Chinese Bulletin of Botany ›› 2019, Vol. 54 ›› Issue (2): 185-193.doi: 10.11983/CBB19013


• EXPERIMENTAL COMMUNICATIONS • Previous Articles     Next Articles

Functional Analysis of Brassinosteroids in Salt Stress Responses in Rice

Li Lulu,Yin Wenchao,Niu Mei,Meng Wenjing,Zhang Xiaoxing,Tong Hongning()   

  1. Institute of Crop Sciences, Chinese Academy of Agricultural Sciences/National Key Facility for Crop Gene Resources and Genetic Improvement, Beijing 100081, China
  • Received:2019-01-18 Accepted:2019-03-19 Online:2019-09-01 Published:2019-03-01
  • Contact: Tong Hongning


Brassinosteroids (BRs) are a class of steroid phytohormones that play diverse roles in plant growth and development and stress responses. Rapid progresses have been made in how BRs regulate plant growth and development in recent years. However, the roles of BRs in stress response in Oryza sativa remain unclear. Here, we investigated the relation between salinity stress and BR synthesis in rice. Both salt stress and abscisic acid, the well-known stress hormone, strongly inhibited the expression of two BR-synthetic genes, D2 and D11. In addition, both d2-2, the BR synthetic mutant, and d61-1, the BR receptor mutant, showed impaired tolerance to salt stress. Moreover, by using transgenic plants overexpressing OsBZR1, the key BR signaling transcriptional factor, we found that BRs strongly induced dephosphorylation of OsBZR1, but high concentrations of salt suppressed OsBZR1 protein accumulation as well as its dephosphorylation. Furthermore, transcriptome analyses revealed that 38.4% of BR-regulated genes were also regulated by high concentrations of salt, and importantly, 91.5% of the co-regulated genes are consistently up- or downregulated by both BR and salt. Gene Ontology analyses revealed that these overlapping genes were highly enriched in the biological process “response to stimulus”. Taken together, our results suggest that BRs contribute to salt stress tolerance, and salt stress suppresses BR synthesis to restrict rice growth.

Key words: brassinosteroid, rice, salt stress, abscisic acid, OsBZR1

Figure 1

Time-course expression of BR synthetic genes in rice following salt or ABA treatment(A) D2 expression after NaCl treatment; (B) D11 expression after NaCl treatment; (C) D2 expression after ABA treatment; (D) D11 expression after ABA treatment. * P<0.05; *** P<0.001"

Figure 2

Survival rate of rice BR defective mutants and the wild type under salt stress(A) Growth status of d2-2 mutant and the wild type after salt treatment; (B) Statistic data of the survival rate of d2-2 and the wild type after salt treatment; (C) Growth status of d61-1 mutant and the wild type after salt treatment; (D) Statistic data of the survival rate of d61-1 and the wild type after salt treatment. ** P<0.01"

Figure 3

Effects of BR and salt stress on OsBZR1 proteins in rice(A) Effect of BR treatment on OsBZR1 proteins; (B) Effect of salt treatment on OsBZR1 proteins"

Figure 4

Co-regulation analyses of BR-, ABA- and NaCl-regulated genes of rice(A) Co-regulated gene numbers between BR-, ABA- and NaCl-regulated different expression genes (DEGs); (B) Co-regulation analyses among BR-upregulated (BR-UP), BR-downregulated (BR-DN), NaCl-upregulated (NaCl-UP) and NaCl-downregulated (NaCl-DN) genes. Distribution of the gene numbers was indicated."

Figure 5

Gene Ontology analyses of the 189 BR-NaCl co-regulated genes of rice(A) GO analyses in term of the biological process; (B) GO analyses in terms of biological process, cellular component, and molecular function"

Figure 6

Proposed model for BR function in salt stress res- ponses in rice"

[1] 李钱峰, 鲁军, 余佳雯, 张昌泉, 刘巧泉 ( 2018). 油菜素内酯与脱落酸互作调控植物生长与抗逆的分子机制研究进展. 植物生理学报 54, 370-378.
[2] 王沛雅, 周剑平, 王治业, 张军, 强维亚, 杨涛, 郭琪, 杨晖 ( 2014). 油菜素内酯合成酶基因DAS5促进杨树生长及提高抗旱性的作用. 植物学报 49, 407-416.
[3] 吴家富, 杨博文, 向珣朝, 许亮, 颜李梅 ( 2017). 不同水稻种质在不同生育期耐盐鉴定的差异. 植物学报 52, 77-88.
[4] 俞仁培, 陈德明 ( 1999). 我国盐渍土资源及其开发利用. 土壤通报 30, 158-159.
[5] Choe S ( 2006). Brassinosteroid biosynthesis and inactiva- tion. Physiol Plant 126, 539-548.
doi: 10.1111/ppl.2006.126.issue-4
[6] Divi UK, Krishna P ( 2009). Brassinosteroid: a biotechno- logical target for enhancing crop yield and stress tole- rance. N Biotechnol 26, 131-136.
doi: 10.1016/j.nbt.2009.07.006
[7] Feng Y, Yin YH, Fei SZ ( 2015). Down-regulation of BdBRI1, a putative brassinosteroid receptor gene produces a dwarf phenotype with enhanced drought tolerance in Brachy- podium distachyon. Plant Sci 234, 163-173.
[8] Grove MD, Spencer GF, Rohwedder WK, Mandava N, Worley JF, Warthen JD Jr, Steffens GL, Flippen- Anderson JL, Cook JC Jr ( 1979). Brassinolide, a plant growth-promoting steroid isolated from Brassica napus pollen. Nature 281, 216-217.
[9] Ha YM, Shang Y, Nam KH ( 2016). Brassinosteroids modu- late ABA-induced stomatal closure in Arabidopsis. J Exp Bot 67, 6297-6308.
doi: 10.1093/jxb/erw385
[10] He JX, Gendron JM, Sun Y, Gampala SSL, Gendron N, Sun CQ, Wang ZY ( 2005). BZR1 is a transcriptional repressor with dual roles in brassinosteroid homeostasis and growth responses. Science 307, 1634-1638.
doi: 10.1126/science.1107580
[11] He JX, Gendron JM, Yang YL, Li JM, Wang ZY ( 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.
doi: 10.1073/pnas.152342599
[12] Hong Z, Ueguchi-Tanaka M, Matsuoka M ( 2004). Bras- sinosteroids and rice architecture. J Pestic Sci 29, 184-188.
doi: 10.1584/jpestics.29.184
[13] Hong Z, Ueguchi-Tanaka M, Umemura K, Uozu S, Fujioka S, Takatsuto S, Yoshida S, Ashikari M, Kitano H, 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.
[14] Khripach V, Zhabinskii V, De Groot A ( 2000). Twenty years of brassinosteroids: steroidal plant hormones warrant better crops for the XXI century. Ann Bot 86, 441-447.
doi: 10.1006/anbo.2000.1227
[15] Kim TW, Wang ZY ( 2010). Brassinosteroid signal transduc- tion from receptor kinases to transcription factors. Annu Rev Plant Biol 61, 681-704.
doi: 10.1146/annurev.arplant.043008.092057
[16] Krishna P, Prasad BD, Rahman T ( 2017). Brassinosteroid action in plant abiotic stress tolerance. In: Russinova E, Caño-Delgado AI, eds. Brassinosteroids. New York: Hum- ana Press. pp. 193-202.
[17] Morinaka Y, Sakamoto T, Inukai Y, Agetsuma M, Kitano H, Ashikari M, Matsuoka M ( 2006). Morphological alteration caused by brassinosteroid insensitivity increases the biomass and grain production of rice. Plant Physiol 141, 924-931.
