As sessile organisms, plants have evolved sophisticated mechanisms to optimize their growth and development in response to fluctuating nutrient levels. Brassinosteroids (BRs) are a group of plant steroid hormones that play critical roles in plant growth and developmental processes as well as plant responses to environmental stimuli. Recently, multiple molecular mechanisms have been proposed to explain the integration of BRs with different nutrient signaling processes to coordinate gene expression, metabolism, growth, and survival. Here, we review recent advances in understanding the molecular regulatory mechanisms of the BR signaling pathway and the multifaceted roles of BR in the intertwined sensing, signaling, and metabolic processes of sugar, nitrogen, phosphorus, and iron. Further understanding and exploring these BR-related processes and mechanisms will facilitate advances in crop breeding for higher resource efficiency.
|
Amorim-Silva, V., Garcia-Moreno, A., Castillo, A.G., Lakhssassi, N., Esteban Del Valle, A., Perez-Sancho, J., Li, Y., Pose, D., Perez-Rodriguez, J., Lin, J., et al., 2019. TTL proteins scaffold brassinosteroid signaling components at the plasma membrane to optimize signal transduction in Arabidopsis. Plant Cell 31, 1807-1828.
|
|
Anne, P., Azzopardi, M., Gissot, L., Beaubiat, S., Hematy, K., Palauqui, J.C., 2015. OCTOPUS negatively regulates BIN2 to control phloem differentiation in Arabidopsis thaliana. Curr. Biol. 25, 2584-2590.
|
|
Bajguz, A., Chmur, M., Gruszka, D., 2020. Comprehensive overview of the brassinosteroid biosynthesis pathways:substrates, products, inhibitors, and connections. Front. Plant Sci. 11, 1034.
|
|
Cai, Z., Liu, J., Wang, H., Yang, C., Chen, Y., Li, Y., Pan, S., Dong, R., Tang, G., Barajas-Lopez Jde, D., et al., 2014. GSK3-like kinases positively modulate abscisic acid signaling through phosphorylating subgroup III SnRK2s in Arabidopsis. Proc. Natl. Acad. Sci. U. S. A. 111, 9651-9656.
|
|
Chai, S., Chen, J., Yue, X., Li, C., Zhang, Q., de Dios, V.R., Yao, Y., Tan, W., 2022. Interaction of BES1 and LBD37 transcription factors modulates brassinosteroidregulated root forging response under low nitrogen in arabidopsis. Front. Plant Sci. 13, 998961.
|
|
Chaiwanon, J., Garcia, V.J., Cartwright, H., Sun, Y., Wang, Z.Y., 2016a. Immunophilin-like FKBP42/TWISTED DWARF1 interacts with the receptor kinase BRI1 to regulate brassinosteroid signaling in Arabidopsis. Mol. Plant 9, 593-600.
|
|
Chaiwanon, J., Wang, W., Zhu, J.Y., Oh, E., Wang, Z.Y., 2016b. Information integration and communication in plant growth regulation. Cell 164, 1257-1268.
|
|
Chaiwanon, J., Wang, Z.Y., 2015. Spatiotemporal brassinosteroid signaling and antagonism with auxin pattern stem cell dynamics in Arabidopsis roots. Curr. Biol. 25, 1031-1042.
|
|
Chen, L.G., Gao, Z., Zhao, Z., Liu, X., Li, Y., Zhang, Y., Liu, X., Sun, Y., Tang, W., 2019. BZR1 family transcription factors function redundantly and indispensably in BR signaling but exhibit BRI1-independent function in regulating anther development in Arabidopsis. Mol. Plant 12, 1408-1415.
|
|
Choe, S., Dilkes, B.P., Fujioka, S., Takatsuto, S., Sakurai, A., Feldmann, K.A., 1998. The DWF4 gene of Arabidopsis encodes a cytochrome P450 that mediates multiple 22alpha-hydroxylation steps in brassinosteroid biosynthesis. Plant Cell 10, 231-243.
|
|
Chu, X., Li, M., Zhang, S., Fan, M., Han, C., Xiang, F., Li, G., Wang, Y., Xiang, C.B., Wang, J.G., et al., 2021a. HBI1-TCP20 interaction positively regulates the CEPsmediated systemic nitrate acquisition. J. Integr. Plant Biol. 63, 902-912.
|
|
Chu, X., Wang, J.G., Li, M., Zhang, S., Gao, Y., Fan, M., Han, C., Xiang, F., Li, G., Wang, Y., et al., 2021b. HBI transcription factor-mediated ROS homeostasis regulates nitrate signal transduction. Plant Cell 33, 3004-3021.
|
|
Clark, N.M., Nolan, T.M., Wang, P., Song, G., Montes, C., Valentine, C.T., Guo, H., Sozzani, R., Yin, Y., Walley, J.W., 2021. Integrated omics networks reveal the temporal signaling events of brassinosteroid response in Arabidopsis. Nat. Commun. 12, 5858.
|
|
Clouse, S.D., 2011. Brassinosteroids. Arabidopsis Book 9, e0151.
|
|
Dobrenel, T., Caldana, C., Hanson, J., Robaglia, C., Vincentz, M., Veit, B., Meyer, C., 2016. TOR signaling and nutrient sensing. Annu. Rev. Plant Biol. 67, 261-285.
