植物学报 ›› 2019, Vol. 54 ›› Issue (2): 185-193.doi: 10.11983/CBB19013

所属专题: 逆境生物学专辑

• 研究报告 • 上一篇    下一篇

油菜素甾醇调控水稻盐胁迫应答的作用研究

栗露露,殷文超,牛梅,孟文静,张晓星,童红宁()   

  1. 农作物基因资源与基因改良国家重大科学工程/中国农业科学院作物科学研究所, 北京 100081
  • 收稿日期:2019-01-18 接受日期:2019-03-19 出版日期:2019-03-01 发布日期:2019-09-01
  • 通讯作者: 童红宁 E-mail:tonghongning@caas.cn
  • 基金资助:
    国家自然科学基金(91735302);国家自然科学基金(31871587);国家自然科学基金(31722037)

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:2019-03-01 Published:2019-09-01
  • Contact: Tong Hongning E-mail:tonghongning@caas.cn

摘要:

油菜素甾醇(BR)作为植物内源激素, 广泛参与植物的生长发育过程及逆境应答。虽然BR调控生长发育的分子机制目前已相对清楚, 但在水稻(Oryza sativa)中, BR在逆境反应中的功能还鲜有报道。该研究系统分析了BR在高盐胁迫过程中的作用, 表明盐胁迫和逆境激素脱落酸可抑制BR合成基因D2D11的表达, 典型的BR缺陷突变体(如d2-2d61-1)则表现出对盐胁迫敏感性增强。此外, 通过对BR核心转录因子OsBZR1的过表达株系进行分析, 发现BR可显著诱导OsBZR1的去磷酸化, 盐胁迫对OsBZR1蛋白的积累水平和磷酸化状态均有调控作用。转录组数据分析表明, BR处理前后差异表达基因中有38.4%同时受到盐胁迫调控, 其中91.5%受到BR和高盐一致调控, 并显著富集在应激反应过程中。研究结果表明, BR正调控水稻的耐盐性, 而盐胁迫通过抑制BR合成来限制水稻的生长。

关键词: 油菜素甾醇, 水稻, 盐胁迫, 脱落酸, OsBZR1

Abstract:

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

图1

不同时间高盐和ABA处理对水稻BR合成基因表达的影响(A) 盐处理后D2基因的表达; (B) 盐处理后D11基因的表达; (C) ABA处理后D2基因的表达; (D) ABA处理后D11基因的表达。* P< 0.05; *** P<0.001"

图2

盐胁迫下水稻BR缺陷突变体及其野生型的存活率(A) 盐处理后d2-2突变体及其野生型的生长情况; (B) 盐处理后d2-2突变体及其野生型的存活率统计; (C) 盐处理后d61-1突变体及其野生型的生长情况; (D) 盐处理后d61-1突变体及其野生型的存活率统计。** P<0.01"

图3

不同时间BR和盐处理对水稻OsBZR1蛋白的影响(A) BR处理对OsBZR1蛋白的影响; (B) 盐处理对OsBZR1蛋白的影响"

图4

BR、ABA和盐处理后水稻差异基因共调控分析(A) BR和ABA与盐差异调控基因的共调控分析; (B) BR上调(BR-UP)和下调(BR-DN)以及NaCl上调(NaCl-UP)和下调(NaCl-DN)基因的共调控分析。图中显示差异基因的分布及数目。"

图5

水稻189个BR和盐共调控基因的聚类分析(A) 生物学途径聚类分析; (B) 生物学途径、细胞组分及分子功能的聚类分析"

图6

BR在水稻盐胁迫反应中的作用模型"

