Skip to main content
Log in

Crosstalk between brassinosteroid signaling and variable nutrient environments

  • Review
  • Published:
Science China Life Sciences Aims and scope Submit manuscript

Abstract

Brassinosteroid (BR) represents a group of steroid hormones that regulate plant growth and development as well as environmental adaptation. The fluctuation of external nutrient elements is a situation that plants frequently face in the natural environment, in which nitrogen (N) and phosphorus (P) are two of the most critical nutrients restraint of the early growth of plants. As the macronutrients, N and P are highly required by plants, but their availability or solubility in the soil is relatively low. Since iron (Fe) and P always modulate each other’s content and function in plants mutually antagonistically, the regulatory mechanisms of Fe and P are inextricably linked. Recently, BR has emerged as a critical regulator in nutrient acquisition and phenotypic plasticity in response to the variable nutrient levels in Arabidopsis and rice. Here, we review the current understanding of the crosstalk between BR and the three major nutrients (N, P, and Fe), highlighting how nutrient signaling regulates BR synthesis and signaling to accommodate plant growth and development in Arabidopsis and rice.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Anwar, A., Liu, Y., Dong, R., Bai, L., Yu, X., and Li, Y. (2018). The physiological and molecular mechanism of brassinosteroid in response to stress: a review. Biol Res 51, 46.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bai, M.Y., Zhang, L.Y., Gampala, S.S., Zhu, S.W., Song, W.Y., Chong, K., and Wang, Z.Y. (2007). Functions of OsBZR1 and 14-3-3 proteins in brassinosteroid signaling in rice. Proc Natl Acad Sci USA 104, 13839–13844.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Balzergue, C., Dartevelle, T., Godon, C., Laugier, E., Meisrimler, C., Teulon, J.M., Creff, A., Bissler, M., Brouchoud, C., Hagège, A., et al. (2017). Low phosphate activates STOP1-ALMT1 to rapidly inhibit root cell elongation. Nat Commun 8, 15300.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beier, M.P., Obara, M., Taniai, A., Sawa, Y., Ishizawa, J., Yoshida, H., Tomita, N., Yamanaka, T., Ishizuka, Y., Kudo, S., et al. (2018). Lack of ACTPK1, an STY kinase, enhances ammonium uptake and use, and promotes growth of rice seedlings under sufficient external ammonium. Plant J 93, 992–1006.

    Article  CAS  PubMed  Google Scholar 

  • Chai, S., Chen, J., Yue, X., Li, C., Zhang, Q., de Dios, V.R., Yao, Y., and Tan, W. (2022). Interaction of BES1 and LBD37 transcription factors modulates brassinosteroid-regulated root forging response under low nitrogen in Arabidopsis. Front Plant Sci 13, 998961.

    Article  PubMed  PubMed Central  Google Scholar 

  • Che, R., Tong, H., Shi, B., Liu, Y., Fang, S., Liu, D., Xiao, Y., Hu, B., Liu, L., Wang, H., et al. (2015). Control of grain size and rice yield by GL2-mediated brassinosteroid responses. Nat Plants 2, 15195.

    Article  PubMed  Google Scholar 

  • Chen, R., Deng, Y., Ding, Y., Guo, J., Qiu, J., Wang, B., Wang, C., Xie, Y., Zhang, Z., Chen, J., et al. (2022). Rice functional genomics: decades’ efforts and roads ahead. Sci China Life Sci 65, 33–92.

    Article  PubMed  Google Scholar 

  • Chiou, T.J., and Lin, S.I. (2011). Signaling network in sensing phosphate availability in plants. Annu Rev Plant Biol 62, 185–206.

    Article  CAS  PubMed  Google Scholar 

  • Devi, L.L., Pandey, A., Gupta, S., and Singh, A.P. (2022). The interplay of auxin and brassinosteroid signaling tunes root growth under low and different nitrogen forms. Plant Physiol 189, 1757–1773.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Duan, P., Ni, S., Wang, J., Zhang, B., Xu, R., Wang, Y., Chen, H., Zhu, X., and Li, Y. (2015). Regulation of OsGRF4 by OsmiR396 controls grain size and yield in rice. Nat Plants 2, 15203.