|
|
Dong, H., Liu, J., He, G., Liu, P., Sun, J., 2020. Photoexcited phytochrome B interacts with brassinazole resistant 1 to repress brassinosteroid signaling in Arabidopsis. J. Integr. Plant Biol. 62, 652-667.
|
|
Fang, L., Ma, L., Zhao, S., Cao, R., Jiao, G., Hu, P., Wei, X., 2022. Alanine aminotransferase (OsAlaAT1) modulates nitrogen utilization, grain yield, and quality in rice. J. Genet. Genomics 49, 510-513.
|
|
Fujioka, S., Noguchi, T., Watanabe, T., Takatsuto, S., Yoshida, S., 2000. Biosynthesis of brassinosteroids in cultured cells of Catharanthus roseus. Phytochemistry 53, 549-553.
|
|
Gampala, S.S., Kim, T.W., He, J.X., Tang, W., Deng, Z., Bai, M.Y., Guan, S., Lalonde, S., Sun, Y., Gendron, J.M., et al., 2007. An essential role for 14-3-3 proteins in brassinosteroid signal transduction in Arabidopsis. Dev. Cell 13, 177-189.
|
|
Gao, X., Zhang, J.Q., Zhang, X., Zhou, J., Jiang, Z., Huang, P., Tang, Z., Bao, Y., Cheng, J., Tang, H., et al., 2019. Rice qGL3/OsPPKL1 functions with the GSK3/SHAGGY-Like kinase OsGSK3 to modulate brassinosteroid signaling. Plant Cell 31, 1077-1093.
|
|
Gong, L., Liao, S., Duan, W., Liu, Y., Zhu, D., Zhou, X., Xue, B., Chu, C., Liang, Y.K., 2022. OsCPL3 is involved in brassinosteroid signaling by regulating OsGSK2 stability. J. Integr. Plant Biol. 64, 1560-1574.
|
|
Gudesblat, G.E., Schneider-Pizon, J., Betti, C., Mayerhofer, J., Vanhoutte, I., van Dongen, W., Boeren, S., Zhiponova, M., de Vries, S., Jonak, C., et al., 2012. SPEECHLESS integrates brassinosteroid and stomata signalling pathways. Nat. Cell Biol. 14, 548-554.
|
|
Gui, J., Zheng, S., Liu, C., Shen, J., Li, J., Li, L., 2016. OsREM4.1 interacts with OsSERK1 to coordinate the interlinking between abscisic acid and brassinosteroid signaling in rice. Dev. Cell 38, 201-213.
|
|
Guo, M., Wang, Q., Zong, Y., Nian, J., Li, H., Li, J., Wang, T., Gao, C., Zuo, J., 2021. Genetic manipulations of TaARE1 boost nitrogen utilization and grain yield in wheat. J. Genet. Genomics 48, 950-953.
|
|
Guo, M., Zhang, Y., Jia, X., Wang, X., Zhang, Y., Liu, J., Yang, Q., Ruan, W., Yi, K., 2022. Alternative splicing of REGULATOR OF LEAF INCLINATION 1 modulates phosphate starvation signaling and growth in plants. Plant Cell 34, 3319-3338.
|
|
Gupta, A., Singh, M., Laxmi, A., 2015. Multiple interactions between glucose and brassinosteroid signal transduction pathways in Arabidopsis are uncovered by whole-genome transcriptional profiling. Plant Physiol. 168, 1091-1105.
|
|
Han, C., Hua, W., Li, J., Qiao, Y., Yao, L., Hao, W., Li, R., Fan, M., De Jaeger, G., Yang, W., et al., 2022. TOR promotes guard cell starch degradation by regulating the activity of beta-AMYLASE1 in Arabidopsis. Plant Cell 34, 1038-1053.
|
|
Hao, Y., Wang, H., Qiao, S., Leng, L., Wang, X., 2016. Histone deacetylase HDA6 enhances brassinosteroid signaling by inhibiting the BIN2 kinase. Proc. Natl. Acad. Sci. U. S. A. 113, 10418-10423.
|
|
He, G., Liu, J., Dong, H., Sun, J., 2019. The blue-light receptor CRY1 interacts with BZR1 and BIN2 to modulate the phosphorylation and nuclear function of BZR1 in repressing BR signaling in Arabidopsis. Mol. Plant 12, 689-703.
|
|
He, J.X., Gendron, J.M., Sun, Y., Gampala, S.S., Gendron, N., Sun, C.Q., Wang, Z.Y., 2005. BZR1 is a transcriptional repressor with dual roles in brassinosteroid homeostasis and growth responses. Science 307, 1634-1638.
|
|
Hirano, K., Kawamura, M., Araki-Nakamura, S., Fujimoto, H., Ohmae-Shinohara, K., Yamaguchi, M., Fujii, A., Sasaki, H., Kasuga, S., Sazuka, T., 2017. Sorghum DW1 positively regulates brassinosteroid signaling by inhibiting the nuclear localization of BRASSINOSTEROID INSENSITIVE 2. Sci. Rep. 7, 126.
|
|
Hou, J., Zheng, X., Ren, R., Shi, Q., Xiao, H., Chen, Z., Yue, M., Wu, Y., Hou, H., Li, L., 2022. The histone deacetylase 1/GSK3/SHAGGY-like kinase 2/BRASSINAZOLERESISTANT 1 module controls lateral root formation in rice. Plant Physiol. 189, 858-873.
