水稻独脚金内酯信号感知的激活和终止

doi:10.11983/CBB24163

植物学报 ›› 2024, Vol. 59 ›› Issue (6): 873-877.DOI: 10.11983/CBB24163 cstr: 32102.14.CBB24163

水稻独脚金内酯信号感知的激活和终止

姚瑞枫¹^,^*(), 谢道昕²^,^*()

¹湖南大学生物学院, 化学生物传感与计量学国家重点实验室, 植物功能基因组学与发育调控湖南省重点实验室, 长沙 410082
²清华大学生命科学学院, 生物信息学教育部重点实验室, 清华-北大生命科学联合中心, 北京 100084

收稿日期:2024-10-28 接受日期:2024-11-02 出版日期:2024-11-10 发布日期:2024-11-04
通讯作者: *谢道昕, 清华大学教授, 中国科学院院士。现任清华大学学术委员会副主任, 学风道德建设委员会主任, 科技伦理委员会主任, 中国植物学会副理事长, 国际种业科学家联合体副主席, 中国进出境生物安全研究会副会长, 国家农业生物安全委员会副主任。长期致力于植物激素研究, 阐明了植物分枝激素独脚金内酯和植物抗性激素茉莉素的受体感知机制, 揭示了茉莉素调控植物抗性和育性的信号转导机制。E-mail: daoxinlab@tsinghua.edu.cn;
姚瑞枫, 湖南大学教授, 博士生导师, 教育部“青年长江学者”, 国家重点研发“青年首席”。主要从事植物激素作用机理和生物育种研究, 在新型激素独脚金内酯的感知和信号转导机制方面做出了一定的学术贡献, 相关成果以通讯作者或第一作者发表在Nature、Nat Comm、Plant Cell、Mol Plant和Cell Res等期刊。其中“植物分枝激素独脚金内酯的受体感知机制”曾入选中国生命科学十大进展、中国高等学校十大科技进展。兼任中国蛋白质组学专委会委员、中国植物学会植物整合组学专委会委员, 作为秘书长参与组织了第3届国际独脚金内酯大会。E-mail: ryao@hnu.edu.cn
基金资助:
国家重点研发计划青年科学家项目(2022YFF1002000)

Activation and Termination of Strigolactone Signal Perception in Rice

Ruifeng Yao¹^,^*(), Daoxin Xie²^,^*()

¹Hunan Provincial Key Laboratory of Plant Functional Genomics and Developmental Regulation, State Key Laboratory of Chemo/Biosensing and Chemometrics, College of Biology, Hunan University, Changsha 410082, China
²MOE Key Laboratory of Bioinformatics, Tsinghua-Peking Joint Center for Life Sciences, School of Life Sciences, Tsinghua University, Beijing 100084, China

Received:2024-10-28 Accepted:2024-11-02 Online:2024-11-10 Published:2024-11-04
Contact: *E-mail: daoxinlab@tsinghua.edu.cn;ryao@hnu.edu.cn

摘要/Abstract

摘要： 独脚金内酯(strigolactone, SL)是调控植物分枝等重要生长发育过程的新型植物激素。水稻(Oryza sativa)中SL受体D14感知SL信号, 结合F-box蛋白D3并招募转录抑制子D53, 诱导D53泛素化降解, 从而触发信号传递、抑制分蘖。最近的一项研究发现, 低氮信号诱导D14的N端无序区(NTD)特异位点发生磷酸化修饰, 造成D14的泛素化降解减弱, 从而增强SL信号通路。此外, 低氮信号本身可以诱导SL合成, 通过这两种机制的协同作用强化SL信号转导, 从而强烈抑制分蘖, 使水稻适应低氮逆境。该研究还发现, SL诱导的D14-D3相互作用也促进了D14的泛素化降解, 从而介导SL信号感知的终止。这些重要发现阐明了水稻中SL信号感知的激活和终止机制, 揭示了SL信号在控制水稻分蘖以适应低氮逆境中的重要作用, 为理解植物如何适应营养匮乏等外界环境变化提供了新的重要见解, 对作物株型的精准改良以及减肥增产水稻分子设计育种具有重要指导意义。