    Article  PubMed  Google Scholar 

  • Favero, D.S. (2023). Shaping transcriptional responses to a phytohormone. Commun Biol 6, 45.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Giehl, R.F.H., and von Wiren, N. (2014). Root nutrient foraging. Plant Physiol 166, 509–517.

    Article  PubMed  PubMed Central  Google Scholar 

  • Godon, C., Mercier, C., Wang, X., David, P., Richaud, P., Nussaume, L., Liu, D., and Desnos, T. (2019). Under phosphate starvation conditions, Fe and Al trigger accumulation of the transcription factor STOP1 in the nucleus of Arabidopsis root cells. Plant J 99, 937–949.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grove, M.D., Spencer, G.F., Rohwedder, W.K., Mandava, N., Worley, J.F., Warthen Jr, J.D., Steffens, G.L., Flippen-Anderson, J.L., and Cook Jr, J. C. (1979). Brassinolide, a plant growth-promoting steroid isolated from Brassica napus pollen. Nature 281, 216–217.

    Article  CAS  Google Scholar 

  • Guo, M., Ruan, W., Li, C., Huang, F., Zeng, M., Liu, Y., Yu, Y., Ding, X., Wu, Y., Wu, Z., et al. (2015). Integrative comparison of the role of the PHOSPHATE RESPONSE1 subfamily in phosphate signaling and homeostasis in rice. Plant Physiol 168, 1762–1776.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo, M., Ruan, W., Zhang, Y., Zhang, Y., Wang, X., Guo, Z., Wang, L., Zhou, T., Paz-Ares, J., and Yi, K. (2022a). A reciprocal inhibitory module for Pi and iron signaling. Mol Plant 15, 138–150.

    Article  CAS  PubMed  Google Scholar 

  • Guo, M., Zhang, Y., Jia, X., Wang, X., Zhang, Y., Liu, J., Yang, Q., Ruan, W., and Yi, K. (2022b). Alternative splicing of REGULATOR OF LEAF INCLINATION 1 modulates phosphate starvation signaling and growth in plants. Plant Cell 34, 3319–3338.

    Article  PubMed  PubMed Central  Google Scholar 

  • He, J.X., Gendron, J.M., Yang, Y., Li, J., and Wang, Z.Y. (2002). The GSK3-like kinase BIN2 phosphorylates and destabilizes BZR1, a positive regulator of the brassinosteroid signaling pathway in Arabidopsis. Proc Natl Acad Sci USA 99, 10185–10190.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hirano, K., Yoshida, H., Aya, K., Kawamura, M., Hayashi, M., Hobo, T., Sato-Izawa, K., Kitano, H., Ueguchi-Tanaka, M., and Matsuoka, M. (2017). SMALL ORGAN SIZE 1 and SMALL ORGAN SIZE 2/DWARF AND LOW-TILLERING form a complex to integrate auxin and brassinosteroid signaling in rice. Mol Plant 10, 590–604.

    Article  CAS  PubMed  Google Scholar 

  • Hirsch, J., Marin, E., Floriani, M., Chiarenza, S., Richaud, P., Nussaume, L., and Thibaud, M.C. (2006). Phosphate deficiency promotes modification of iron distribution in Arabidopsis plants. Biochimie 88, 1767–1771.

    Article  CAS  PubMed  Google Scholar 

  • Ho, C.H., Lin, S.H., Hu, H.C., and Tsay, Y.F. (2009). CHL1 functions as a nitrate sensor in plants. Cell 138, 1184–1194.

    Article  CAS  PubMed  Google Scholar 

  • Hu, B., Jiang, Z., Wang, W., Qiu, Y., Zhang, Z., Liu, Y., Li, A., Gao, X., Liu, L., Qian, Y., et al. (2019). Nitrate-NRT1.1B-SPX4 cascade integrates nitrogen and phosphorus signalling networks in plants. Nat Plants 5, 401–413.

    Article  CAS  PubMed  Google Scholar 

  • Hu, B., Wang, W., Chen, J., Liu, Y., and Chu, C. (2022). Genetic improvement toward nitrogen-use efficiency in rice: lessons and perspectives. Mol Plant 16, 64–74.

    Article  CAS  PubMed  Google Scholar 

  • Hu, B., Wang, W., Ou, S., Tang, J., Li, H., Che, R., Zhang, Z., Chai, X., Wang, H., Wang, Y., et al. (2015). Variation in NRT1.1B contributes to nitrate-use divergence between rice subspecies. Nat Genet 47, 834–838.