|
|
Houbaert, A., Zhang, C., Tiwari, M., Wang, K., de Marcos Serrano, A., Savatin, D.V., Urs, M.J., Zhiponova, M.K., Gudesblat, G.E., Vanhoutte, I., et al., 2018. POLARguided signalling complex assembly and localization drive asymmetric cell division. Nature 563, 574-578.
|
|
Ibanez, C., Delker, C., Martinez, C., Burstenbinder, K., Janitza, P., Lippmann, R., Ludwig, W., Sun, H., James, G.V., Klecker, M., et al., 2018. Brassinosteroids dominate hormonal regulation of plant thermomorphogenesis via BZR1. Curr. Biol. 28, 303-310.
|
|
Imkampe, J., Halter, T., Huang, S., Schulze, S., Mazzotta, S., Schmidt, N., Manstretta, R., Postel, S., Wierzba, M., Yang, Y., et al., 2017. The Arabidopsis leucine-rich repeat receptor kinase BIR3 negatively regulates BAK1 receptor complex formation and stabilizes BAK1. Plant Cell 29, 2285-2303.
|
|
Jia, Z., Giehl, R.F.H., Meyer, R.C., Altmann, T., von Wiren, N., 2019. Natural variation of BSK3 tunes brassinosteroid signaling to regulate root foraging under low nitrogen. Nat. Commun. 10, 2378.
|
|
Jia, Z., Giehl, R.F.H., von Wiren, N., 2020. The root foraging response under low nitrogen depends on DWARF1-mediated brassinosteroid biosynthesis. Plant Physiol. 183, 998-1010.
|
|
Jia, Z., Giehl, R.F.H., von Wiren, N., 2022. Nutrient-hormone relations:driving root plasticity in plants. Mol. Plant 15, 86-103.
|
|
Jiao, X., Wang, H., Yan, J., Kong, X., Liu, Y., Chu, J., Chen, X., Fang, R., Yan, Y., 2020. Promotion of BR biosynthesis by miR444 is required for ammoniumtriggered inhibition of root growth. Plant Physiol. 182, 1454-1466.
|
|
Kang, S., Yang, F., Li, L., Chen, H., Chen, S., Zhang, J., 2015. The Arabidopsis transcription factor BRASSINOSTEROID INSENSITIVE1-ETHYL METHANESULFONATE-SUPPRESSOR1 is a direct substrate of MITOGENACTIVATED PROTEIN KINASE6 and regulates immunity. Plant Physiol. 167, 1076-1086.
|
|
Kim, E.J., Lee, S.H., Park, C.H., Kim, S.H., Hsu, C.C., Xu, S., Wang, Z.Y., Kim, S.K., Kim, T.W., 2019. Plant U-Box40 mediates degradation of the brassinosteroidresponsive transcription factor BZR1 in Arabidopsis Roots. Plant Cell 31, 791-808.
|
|
Kim, M.H., Kim, Y., Kim, J.W., Lee, H.S., Lee, W.S., Kim, S.K., Wang, Z.Y., Kim, S.H., 2013. Identification of Arabidopsis BAK1-associating receptor-like kinase 1(BARK1) and characterization of its gene expression and brassinosteroidregulated root phenotypes. Plant Cell Physiol. 54, 1620-1634.
|
|
Kim, T.W., Guan, S., Burlingame, A.L., Wang, Z.Y., 2011. The CDG1 kinase mediates brassinosteroid signal transduction from BRI1 receptor kinase to BSU1 phosphatase and GSK3-like kinase BIN2. Mol. Cell 43, 561-571.
|
|
Kim, T.W., Guan, S., Sun, Y., Deng, Z., Tang, W., Shang, J.X., Sun, Y., Burlingame, A.L., Wang, Z.Y., 2009. Brassinosteroid signal transduction from cell-surface receptor kinases to nuclear transcription factors. Nat. Cell Biol. 11, 1254-1260.
|
|
Kim, T.W., Wang, Z.Y., 2010. Brassinosteroid signal transduction from receptor kinases to transcription factors. Annu. Rev. Plant Biol. 61, 681-704.
|
|
Korbei, B., Luschnig, C., 2021. Plants on (brassino)steroids. Nat. Plants 7, 548-549.
|
|
Lambers, H., 2022. Phosphorus acquisition and utilization in plants. Annu. Rev. Plant Biol. 73, 17-42.
|
|
Li, C., Zhang, B., Yu, H., 2021a. GSK3s:nodes of multilayer regulation of plant development and stress responses. Trends Plant Sci. 26, 1286-1300.
|
|
Li, H., Nian, J., Fang, S., Guo, M., Huang, X., Zhang, F., Wang, Q., Zhang, J., Bai, J., Dong, G., et al., 2022a. Regulation of nitrogen starvation responses by the alarmone (p)ppGpp in rice. J. Genet. Genomics 49, 469-480.
|
|
Li, J., Chory, J., 1997. A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell 90, 929-938.
|
|
Li, J., Nam, K.H., 2002. Regulation of brassinosteroid signaling by a GSK3/SHAGGYlike kinase. Science 295, 1299-1301.
|
|
Li, J., Terzaghi, W., Gong, Y., Li, C., Ling, J.J., Fan, Y., Qin, N., Gong, X., Zhu, D., Deng, X.W., 2020a. Modulation of BIN2 kinase activity by HY5 controls hypocotyl elongation in the light. Nat. Commun. 11, 1592.