关键词: 水稻, 独脚金内酯, 受体D14, 低氮信号, 磷酸化, 泛素化

Abstract: Strigolactone (SL) is a novel plant hormone that regulates important growth and developmental processes such as plant branching. In rice, the SL receptor D14 perceives SL signals, binds with the F-box protein D3, and recruits the transcriptional repressor D53, inducing the ubiquitination and degradation of D53, thereby triggering signal transduction and inhibiting tillering. A recent study discovered that nitrogen limitation induces SL biosynthesis in rice to activate the receptor D14, triggering SL signal transduction. Concurrently, nitrogen limitation also induces phosphorylation of the N-terminal disordered region (NTD) of D14, reducing the ubiquitination and degradation of receptor D14, thereby further enhancing SL perception. Through these two synergistic mechanisms, nitrogen limitation stimulates SL signal transduction, strongly inhibiting tillering and enabling rice to adapt to low nitrogen stress conditions. The study also found that the D14-D3 interaction induced by SL promotes the ubiquitination and degradation of D14, thereby mediating the termination of SL signal perception. These significant findings elucidate the mechanisms of activation and termination of SL perception in rice, revealing the crucial regulatory role of SL signals in controlling rice tillering under low nitrogen stress. This would provide key insights into plant adaptation to nutrient scarcity and guide the precise improvement of crop architecture and molecular breeding of rice for reduced fertilizer use and increased yield.

Key words: rice, strigolactone, receptor D14, nitrogen limitation, phosphorylation, ubiquitination

姚瑞枫, 谢道昕. 水稻独脚金内酯信号感知的激活和终止. 植物学报, 2024, 59(6): 873-877.

Ruifeng Yao, Daoxin Xie. Activation and Termination of Strigolactone Signal Perception in Rice. Chinese Bulletin of Botany, 2024, 59(6): 873-877.

导出引用管理器 EndNote|Ris|BibTeX

链接本文: https://www.chinbullbotany.com/CN/10.11983/CBB24163

https://www.chinbullbotany.com/CN/Y2024/V59/I6/873

图/表 1

图1 水稻中独脚金内酯信号感知的激活和终止模型水稻在氮素缺乏时诱导独脚金内酯(SL)的生物合成, SL结合并诱导受体D14发生口袋从“开放”到“闭合”的构象变化, 与F-box蛋白D3及转录抑制子D53形成复合体, 促进D53的泛素化降解, 从而激活SL信号转导; 同时, 低氮信号还诱导D14的N端无序区(NTD)发生磷酸化, 减弱受体D14的泛素化降解, 进一步增强SL信号感知。低氮信号通过这两种机制的协同作用, 确保SL信号转导激活, 抑制水稻分蘖。SL触发的D14-D3相互作用也促进了D14的泛素化降解, 从而介导SL信号转导终止。

Figure 1 Model of activation and termination of strigolactone perception in rice Under nitrogen deficiency, rice induces the biosynthesis of strigolactone (SL), which binds to and induces a conformational change in the receptor D14 from an "open" to a "closed" pocket. This forms a complex with the F-box protein D3 and the transcriptional repressor D53, promoting the ubiquitination and degradation of D53, thereby activating SL signal transduction. Concurrently, nitrogen limitation induces phosphorylation of the N-terminal disordered region (NTD) of D14, reducing its ubiquitination and degradation, and further enhancing SL perception. Through these two synergistic mechanisms, low nitrogen signaling ensures the activation of SL signal transduction, inhibiting rice tillering. The SL-triggered D14-D3 interaction also promotes the ubiquitination and degradation of D14, thus mediating the termination of SL signal transduction.

参考文献 19

[1]	Chen JM, Shukla D (2023). Effect of histidine covalent modification on strigolactone receptor activation and selectivity. Biophys J 122, 1219-1228. DOI PMID
[2]	Chevalier F, Nieminen K, Sánchez-Ferrero JC, Rodríguez ML, Chagoyen M, Hardtke CS, Cubas P (2014). Strigolactone promotes degradation of DWARF14, an α/β hydrolase essential for strigolactone signaling in Arabidopsis. Plant Cell 26, 1134-1150.
[3]	de Saint Germain A, Clavé G, Badet-Denisot MA, Pillot JP, Cornu D, Le Caer JP, Burger M, Pelissier F, Retailleau P, Turnbull C, Bonhomme S, Chory J, Rameau C, Boyer FD (2016). An histidine covalent receptor and butenolide complex mediates strigolactone perception. Nat Chem Biol 12, 787-794. DOI PMID
[4]	Gomez-Roldan V, Fermas S, Brewer PB, Puech-Pagès V, Dun EA, Pillot JP, Letisse F, Matusova R, Danoun S, Portais JC, Bouwmeester H, Bécard G, Beveridge CA, Rameau C, Rochange SF (2008). Strigolactone inhibition of shoot branching. Nature 455, 189-194.
[5]	Hu QL, He YJ, Wang L, Liu SM, Meng XB, Liu GF, Jing YH, Chen MJ, Song XG, Jiang L, Yu H, Wang B, Li JY (2017). DWARF14, a receptor covalently linked with the active form of strigolactones, undergoes strigolactone- dependent degradation in rice. Front Plant Sci 8, 1935.
[6]	Hu QL, Liu HH, He YJ, Hao YR, Yan JJ, Liu SM, Huang XH, Yan ZY, Zhang DH, Ban XW, Zhang H, Li QQ, Zhang JK, Xin PY, Jing YH, Kou LQ, Sang DJ, Wang YH, Wang YC, Meng XB, Fu XD, Chu JF, Wang B, Li JY (2024). Regulatory mechanisms of strigolactone perception in rice. Cell https://doi.org/10.1016/j.cell.2024.10.009.
[7]	Jiang L, Liu X, Xiong GS, Liu HH, Chen FL, Wang L, Meng XB, Liu GF, Yu H, Yuan YD, Yi W, Zhao LH, Ma HL, He YZ, Wu ZS, Melcher K, Qian Q, Xu H E, Wang YH, Li JY (2013). DWARF 53 acts as a repressor of strigolactone signaling in rice. Nature 504, 401-405.
[8]	Shabek N, Ticchiarelli F, Mao HB, Hinds TR, Leyser O, Zheng N (2018). Structural plasticity of D3-D14 ubiquitin ligase in strigolactone signaling. Nature 563, 652-656.
[9]	Umehara M, Hanada A, Yoshida S, Akiyama K, Arite T, Takeda-Kamiya N, Magome H, Kamiya Y, Shirasu K, Yoneyama K, Kyozuka J, Yamaguchi S (2008). Inhibition of shoot branching by new terpenoid plant hormones. Nature 455, 195-200.
[10]	Uraguchi D, Kuwata K, Hijikata Y, Yamaguchi R, Imaizumi H, Am S, Rakers C, Mori N, Akiyama K, Irle S, McCourt P, Kinoshita T, Ooi T, Tsuchiya Y (2018). A femtomolar-range suicide germination stimulant for the parasitic plant Striga hermonthica. Science 362, 1301-1305. DOI PMID
[11]	Wang B, Smith SM, Li JY (2018). Genetic regulation of shoot architecture. Annu Rev Plant Biol 69, 437-468. DOI PMID
[12]	Wang DW, Pang ZL, Yu HY, Thiombiano B, Walmsley A, Yu SY, Zhang YY, Wei T, Liang L, Wang J, Wen X, Bouwmeester HJ, Yao RF, Xi Z (2022). Probing strigolactone perception mechanisms with rationally designed small-molecule agonists stimulating germination of root parasitic weeds. Nat Commun 13, 3987. DOI PMID
[13]	Wang L, Wang B, Yu H, Guo HY, Lin T, Kou LQ, Wang AQ, Shao N, Ma HY, Xiong GS, Li XQ, Yang J, Chu JF, Li JY (2020a). Transcriptional regulation of strigolactone signaling in Arabidopsis. Nature 583, 277-281.
[14]	Wang YX, Shang LG, Yu H, Zeng LJ, Hu J, Ni S, Rao YC, Li SF, Chu JF, Meng XB, Wang L, Hu P, Yan JJ, Kang SJ, Qu MH, Lin H, Wang T, Wang Q, Hu XM, Chen HQ, Wang B, Gao ZY, Guo LB, Zeng DL, Zhu XD, Xiong GS, Li JY, Qian Q (2020b). A strigolactone biosynthesis gene contributed to the Green Revolution in rice. Mol Plant 13, 923-932.
[15]	Yao RF, Ming ZH, Yan LM, Li SH, Wang F, Ma S, Yu CT, Yang M, Chen L, Chen LH, Li YW, Yan C, Miao D, Sun ZY, Yan JB, Sun YN, Wang L, Chu JF, Fan SL, He W, Deng HT, Nan FJ, Li JY, Rao ZH, Lou ZY, Xie DX (2016). DWARF14 is a non-canonical hormone receptor for strigolactone. Nature 536, 469-473.
[16]	Yao RF, Wang L, Li YW, Chen L, Li SH, Du XX, Wang B, Yan JB, Li JY, Xie DX (2018). Rice DWARF14 acts as an unconventional hormone receptor for strigolactone. J Exp Bot 69, 2355-2365. DOI PMID
[17]	Yu HQ, Matouschek A (2017). Recognition of client proteins by the proteasome. Annu Rev Biophys 46, 149-173. DOI PMID
[18]	Yuan K, Zhang H, Yu CJ, Luo N, Yan JJ, Zheng S, Hu QL, Zhang DH, Kou LQ, Meng XB, Jing YH, Chen MJ, Ban XW, Yan ZY, Lu ZF, Wu J, Zhao Y, Liang Y, Wang YH, Xiong GS, Chu JF, Wang ET, Li JY, Wang B (2023). Low phosphorus promotes NSP1-NSP2 heterodimerization to enhance strigolactone biosynthesis and regulate shoot and root architecture in rice. Mol Plant 16, 1811-1831. DOI PMID
[19]	Zhou F, Lin QB, Zhu LH, Ren YL, Zhou KN, Shabek N, Wu FQ, Mao HB, Dong W, Gan L, Ma WW, Gao H, Chen J, Yang C, Wang D, Tan JJ, Zhang X, Guo XP, Wang JL, Jiang L, Liu X, Chen WQ, Chu JF, Yan CY, Ueno K, Ito S, Asami T, Cheng ZJ, Wang J, Lei CL, Zhai HQ, Wu CY, Wang HY, Zheng N, Wan JM (2013). D14-SCF (D3)-dependent degradation of D53 regulates strigolactone signaling. Nature 504, 406-410.

