Boosting crop yields with plant steroids

Plant Cell

Volumn 24, Issue 3, 2012, Pages 842-857

  Vriet, Cécile ^a   Russinova, Eugenia ^b,c   Reuzeaua, Christophe ^a  

^a BASF Belgium SA   (Belgium)

^b DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^c GHENT UNIVERSITY   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84860177783     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.111.094912     Document Type: Review

References (174)

1. Albrecht, C., Boutrot, F., Segonzac, C., Schwessinger, B., Gimenez-Ibanez, S., Chinchilla, D., Rathjen, J.P., de Vries, S.C., and Zipfel, C. (2012). Brassinosteroids inhibit pathogen-associated molecular pattern-triggered immune signaling independent of the receptor kinase BAK1. Proc. Natl. Acad. Sci. USA 109: 303-308.
2. Arnqvist, L., Dutta, P.C., Jonsson, L., and Sitbon, F. (2003). Reduction of cholesterol and glycoalkaloid levels in transgenic potato plants by overexpression of a type 1 sterol methyltransferase cDNA. Plant Physiol. 131: 1792-1799.
3. Ashikari, M., Wu, J., Yano, M., Sasaki, T., and Yoshimura, A. (1999). Rice gibberellin-insensitive dwarf mutant gene Dwarf 1 encodes the a-subunit of GTP-binding protein. Proc. Natl. Acad. Sci. USA 96: 10284-10289.
4. Athwal, D.S. (1971). Semidwarf rice and wheat in global food needs. Q. Rev. Biol. 46: 1-34.
5. Awad, A.B., and Fink, C.S. (2000). Phytosterols as anticancer dietary components: Evidence and mechanism of action. J. Nutr. 130: 2127-2130.
6. Azpiroz, R., Wu, Y., LoCascio, J.C., and Feldmann, K.A. (1998). An Arabidopsis brassinosteroid-dependent mutant is blocked in cell elongation. Plant Cell 10: 219-230.
7. Bajguz, A., and Hayat, S. (2009). Effects of brassinosteroids on the plant responses to environmental stresses. Plant Physiol. Biochem. 47: 1-8.
8. Bao, F., Shen, J., Brady, S.R., Muday, G.K., Asami, T., and Yang, Z. (2004). Brassinosteroids interact with auxin to promote lateral root development in Arabidopsis. Plant Physiol. 134: 1624-1631.
9. Bari, R., and Jones, J.D.G. (2009). Role of plant hormones in plant defence responses. Plant Mol. Biol. 69: 473-488.
10. Baud, S., et al. (2009). Regulation of HSD1 in seeds of Arabidopsis thaliana. Plant Cell Physiol. 50: 1463-1478.
11. Belkhadir, Y., Jaillais, Y., Epple, P., Balsemão-Pires, E., Dangl, J.L., and Chory, J. (2012). Brassinosteroids modulate the efficiency of plant immune responses to microbe-associated molecular patterns. Proc. Natl. Acad. Sci. USA 109: 297-302.
12. Bishop, G.J., and Koncz, C. (2002). Brassinosteroids and plant steroid hormone signaling. Plant Cell 14 (suppl.): S97-S110.
13. Bouic, P.J.D. (2001). The role of phytosterols and phytosterolins in immune modulation: A review of the past 10 years. Curr. Opin. Clin. Nutr. Metab. Care 4: 471-475.
14. Bou-Torrent, J., Roig-Villanova, I., Galstyan, A., and Martínez-García, J.F. (2008). PAR1 and PAR2 integrate shade and hormone transcriptional networks. Plant Signal. Behav. 3: 453-454.
15. Bradford, P.G., and Awad, A.B. (2007). Phytosterols as anticancer compounds. Mol. Nutr. Food Res. 51: 161-170.
16. Caño-Delgado, A., Lee, J.-Y., and Demura, T. (2010). Regulatory mechanisms for specification and patterning of plant vascular tissues. Annu. Rev. Cell Dev. Biol. 26: 605-637.
17. Caño-Delgado, A., Yin, Y., Yu, C., Vafeados, D., Mora-García, S., Cheng, J.-C., Nam, K.H., Li, J., and Chory, J. (2004). BRL1 and BRL3 are novel brassinosteroid receptors that function in vascular differentiation in Arabidopsis. Development 131: 5341-5351.
18. Cao, S., Xu, Q., Cao, Y., Qian, K., An, K., Zhu, Y., Hu, B., Zhao, H., and Kuai, B. (2005). Loss-of-function mutations in DET2 gene lead to an enhanced resistance to oxidative stress in Arabidopsis. Physiol. Plant. 123: 57-66.
19. Castilla, V., Larzábal, M., Sgalippa, N.A., Wachsman, M.B., and Coto, C.E. (2005). Antiviral mode of action of a synthetic brassinosteroid against Junin virus replication. Antiviral Res. 68: 88-95.
20. Catterou, M., Dubois, F., Schaller, H., Aubanelle, L., Vilcot, B., Sangwan-Norreel, B.S., and Sangwan, R.S. (2001). Brassinosteroids, microtubules and cell elongation in Arabidopsis thaliana. I. Molecular, cellular and physiological characterization of the Arabidopsis bull mutant, defective in the D7-sterol-C5-desaturation step leading to brassinosteroid biosynthesis. Planta 212: 659-672.
21. Ceserani, T., Trofka, A., Gandotra, N., and Nelson, T. (2009). VH1/BRL2 receptor-like kinase interacts with vascular-specific adaptor proteins VIT and VIK to influence leaf venation. Plant J. 57: 1000-1014.