|
|
Li, J., Wen, J., Lease, K.A., Doke, J.T., Tax, F.E., Walker, J.C., 2002. BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. Cell 110, 213-222.
|
|
Li, J., Zhou, H., Zhang, Y., Li, Z., Yang, Y., Guo, Y., 2020b. The GSK3-like kinase BIN2 is a molecular switch between the salt stress response and growth recovery in Arabidopsis thaliana. Dev. Cell 55, 367-380.
|
|
Li, J.G., Fan, M., Hua, W., Tian, Y., Chen, L.G., Sun, Y., Bai, M.Y., 2020c. Brassinosteroid and hydrogen peroxide interdependently induce stomatal opening by promoting guard cell starch degradation. Plant Cell 32, 984-999.
|
|
Li, L., Liu, K.H., Sheen, J., 2021b. Dynamic nutrient signaling networks in plants. Annu. Rev. Cell Dev. Biol. 37, 341-367.
|
|
Li, M., Liu, C., Hepworth, S.R., Ma, C., Li, H., Li, J., Wang, S.M., Yin, H., 2022b. SAUR15 interaction with BRI1 activates plasma membrane H+-ATPase to promote organ development of Arabidopsis. Plant Physiol. 189, 2454-2466.
|
|
Li, Q., Xu, F., Chen, Z., Teng, Z., Sun, K., Li, X., Yu, J., Zhang, G., Liang, Y., Huang, X., et al., 2021c. Synergistic interplay of ABA and BR signal in regulating plant growth and adaptation. Nat. Plants 7, 1108-1118.
|
|
Liang, T., Mei, S., Shi, C., Yang, Y., Peng, Y., Ma, L., Wang, F., Li, X., Huang, X., Yin, Y., et al., 2018. UVR8 interacts with BES1 and BIM1 to regulate transcription and photomorphogenesis in Arabidopsis. Dev. Cell 44, 512-523.
|
|
Liao, C.Y., Pu, Y., Nolan, T.M., Montes, C., Guo, H., Walley, J.W., Yin, Y., Bassham, D.C., 2023. Brassinosteroids modulate autophagy through phosphorylation of RAPTOR1B by the GSK3-like kinase BIN2 in Arabidopsis. Autophagy 19, 1293-1310.
|
|
Ling, J.J., Li, J., Zhu, D., Deng, X.W., 2017. Noncanonical role of Arabidopsis COP1/SPA complex in repressing BIN2-mediated PIF3 phosphorylation and degradation in darkness. Proc. Natl. Acad. Sci. U. S. A. 114, 3539-3544.
|
|
Liu, D., 2021. Root developmental responses to phosphorus nutrition. J. Integr. Plant Biol. 63, 1065-1090.
|
|
Liu, D., Yu, Z., Zhang, G., Yin, W., Li, L., Niu, M., Meng, W., Zhang, X., Dong, N., Liu, J., et al., 2021a. Diversification of plant agronomic traits by genome editing of brassinosteroid signaling family genes in rice. Plant Physiol. 187, 2563-2576.
|
|
Liu, D., Zhang, X., Li, Q., Xiao, Y., Zhang, G., Yin, W., Niu, M., Meng, W., Dong, N., Liu, J., et al., 2022a. The U-box ubiquitin ligase TUD1 promotes brassinosteroidinduced GSK2 degradation in rice. Plant Commun. 4, 100450.
|
|
Liu, J., Chen, J., Zheng, X., Wu, F., Lin, Q., Heng, Y., Tian, P., Cheng, Z., Yu, X., Zhou, K., et al., 2017. GW5 acts in the brassinosteroid signalling pathway to regulate grain width and weight in rice. Nat. Plants 3, 17043.
|
|
Liu, T., Deng, S., Zhang, C., Yang, X., Shi, L., Xu, F., Wang, S., Wang, C., 2023. Brassinosteroid signaling regulates phosphate starvation-induced malate secretion in plants. J. Integr. Plant Biol. 1-14.
|
|
Liu, X., Hu, B., Chu, C., 2022b. Nitrogen assimilation in plants:current status and future prospects. J. Genet. Genomics 49, 394-404.
|
|
Liu, Y., Wang, H., Jiang, Z., Wang, W., Xu, R., Wang, Q., Zhang, Z., Li, A., Liang, Y., Ou, S., et al., 2021b. Genomic basis of geographical adaptation to soil nitrogen in rice. Nature 590, 600-605.
|
|
Lu, Q., Houbaert, A., Ma, Q., Huang, J., Sterck, L., Zhang, C., Benjamins, R., Coppens, F., Van Breusegem, F., Russinova, E., 2022. Adenosine monophosphate deaminase modulates BIN2 activity through hydrogen peroxideinduced oligomerization. Plant Cell 34, 3844-3859.
|
|
Luo, Y., Takagi, J., Claus, L.A.N., Zhang, C., Yasuda, S., Hasegawa, Y., Yamaguchi, J., Shan, L., Russinova, E., Sato, T., 2022. Deubiquitinating enzymes UBP12 and UBP13 stabilize the brassinosteroid receptor BRI1. EMBO Rep. 23, e53354.
|
|
Lv, M., Li, J., 2020. Molecular mechanisms of brassinosteroid-mediated responses to changing environments in Arabidopsis. Int. J. Mol. Sci. 21, 2737.