doi: 10.1104/pp.106.077081
[18] Nakashima K, Yamaguchi-Shinozaki K ( 2013). ABA signaling in stress-response and seed development. Plant Cell Rep 32, 959-970.
doi: 10.1007/s00299-013-1418-1
[19] Nolan TM, Brennan B, Yang MR, Chen JN, Zhang MC, Li ZH, Wang XL, Bassham DC, Walley J, Yin YH ( 2017). Selective autophagy of BES1 mediated by DSK2 balances plant growth and survival. Dev Cell 41, 33-46.e7.
[20] Peleg Z, Blumwald E ( 2011). Hormone balance and abiotic stress tolerance in crop plants. Curr Opin Plant Biol 14, 290-295.
doi: 10.1016/j.pbi.2011.02.001
[21] Ryu H, Kim K, Cho H, Park J, Choe S, Hwang I ( 2007). Nucleocytoplasmic shuttling of BZR1 mediated by phos- phorylation is essential in Arabidopsis brassinosteroid signaling. Plant Cell 19, 2749-2762.
doi: 10.1105/tpc.107.053728
[22] Sakamoto T, Morinaka Y, Ohnishi T, Sunohara H, Fujioka S, Ueguchi-Tanaka M, Mizutani M, Sakata K, Takatsuto S, Yoshida S, Tanaka H, Kitano H, Matsuoka M ( 2006). Erect leaves caused by brassinosteroid deficiency inc- rease biomass production and grain yield in rice. Nat Bio- technol 24, 105-109.
doi: 10.1038/nbt1173
[23] Singh AP, Savaldi-Goldstein S ( 2015). Growth control: brassinosteroid activity gets context. J Exp Bot 66, 1123-1132.
doi: 10.1093/jxb/erv026
[24] Sun Y, Fan XY, Cao DM, Tang WQ, He K, Zhu JY, He JX, Bai MY, Zhu SW, Oh E, Patil S, Kim TW, Ji HK, Wong WH, Rhee SY, Wang ZY ( 2010). Integration of bras- sinosteroid signal transduction with the transcription network for plant growth regulation in Arabidopsis. Dev Cell 19, 765-777.
doi: 10.1016/j.devcel.2010.10.010
[25] Tong HN, Chu CC ( 2016). Reply: brassinosteroid regulates gibberellin synthesis to promote cell elongation in rice: critical comments on ross and quittenden's letter. Plant Cell 28, 833-835.
[26] Tong HN, Chu CC ( 2018). Functional specificities of bras- sinosteroid and potential utilization for crop improvement. Trends Plant Sci 23, 1016-1028.
[27] Tong HN, Liu LC, Jin Y, Du L, Yin YH, Qian Q, Zhu LH, Chu CC ( 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.
doi: 10.1105/tpc.112.097394
[28] Tong HN, Xiao YH, Liu DP, Gao SP, Liu LC, Yin YH, Jin Y, Qian Q, Chu CC ( 2014). Brassinosteroid regulates cell elongation by modulating gibberellin metabolism in rice. Plant Cell 26, 4376-4393.
doi: 10.1105/tpc.114.132092
[29] Wang ZY, Nakano T, Gendron J, He JX, Chen M, Vafeados D, Yang YL, Fujioka S, Yoshida S, Asami T, Chory J ( 2002). Nuclear-localized BZR1 mediates bras- sinosteroid-induced growth and feedback suppression of brassinosteroid biosynthesis. Dev Cell 2, 505-513.
doi: 10.1016/S1534-5807(02)00153-3
[30] Wu CY, Trieu A, Radhakrishnan P, Kwok SF, Harris S, Zhang K, Wang JL, Wan JM, Zhai HQ, Takatsuto S, Matsumoto S, Fujioka S, Feldmann KA, Pennell RI ( 2008). Brassinosteroids regulate grain filling in rice. Plant Cell 20, 2130-2145.
doi: 10.1105/tpc.107.055087
