J. B., Yokota T.. Brassinosteroid deficiency due to truncated steroid 5a-reductase causes dwarfism in the lk mutant of pea.  Plant Physiology. (2004);  135 2220-2229
• 64 Nomura T., Kitasaka Y., Takatsuto S., Reid J. B., Fukami M., Yokota T.. Brassinosteroid/sterol synthesis and plant growth as affected by lka and lkb mutations of pea.  Plant Physiology. (1999);  119 1517-1526
• 65 Nomura T., Nakayama M., Reid J. B., Takeuchi Y., Yokota T.. Blockage of brassinosteroid biosynthesis and sensitivity causes dwarfism in garden pea.  Plant Physiology. (1997);  113 31-37
• 66 Oh M. H., Romanow W. G., Smith R. C., Zamski E., Sasse J., Clouse S. D.. Soybean BRU1 encodes a functional xyloglucan endotransglycosylase that is highly expressed in inner epicotyl tissues during brassinosteroid-promoted elongation.  Plant and Cell Physiology. (1998);  39 124-130
• 67 Park W. J.. Effect of epibrassinolide on hypocotyl growth of the tomato mutant diageotropica. .  Planta. (1998);  207 120-124
• 68 Peng P., Li J. M.. Brassinosteroid signal transduction: a mix of conservation and novelty.  Journal of Plant Growth Regulation. (2003);  22 298-312
• 69 Perez-Perez J. M., Ponce M. R., Micol J. L.. The UCU1 Arabidopsis gene encodes a SHAGGY/GSK3-like kinase required for cell expansion along the proximodistal axis.  Developmental Biology. (2002);  242 161-173
• 70 Ramahaleo T., Morillon R., Joel A., Lassalles J.-P.. Osmotic water permeability of isolated protoplasts. Modifications during development.  Plant Physiology. (1999);  119 885-896
• 71 Roddick J. G., Guan M.. Brassinosteroids and root development. Cutler, H. G., Yokota, T., and Adam, G., eds. Brassinosteroids: Chemistry, Bioactivity, and Applications. Washington, D.C.; American Chemical Society (1991): 231-245
• 72 Roddick J. G., Ikekawa N.. Modification of root and shoot development in monocotyledon and dicotyledon seedlings by 24-epibrassinolide.  Journal of Plant Physiology. (1992);  140 70-74
• 73 Sasse J.. Physiological actions of brassinosteroids. Sakurai, A., Yokota, T., and Clouse, S. D., eds. Brassinosteroids: Steroidal Plant Hormones. Berlin, New York; Springer (1999): 137-161
• 74 Sasse J. M.. Physiological actions of brassinosteroids: an update.  Journal of Plant Growth Regulation. (2003);  22 276-288
• 75 Schultz L., Kerckhoffs L. H. J., Klahre U., Yokota T., Reid J. B.. Molecular characterization of the brassinosteroid-deficient lkb mutant in pea.  Plant Molecular Biology. (2001);  47 491-498
• 76 Sekimoto H., Hoshi M., Nomura T., Yokota T.. Zinc deficiency affects the levels of endogenous gibberellins in Zea mays L.  Plant and Cell Physiology. (1997);  38 1087-1090
• 77 Steber C. M., McCourt P.. A role for brassinosteroids in germination in Arabidopsis. .  Plant Physiology. (2001);  125 763-769
• 78 Symons G. M., Reid J. B.. Hormone levels and response during de-etiolation in pea.  Planta. (2003 a);  216 422-431
• 79 Symons G. M., Reid J. B.. Interactions between light and plant hormones during de-etiolation.  Journal of Plant Growth Regulation. (2003 b);  22 3-14
• 80 Symons G. M., Reid J. B.. Brassinosteroids do not undergo long-distance transport in pea. Implications for the regulation of endogenous brassinosteroid levels.  Plant Physiology. (2004);  135 2196-2206
• 81 Symons G. M., Schultz L., Kerckhoffs L. H. J., Davies N. W., Gregory D., Reid J. B.. Uncoupling brassinosteroid levels and de-etiolation in pea.  Physiologia Plantarum. (2002);  115 311-319
• 82 Szekeres M., Nemeth K., Koncz-Kalman Z., Mathur J., Kauschmann A., Altmann T., Redei G. P., Nagy F., Schell J., Koncz C.. Brassinosteroids rescue the deficiency of CYP90, a cytochrome P450, controlling cell elongation and de-etiolation in Arabidopsis. .  Cell. (1996);  85 171-182
• 83 Takahashi T., Gasch A., Nishizawa N., Chua N. H.. The DIMINUTO gene of Arabidopsis is involved in regulating cell elongation.  Genes & Development. (1995);  9 97-107
• 84 Tanaka K., Nakamura Y., Asami T., Yoshida S., Matsuo T., Okamoto S.. Physiological roles of brassinosteroids in early growth of Arabidopsis: brassinosteroids have a synergistic relationship with gibberellin as well as auxin in light-grown hypocotyl elongation.  Journal of Plant Growth Regulation. (2003);  22 259-271
• 85 Thompson M. J., Meudt W. J., Mandava N. B., Dutky S. R., Lusby W. R., Spaulding D. W.. Synthesis of brassinosteroids and relationship of structure to plant growth promoting effects.  Steroids. (1982);  39 89-106
• 86 Tominaga R., Sakurai N., Kuraishi S.. Brassinolide-induced elongation of inner tissues of segments of squash (Cucurbita maxima Duch.) hypocotyls.  Plant and Cell Physiology. (1994);  35 1103-1106
• 87 Vardhini B. V., Rao S. S. R.. Effect of brassinosteroids on growth, metabolite content and yield of Arachis hypogaea. .  Phytochemistry. (1998);  48 927-930
• 88 Wang T.-W., Cosgrove D. J., Arteca R. N.. Brassinosteroid stimulation of hypocotyl elongation and wall relaxation in pakchoi (Brassica chinensis cv. Lei-Choi).  Plant Physiology. (1993);  101 965-968
• 89 Wang Z. Y., Nakano T., Gendron J., He J. X., Chen M., Vafeados D., Yang Y. L., Fujioka S., Yoshida S., Asami T., Chory J.. Nuclear-localized BZR1 mediates brassinosteroid-induced growth and feedback suppression of brassinosteroid biosynthesis.  Developmental Cell. (2002);  2 505-513
• 90 Wehling M.. Specific, nongenomic actions of steroid hormones.  Annual Review of Physiology. (1997);  59 365-393
• 91 Woeste K. E., Vogel J. P., Kieber J. J.. Factors regulating ethylene biosynthesis in etiolated Arabidopsis thaliana seedlings.  Physiologia Plantarum. (1999);  105 478-484
• 92 Xu W., Purugganan M. M., Polisensky D. H., Antosiewicz D. M., Fry S. C., Braam J.. Arabidopsis TCH4, regulated by hormones and the environment, encodes a xyloglucan endotransglycosylase.  Plant Cell. (1995);  7 1555-1567
• 93 Yamamuro C., Ihara Y., Wu X., Noguchi T., Fujioka S., Takatsuto S., Ashikari M., Kitano H., Matsuoka M.. Loss of function of a rice brassinosteroid insensitive1 homolog prevents internode elongation and bending of the lamina joint.  Plant Cell. (2000);  12 1591-1605
• 94 Yin Y. H., Wang Z. Y., Mora-Garcia S., Li J. M., Yoshida S., Asami T., Chory J.. BES1 accumulates in the nucleus in response to brassinosteroids to regulate gene expression and promote stem elongation.  Cell. (2002);  109 181-191
• 95 Yokota T., Sato T., Takeuchi Y., Nomura T., Uno K., Watanabe T., Takatsuto S.. Roots and shoots of tomato produce 6-deoxo-28-norcathasterone, 6-deoxo-28-nortyphasterol and 6-deoxo-28-norcastasterone, possible precursors of 28-norcastasterone.  Phytochemistry. (2001);  58 233-238
• 96 Yopp J. H., Colclasure G. C., Mandava N.. Effects of brassin-complex on auxin and gibberellin mediated events in the morphogenesis of the etiolated bean hypocotyl.  Physiologia Plantarum. (1979);  46 247-254
• 97 Yopp J. H., Mandava N. B., Sasse J. M.. Brassinolide, a growth promoting steroidal lactone I. Activity in selected auxin bioassays.  Physiologia Plantarum. (1981);  53 445-452
• 98 Zurek D. M., Clouse S. D.. Molecular cloning and characterization of a brassinosteroid-regulated gene from elongating soybean (Glycine max L.) epicotyls.  Plant Physiology. (1994);  104 161-170
• 99 Zurek D. M., Rayle D. L., McMorris T. C., Clouse S. D.. Investigation of gene expression, growth kinetics, and wall extensibility during brassinosteroid-regulated stem elongation.  Plant Physiology. (1994);  104 505-513

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