|
|
Marshall, R.S., Vierstra, R.D., 2018. Autophagy:the master of bulk and selective recycling. Annu. Rev. Plant Biol. 69, 173-208.
|
|
Martinez, C., Espinosa-Ruiz, A., de Lucas, M., Bernardo-Garcia, S., FrancoZorrilla, J.M., Prat, S., 2018. PIF4-induced BR synthesis is critical to diurnal and thermomorphogenic growth. EMBO J. 37, e99552.
|
|
Montes, C., Wang, P., Liao, C.Y., Nolan, T.M., Song, G., Clark, N.M., Elmore, J.M., Guo, H., Bassham, D.C., Yin, Y., et al., 2022. Integration of multi-omics data reveals interplay between brassinosteroid and Target of Rapamycin Complex signaling in Arabidopsis. New Phytol. 236, 893-910.
|
|
Mouchel, C.F., Osmont, K.S., Hardtke, C.S., 2006. BRX mediates feedback between brassinosteroid levels and auxin signalling in root growth. Nature 443, 458-461.
|
|
Muller, J., Toev, T., Heisters, M., Teller, J., Moore, K.L., Hause, G., Dinesh, D.C., Burstenbinder, K., Abel, S., 2015. Iron-dependent callose deposition adjusts root meristem maintenance to phosphate availability. Dev. Cell 33, 216-230.
|
|
Nam, K.H., Li, J., 2002. BRI1/BAK1, a receptor kinase pair mediating brassinosteroid signaling. Cell 110, 203-212.
|
|
Noguchi, T., Fujioka, S., Choe, S., Takatsuto, S., Tax, F.E., Yoshida, S., Feldmann, K.A., 2000. Biosynthetic pathways of brassinolide in Arabidopsis. Plant Physiol. 124, 201-210.
|
|
Nolan, T.M., Brennan, B., Yang, M., Chen, J., Zhang, M., Li, Z., Wang, X., Bassham, D.C., Walley, J., Yin, Y., 2017. Selective autophagy of BES1 mediated by DSK2 balances plant growth and survival. Dev. Cell 41, 33-46.
|
|
Nolan, T.M., Vukasinovic, N., Liu, D., Russinova, E., Yin, Y., 2020. Brassinosteroids:multidimensional regulators of plant growth, development, and stress responses. Plant Cell 32, 295-318.
|
|
Nosaki, S., Mitsuda, N., Sakamoto, S., Kusubayashi, K., Yamagami, A., Xu, Y., Bui, T.B.C., Terada, T., Miura, K., Nakano, T., et al., 2022. Brassinosteroidinduced gene repression requires specific and tight promoter binding of BIL1/BZR1 via DNA shape readout. Nat. Plants 8, 1440-1452.
|
|
Nosaki, S., Miyakawa, T., Xu, Y., Nakamura, A., Hirabayashi, K., Asami, T., Nakano, T., Tanokura, M., 2018. Structural basis for brassinosteroid response by BIL1/BZR1. Nat. Plants 4, 771-776.
|
|
Park, S.H., Jeong, J.S., Zhou, Y., Binte Mustafa, N.F., Chua, N.H., 2022. Deubiquitination of BES1 by UBP12/UBP13 promotes brassinosteroid signaling and plant growth. Plant Commun. 3, 100348.
|
|
Peng, Y., Chen, L., Li, S., Zhang, Y., Xu, R., Liu, Z., Liu, W., Kong, J., Huang, X., Wang, Y., et al., 2018. BRI1 and BAK1 interact with G proteins and regulate sugarresponsive growth and development in Arabidopsis. Nat. Commun. 9, 1522.
|
|
Poppenberger, B., Rozhon, W., Khan, M., Husar, S., Adam, G., Luschnig, C., Fujioka, S., Sieberer, T., 2011. CESTA, a positive regulator of brassinosteroid biosynthesis. EMBO J. 30, 1149-1161.
|
|
Rolland, F., Baena-Gonzalez, E., Sheen, J., 2006. Sugar sensing and signaling in plants:conserved and novel mechanisms. Annu. Rev. Plant Biol. 57, 675-709.
|
|
Ruan, W., Guo, M., Xu, L., Wang, X., Zhao, H., Wang, J., Yi, K., 2018. An SPX-RLI1 module regulates leaf inclination in response to phosphate availability in rice. Plant Cell 30, 853-870.
|
|
Shimada, Y., Goda, H., Nakamura, A., Takatsuto, S., Fujioka, S., Yoshida, S., 2003. Organ-specific expression of brassinosteroid-biosynthetic genes and distribution of endogenous brassinosteroids in Arabidopsis. Plant Physiol. 131, 287-297.
|
|
Singh, A.P., Fridman, Y., Holland, N., Ackerman-Lavert, M., Zananiri, R., Jaillais, Y., Henn, A., Savaldi-Goldstein, S., 2018. Interdependent nutrient availability and steroid hormone signals facilitate root growth plasticity. Dev. Cell 46, 59-72.
|
|
Song, L., Shi, Q.M., Yang, X.H., Xu, Z.H., Xue, H.W., 2009. Membrane steroid-binding protein 1 (MSBP1) negatively regulates brassinosteroid signaling by enhancing the endocytosis of BAK1. Cell Res. 19, 864-876.