    Article  CAS  PubMed  Google Scholar 

  • Hu, J., Ji, Y., Hu, X., Sun, S., and Wang, X. (2020a). BES1 functions as the co-regulator of D53-like SMXLs to inhibit BRC1 expression in strigolactone-regulated shoot branching in Arabidopsis. Plant Commun 1, 100014.

    Article  PubMed  Google Scholar 

  • Hu, J., Sun, S., and Wang, X. (2020b). Regulation of shoot branching by strigolactones and brassinosteroids: conserved and specific functions of Arabidopsis BES1 and rice BZR1. Mol Plant 13, 808–810.

    Article  CAS  PubMed  Google Scholar 

  • Hu, X., Qian, Q., Xu, T., Zhang, Y., Dong, G., Gao, T., Xie, Q., and Xue, Y. (2013) The U-box E3 ubiquitin ligase TUD1 functions with a heterotrimeric G alpha subunit to regulate Brassinosteroid-mediated growth in rice. PLoS Genet 9, e1003391.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang, G., and Zhang, D. (2020). The plasticity of root systems in response to external phosphate. Int J Mol Sci 21, 5955.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jang, S., An, G., and Li, H.Y. (2017). Rice leaf angle and grain size are affected by the OsBUL1 transcriptional activator complex. Plant Physiol 173, 688–702.

    Article  CAS  PubMed  Google Scholar 

  • Je, B.I., Piao, H.L., Park, S.J., Park, S.H., Kim, C.M., Xuan, Y.H., Park, S. H., Huang, J., Do Choi, Y., An, G., et al. (2010). RAV-Like1 maintains brassinosteroid homeostasis via the coordinated activation of BRI1 and biosynthetic genes in rice. Plant Cell 22, 1777–1791.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jia, Z., Giehl, R.F.H., Meyer, R.C., Altmann, T., and von Wirén, N. (2019). Natural variation of BSK3 tunes brassinosteroid signaling to regulate root foraging under low nitrogen. Nat Commun 10, 2378.

    Article  PubMed  PubMed Central  Google Scholar 

  • Jia, Z., Giehl, R.F.H., and von Wirén, N. (2020). The root foraging response under low nitrogen depends on DWARF1-mediated brassinosteroid biosynthesis. Plant Physiol 183, 998–1010.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jia, Z., Giehl, R.F.H., and von Wirén, N. (2021). Local auxin biosynthesis acts downstream of brassinosteroids to trigger root foraging for nitrogen. Nat Commun 12, 5437.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiao, X., Wang, H., Yan, J., Kong, X., Liu, Y., Chu, J., Chen, X., Fang, R., and Yan, Y. (2020). Promotion of BR biosynthesis by miR444 is required for ammonium-triggered inhibition of root growth. Plant Physiol 182, 1454–1466.

    Article  CAS  PubMed  Google Scholar 

  • Kim, B., Jeong, Y.J., Corvalán, C., Fujioka, S., Cho, S., Park, T., and Choe, S. (2014). Darkness and gulliver2/phyB mutation decrease the abundance of phosphorylated BZR1 to activate brassinosteroid signaling in Arabidopsis. Plant J 77, 737–747.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim, E.J., Lee, S.H., Park, C.H., Kim, S.H., Hsu, C.C., Xu, S., Wang, Z.Y., Kim, S.K., and Kim, T.W. (2021). Corrigendum to: Plant U-Box 40 mediates degradation of the brassinosteroid-responsive transcription factor BZR1 in Arabidopsis roots. Plant Cell 33, 2900.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kim, T.W., Guan, S., Burlingame, A.L., and 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kobayashi, T., Nagasaka, S., Senoura, T., Itai, R.N., Nakanishi, H., and Nishizawa, N.K. (2013). Iron-binding haemerythrin RING ubiquitin ligases regulate plant iron responses and accumulation. Nat Commun 4, 2792.

    Article  PubMed  Google Scholar 

  • Lambers, H., Hayes, P.E., Laliberté, E., Oliveira, R.S., and Turner, B.L. (2015). Leaf manganese accumulation and phosphorus-acquisition efficiency. Trends Plant Sci 20, 83–90.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Li, H., Hu, B., and Chu, C. (2017). Nitrogen use efficiency in crops: lessons from Arabidopsis and rice. J Exp Bot 68, 2477–2488.