[31] Yamamuro C, Ihara Y, Wu X, Noguchi T, Fujioka S, Takatsuto S, Ashikari M, Kitano H, Matsuoka M ( 2000). Loss of function of a rice brassinosteroid insensitive 1 homolog prevents internode elongation and bending of the lamina joint. Plant Cell 12, 1591-1606.
[32] Yang MR, Li CX, Cai ZY, Hu YM, Nolan T, Yu FF, Yin YH, Xie Q, Tang GL, Wang XL ( 2017). SINAT E3 ligases control the light-mediated stability of the brassinosteroid- activated transcription factor BES1 in Arabidopsis. Dev Cell 41, 47-58.e4.
[33] Yin WC, Dong NN, Niu M, Zhang XX, Li LL, Liu J, Liu B, Tong HN ( 2018). Brassinosteroid-regulated plant growth and development and gene expression in soybean. Crop J. DOI: 10.1016/j.cj.2018.10.003.
[34] Yin YH, Wang ZY, Mora-Garcia S, Li JM, 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.
doi: 10.1016/S0092-8674(02)00721-3
[35] Yu XF, Li L, Zola J, Aluru M, Ye HX, Foudree A, Guo HQ, Anderson S, Aluru S, Liu P, Rodermel S, Yin YH ( 2011). A brassinosteroid transcriptional network revealed by genome-wide identification of BESI target genes in Ara- bidopsis thaliana . Plant J 65, 634-646.
[36] Zhao X, Dou LR, Gong ZZ, Wang XF, Mao TL ( 2019). BES1 hinders ABSCISIC ACID INSENSITIVE5 and promotes seed germination in Arabidopsis. New Phytol 221, 908-918.
doi: 10.1111/nph.15437
[37] Zhu JK ( 2001). Plant salt tolerance. Trends Plant Sci 6, 66-71.
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[1] Zhang Zhen-jue. Some Principles Governing Shedding of Flowers and Fruits in Vanilla fragrans[J]. Chinese Bulletin of Botany, 1985, 3(05): 36 -37 .
[2] Qian Gao;Yuying Liu;Yinan Fei;Dapeng Li;Xianglin Liu* . Research Advances into the Root Radial Patterning Gene SHORT-ROOT[J]. Chinese Bulletin of Botany, 2008, 25(03): 363 -372 .
[3] Wang Bao-shan;Zou Qi and Zhao Ke-fu. Advances in Mechanism of Crop Salt Tolerance and Strategies for Raising Crop Salt Tolerance[J]. Chinese Bulletin of Botany, 1997, 14(增刊): 25 -30 .
[4] HE Feng WU Zhen-Bin. Application of Aquatic Plants in Sewage Treatment and Water Quality Improvement[J]. Chinese Bulletin of Botany, 2003, 20(06): 641 -647 .
[5] JIA Hu-Sen LI De-QuanHAN Ya-Qin. Cytochrome b-559 in Chloroplasts[J]. Chinese Bulletin of Botany, 2001, 18(02): 158 -162 .
[6] Wei Sun;Chonghui Li;Liangsheng Wang;Silan Dai*. Analysis of Anthocyanins and Flavones in Different-colored Flowers of Chrysanthemum[J]. Chinese Bulletin of Botany, 2010, 45(03): 327 -336 .
[7] . Phosphate_Stress Protein and Iron_Stress Protein in Plants[J]. Chinese Bulletin of Botany, 2001, 18(05): 571 -576 .
[8] ZHANG Da-Yong, JIANG Xin-Hua. An Ecological Perspective on Crop Prduction[J]. Chin J Plan Ecolo, 2000, 24(3): 383 -384 .
[9] Gui Ji-xun, Zhu Ting-cheng. Study of Energy Flow Between Litter and Decomposers in Aneurolepidium chinese Grassland[J]. Chin J Plan Ecolo, 1992, 16(2): 143 -148 .
[10] YAN Xiu-Feng. Ecology of Plant secondary Metabolism[J]. Chin J Plan Ecolo, 2001, 25(5): 639 -640 .