|
|
Song, S., Wang, H., Sun, M., Tang, J., Zheng, B., Wang, X., Tan, Y.W., 2019. Reactive oxygen species-mediated BIN2 activity revealed by single-molecule analysis. New Phytol. 223, 692-704.
|
|
Song, Y., Niu, R., Yu, H., Guo, J., Du, C., Zhang, Z., Wei, Y., Li, J., Zhang, S., 2022. OsSLA1 functions in leaf angle regulation by enhancing the interaction between OsBRI1 and OsBAK1 in rice. Plant J. 110, 1111-1127.
|
|
Srivastava, M., Srivastava, A.K., Orosa-Puente, B., Campanaro, A., Zhang, C., Sadanandom, A., 2020. SUMO conjugation to BZR1 enables brassinosteroid signaling to integrate environmental cues to shape plant growth. Curr. Biol. 30, 1410-1423.
|
|
Sun, Y., Fan, X.Y., Cao, D.M., Tang, W., He, K., Zhu, J.Y., He, J.X., Bai, M.Y., Zhu, S., Oh, E., et al., 2010. Integration of brassinosteroid signal transduction with the transcription network for plant growth regulation in Arabidopsis. Dev. Cell 19, 765-777.
|
|
Symons, G.M., Reid, J.B., 2004. Brassinosteroids do not undergo long-distance transport in pea. Implications for the regulation of endogenous brassinosteroid levels. Plant Physiol. 135, 2196-2206.
|
|
Tang, W., Kim, T.W., Oses-Prieto, J.A., Sun, Y., Deng, Z., Zhu, S., Wang, R., Burlingame, A.L., Wang, Z.Y., 2008. BSKs mediate signal transduction from the receptor kinase BRI1 in Arabidopsis. Science 321, 557-560.
|
|
Tang, W., Yuan, M., Wang, R., Yang, Y., Wang, C., Oses-Prieto, J.A., Kim, T.W., Zhou, H.W., Deng, Z., Gampala, S.S., et al., 2011. PP2A activates brassinosteroid-responsive gene expression and plant growth by dephosphorylating BZR1. Nat. Cell Biol. 13, 124-131.
|
|
Tian, Y., Fan, M., Qin, Z., Lv, H., Wang, M., Zhang, Z., Zhou, W., Zhao, N., Li, X., Han, C., et al., 2018. Hydrogen peroxide positively regulates brassinosteroid signaling through oxidation of the BRASSINAZOLE-RESISTANT1 transcription factor. Nat. Commun. 9, 1063.
|
|
Tong, H., Chu, C., 2018. Functional specificities of brassinosteroid and potential utilization for crop improvement. Trends Plant Sci. 23, 1016-1028.
|
|
Tong, H., Liu, L., Jin, Y., Du, L., Yin, Y., Qian, Q., Zhu, L., Chu, C., 2012. DWARF AND LOW-TILLERING acts as a direct downstream target of a GSK3/SHAGGYlike kinase to mediate brassinosteroid responses in rice. Plant Cell 24, 2562-2577.
|
|
Vukasinovic, N., Wang, Y., Vanhoutte, I., Fendrych, M., Guo, B., Kvasnica, M., Jiroutova, P., Oklestkova, J., Strnad, M., Russinova, E., 2021. Local brassinosteroid biosynthesis enables optimal root growth. Nat. Plants 7, 619-632.
|
|
Wang, C., Shang, J.X., Chen, Q.X., Oses-Prieto, J.A., Bai, M.Y., Yang, Y., Yuan, M., Zhang, Y.L., Mu, C.C., Deng, Z., et al., 2013a. Identification of BZR1-interacting proteins as potential components of the brassinosteroid signaling pathway in Arabidopsis through tandem affinity purification. Mol. Cell. Proteomics 12, 3653-3665.
|
|
Wang, H., Tang, J., Liu, J., Hu, J., Liu, J., Chen, Y., Cai, Z., Wang, X., 2018a. Abscisic acid signaling inhibits brassinosteroid signaling through dampening the dephosphorylation of BIN2 by ABI1 and ABI2. Mol. Plant 11, 315-325.
|
|
Wang, J., Sun, N., Zheng, L., Zhang, F., Xiang, M., Chen, H., Deng, X.W., Wei, N., 2022. Brassinosteroids promote etiolated apical structures in darkness by amplifying the ethylene response via the EBF-EIN3/PIF3 circuit. Plant Cell 35, 390-408.
|
|
Wang, P., Du, Y., Hou, Y.J., Zhao, Y., Hsu, C.C., Yuan, F., Zhu, X., Tao, W.A., Song, C.P., Zhu, J.K., 2015. Nitric oxide negatively regulates abscisic acid signaling in guard cells by S-nitrosylation of OST1. Proc. Natl. Acad. Sci. U. S. A. 112, 613-618.
|
|
Wang, P., Nolan, T.M., Clark, N.M., Jiang, H., Montes-Serey, C., Guo, H., Bassham, D.C., Walley, J.W., Yin, Y., 2021a. The F-box E3 ubiquitin ligase BAF1 mediates the degradation of the brassinosteroid-activated transcription factor BES1 through selective autophagy in Arabidopsis. Plant Cell 33, 3532-3554.
|
|
Wang, R., Liu, M., Yuan, M., Oses-Prieto, J.A., Cai, X., Sun, Y., Burlingame, A.L., Wang, Z.Y., Tang, W., 2016. The Brassinosteroid-Activated BRI1 receptor kinase is switched off by dephosphorylation mediated by cytoplasm-localized PP2A B' subunits. Mol. Plant 9, 148-157.