22. Che, P., Bussell, J.D., Zhou, W., Estavillo, G.M., Pogson, B.J., and Smith, S.M. (2010). Signaling from the endoplasmic reticulum activates brassinosteroid signaling and promotes acclimation to stress in Arabidopsis. Sci. Signal. 3: ra69.
23. Chinchilla, D., Zipfel, C., Robatzek, S., Kemmerling, B., Nürnberger, T., Jones, J.D.G., Felix, G., and Boller, T. (2007). A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448: 497-500.
24. Choe, S. (2006). Brassinosteroid biosynthesis and inactivation. Physiol. Plant. 126: 539-548.
25. Choe, S., Fujioka, S., Noguchi, T., Takatsuto, S., Yoshida, S., and Feldmann, K.A. (2001). Overexpression of DWARF4 in the brassinosteroid biosynthetic pathway results in increased vegetative growth and seed yield in Arabidopsis. Plant J. 26: 573-582.
26. Choe, S., Tanaka, A., Noguchi, T., Fujioka, S., Takatsuto, S., Ross, A.S., Tax, F.E., Yoshida, S., and Feldmann, K.A. (2000). Lesions in the stero D7 reductase gene of Arabidopsis cause dwarfism due to a block in brassinosteroid biosynthesis. Plant J. 21: 431-443.
27. Chono, M., Honda, I., Zeniya, H., Yoneyama, K., Saisho, D., Takeda, K., Takatsuto, S., Hoshino, T., and Watanabe, Y. (2003). A semidwarf phenotype of barley uzu results from a nucleotide substitution in the gene encoding a putative brassinosteroid receptor. Plant Physiol. 133: 1209-1219.
28. Chory, J., Nagpal, P., and Peto, C.A. (1991). Phenotypic and genetic analysis of det2, a new mutant that affects light-regulated seedling development in Arabidopsis. Plant Cell 3: 445-459.
29. Clouse, S.D. (2008). The molecular intersection of brassinosteroidregulated growth and flowering in Arabidopsis. Proc. Natl. Acad. Sci. USA 105: 7345-7346.
30. Clouse, S.D. (2011). Brassinosteroid signal transduction: From receptor kinase activation to transcriptional networks regulating plant development. Plant Cell 23: 1219-1230.
31. Clouse, S.D., and Sasse, J.M. (1998). Brassinosteroids: Essential regulators of plant growth and development. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49: 427-451.
32. Crocco, C.D., Holm, M., Yanovsky, M.J., and Botto, J.F. (2011). Function of B-BOX proteins under shade. Plant Signal. Behav. 6: 101-104.
33. Dhaubhadel, S., Browning, K.S., Gallie, D.R., and Krishna, P. (2002). Brassinosteroid functions to protect the translational machinery and heat-shock protein synthesis following thermal stress. Plant J. 29: 681-691.
34. Dhaubhadel, S., Chaudhary, S., Dobinson, K.F., and Krishna, P. (1999). Treatment with 24-epibrassinolide, a brassinosteroid, increases the basic thermotolerance of Brassica napus and tomato seedlings. Plant Mol. Biol. 40: 333-342.
35. Divi, U.K., and Krishna, P. (2010). Overexpression of the brassinosteroid biosynthetic gene AtDWF4 in Arabidopsis seeds overcomes abscisic acid-induced inhibition of germination and increases cold tolerance in transgenic seedlings. J. Plant Growth Regul. 29: 385-393.
36. Divi, U.K., and Krishna, P. (2009). Brassinosteroid: A biotechnological target for enhancing crop yield and stress tolerance. New Biotechnol. 26: 131-136.
37. Divi, U.K., Rahman, T., and Krishna, P. (2010). Brassinosteroid-mediated stress tolerance in Arabidopsis shows interactions with abscisic acid, ethylene and salicylic acid pathways. BMC Plant Biol. 10: 151.
38. Domagalska, M.A., Sarnowska, E., Nagy, F., and Davis, S.J. (2010). Genetic analyses of interactions among gibberellin, abscisic acid, and brassinosteroids in the control of flowering time in Arabidopsis thaliana. PLoS ONE 5: e14012.
39. Domagalska, M.A., Schomburg, F.M., Amasino, R.M., Vierstra, R.D., Nagy, F., and Davis, S.J. (2007). Attenuation of brassinosteroid signaling enhances FLC expression and delays flowering. Development 134: 2841-2850.
40. Fàbregas, N., Ibañes, M., and Caño-Delgado, A.I. (2010). A systems biology approach to dissect the contribution of brassinosteroid and auxin hormones to vascular patterning in the shoot of Arabidopsis thaliana. Plant Signal. Behav. 5: 903-906.
41. Ferguson, B.J., Ross, J.J., and Reid, J.B. (2005). Nodulation phenotypes of gibberellin and brassinosteroid mutants of pea. Plant Physiol. 138: 2396-2405.
42. Finch-Savage, W.E., and Leubner-Metzger, G. (2006). Seed dormancy and the control of germination. New Phytol. 171: 501-523.
43. Fitter, D.W., Martin, D.J., Copley, M.J., Scotland, R.W., and Langdale, J.A. (2002). GLK gene pairs regulate chloroplast development in diverse plant species. Plant J. 31: 713-727.
44. Fitzgerald, M.A., McCouch, S.R., and Hall, R.D. (2009). Not just a grain of rice: The quest for quality. Trends Plant Sci. 14: 133-139.
45. Friedman, M. (2006). Potato glycoalkaloids and metabolites: Roles in the plant and in the diet. J. Agric. Food Chem. 54: 8655-8681.
46. Fujii, S., and Saka, H. (2001). Distribution of assimilates to each organ in rice plants exposed to a low temperature at the ripening stage, and the effect of brassinolide on the distribution. Plant Prod. Sci. 4: 136-144.
47. Gomes, M.M.A. (2011). Physiological effects related to brassinosteroid application in plants. In Brassinosteroids: A Class of Plant Hormone, S. Hayat and A. Ahmad, eds (Dordrecht, The Netherlands: Springer), pp. 193-242.
48. González-García, M.-P., Vilarrasa-Blasi, J., Zhiponova, M., Divol, F., Mora-García, S., Russinova, E., and Caño-Delgado, A.I. (2011). Brassinosteroids control meristem size by promoting cell cycle progression in Arabidopsis roots. Development 138: 849-859.
49. Gudesblat, G.E., and Russinova, E. (2011). Plants grow on brassinosteroids. Curr. Opin. Plant Biol. 14: 530-537.
50. Hacham, Y., Holland, N., Butterfield, C., Ubeda-Tomas, S., Bennett, M.J., Chory, J., and Savaldi-Goldstein, S. (2011). Brassinosteroid perception in the epidermis controls root meristem size. Development 138: 839-848.
51. Hartmann, M.-A. (1998). Plant sterols and the membrane environment. Trends Plant Sci. 3: 170-175.
52. Hartwig, T., Chuck, G.S., Fujioka, S., Klempien, A., Weizbauer, R., Potluri, D.P.V., Choe, S., Johal, G.S., and Schulz, B. (2011). Brassinosteroid control of sex determination in maize. Proc. Natl. Acad. Sci. USA 108: 19814-19819.
53. Hasan, S.A., Hayat, S., and Ahmad, A. (2011). Brassinosteroids protect photosynthetic machinery against the cadmium induced oxidative stress in two tomato cultivars. Chemosphere 84: 1446-1451.
54. He, Y.-J., Xu, R.-J., and Zhao, Y.-J. (1996). Enhancement of senescence by epibrassinolide in leaves of mung bean seedling. Acta Phytophysiol. Sinica 22: 58-62.
55. Heese, A., Hann, D.R., Gimenez-Ibanez, S., Jones, A.M.E., He, K., Li, J., Schroeder, J.I., Peck, S.C., and Rathjen, J.P. (2007). The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. Proc. Natl. Acad. Sci. USA 104: 12217-12222.
56. Hong, Z., Ueguchi-Tanaka, M., Fujioka, S., Takatsuto, S., Yoshida, S., Hasegawa, Y., Ashikari, M., Kitano, H., and Matsuoka, M. (2005). The rice brassinosteroid-deficient dwarf2 mutant, defective in the rice homolog of Arabidopsis DIMINUTO/DWARF1, is rescued by the endogenously accumulated alternative bioactive brassinosteroid, dolichosterone. Plant Cell 17: 2243-2254.
57. Hong, Z., Ueguchi-Tanaka, M., and Matsuoka, M. (2004). Brassinosteroids and rice architecture. J. Pestic. Sci. 29: 184-188.
58. Hong, Z., Ueguchi-Tanaka, M., Umemura, K., Uozu, S., Fujioka, S., Takatsuto, S., Yoshida, S., Ashikari, M., Kitano, H., and Matsuoka, M. (2003). A rice brassinosteroid-deficient mutant, ebisu dwarf (d2), is caused by a loss of function of a new member of cytochrome P450. Plant Cell 15: 2900-2910.
59. Horton, P. (2000). Prospects for crop improvement through the genetic manipulation of photosynthesis: morphological and biochemical aspects of light capture. J. Exp. Bot. 51: 475-485.
60. Huang, Y., Han, C., Peng, W., Peng, Z., Xiong, X., Zhu, Q., Gao, B., Xie, D., and Ren, C. (2010). Brassinosteroid negatively regulates jasmonate inhibition of root growth in Arabidopsis. Plant Signal. Behav. 5: 140-142.
61. Ibañes, M., Fàbregas, N., Chory, J., and Caño-Delgado, A.I. (2009). Brassinosteroid signaling and auxin transport are required to establish the periodic pattern of Arabidopsis shoot vascular bundles. Proc. Natl. Acad. Sci. USA 106: 13630-13635.
62. Janeczko, A., Biesaga-Kościelniak, J., and Dziurka, M. (2009). 24-Epibrassinolide modifies seed composition in soybean, oilseed rape and wheat. Seed Sci. Technol. 37: 625-639.
63. Janeczko, A., Biesaga-Kościelniak, J., Oklešt'ková, J., Filek, M., Dziurka, M., Szarek-Łukaszewska, G., and Kościelniak, J. (2010). Role of 24-epibrassinolide in wheat production: Physiological effects and uptake. J. Agron. Crop Sci. 196: 311-321.
64. Kagale, S., Divi, U.K., Krochko, J.E., Keller, W.A., and Krishna, P. (2007). Brassinosteroid confers tolerance in Arabidopsis thaliana and Brassica napus to a range of abiotic stresses. Planta 225: 353-364.
65. Kebrom, T.H., and Brutnell, T.P. (2007). The molecular analysis of the shade avoidance syndrome in the grasses has begun. J. Exp. Bot. 58: 3079-3089.