[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.
[1] 田怀东 李菁 田保华 牛鹏飞 李珍 岳忠孝 屈雅娟 姜建芳 王广元 岑慧慧 李南 闫枫. 水稻两性生殖细胞的N-甲基-N-亚硝基脲诱变方法[J]. 植物学报, 2019, 54(5): 0-0.
[2] 王跃星 饶玉春 焦然 周纯 林晗 徐娜 胡娟 胡萍 吴先美. 水稻早衰突变体LS-es1的基因定位及候选基因分析[J]. 植物学报, 2019, 54(5): 0-0.
[3] 吴昌银. 长链非编码RNA基因Ef-cd 平衡水稻的早熟与稳产[J]. 植物学报, 2019, 54(5): 0-0.
[4] 刘栋峰, 唐永严, 雒胜韬, 罗伟, 李志涛, 种康, 徐云远. 利用低温水浴鉴定水稻苗期耐寒性[J]. 植物学报, 2019, 54(4): 509-514.
[5] 刘进, 姚晓云, 余丽琴, 李慧, 周慧颖, 王嘉宇, 黎毛毛. 水稻耐储藏特性三年动态鉴定与QTL分析[J]. 植物学报, 2019, 54(4): 464-473.
[6] 程新杰, 于恒秀, 程祝宽. 水稻减数分裂染色体分析方法[J]. 植物学报, 2019, 54(4): 503-508.
[7] 张静,侯岁稳. 蛋白质翻译后修饰在ABA信号转导中的作用[J]. 植物学报, 2019, 54(3): 300-315.
[8] 王孝林,王二涛. 根际微生物促进水稻氮利用的机制[J]. 植物学报, 2019, 54(3): 285-287.
[9] 陈琳,林焱,陈鹏飞,王绍华,丁艳锋. 水稻响应缺铁的韧皮部汁液蛋白质组学分析[J]. 植物学报, 2019, 54(2): 194-207.
[10] 叶雯澜,马国兰,袁李亚男,郑士仪,程琳乔,方媛,饶玉春. 水稻细菌性穗枯病的病原特性和抗性研究进展[J]. 植物学报, 2019, 54(2): 277-283.
[11] 朱丽, 钱前. 虾青素功能米: 生物强化新思路, 优质米培育新资源[J]. 植物学报, 2019, 54(1): 4-8.
[12] 薛治慧, 种康. 中国科学家在杂种F1克隆繁殖研究领域取得突破性进展[J]. 植物学报, 2019, 54(1): 1-3.
[13] 周亭亭, 饶玉春, 任德勇. 水稻卷叶细胞学与分子机制研究进展[J]. 植物学报, 2018, 53(6): 848-855.
[14] 鲁丹, 王丽, 宋凡, 陶菊红, 张大兵, 袁政. 水稻OsJMJ718基因可选择性多聚腺苷酸化序列的 克隆及生殖发育期表达模式[J]. 植物学报, 2018, 53(5): 594-602.
[15] 刘魏, 童永鳌, 白洁. 水稻雄配子体发育过程中tRNA片段的生物信息学分析[J]. 植物学报, 2018, 53(5): 625-633.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed   
[1] 安然, 龚吉蕊, 尤鑫, 葛之葳, 段庆伟, 晏欣. 不同龄级速生杨人工林土壤微生物数量与养分动态变化[J]. 植物生态学报, 2011, 35(4): 389 -401 .
[2] 刘敏, 孙杉, 李庆军. 两种姜科花柱卷曲性植物柱头的位置与其可授性的关系[J]. 生物多样性, 2007, 15(6): 639 -644 .
[3] 殷根深, 杨志云, 蒋镇宇, 龚洵. 基于比较核型分析方法追溯百合族 (百合科) 二型性核型的起源[J]. Plant Diversity, 2014, 36(06): 737 -746 .
[4] 蒋样明, 崔伟宏, 董前林. 基于空间技术的烤烟种植生态环境综合评价分析[J]. 植物生态学报, 2012, 36(1): 47 -54 .
[5] 郗厚诚, 孙瑶, 薛春迎. 基于ITS和matK序列的獐牙菜亚族 (龙胆科龙胆族)分子系统学[J]. Plant Diversity, 2014, 36(02): 145 -156 .
[6] . [J]. Journal of Integrative Plant Biology, 2019, 61(5): 564 -580 .
[7] 李伏生, 康绍忠. 不同氮和水分条件下CO2浓度升高对小麦碳氮比和碳磷比的影响[J]. 植物生态学报, 2002, 26(3): 295 -302 .
[8] 罗菲, 汪涯, 曾庆桂, 颜日明, 张志斌, 朱笃. 东乡野生稻根际可培养细菌多样性及其植物促生活性分析[J]. 生物多样性, 2011, 19(4): 476 -484 .
[9] 李超伦, 王敏晓, 程方平, 孙松. DNA条形码及其在海洋浮游动物生态学研究中的应用[J]. 生物多样性, 2011, 19(6): 805 -814 .
[10] Zhao Zuo-Cheng. [J]. Journal of Systematics and Evolution, 1988, 26(4): 290 -298 .