|
|
Wang, R., Wang, R., Liu, M., Yuan, W., Zhao, Z., Liu, X., Peng, Y., Yang, X., Sun, Y., Tang, W., 2021b. Nucleocytoplasmic trafficking and turnover mechanisms of BRASSINAZOLE RESISTANT1 in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U. S. A. 118, e2101838118.
|
|
Wang, W., Lu, X., Li, L., Lian, H., Mao, Z., Xu, P., Guo, T., Xu, F., Du, S., Cao, X., et al., 2018b. Photoexcited CRYPTOCHROME1 interacts with dephosphorylated BES1 to regulate brassinosteroid signaling and photomorphogenesis in Arabidopsis. Plant Cell 30, 1989-2005.
|
|
Wang, X., Chory, J., 2006. Brassinosteroids regulate dissociation of BKI1, a negative regulator of BRI1 signaling, from the plasma membrane. Science 313, 1118-1122.
|
|
Wang, X., Li, X., Meisenhelder, J., Hunter, T., Yoshida, S., Asami, T., Chory, J., 2005. Autoregulation and homodimerization are involved in the activation of the plant steroid receptor BRI1. Dev. Cell 8, 855-865.
|
|
Wang, X., Wang, Z., Zheng, Z., Dong, J., Song, L., Sui, L., Nussaume, L., Desnos, T., Liu, D., 2019a. Genetic dissection of Fe-dependent signaling in root developmental responses to phosphate deficiency. Plant Physiol. 179, 300-316.
|
|
Wang, Y., Cao, J.J., Wang, K.X., Xia, X.J., Shi, K., Zhou, Y.H., Yu, J.Q., Zhou, J., 2019b. BZR1 mediates brassinosteroid-induced autophagy and nitrogen starvation in tomato. Plant Physiol. 179, 671-685.
|
|
Wang, Y., Sun, S., Zhu, W., Jia, K., Yang, H., Wang, X., 2013b. Strigolactone/MAX2-induced degradation of brassinosteroid transcriptional effector BES1 regulates shoot branching. Dev. Cell 27, 681-688.
|
|
Wang, Z.Y., Nakano, T., Gendron, J., He, J., Chen, M., Vafeados, D., Yang, Y., Fujioka, S., Yoshida, S., Asami, T., et al., 2002. Nuclear-localized BZR1 mediates brassinosteroid-induced growth and feedback suppression of brassinosteroid biosynthesis. Dev. Cell 2, 505-513.
|
|
Xiong, J., Yang, F., Yao, X., Zhao, Y., Wen, Y., Lin, H., Guo, H., Yin, Y., Zhang, D., 2022a. The deubiquitinating enzymes UBP12 and UBP13 positively regulate recovery after carbon starvation by modulating BES1 stability in Arabidopsis thaliana. Plant Cell 34, 4516-4530.
|
|
Xiong, M., Yu, J., Wang, J., Gao, Q., Huang, L., Chen, C., Zhang, C., Fan, X., Zhao, D., Liu, Q.Q., et al., 2022b. Brassinosteroids regulate rice seed germination through the BZR1-RAmy3D transcriptional module. Plant Physiol. 189, 402-418.
|
|
Xiong, Y., Wu, B., Du, F., Guo, X., Tian, C., Hu, J., Lu, S., Long, M., Zhang, L., Wang, Y., et al., 2021. A crosstalk between auxin and brassinosteroid regulates leaf shape by modulating growth anisotropy. Mol. Plant 14, 949-962.
|
|
Xuan, Y., Duan, F., Je, B., Kim, C., Li, T., Liu, J., Park, S., Cho, J., Kim, T., von Wiren, N., et al., 2017. Related to ABI3/VP1-Like 1 (RAVL1) regulates brassinosteroid-mediated activation of AMT1;2 in rice (Oryza sativa). J. Exp. Bot. 68, 727-737.
|
|
Yang, M., Li, C., Cai, Z., Hu, Y., Nolan, T., Yu, F., Yin, Y., Xie, Q., Tang, G., Wang, X., 2017. SINAT E3 ligases control the light-mediated stability of the brassinosteroidactivated transcription factor BES1 in Arabidopsis. Dev. Cell 41, 47-58 e44.
|
|
Yin, Y., Vafeados, D., Tao, Y., Yoshida, S., Asami, T., Chory, J., 2005. A new class of transcription factors mediates brassinosteroid-regulated gene expression in Arabidopsis. Cell 120, 249-259.
|
|
Yin, Y., Wang, Z.Y., Mora-Garcia, S., Li, J., Yoshida, S., Asami, T., Chory, J., 2002. BES1 accumulates in the nucleus in response to brassinosteroids to regulate gene expression and promote stem elongation. Cell 109, 181-191.
|
|
Yokota, T., Ohnishi, T., Shibata, K., Asahina, M., Nomura, T., Fujita, T., Ishizaki, K., Kohchi, T., 2017. Occurrence of brassinosteroids in non-flowering land plants, liverwort, moss, lycophyte and fern. Phytochemistry 136, 46-55.