66. Keller, M.M., Jaillais, Y., Pedmale, U.V., Moreno, J.E., Chory, J., and Ballaré, C.L. (2011). Cryptochrome 1 and phytochrome B control shade-avoidance responses in Arabidopsis via partially independent hormonal cascades. Plant J. 67: 195-207.
67. Kemmerling, B., et al. (2007). The BRI1-associated kinase 1, BAK1, has a brassinolide-independent role in plant cell-death control. Curr. Biol. 17: 1116-1122.
68. Khripach, V., Zhabinskii, V., and De Groot, A. (2000). Twenty years of brassinosteroids: Steroidal plant hormones warrant better crops for the XXI century. Ann. Bot. (Lond.) 86: 441-447.
69. Kim, S.Y., Kim, B.H., Lim, C.J., Lim, C.O., and Nam, K.H. (2010). Constitutive activation of stress-inducible genes in a brassinosteroidinsensitive 1 (bri1) mutant results in higher tolerance to cold. Physiol. Plant. 138: 191-204.
70. Koh, S., Lee, S.-C., Kim, M.-K., Koh, J.H., Lee, S., An, G., Choe, S., and Kim, S.-R. (2007). T-DNA tagged knockout mutation of rice OsGSK1, an orthologue of Arabidopsis BIN2, with enhanced tolerance to various abiotic stresses. Plant Mol. Biol. 65: 453-466.
71. Komatsu, T., et al. (2010). The chloroplast protein BPG2 functions in brassinosteroid-mediated post-transcriptional accumulation of chloroplast rRNA. Plant J. 61: 409-422.
72. Kozuka, T., Kobayashi, J., Horiguchi, G., Demura, T., Sakakibara, H., Tsukaya, H., and Nagatani, A. (2010). Involvement of auxin and brassinosteroid in the regulation of petiole elongation under the shade. Plant Physiol. 153: 1608-1618.
73. Krishna, P. (2003). Brassinosteroid-mediated stress responses. J. Plant Growth Regul. 22: 289-297.
74. Kuppusamy, K.T., Chen, A.Y., and Nemhauser, J.L. (2009). Steroids are required for epidermal cell fate establishment in Arabidopsis roots. Proc. Natl. Acad. Sci. USA 106: 8073-8076.
75. Laquitaine, L., Gomès, E., François, J., Marchive, C., Pascal, S., Hamdi, S., Atanassova, R., Delrot, S., and Coutos-Thévenot, P. (2006). Molecular basis of ergosterol-induced protection of grape against Botrytis cinerea: Induction of type I LTP promoter activity, WRKY, and stilbene synthase gene expression. Mol. Plant Microbe Interact. 19: 1103-1112.
76. Laxmi, A., Paul, L.K., Peters, J.L., and Khurana, J.P. (2004). Arabidopsis constitutive photomorphogenic mutant, bls1, displays altered brassinosteroid response and sugar sensitivity. Plant Mol. Biol. 56: 185-201.
77. Li, D., Wang, L., Wang, M., Xu, Y.-Y., Luo, W., Liu, Y.-J., Xu, Z.-H., Li, J., and Chong, K. (2009). Engineering OsBAK1 gene as a molecular tool to improve rice architecture for high yield. Plant Biotechnol. J. 7: 791-806.
78. Li, F., Asami, T., Wu, X., Tsang, E.W.T., and Cutler, A.J. (2007). A putative hydroxysteroid dehydrogenase involved in regulating plant growth and development. Plant Physiol. 145: 87-97.
79. Li, J., and Chory, J. (1997). A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell 90: 929-938.
80. Li, J., Li, Y., Chen, S., and An, L. (2010). Involvement of brassinosteroid signals in the floral-induction network of Arabidopsis. J. Exp. Bot. 61: 4221-4230.
81. Li, J., Nagpal, P., Vitart, V., McMorris, T.C., and Chory, J. (1996). A role for brassinosteroids in light-dependent development of Arabidopsis. Science 272: 398-401.
82. Lisso, J., Altmann, T., and Müssig, C. (2006). Metabolic changes in fruits of the tomato dx mutant. Phytochemistry 67: 2232-2238.
83. Lochman, J., and Mikes, V. (2006). Ergosterol treatment leads to the expression of a specific set of defence-related genes in tobacco. Plant Mol. Biol. 62: 43-51.
84. Long, S.P., Zhu, X.-G., Naidu, S.L., and Ort, D.R. (2006). Can improvement in photosynthesis increase crop yields? Plant Cell Environ. 29: 315-330.
85. Luo, M., Xiao, Y., Li, X., Lu, X., Deng, W., Li, D., Hou, L., Hu, M., Li, Y., and Pei, Y. (2007). GhDET2, a steroid 5a-reductase, plays an important role in cotton fiber cell initiation and elongation. Plant J. 51: 419-430.
86. Luo, X.-M., et al. (2010). Integration of light- and brassinosteroidsignaling pathways by a GATA transcription factor in Arabidopsis. Dev. Cell 19: 872-883.
87. Makarevitch, I., Thompson, A., Muehlbauer, G.J., and Springer, N.M. (2012). Brd1 gene in maize encodes a brassinosteroid C-6 oxidase. PLoS ONE 7: e30798.
88. Malíková, J., Swaczynová, J., Kolár, Z., and Strnad, M. (2008). Anticancer and antiproliferative activity of natural brassinosteroids. Phytochemistry 69: 418-426.
89. Manavalan, L.P., Chen, X., Clarke, J., Salmeron, J., and Nguyen, H.T. (2012). RNAi-mediated disruption of squalene synthase improves drought tolerance and yield in rice. J. Exp. Bot. 63: 163-175.
90. Moreau, R.A., Whitaker, B.D., and Hicks, K.B. (2002). Phytosterols, phytostanols, and their conjugates in foods: Structural diversity, quantitative analysis, and health-promoting uses. Prog. Lipid Res. 41: 457-500.
91. Mori, M., Nomura, T., Ooka, H., Ishizaka, M., Yokota, T., Sugimoto, K., Okabe, K., Kajiwara, H., Satoh, K., Yamamoto, K., Hirochika, H., and Kikuchi, S. (2002). Isolation and characterization of a rice dwarf mutant with a defect in brassinosteroid biosynthesis. Plant Physiol. 130: 1152-1161.
92. Morillo, S.A., and Tax, F.E. (2006). Functional analysis of receptor-like kinases in monocots and dicots. Curr. Opin. Plant Biol. 9: 460-469.
93. Morinaka, Y., Sakamoto, T., Inukai, Y., Agetsuma, M., Kitano, H., Ashikari, M., and Matsuoka, M. (2006). Morphological alteration caused by brassinosteroid insensitivity increases the biomass and grain production of rice. Plant Physiol. 141: 924-931.
94. Müssig, C., Shin, G.-H., and Altmann, T. (2003). Brassinosteroids promote root growth in Arabidopsis. Plant Physiol. 133: 1261-1271.
95. Nagata, N., Asami, T., and Yoshida, S. (2001). Brassinazole, an inhibitor of brassinosteroid biosynthesis, inhibits development of secondary xylem in cress plants (Lepidium sativum). Plant Cell Physiol. 42: 1006-1011.
96. Nakamura, A., et al. (2006). The role of OsBRI1 and its homologous genes, OsBRL1 and OsBRL3, in rice. Plant Physiol. 140: 580-590.
97. Nakashita, H., Yasuda, M., Nitta, T., Asami, T., Fujioka, S., Arai, Y., Sekimata, K., Takatsuto, S., Yamaguchi, I., and Yoshida, S. (2003). Brassinosteroid functions in a broad range of disease resistance in tobacco and rice. Plant J. 33: 887-898.
98. Nam, K.H., and Li, J. (2004). The Arabidopsis transthyretin-like protein is a potential substrate of BRASSINOSTEROID-INSENSITIVE1. Plant Cell 16: 2406-2417.
99. Nole-Wilson, S., Rueschhoff, E.E., Bhatti, H., and Franks, R.G. (2010). Synergistic disruptions in seuss cyp85A2 double mutants reveal a role for brassinolide synthesis during gynoecium and ovule development. BMC Plant Biol. 10: 198.
100. Nomura, T., et al. (2004). Brassinosteroid deficiency due to truncated steroid 5a-reductase causes dwarfism in the lk mutant of pea. Plant Physiol. 135: 2220-2229.
101. Nomura, T., Ueno, M., Yamada, Y., Takatsuto, S., Takeuchi, Y., and Yokota, T. (2007). Roles of brassinosteroids and related mRNAs in pea seed growth and germination. Plant Physiol. 143: 1680-1688.
102. Oh, M.-H., Sun, J., Oh, D.H., Zielinski, R.E., Clouse, S.D., and Huber, S.C. (2011). Enhancing Arabidopsis leaf growth by engineering the BRASSINOSTEROID INSENSITIVE1 receptor kinase. Plant Physiol. 157: 120-131.
103. Ohnishi, T., Szatmari, A.-M., Watanabe, B., Fujita, S., Bancos, S., Koncz, C., Lafos, M., Shibata, K., Yokota, T., Sakata, K., Szekeres, M., and Mizutani, M. (2006). C-23 hydroxylation by Arabidopsis CYP90C1 and CYP90D1 reveals a novel shortcut in brassinosteroid biosynthesis. Plant Cell 18: 3275-3288.
104. Oki, K., Inaba, N., Kitagawa, K., Fujioka, S., Kitano, H., Fujisawa, Y., Kato, H., and Iwasaki, Y. (2009). Function of the a subunit of rice heterotrimeric G protein in brassinosteroid signaling. Plant Cell Physiol. 50: 161-172.
105. Ovečka, M., Berson, T., Beck, M., Derksen, J., Šamaj, J., Baluška, F., and Lichtscheidl, I.K. (2010). Structural sterols are involved in both the initiation and tip growth of root hairs in Arabidopsis thaliana. Plant Cell 22: 2999-3019.
106. Park, W., Kim, H.B., Kim, W.T., Park, P.B., An, G., and Choe, S. (2006). Rice bending lamina 2 (bla2) mutants are defective in a cytochrome P450 (CYP734A6) gene predicted to mediate brassinosteroid catabolism. J. Plant Biol. 49: 469-476.
107. Pérez-España, V.H., Sánchez-León, N., and Vielle-Calzada, J.-P. (2011). CYP85A1 is required for the initiation of female gametogenesis in Arabidopsis thaliana. Plant Signal. Behav. 6: 321-326.
108. Pérez-Pérez, J.M., Ponce, M.R., and Micol, J.L. (2002). The UCU1 Arabidopsis gene encodes a SHAGGY/GSK3-like kinase required for cell expansion along the proximodistal axis. Dev. Biol. 242: 161-173.
109. Pieterse, C.M.J., Leon-Reyes, A., Van der Ent, S., and Van Wees, S.C.M. (2009). Networking by small-molecule hormones in plant immunity. Nat. Chem. Biol. 5: 308-316.
110. Piroux, N., Saunders, K., Page, A., and Stanley, J. (2007). Geminivirus pathogenicity protein C4 interacts with Arabidopsis thaliana shaggyrelated protein kinase AtSKh, a component of the brassinosteroid signalling pathway. Virology 362: 428-440.
111. Pullen, M., Clark, N., Zarinkamar, F., Topping, J., and Lindsey, K. (2010). Analysis of vascular development in the hydra sterol biosynthetic mutants of Arabidopsis. PLoS ONE 5: e12227.
112. Quílez, J., García-Lorda, P., and Salas-Salvadó, J. (2003). Potential uses and benefits of phytosterols in diet: Present situation and future directions. Clin. Nutr. 22: 343-351.
113. Reinhardt, D., and Kuhlemeier, C. (2002). Plant architecture. EMBO Rep. 3: 846-851.
114. Reinhold, H., Soyk, S., Šimková, K., Hostettler, C., Marafino, J., Mainiero, S., Vaughan, C.K., Monroe, J.D., and Zeeman, S.C. (2011). b-Amylase-like proteins function as transcription factors in Arabidopsis, controlling shoot growth and development. Plant Cell 23: 1391-1403.
115. Reuzeau, C., Pen, J., Frankard, V., de Wolf, J., Peerbolte, R., Broekaert, W., and Van Camp, W. (2005). TraitMill: A discovery engine for identifying yield enhancement genes in cereals. Mol. Plant Breed. 5: 753-759.
116. Romanutti, C., Castilla, V., Coto, C.E., and Wachsman, M.B. (2007). Antiviral effect of a synthetic brassinosteroid on the replication of vesicular stomatitis virus in Vero cells. Int. J. Antimicrob. Agents 29: 311-316.
117. Roux, M., Schwessinger, B., Albrecht, C., Chinchilla, D., Jones, A., Holton, N., Malinovsky, F.G., Tör, M., de Vries, S., and Zipfel, C. (2011). The Arabidopsis leucine-rich repeat receptor-like kinases BAK1/SERK3 and BKK1/SERK4 are required for innate immunity to hemibiotrophic and biotrophic pathogens. Plant Cell 23: 2440-2455.
118. Saǧlam-Çaǧ, S. (2007). The effect of epibrassinolide on senescence in wheat leaves. Biotechnol. Biotechnol. Equip. 21: 63-65.
119. Sakamoto, T., and Matsuoka, M. (2008). Identifying and exploiting grain yield genes in rice. Curr. Opin. Plant Biol. 11: 209-214.
120. Sakamoto, T., et al. (2006). Erect leaves caused by brassinosteroid deficiency increase biomass production and grain yield in rice. Nat. Biotechnol. 24: 105-109.
121. Salas Fernandez, M.G., Becraft, P.W., Yin, Y., and Lübberstedt, T. (2009). From dwarves to giants? Plant height manipulation for biomass yield. Trends Plant Sci. 14: 454-461.
122. Schaller, H. (2004). New aspects of sterol biosynthesis in growth and development of higher plants. Plant Physiol. Biochem. 42: 465-476.
123. Schlüter, U., Köpke, D., Altmann, T., and Müssig, C. (2002). Analysis of carbohydrate metabolism of CPD antisense plants and the brassinosteroid-deficient cbb1 mutant. Plant Cell Environ. 25: 783-791.
124. Schrick, K., Fujioka, S., Takatsuto, S., Stierhof, Y.-D., Stransky, H., Yoshida, S., and Jürgens, G. (2004). A link between sterol biosynthesis, the cell wall, and cellulose in Arabidopsis. Plant J. 38: 227-243.
125. Schröder, F., Lisso, J., and Müssig, C. (2011). EXORDIUM-LIKE1 promotes growth during low carbon availability in Arabidopsis. Plant Physiol. 156: 1620-1630.
126. Schwessinger, B., Roux, M., Kadota, Y., Ntoukakis, V., Sklenar, J., Jones, A., and Zipfel, C. (2011). Phosphorylation-dependent differential regulation of plant growth, cell death, and innate immunity by the regulatory receptor-like kinase BAK1. PLoS Genet. 7: e1002046.
127. Sinclair, T.R., and Sheehy, J.E. (1999). Erect leaves and photosynthesis in rice. Science 283: 1456-1457.
128. Song, L., Zhou, X.-Y., Li, L., Xue, L.-J., Yang, X., and Xue, H.-W. (2009). Genome-wide analysis revealed the complex regulatory network of brassinosteroid effects in photomorphogenesis. Mol. Plant 2: 755-772.
129. Sorin, C., Salla-Martret, M., Bou-Torrent, J., Roig-Villanova, I., and Martínez-García, J.F. (2009). ATHB4, a regulator of shade avoidance, modulates hormone response in Arabidopsis seedlings. Plant J. 59: 266-277.
130. Souter, M., Topping, J., Pullen, M., Friml, J., Palme, K., Hackett, R., Grierson, D., and Lindsey, K. (2002). hydra mutants of Arabidopsis are defective in sterol profiles and auxin and ethylene signaling. Plant Cell 14: 1017-1031.
131. Srikanth, A., and Schmid, M. (2011). Regulation of flowering time: All roads lead to Rome. Cell. Mol. Life Sci. 68: 2013-2037.
132. Steber, C.M., and McCourt, P. (2001). A role for brassinosteroids in germination in Arabidopsis. Plant Physiol. 125: 763-769.
133. Steigerová, J., Oklešt'ková, J., Levková, M., Rárová, L., Kolář, Z., and Strnad, M. (2010). Brassinosteroids cause cell cycle arrest and apoptosis of human breast cancer cells. Chem. Biol. Interact. 188: 487-496.
134. Sun, Y., et al. (2010). Integration of brassinosteroid signal transduction with the transcription network for plant growth regulation in Arabidopsis. Dev. Cell 19: 765-777.
135. Swan, T.M., and Watson, K. (1998). Stress tolerance in a yeast sterol auxotroph: Role of ergosterol, heat shock proteins and trehalose. FEMS Microbiol. Lett. 169: 191-197.
136. Symons, G.M., Davies, C., Shavrukov, Y., Dry, I.B., Reid, J.B., and Thomas, M.R. (2006). Grapes on steroids. Brassinosteroids are involved in grape berry ripening. Plant Physiol. 140: 150-158.
137. Symons, G.M., and Reid, J.B. (2008). Brassinosteroids, de-etiolation and the re-emerging art of plant hormone quantification. Plant Signal. Behav. 3: 868-870.
138. Symons, G.M., Schultz, L., Kerckhoffs, L.H.J., Davies, N.W., Gregory, D., and Reid, J.B. (2002). Uncoupling brassinosteroid levels and de-etiolation in pea. Physiol. Plant. 115: 311-319.
139. Symons, G.M., Smith, J.J., Nomura, T., Davies, N.W., Yokota, T., and Reid, J.B. (2008). The hormonal regulation of de-etiolation. Planta 227: 1115-1125.
140. Szekeres, M., Németh, K., Koncz-Kálmán, Z., Mathur, J., Kauschmann, A., Altmann, T., Rédei, G.P., Nagy, F., Schell, J., and Koncz, C. (1996). Brassinosteroids rescue the deficiency of CYP90, a cytochrome P450, controlling cell elongation and de-etiolation in Arabidopsis. Cell 85: 171-182.
141. Tanabe, S., Ashikari, M., Fujioka, S., Takatsuto, S., Yoshida, S., Yano, M., Yoshimura, A., Kitano, H., Matsuoka, M., Fujisawa, Y., Kato, H., and Iwasaki, Y. (2005). A novel cytochrome P450 is implicated in brassinosteroid biosynthesis via the characterization of a rice dwarf mutant, dwarf11, with reduced seed length. Plant Cell 17: 776-790.
142. Tanaka, A., et al. (2009). BRASSINOSTEROID UPREGULATED1, encoding a helix-loop-helix protein, is a novel gene involved in brassinosteroid signaling and controls bending of the lamina joint in rice. Plant Physiol. 151: 669-680.
143. Tao, Y., Zheng, J., Xu, Z., Zhang, X., Zhang, K., and Wang, G. (2004). Functional analysis of ZmDWF1, a maize homolog of the Arabidopsis brassinosteroids biosynthetic DWF1/DIM gene. Plant Sci. 167: 743-751.
144. Terakado, J., Fujihara, S., Goto, S., Kuratani, R., Suzuki, Y., Yoshida, S., and Yoneyama, T. (2005). Systemic effect of a brassinosteroid on root nodule formation in soybean as revealed by the application of brassinolide and brassinazole. Soil Sci. Plant Nutr. 51: 389-395.
145. Turk, E.M., Fujioka, S., Seto, H., Shimada, Y., Takatsuto, S., Yoshida, S., Denzel, M.A., Torres, Q.I., and Neff, M.M. (2003). CYP72B1 inactivates brassinosteroid hormones: An intersection between photomorphogenesis and plant steroid signal transduction. Plant Physiol. 133: 1643-1653.
146. Turk, E.M., et al. (2005). BAS1 and SOB7 act redundantly to modulate Arabidopsis photomorphogenesis via unique brassinosteroid inactivation mechanisms. Plant J. 42: 23-34.
147. Upreti, K.K., and Murti, G.S.R. (2004). Effects of brassinosteroids on growth, nodulation, phytohormone content and nitrogenase activity in French bean under water stress. Biol. Plant. 48: 407-411.
148. Van Camp, W. (2005). Yield enhancement genes: seeds for growth. Curr. Opin. Biotechnol. 16: 147-153.
149. Vardhini, B.V., and Rao, S.S.R. (2002). Acceleration of ripening of tomato pericarp discs by brassinosteroids. Phytochemistry 61: 843-847.
150. Wachsman, M.B., López, E.M.F., Ramirez, J.A., Galagovsky, L.R., and Coto, C.E. (2000). Antiviral effect of brassinosteroids against herpes virus and arenaviruses. Antivir. Chem. Chemother. 11: 71-77.
151. Wachsman, M.B., Ramirez, J.A., Galagovsky, L.R., and Coto, C.E. (2002). Antiviral activity of brassinosteroids derivatives against measles virus in cell cultures. Antivir. Chem. Chemother. 13: 61-66.
152. Wang, H., Nagegowda, D.A., Rawat, R., Bouvier-Navé, P., Guo, D., Bach, T.J., and Chye, M.-L. (2012). Overexpression of Brassica juncea wild-type and mutant HMG-CoA synthase 1 in Arabidopsis upregulates genes in sterol biosynthesis and enhances sterol production and stress tolerance. Plant Biotechnol. J. 10: 31-42.
153. Wang, L., Xu, Y., Zhang, C., Ma, Q., Joo, S.-H., Kim, S.-K., Xu, Z., and Chong, K. (2008). OsLIC, a novel CCCH-type zinc finger protein with transcription activation, mediates rice architecture via brassinosteroids signaling. PLoS ONE 3: e3521.
154. Waters, M.T., Moylan, E.C., and Langdale, J.A. (2008). GLK transcription factors regulate chloroplast development in a cell-autonomous manner. Plant J. 56: 432-444.
155. Waters, M.T., Wang, P., Korkaric, M., Capper, R.G., Saunders, N.J., and Langdale, J.A. (2009). GLK transcription factors coordinate expression of the photosynthetic apparatus in Arabidopsis. Plant Cell 21: 1109-1128.
156. Werner, A.K., and Witte, C.-P. (2011). The biochemistry of nitrogen mobilization: Purine ring catabolism. Trends Plant Sci. 16: 381-387.
157. Williams, M.E. (November 22, 2011). Brassinosteroids: Plant steroid hormones. Teaching Tools in Plant Biology: Lecture Notes. The Plant Cell (online), doi/10.1105/tpc.110.tt0910.
158. Woyengo, T.A., Ramprasath, V.R., and Jones, P.J.H. (2009). Anticancer effects of phytosterols. Eur. J. Clin. Nutr. 63: 813-820.
159. Wu, C.Y., et al. (2008). Brassinosteroids regulate grain filling in rice. Plant Cell 20: 2130-2145.
160. Xi, W., and Yu, H. (2010). MOTHER OF FT AND TFL1 regulates seed germination and fertility relevant to the brassinosteroid signaling pathway. Plant Signal. Behav. 5: 1315-1317.
161. Xia, X.-J., Huang, L.-F., Zhou, Y.-H., Mao, W.-H., Shi, K., Wu, J.-X., Asami, T., Chen, Z., and Yu, J.-Q. (2009a). Brassinosteroids promote photosynthesis and growth by enhancing activation of Rubisco and expression of photosynthetic genes in Cucumis sativus. Planta 230: 1185-1196.
162. Xia, X.-J., Wang, Y.-J., Zhou, Y.-H., Tao, Y., Mao, W.-H., Shi, K., Asami, T., Chen, Z., and Yu, J.-Q. (2009b). Reactive oxygen species are involved in brassinosteroid-induced stress tolerance in cucumber. Plant Physiol. 150: 801-814.
163. Xia, X.J., Zhang, Y., Wu, J.X., Wang, J.T., Zhou, Y.H., Shi, K., Yu, Y.L., and Yu, J.Q. (2009c). Brassinosteroids promote metabolism of pesticides in cucumber. J. Agric. Food Chem. 57: 8406-8413.
164. Xia, X.-J., Zhou, Y.-H., Ding, J., Shi, K., Asami, T., Chen, Z., and Yu, J.-Q. (2011). Induction of systemic stress tolerance by brassinosteroid in Cucumis sativus. New Phytol. 191: 706-720.
165. Xie, G., and Peng, L. (2011). Genetic engineering of energy crops: A strategy for biofuel production in China. J. Integr. Plant Biol. 53: 143-150.
166. Xie, L., Yang, C., and Wang, X. (2011). Brassinosteroids can regulate cellulose biosynthesis by controlling the expression of CESA genes in Arabidopsis. J. Exp. Bot. 62: 4495-4506.
167. Xue, L.-W., Du, J.-B., Yang, H., Xu, F., Yuan, S., and Lin, H.-H. (2009). Brassinosteroids counteract abscisic acid in germination and growth of Arabidopsis. Z. Naturforsch. C. 64: 225-230.
168. Yang, D.-H., Hettenhausen, C., Baldwin, I.T., and Wu, J. (2011). BAK1 regulates the accumulation of jasmonic acid and the levels of trypsin proteinase inhibitors in Nicotiana attenuata's responses to herbivory. J. Exp. Bot. 62: 641-652.
169. Ye, Q., Zhu, W., Li, L., Zhang, S., Yin, Y., Ma, H., and Wang, X. (2010). Brassinosteroids control male fertility by regulating the expression of key genes involved in Arabidopsis anther and pollen development. Proc. Natl. Acad. Sci. USA 107: 6100-6105.
170. Yu, X., Li, L., Li, L., Guo, M., Chory, J., and Yin, Y. (2008). Modulation of brassinosteroid-regulated gene expression by jumonji domaincontaining proteins ELF6 and REF6 in Arabidopsis. Proc. Natl. Acad. Sci. USA 105: 7618-7623.
171. Yu, X., Li, L., Zola, J., Aluru, M., Ye, H., Foudree, A., Guo, H., Anderson, S., Aluru, S., Liu, P., Rodermel, S., and Yin, Y. (2011). A brassinosteroid transcriptional network revealed by genome-wide identification of BESI target genes in Arabidopsis thaliana. Plant J. 65: 634-646.
172. Zeng, H., Tang, Q., and Hua, X. (2010). Arabidopsis brassinosteroid mutants det2-1 and bin2-1 display altered salt tolerance. J. Plant Growth Regul. 29: 44-52.
173. Zinn, K.E., Tunc-Ozdemir, M., and Harper, J.F. (2010). Temperature stress and plant sexual reproduction: Uncovering the weakest links. J. Exp. Bot. 61: 1959-1968.
174. Zullo, M.A.T., and Adam, G. (2002). Brassinosteroid phytohormones: Structure, bioactivity and applications. Braz. J. Plant Physiol. 14: 143-181.