    Article  CAS  PubMed  Google Scholar 

  • Li, J., and Chory, J. (1997). A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell 90, 929–938.

    Article  CAS  PubMed  Google Scholar 

  • Li, J., and Nam, K.H. (2002). Regulation of brassinosteroid signaling by a GSK3/SHAGGY-like kinase. Science 295, 1299–1301.

    Article  CAS  PubMed  Google Scholar 

  • Li, J., Nam, K.H., Vafeados, D., and Chory, J. (2001). BIN2, a new brassinosteroid-insensitive locus in Arabidopsis. Plant Physiol 127, 14–22.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li, J., Wen, J., Lease, K.A., Doke, J.T., Tax, F.E., and Walker, J.C. (2002). BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. Cell 110, 213–222.

    Article  CAS  PubMed  Google Scholar 

  • Li, S., Tian, Y., Wu, K., Ye, Y., Yu, J., Zhang, J., Liu, Q., Hu, M., Li, H., Tong, Y., et al. (2018). Modulating plant growth-metabolism coordination for sustainable agriculture. Nature 560, 595–600.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 brassinosteroid-induced GSK2 degradation in rice. Plant Commun 100450.

  • Liu, K.H., Liu, M., Lin, Z., Wang, Z.F., Chen, B., Liu, C., Guo, A., Konishi, M., Yanagisawa, S., Wagner, G., et al. (2022b). NIN-like protein 7 transcription factor is a plant nitrate sensor. Science 377, 1419–1425.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu, K.H., Niu, Y., Konishi, M., Wu, Y., Du, H., Sun Chung, H., Li, L., Boudsocq, M., McCormack, M., Maekawa, S., et al. (2017). Discovery of nitrate-CPK-NLP signalling in central nutrient-growth networks. Nature 545, 311–316.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu, K.H., and Tsay, Y.F. (2003). Switching between the two action modes of the dual-affinity nitrate transporter CHL1 by phosphorylation. EMBO J 22, 1005–1013.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu, T., Deng, S., Zhang, C., Yang, X., Shi, L., Xu, F., Wang, S., and Wang, C. (2023). Brassinosteroid signaling regulates phosphate starvation-induced malate secretion in plants. J Integr Plant Biol, doi: https://doi.org/10.1111/jipb.13443.

  • Liu, Y., Hu, B., and Chu, C. (2022c). Toward improving nitrogen use efficiency in rice: utilization, coordination, and availability. Curr Opin Plant Biol 71, 102327.

    Article  PubMed  Google Scholar 

  • Liu, Y., Wang, H., Jiang, Z., Wang, W., Xu, R., Wang, Q., Zhang, Z., Li, A., Liang, Y., Ou, S., et al. (2021). Genomic basis of geographical adaptation to soil nitrogen in rice. Nature 590, 600–605.

    Article  CAS  PubMed  Google Scholar 

  • López-Arredondo, D.L., Leyva-González, M.A., González-Morales, S.I., López-Bucio, J., and Herrera-Estrella, L. (2014). Phosphate nutrition: improving low-phosphate tolerance in crops. Annu Rev Plant Biol 65, 95–123.

    Article  PubMed  Google Scholar 

  • Lopez-Bucio, J., Hernandez-Abreu, E., Sanchez-Calderon, L., Nieto-Jacobo, M.i.F., Simpson, J., and Herrera-Estrella, L. (2002). Phosphate availability alters architecture and causes changes in hormone sensitivity in the Arabidopsis root system. Plant Physiol 129, 244–256.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Loqué, D., Lalonde, S., Looger, L.L., von Wirén, N., and Frommer, W.B. (2007). A cytosolic trans-activation domain essential for ammonium uptake. Nature 446, 195–198.

    Article  PubMed  Google Scholar 

  • Lv, Q., Zhong, Y., Wang, Y., Wang, Z., Zhang, L., Shi, J., Wu, Z., Liu, Y., Mao, C., Yi, K., et al. (2014). SPX4 negatively regulates phosphate signaling and homeostasis through its interaction with PHR2 in rice. Plant Cell 26, 1586–1597.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Müller, J., Toev, T., Heisters, M., Teller, J., Moore, K.L., Hause, G., Dinesh, D.C., Bürstenbinder, K., and Abel, S. (2015). Iron-dependent callose deposition adjusts root meristem maintenance to phosphate availability. Dev Cell 33, 216–230.

    Article  PubMed  Google Scholar 

  • Maathuis, F.J. (2009). Physiological functions of mineral macronutrients. Curr Opin Plant Biol 12, 250–258.

    Article  CAS  PubMed  Google Scholar 

  • Mghase, J.J., Hironobu, S., Hisamitsu, T., and Irie, K. (2011). Nutrition deficiencies and their symptoms in upland rice. J ISSAAS 17, 59–67.

    Google Scholar 

  • Mitchell, J.W., Mandava, N., Worley, J.F., Plimmer, J.R., and Smith, M.V. (1970). Brassins—a new family of plant hormones from rape pollen. Nature 225, 1065–1066.

    Article  CAS  PubMed  Google Scholar 

  • Mora-García, S., Vert, G., Yin, Y., Caño-Delgado, A., Cheong, H., and Chory, J. (2004). Nuclear protein phosphatases with Kelch-repeat domains modulate the response to brassinosteroids in Arabidopsis. Genes Dev 18, 448–460.

    Article  PubMed  PubMed Central  Google Scholar 

  • Nam, K.H., and Li, J. (2002). BRI1/BAK1, a receptor kinase pair mediating brassinosteroid signaling. Cell 110, 203–212.

    Article  CAS  PubMed  Google Scholar 

  • Näsholm, T., Kielland, K., and Ganeteg, U. (2009). Uptake of organic nitrogen by plants. New Phytol 182, 31–48.

    Article  PubMed  Google Scholar 

  • Negi, M., Sanagala, R., Rai, V., and Jain, A. (2016). Deciphering phosphate deficiency-mediated temporal effects on different root traits in rice grown in a modified hydroponic system. Front Plant Sci 7, 550.

    Article  PubMed  PubMed Central  Google Scholar 

  • Nolan, T.M., Vukašinović, N., Liu, D., Russinova, E., and Yin, Y. (2020). Brassinosteroids: multidimensional regulators of plant growth, development, and stress responses. Plant Cell 32, 295–318.

    Article  CAS  PubMed  Google Scholar 

  • Nosaki, S., Miyakawa, T., Xu, Y., Nakamura, A., Hirabayashi, K., Asami, T., Nakano, T., and Tanokura, M. (2018). Structural basis for brassinosteroid response by BIL1/BZR1. Nat Plants 4, 771–776.

    Article  CAS  PubMed  Google Scholar 

  • Puga, M.I., Mateos, I., Charukesi, R., Wang, Z., Franco-Zorrilla, J.M., de Lorenzo, L., Irigoyen, M.L., Masiero, S., Bustos, R., Rodríguez, J., et al. (2014). SPX1 is a phosphate-dependent inhibitor of PHOSPHATE STARVATION RESPONSE 1 in Arabidopsis. Proc Natl Acad Sci USA 111, 14947–14952.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qiao, S., Sun, S., Wang, L., Wu, Z., Li, C., Li, X., Wang, T., Leng, L., Tian, W., Lu, T., et al. (2017). The RLA1/SMOS1 transcription factor functions with OsBZR1 to regulate brassinosteroid signaling and rice architecture. Plant Cell 29, 292–309.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Romera, F.J., and Alcántara, E. (2004). Ethylene involvement in the regulation of Fe-deficiency stress responses by Strategy I plants. Funct Plant Biol 31, 315–328.

    Article  CAS  PubMed  Google Scholar 

  • Ruan, W., Guo, M., Xu, L., Wang, X., Zhao, H., Wang, J., and Yi, K. (2018). An SPX-RLI1 module regulates leaf inclination in response to phosphate availability in rice. Plant Cell 30, 853–870.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ryu, H., Kim, K., Cho, H., Park, J., Choe, S., and Hwang, I. (2007). Nucleocytoplasmic shuttling of BZR1 mediated by phosphorylation is essential in Arabidopsis brassinosteroid signaling. Plant Cell 19, 2749–2762.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saenchai, C., Bouain, N., Kisko, M., Prom-u-thai, C., Doumas, P., and Rouached, H. (2016). The involvement of OsPHO1;1 in the regulation of iron transport through integration of phosphate and zinc deficiency signaling. Front Plant Sci 7, 396.

    Article  PubMed  PubMed Central  Google Scholar 

  • Secco, D., Wang, C., Arpat, B.A., Wang, Z., Poirier, Y., Tyerman, S.D., Wu, P., Shou, H., and Whelan, J. (2012). The emerging importance of the SPX domain-containing proteins in phosphate homeostasis. New Phytol 193, 842–851.

    Article  CAS  PubMed  Google Scholar 

  • Shen, J., Yuan, L., Zhang, J., Li, H., Bai, Z., Chen, X., Zhang, W., and Zhang, F. (2011). Phosphorus dynamics: from soil to plant. Plant Physiol 156, 997–1005.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh, A.P., Fridman, Y., Friedlander-Shani, L., Tarkowska, D., Strnad, M., and Savaldi-Goldstein, S. (2014). Activity of the brassinosteroid transcription factors BRASSINAZOLE RESISTANT1 and BRASS-INOSTEROID INSENSITIVE1-ETHYL METHANESULFONATE-SUPPRESSOR1/BRASSINAZOLE RESISTANT2 blocks developmental reprogramming in response to low phosphate availability. Plant Physiol 166, 678–688.

    Article  PubMed  PubMed Central  Google Scholar 

  • Singh, A.P., Fridman, Y., Holland, N., Ackerman-Lavert, M., Zananiri, R., Jaillais, Y., Henn, A., and Savaldi-Goldstein, S. (2018). Interdependent nutrient availability and steroid hormone signals facilitate root growth plasticity. Dev Cell 46, 59–72.e4.

    Article  CAS  PubMed  Google Scholar 

  • Song, X., Li, J., Lyu, M., Kong, X., Hu, S., Song, Q., and Zuo, K. (2021). CALMODULIN-LIKE-38 and PEP1 RECEPTOR 2 integrate nitrate and brassinosteroid signals to regulate root growth. Plant Physiol 187, 1779–1794.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun, L., Lu, Y., Yu, F., Kronzucker, H.J., and Shi, W. (2016). Biological nitrification inhibition by rice root exudates and its relationship with nitrogen-use efficiency. New Phytol 212, 646–656.

    Article  CAS  PubMed  Google Scholar 

  • Sun, S., Chen, D., Li, X., Qiao, S., Shi, C., Li, C., Shen, H., and Wang, X. (2015). Brassinosteroid signaling regulates leaf erectness in Oryza sativa via the control of a specific U-type cyclin and cell proliferation. Dev Cell 34, 220–228.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tanaka, A., Nakagawa, H., Tomita, C., Shimatani, Z., Ohtake, M., Nomura, T., Jiang, C.J., Dubouzet, J.G., Kikuchi, S., Sekimoto, H., 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tang, W., Kim, T.W., Oses-Prieto, J.A., Sun, Y., Deng, Z., Zhu, S., Wang, R., Burlingame, A.L., and Wang, Z.Y. (2008). BSKs mediate signal transduction from the receptor kinase BRI1 in Arabidopsis. Science 321, 557–560.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tong, H., and Chu, C. (2018). Functional specificities of brassinosteroid and potential utilization for crop improvement. Trends Plant Sci 23, 1016–1028.

    Article  CAS  PubMed  Google Scholar 

  • Tong, H., Jin, Y., Liu, W., Li, F., Fang, J., Yin, Y., Qian, Q., Zhu, L., and Chu, C. (2009). DWARF AND LOW-TILLERING, a new member of the GRAS family, plays positive roles in brassinosteroid signaling in rice. Plant J 58, 803–816.

    Article  CAS  PubMed  Google Scholar 

  • Tong, H., Liu, L., Jin, Y., Du, L., Yin, Y., Qian, Q., Zhu, L., and Chu, C. (2012). DWARF AND LOW-TILLERING acts as a direct downstream target of a GSK3/SHAGGY-like kinase to mediate brassinosteroid responses in rice. Plant Cell 24, 2562–2577.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tong, H., Xiao, Y., Liu, D., Gao, S., Liu, L., Yin, Y., Jin, Y., Qian, Q., and Chu, C. (2014). Brassinosteroid regulates cell elongation by modulating gibberellin metabolism in rice. Plant Cell 26, 4376–4393.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vega, A., O’Brien, J.A., and Gutiérrez, R.A. (2019). Nitrate and hormonal signaling crosstalk for plant growth and development. Curr Opin Plant Biol 52, 155–163.