|
|
Yu, X., Li, L., Zola, J., Aluru, M., Ye, H., Foudree, A., Guo, H., Anderson, S., Aluru, S., Liu, P., et al., 2011. A brassinosteroid transcriptional network revealed by genome-wide identification of BESI target genes in Arabidopsis thaliana. Plant J. 65, 634-646.
|
|
Yu, Z., Ma, J., Zhang, M., Li, X., Sun, Y., Zhang, M., Ding, Z., 2023. Auxin promotes hypocotyl elongation by enhancing BZR1 nuclear accumulation in Arabidopsis. Sci. Adv. 9, eade2493.
|
|
Yue, Z.L., Liu, N., Deng, Z.P., Zhang, Y., Wu, Z.M., Zhao, J.L., Sun, Y., Wang, Z.Y., Zhang, S.W., 2022. The receptor kinase OsWAK11 monitors cell wall pectin changes to fine-tune brassinosteroid signaling and regulate cell elongation in rice. Curr. Biol. 32, 2454-2466.
|
|
Zhang, B., Shao, L., Wang, J., Zhang, Y., Guo, X., Peng, Y., Cao, Y., Lai, Z., 2021a. Phosphorylation of ATG18a by BAK1 suppresses autophagy and attenuates plant resistance against necrotrophic pathogens. Autophagy 17, 2093-2110.
|
|
Zhang, D., Tan, W., Yang, F., Han, Q., Deng, X., Guo, H., Liu, B., Yin, Y., Lin, H., 2021b. A BIN2-GLK1 signaling module integrates brassinosteroid and light signaling to repress chloroplast development in the dark. Dev. Cell 56, 310-324.
|
|
Zhang, L., Han, Q., Xiong, J., Zheng, T., Han, J., Zhou, H., Lin, H., Yin, Y., Zhang, D., 2019. Sumoylation of BRI1-EMS-SUPPRESSOR 1 (BES1) by the SUMO E3 Ligase SIZ1 negatively regulates brassinosteroids signaling in Arabidopsis thaliana. Plant Cell Physiol. 60, 2282-2292.
|
|
Zhang, W., Tang, Y., Hu, Y., Yang, Y., Cai, J., Liu, H., Zhang, C., Liu, X., Hou, X., 2021c. Arabidopsis NF-YCs play dual roles in repressing brassinosteroid biosynthesis and signaling during light-regulated hypocotyl elongation. Plant Cell 33, 2360-2374.
|
|
Zhang, Z., Sun, Y., Jiang, X., Wang, W., Wang, Z.Y., 2021d. Sugar inhibits brassinosteroid signaling by enhancing BIN2 phosphorylation of BZR1. PLoS Genet. 17, e1009540.
|
|
Zhang, Z., Zhu, J.Y., Roh, J., Marchive, C., Kim, S.K., Meyer, C., Sun, Y., Wang, W., Wang, Z.Y., 2016. TOR signaling promotes accumulation of BZR1 to balance growth with carbon availability in Arabidopsis. Curr. Biol. 26, 1854-1860.
|
|
Zhao, B., Lv, M., Feng, Z., Campbell, T., Liscum, E., Li, J., 2016. TWISTED DWARF 1 associates with BRASSINOSTEROID-INSENSITIVE 1 to regulate early events of the brassinosteroid signaling pathway. Mol. Plant 9, 582-592.
|
|
Zhao, J., Yang, G., Jiang, L., Zhang, S., Miao, L., Xu, P., Chen, H., Chen, L., Mao, Z., Guo, T., et al., 2022a. Phytochromes A and B mediate light stabilization of BIN2 to regulate brassinosteroid signaling and photomorphogenesis in Arabidopsis. Front. Plant Sci. 13, 865019.
|
|
Zhao, N., Zhao, M., Tian, Y., Wang, Y., Han, C., Fan, M., Guo, H., Bai, M.Y., 2021. Interaction between BZR1 and EIN3 mediates signalling crosstalk between brassinosteroids and ethylene. New Phytol. 232, 2308-2323.
|
|
Zhao, N., Zhao, M., Wang, L., Han, C., Bai, M., Fan, M., 2022b. EBF1 negatively regulates brassinosteroid-induced apical hook development and cell elongation through promoting BZR1 degradation. Int. J. Mol. Sci. 23, 15889.
|
|
Zhao, X., Zhang, T., Bai, L., Zhao, S., Guo, Y., Li, Z., 2022c. CKL2 mediates the crosstalk between abscisic acid and brassinosteroid signaling to promote swift growth recovery after stress in Arabidopsis. J. Integr. Plant Biol. 65, 64-81.
|
|
Zhou, J., Liu, D., Wang, P., Ma, X., Lin, W., Chen, S., Mishev, K., Lu, D., Kumar, R., Vanhoutte, I., et al., 2018. Regulation of Arabidopsis brassinosteroid receptor BRI1 endocytosis and degradation by plant U-box PUB12/PUB13-mediated ubiquitination. Proc. Natl. Acad. Sci. U. S. A. 115, E1906eE1915.
|
|
Zhu, J.Y., Li, Y., Cao, D.M., Yang, H., Oh, E., Bi, Y., Zhu, S., Wang, Z.Y., 2017. The Fbox protein KIB1 mediates brassinosteroid-induced inactivation and degradation of GSK3-like kinases in Arabidopsis. Mol. Cell 66, 648-657 e644.
|
Supported by: Beijing Renhe Information Technology Co. Ltd
DownLoad: