植物学报 ›› 2016, Vol. 51 ›› Issue (6): 827-840.doi: 10.11983/CBB15212

• 专题论坛 • 上一篇    下一篇

植物谷氨酸受体的研究进展

何明洁1, 孙伊辰2, 程晓园2, 时冬雪2, 李迪秦1, 陈益银3, 冯永坤2, 刘璐2, 范腾飞2, 杨超3, 曹凤秋4,,A;*, 刘来华1,2,,A;*   

  1. 1湖南农业大学农学院, 长沙 410128
    2中国农业大学资源与环境学院, 北京 100193
    3重庆烟草科学研究所, 重庆 400716
    4中国科学院上海生命科学研究院植物生理生态研究所, 中国科学院上海植物逆境生物学研究中心, 上海 200032
  • 收稿日期:2015-12-03 接受日期:2016-04-01 出版日期:2016-11-01 发布日期:2016-12-02
  • 通讯作者: 曹凤秋,刘来华
  • 作者简介:

    # 共同第一作者

  • 基金资助:
    国家自然科学基金(No;Y333ZA1D11)、高等学校博士学科点专项科研基金(No.20134320110015)和中国烟草总公司重庆市公司科技计划(No;NY20140401070017)

Current Research Advances on Glutamate Receptors (GLRs) in Plants

Mingjie He1,2†, Yichen Sun2†, Xiaoyuan Cheng2, Dongxue Shi2, Diqin Li1, Yiyin Chen3, Yongkun Feng2, Lu Liu2, Tengfei Fan2, Chao Yang3, Fengqiu Cao4*, Laihua Liu1,2*   

  1. 1College of Agriculture Sciences, Hunan Agricultural University, Changsha 410128, China
    2College of Resources and Environmental Sciences, China Agricultural University, Beijing 100193, China
    3Institute of Tobacco Research of Chongqing, Chongqing 400716, China
    4Shanghai Center for Plant Stress Biology, Institute of Plant Physiology Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200032, China
  • Received:2015-12-03 Accepted:2016-04-01 Online:2016-11-01 Published:2016-12-02
  • Contact: Cao Fengqiu,Liu Laihua
  • About author:

    # Co-first authors

摘要:

离子型谷氨酸受体(iGLuR)是哺乳动物中一类由L-氨基酸(如谷氨酸、甘氨酸)等配体门控的阳离子通道, 具有调节兴奋性神经信号传递和引导神经元发育等分子功能。1998年研究者在拟南芥(Arabidopsis thaliana)中发现了20个与iGLuRs同源的序列(即AtGLRs), 它们的功能涉及植物光信号传递、根尖分生细胞活性、花粉管生长、胞质Ca2+流以及应答多种生物和非生物环境胁迫等。该文从谷氨酸受体(GLR)的结构特征、离子通道激活与配体的关系、表达模式及可能的生物学功能等方面, 综述了近十几年来关于植物GLR和氨基酸信号的研究成果, 旨在为相关领域的同行提供有益的参考。

Abstract:

In mammals, ionotropic glutamate receptors (iGLuR) are amino acids (e.g. glutamate and glycine) -gated cation channels, and exhibit molecular functions in the regulation of excitatory neurotransmission as well as in directing neuron growth. Since 1998 twenty genes homologous to iGLuR have been identified in Arabidopsis genome (termed AtGLRs), with reported functions involved in many biological processes including light signaling, root-tip meristematic cell activity, pollen tube growth, cytosolic calcium ion flux and response to varied biotic and abiotic stresses. This paper comprehensively summarizes research achievements or advances in terms of plant glutamate receptors and amino acid (e.g. glutamate) signaling in the past more than ten years, with major issues focusing on e.g. the protein structure of GLRs, a relationship between activation of ion channels and their ligands, their gene expression patterns as well as possible biological roles in plants, thus hopefully providing valuable information for researchers related to this field.

图1

来自细菌、拟南芥和人类的谷氨酸受体同源蛋白的系统进化树氨基酸序列的对比分析采用Lasergene DNA*软件的Clustal W方法, 并使用PAUP* 4.10b软件分析生成进化树。At: Arabidopsis thaliana (拟南芥); Hs: Homo sapiens (人类); Ssp: Synechocystis sp. (单细胞蓝藻菌属, 菌株PCC6803)。AtGLR蛋白序列取自Tair, HsGLuR1-7及SspGLuR0取自NCBI数据库。基因库登录编号或基因模式所编码的可能性完整蛋白质序列名称如下: AtGLR1.1 (At3g04110)、AtGLR1.2 (At5g48400)、AtGLR1.3 (At5g48410)、AtGLR1.4 (At3g07520)、AtGLR2.1 (At5g27100)、AtGLR2.2 (At2g24720)、AtGLR2.3 (At2g24710)、AtGLR2.4 (At4g31710)、AtGLR2.5 (At5g11210)、AtGLR2.6 (At5g11180)、AtGLR2.7 (At2g29120)、AtGLR2.8 (At2g29110)、AtGLR2.9 (At2g29100)、AtGLR3.1 (At2g17260)、AtGLR3.2 (At4g35290)、AtGLR3.3 (At1g42540)、AtGLR3.4 (At1g05200)、AtGLR3.5 (At2g32390)、AtGLR3.6 (At3g51480)和AtGLR3.7 (At2g32400), HsGLuR1 (NP_000818.1)、HsGLuR2 (NP_786944.1)、HsGLuR3 (NP_015564.1)、HsGLuR4 (NP_000820.1)、HsGLuR5 (NP_000821.1)、 HsGLuR6 (CAC67487.1)和HsGLuR7 (NP_000822)以及SspGLuR0 (BAA17851.1)。"

图2

拟南芥谷氨酸受体的拓扑学结构(以GLR3.5为例)AtGLR3.5序列取自Aramemnon (http://aramemnon.uni-koeln.de/index.ep)。蛋白拓扑学结构(或疏水性)的预测使用http://www.cbs. dtu.dk/services/TMHMM/。AtGLR3.5包含3个跨膜域(M1、M3和M4)、1个嵌入脂质膜内的结构域M2及2个预测的位于胞质外侧的配体结合区S1和S2, 其碳端位于胞质内。图中的数字表示蛋白质肽链的氨基酸残基位置数。"

表1

拟南芥谷氨酸受体AtGLRs表达的时空特异性"

基因名称及
登录号
家族 苗龄 表达位点 参考文献
器官水平 组织水平 亚细胞水平
AtGLR1.1
At3g04110
I 1周 根、茎、叶 根部皮层, 托叶着生部 NR Chiu et al., 2002;
Roy et al., 2008
4周 全展叶叶沿; 根系除根尖外各组织 NR
8周 主要是根、叶; 花、角果中很微弱 花、角果中检测不到GUS信号 NR
AtGLR1.2
At5g48400
4周后 根、茎、叶、花、角果; 主要是根与角果 花粉管 NR
AtGLR1.3
At5g48410
4周 根、茎、叶, 叶中很微弱 NR NR
8周 叶和花中微弱; 主要是根与角果 NR NR
AtGLR1.4
At3g07520
4周后 根、茎、叶、花、角果 NR NR
AtGLR2.1
At5g27100
II 1周后 根、茎、叶、叶柄 根系除根尖外各组织; 托叶着生部位 NR
4周后 根系所有组织; 花药和胚珠检测到微弱且转瞬即逝的GUS信号 NR
AtGLR2.2
At2g24720
4周后 NR NR
AtGLR2.3
At2g24710
4周后 NR NR
AtGLR2.4
At4g31710
4周后 根、角果 NR NR
AtGLR2.5
At5g11210
4周后 根、茎、叶、花、角果 NR NR
AtGLR2.6
At5g11180
4周后 NR NR
AtGLR2.7
At2g29120
4周后 叶、角果, 根中微弱 NR NR
AtGLR2.8
At2g29110
4周后 根、叶柄、叶、角果 NR NR Chiu et al., 2002
Roy et al., 2008
AtGLR2.9
At2g29100
4周 根、叶、茎、叶柄 NR NR
8周 NR NR
AtGLR3.1
At2g17260
III 5天后 根、茎、叶、叶柄 所有维管组织; 保卫细胞 NR Cho et al., 2009
Kim et al., 2001;
Kong et al., 2015;
Meyerhoff et al., 2005
Turano et al., 2002
Teardo et al., 2011
Teardo et al., 2015
8周 根、茎、叶、花、角果 花丝和花药连接部位强烈表达 NR
AtGLR3.2
At4g35290
7天后 根、茎、叶柄、叶 所有维管组织及其邻近的导管, 随着植物生长表达更强烈; 根系韧皮部细胞中表达量远高于邻近细胞, 原生韧皮部更为强烈 NR
8周 根、茎、叶、花、角果, 主要是叶与角果 花、茎维管组织; 花芽; 胚珠, 尤其是外皮层和生长中心 NR
AtGLR3.3
At1g42540
4周后 根、茎、叶柄、叶、角果 NR
AtGLR3.4
At1g05200
4周后 根、茎、叶、花、角果, 莲座叶中最强 叶肉组织; 维管束; 保卫细胞, 排水孔; 根内外皮层, 根毛 细胞质膜, 叶绿体内膜
AtGLR3.5
At2g32390
0 种子发芽时强烈, 随发芽完成降低 胚胎与子叶中强烈表达 线粒体内膜; 叶绿体膜
4周后 根、茎、叶、花、角果 NR
AtGLR3.7
At2g32400
整个生长阶段 所有器官 所有组织 细胞质膜
[1] Aouini A, Matsukura C, Ezura H, Asamizu E (2012). Characterization of 13 glutamate receptor-like genes encoded in the tomato genome by structure phylogeny and expression profiles.Gene 493, 36-43.
[2] Ayalon G, Segev E, Elgavish S, Stern-Bach Y (2005). Two regions in the N-terminal domain of ionotropic glutamate receptor 3 form the subunit oligomerization interfaces that control subtype-specific receptor assembly.J Biol Chem 280, 15053-15060.
[3] Ayalon G, Stern-Bach Y (2001). Functional assembly of AMPA and kainate receptors is mediated by several discrete protein-protein interactions.Neuron 31, 103-113.
[4] Brenner ED, Martinez-Barboza N, Clark AP, Liang QS, Stevenson DW, Coruzzi GM (2000). Arabidopsis mutants resistant to S(+)-β-methyl-α, β-diaminopropionic acid, a cycad-derived glutamate receptor agonist.Plant Physiol 124, 1615-1624.
[5] Chávez AE, Singer JH, Diamond JS (2006). Fast neuro- transmitter release triggered by Ca2+ influx through AMPA- type glutamate receptors.Nature 443, 705-708.
[6] Chen GQ, Cui CH, Mayer ML, Gouaux E (1999). Functional characterization of a potassium-selective prokaryotic glu- tamate receptor.Nature 402, 817-821.
[7] Chiu JC, Brenner ED, Desalle R, Nitabach MN, Holmes TC, Coruzzi GM (2002). Phylogenetic and expression analysis of the glutamate-receptor-like gene family in Arabidopsis thaliana.Mol Biol Evol 19, 1066-1082.
[8] Chiu JC, Desalle R, Lam HM, Meisel L, Coruzzi G (1999). Molecular evolution of glutamate receptors: a primitive signaling mechanism that existed before plants and animals diverged.Mol Biol Evol 16, 826-838.
[9] Cho D, Kim SA, Murata Y, Lee S, Jae SK, Nam HG, Kwak JM (2009). De-regulated expression of the plant gluta- mate receptor homolog AtGLR3.1 impairs long-term Ca2+ programmed stomatal closure.Plant J 58, 437-449.
[10] Davenport R (2002). Glutamate receptors in plants.Ann Bot 90, 549-557.
[11] Dennison KL, Spalding EP (2000). Glutamate-gated calci- um fluxes in Arabidopsis.Plant Physiol 124, 1511-1514.
[12] Dingledine R, Borges K, Bowie D, Traynelis SF (1999). The glutamate receptor ion channels. Pharmacol Rev 51, 7-61.
[13] Dubos C, Huggins D, Grant GH, Knight MR, Campbell MM (2003). A role for glycine in the gating of plant NMDA- like receptors.Plant J 35, 800-810.
[14] Dubos C, Willment J, Huggins D, Grant GH, Campbell MM (2005). Kanamycin reveals the role played by glutamate receptors in shaping plant resource allocation.Plant J 43, 348-355.
[15] Forde BG, Cutler SR, Zaman N, Krysan PJ (2013). Gluta- mate signaling via a MEKK1 kinase-dependent pathway induces changes in Arabidopsis root architecture.Plant J 75, 1-10.
[16] Kang J, Sohum M, Turano FJ (2004). The putative glutamate receptor 1.1 (AtGLR1.1) in Arabidopsis thaliana regulates abscisic acid biosynthesis and signaling to control development and water loss.Plant Cell Physiol 45, 1380-1389.
[17] Kang J, Turano FJ (2003). The putative glutamate receptor 1.1 (AtGLR1.1) functions as a regulator of carbon and nitrogen metabolism in Arabidopsis thaliana.Proc Natl Acad Sci USA 100, 6872-6877.