    Article  CAS  PubMed  Google Scholar 

  • Vriet, C., Russinova, E., and Reuzeau, C. (2013). From squalene to brassinolide: the steroid metabolic and signaling pathways across the plant kingdom. Mol Plant 6, 1738–1757.

    Article  CAS  PubMed  Google Scholar 

  • Wang, B., Li, G., and Zhang, W.H. (2015). Brassinosteroids are involved in Fe homeostasis in rice (Oryza sativa L). J Exp Bot 66, 2749–2761.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, R., Liu, M., Yuan, M., Oses-Prieto, J.A., Cai, X., Sun, Y., Burlingame, A.L., Wang, Z.Y., and 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.

    Article  CAS  PubMed  Google Scholar 

  • Wang, X., and Chory, J. (2006). Brassinosteroids regulate dissociation of BKI1, a negative regulator of BRI1 signaling, from the plasma membrane. Science 313, 1118–1122.

    Article  CAS  PubMed  Google Scholar 

  • Wang, X., Wang, Z., Zheng, Z., Dong, J., Song, L., Sui, L., Nussaume, L., Desnos, T., and Liu, D. (2019). Genetic dissection of Fe-dependent signaling in root developmental responses to phosphate deficiency. Plant Physiol 179, 300–316.

    Article  CAS  PubMed  Google Scholar 

  • Wang, Y., Sun, S., Zhu, W., Jia, K., Yang, H., and Wang, X. (2013). Strigolactone/MAX2-induced degradation of brassinosteroid transcriptional effector BES1 regulates shoot branching. Dev Cell 27, 681–688.

    Article  CAS  PubMed  Google Scholar 

  • Wang, Z., Ruan, W., Shi, J., Zhang, L., Xiang, D., Yang, C., Li, C., Wu, Z., Liu, Y., Yu, Y., et al. (2014). Rice SPX1 and SPX2 inhibit phosphate starvation responses through interacting with PHR2 in a phosphate-dependent manner. Proc Natl Acad Sci USA 111, 14953–14958.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, Z.Y., Bai, M.Y., Oh, E., and Zhu, J.Y. (2012). Brassinosteroid signaling network and regulation of photomorphogenesis. Annu Rev Genet 46, 701–724.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Wang, Z.Y., Seto, H., Fujioka, S., Yoshida, S., and Chory, J. (2001). BRI1 is a critical component of a plasma-membrane receptor for plant steroids. Nature 410, 380–383.

    Article  CAS  PubMed  Google Scholar 

  • Ward, J.T., Lahner, B., Yakubova, E., Salt, D.E., and Raghothama, K.G. (2008). The effect of iron on the primary root elongation of Arabidopsis during phosphate deficiency. Plant Physiol 147, 1181–1191.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu, K., Wang, S., Song, W., Zhang, J., Wang, Y., Liu, Q., Yu, J., Ye, Y., Li, S., Chen, J., et al. (2020). Enhanced sustainable green revolution yield via nitrogen-responsive chromatin modulation in rice. Science 367, eaaz2046.

    Article  CAS  PubMed  Google Scholar 

  • Wu, P., Shou, H., Xu, G., and Lian, X. (2013). Improvement of phosphorus efficiency in rice on the basis of understanding phosphate signaling and homeostasis. Curr Opin Plant Biol 16, 205–212.

    Article  CAS  PubMed  Google Scholar 

  • Xiao, Y., Zhang, G., Liu, D., Niu, M., Tong, H., and Chu, C. (2020). GSK2 stabilizes OFP3 to suppress brassinosteroid responses in rice. Plant J 102, 1187–1201.

    Article  CAS  PubMed  Google Scholar 

  • Xuan, Y.H., Duan, F.Y., Je, B.I., Kim, C.M., Li, T.Y., Liu, J.M., Park, S.J., Cho, J.H., Kim, T.H., 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.