水稻独脚金内酯信号感知的激活和终止

Activation and Termination of Strigolactone Signal Perception in Rice

RichHTML

PDF (PC)

可视化

摘要/Abstract

引用本文

使用本文

图/表 1

参考文献 19

相关文章 15

编辑推荐

Metrics

本文评价

[1]	李建国, 张怡, 张文君. 水稻根系铁膜形成及对磷素吸收的影响[J]. 植物学报, 2025, 60(1): 1-10.
[2]	连锦瑾, 唐璐瑶, 张伊诺, 郑佳兴, 朱超宇, 叶语涵, 王跃星, 商文楠, 傅正浩, 徐昕璇, 吴日成, 路梅, 王长春, 饶玉春. 水稻抗氧化性状遗传位点挖掘及候选基因分析[J]. 植物学报, 2024, 59(5): 738-751.
[3]	黄佳慧, 杨惠敏, 陈欣雨, 朱超宇, 江亚楠, 胡程翔, 连锦瑾, 芦涛, 路梅, 张维林, 饶玉春. 水稻突变体pe-1对弱光胁迫的响应机制[J]. 植物学报, 2024, 59(4): 574-584.
[4]	周俭民. 收放自如的明星战车[J]. 植物学报, 2024, 59(3): 343-346.
[5]	朱超宇, 胡程翔, 朱哲楠, 张芷宁, 汪理海, 陈钧, 李三峰, 连锦瑾, 唐璐瑶, 钟芊芊, 殷文晶, 王跃星, 饶玉春. 水稻穗部性状QTL定位及候选基因分析[J]. 植物学报, 2024, 59(2): 217-230.
[6]	夏婧, 饶玉春, 曹丹芸, 王逸, 柳林昕, 徐雅婷, 牟望舒, 薛大伟. 水稻中乙烯生物合成关键酶OsACS和OsACO调控机制研究进展[J]. 植物学报, 2024, 59(2): 291-301.
[7]	方妍力, 田传玉, 苏如意, 刘亚培, 王春连, 陈析丰, 郭威, 纪志远. 水稻抗细菌性条斑病基因挖掘与初定位[J]. 植物学报, 2024, 59(1): 1-9.
[8]	朱宝, 赵江哲, 张可伟, 黄鹏. 水稻细胞分裂素氧化酶9参与调控水稻叶夹角发育[J]. 植物学报, 2024, 59(1): 10-21.
[9]	贾绮玮, 钟芊芊, 顾育嘉, 陆天麒, 李玮, 杨帅, 朱超宇, 胡程翔, 李三峰, 王跃星, 饶玉春. 水稻茎秆细胞壁相关组分含量QTL定位及候选基因分析[J]. 植物学报, 2023, 58(6): 882-892.
[10]	王文广, 王永红. 百年假说终获解析: 穿梭的LAZY蛋白“唤醒”植物对重力的感应[J]. 植物学报, 2023, 58(5): 677-681.
[11]	戴若惠, 钱心妤, 孙静蕾, 芦涛, 贾绮玮, 陆天麒, 路梅, 饶玉春. 水稻叶色调控机制及相关基因研究进展[J]. 植物学报, 2023, 58(5): 799-812.
[12]	田传玉, 方妍力, 沈晴, 王宏杰, 陈析丰, 郭威, 赵开军, 王春连, 纪志远. 2019-2021年我国南方稻区白叶枯病菌的毒力与遗传多样性调查研究[J]. 植物学报, 2023, 58(5): 743-749.
[13]	孙尚, 胡颖颖, 韩阳朔, 薛超, 龚志云. 水稻染色体双链寡核苷酸荧光原位杂交技术[J]. 植物学报, 2023, 58(3): 433-439.
[14]	刘裕强, 万建民. 寄主监控昆虫唾液蛋白平衡植物抗性与生长发育[J]. 植物学报, 2023, 58(3): 353-355.
[15]	金佳怡, 罗怿婷, 杨惠敏, 芦涛, 叶涵斐, 谢继毅, 王珂欣, 陈芊羽, 方媛, 王跃星, 饶玉春. 水稻叶绿素含量QTL定位与候选基因表达分析[J]. 植物学报, 2023, 58(3): 394-403.