    CAS  PubMed  Google Scholar 

  • Yamamuro, C., Ihara, Y., Wu, X., Noguchi, T., Fujioka, S., Takatsuto, S., Ashikari, M., Kitano, H., and Matsuoka, M. (2000). Loss of function of a rice brassinosteroid insensitive1 homolog prevents internode elongation and bending of the lamina joint. Plant Cell 12, 1591–1605.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang, C., Shen, W., He, Y., Tian, Z., Li, J. (2016) OVATE family protein 8 positively mediates brassinosteroid signaling through interacting with the GSK3-like kinase in rice. PLoS Genet 12: e1006118.

    Article  PubMed  PubMed Central  Google Scholar 

  • Yang, M., Li, C., Cai, Z., Hu, Y., Nolan, T., Yu, F., Yin, Y., Xie, Q., Tang, G., and Wang, X. (2017). SINAT E3 ligases control the light-mediated stability of the brassinosteroid-activated transcription factor BES1 in Arabidopsis. Dev Cell 41, 47–58.e4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yin, W., Li, L., Yu, Z., Zhang, F., Liu, D., Wu, H., Niu, M., Meng, W., Zhang, X., Dong, N., et al. (2022). The divergence of brassinosteroid sensitivity between rice subspecies involves natural variation conferring altered internal auto-binding of OsBSK2. J Integr Plant Biol 64, 1614–1630.

    Article  CAS  PubMed  Google Scholar 

  • Yin, Y., Wang, Z.Y., Mora-Garcia, S., Li, J., Yoshida, S., Asami, T., and Chory, J. (2002). BES1 accumulates in the nucleus in response to brassinosteroids to regulate gene expression and promote stem elongation. Cell 109, 181–191.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, B., Wang, X., Zhao, Z., Wang, R., Huang, X., Zhu, Y., Yuan, L., Wang, Y., Xu, X., Burlingame, A.L., et al. (2016). OsBRI1 activates BR signaling by preventing binding between the TPR and kinase domains of OsBSK3 via phosphorylation. Plant Physiol 170, 1149–1161.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, C., Xu, Y., Guo, S., Zhu, J., Huan, Q., Liu, H., Wang, L., Luo, G., Wang, X., and Chong, K. (2012). Dynamics of brassinosteroid response modulated by negative regulator LIC in rice. PLoS Genet 8, e1002686.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, L.Y., Bai, M.Y., Wu, J., Zhu, J.Y., Wang, H., Zhang, Z., Wang, W., Sun, Y., Zhao, J., Sun, X., et al. (2009). Antagonistic HLH/bHLH transcription factors mediate brassinosteroid regulation of cell elongation and plant development in rice and Arabidopsis. Plant Cell 21, 3767–3780.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao, B.T., Zhu, X.F., Jung, J.H., and Xuan, Y.H. (2016). Effect of brassinosteroids on ammonium uptake via regulation of ammonium transporter and N-metabolism genes in Arabidopsis. Biologia Plant 60, 563–571.

    Article  CAS  Google Scholar 

  • Zheng, L., Huang, F., Narsai, R., Wu, J., Giraud, E., He, F., Cheng, L., Wang, F., Wu, P., Whelan, J., et al. (2009). Physiological and transcriptome analysis of iron and phosphorus interaction in rice seedlings. Plant Physiol 151, 262–274.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou, Z., Wang, Z., Lv, Q., Shi, J., Zhong, Y., Wu, P., and Mao, C. (2015). SPX proteins regulate Pi homeostasis and signaling in different subcellular level. Plant Signal Behav 10, e1061163.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhu, J.Y., Li, Y., Cao, D.M., Yang, H., Oh, E., Bi, Y., Zhu, S., and Wang, Z. Y. (2017). The F-box protein KIB1 mediates brassinosteroid-induced inactivation and degradation of GSK3-like kinases in Arabidopsis. Mol Cell 66, 648–657.e4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (32130095) and the National Key Research and Development Program of China (2022YFF1001600).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Hongning Tong or Chengcai Chu.

Additional information

Compliance and ethics

The author(s) declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, G., Liu, Y., Xie, Q. et al. Crosstalk between brassinosteroid signaling and variable nutrient environments. Sci. China Life Sci. 66, 1231–1244 (2023). https://doi.org/10.1007/s11427-022-2319-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11427-022-2319-0

Keywords

Navigation