[18] Kang S, Kim HB, Lee H, Choi JY, Heu S, Oh CJ, Kwon SI, An CS (2006). Overexpression in Arabidopsis of a plasma membrane-targeting glutamate receptor from small radish increases glutamate-mediated Ca2+ influx and delays fun- gal infection.Mol Cell 21, 418-427.
[19] Kim SA, Kwak JM, Jae SK, Wang MH, Nam HG (2001). Overexpression of the AtGluR2 gene encoding an Arabi- dopsis homolog of mammalian glutamate receptors impairs calcium utilization and sensitivity to ionic stress in transgenic plants.Plant Cell Physiol 42, 74-84.
[20] Kong DD, Ju CL, Parihar A, Kim S, Cho D, Kwak JM (2015). Arabidopsis glutamate receptor homolog atglr3.5 modulates cytosolic Ca2+ level to counteract effect of abscisic acid in seed germination.Plant Physiol 167, 1630-1642.
[21] Kushwaha R, Singh A, Chattopadhyay S (2008). Calmo- dulin7 plays an important role as transcriptional regulator in Arabidopsis seedling development.Plant Cell 20, 1747-1759.
[22] Lacombe B (2001). The identity of plant glutamate recap- tors.Science 292, 1486-1487.
[23] Lam H, Chiu J, Hsieh M, Lee M, Oliveira IC, Shin M, Coruzzi G (1998). Glutamate-receptor genes in plants.Nature 396, 125-126.
[24] Li HJ, Yang WC (2012). Emerging role of ER quality control in plant cell signal perception.Protein Cell 3, 10-16.
[25] Li J, Zhu SH, Song XW, Shen Y, Chen HM, Yu J, Yi K, Liu YF, Karplus VJ, Wu P, Deng XW (2006). A rice glutamate receptor-like gene is critical for the division and survival of individual cells in the root apical meristem.Plant Cell 18, 340-349.
[26] Manzoor H, Kelloniemi J, Chiltz A, Wendehenne D, Pugin A, Poinssot B, Garcia-Brugger A (2013). Involvement of the glutamate receptor AtGLR3.3 in plant defense sig- naling and resistance to Hyaloperonospora arabidopsidis.Plant J 76, 466-480.
[27] McFeeters RL, Oswald RE (2004). Emerging structural explanations of ionotropic glutamate receptor function.FASEB J 18, 428-438.
[28] Meyerhoff O, Müller K, Roelfsema MR, Latz A, Lacombe B, Hedrich R, Dietrich P, Becker D (2005). AtGLR3.4, a glutamate receptor channel-like gene is sensitive to touch and cold.Planta 222, 418-427.
[29] Michard E, Lima PT, Borges F, Silva AC, Portes MT, Carvalho JE, Gilliham MG, Liu LH, Obermeyer G, Feijó J (2011). Glutamate receptor-like genes form Ca2+ chan- nels in pollen tubes and are regulated by pistil D-serine.Science 332, 434-437.
[30] Mousavi SAR, Chauvin A, Pascaud F, Kellenberger S, Farmer EE (2013). GLUTAMATE RECEPTOR-LIKE ge- nes mediate leaf-to-leaf wound signaling.Nature 500, 422-441.
[31] Nagata T, Iizumi S, Satoh K, Ooka H, Kawai J, Carninci P, Hayashizaki Y, Otomo Y, Murakami K, Matsubara K, Kikuchi S (2004). Comparative analysis of plant and animal calcium signal transduction element using plant full-length cDNA data.Mol Biol Evol 21, 1855-1870.
[32] Parsons CG, Panchenko VA, Pinchenko VO, Tsyndreko AY, Krishtal OA (1966). Comparative patch-clamp stud- ies with freshly dissociated rat hippocampal and striatal neurons on the NMDA receptor antagonistic effects of amantadine and memantin.Eur J Neurosci 8, 446-454.
[33] Penn AC, Williams SR, Greger IH (2008). Gating motions underlie AMPA receptor secretion from the endoplasmic reticulum.EMBO J 27, 3056-3068.
[34] Price MB, Jelesko J, Okumoto S (2013). Glutamate receptor homologs in plants: functions and evolutionary origins.Front Plant Sci 3, 1-10.
[35] Price MB, Kong DD, Okumoto S (2013). Inter-subunit in- teractions between glutamate-like receptors in Arabi- dopsis.Plant Signal Behav 8, e27034.
[36] Qi Z, Stephens NR, Spalding EP (2006). Calcium entry me- diated by glr3.3, an Arabidopsis glutamate receptor with a broad agonist profile.Plant Physiol 142, 963-971.
[37] Roy SJ, Gilliham M, Berger B, Essah PA, Cheffings C, Miller AJ, Davenport RJ, Liu LH, Skynner MJ, Davies JM, Richardson P, Leigh RA, Tester M (2008). Investi- gating glutamate receptor-like gene co-expression in Ara- bidopsis thaliana.Plant Cell Environ 31, 861-871.
[38] Singh A, Kanwar P, Yadav AK, Mishra M, Jha SK, Baranwal V, Pandey A, Kappor S, Tyagi AK, Pandey GK (2014). Genome-wide expressional and functional analysis of calcium transport elements during abiotic stress and development in rice.FEBS J 281, 894-915.
[39] Sivaguru M, Pike S, Gassmann W, Baskin TI (2003). Aluminum rapidly depolymerized cortical microtubules and depolarizes the plasma membrane: evidence that these responses are mediated by a glutamate receptor.Plant Cell Physiol 44, 667-675.
[40] Sobolevsky AI, Rosconi MP, Gouaux E (2009). X-ray structure, symmetry and mechanism of an AMPA-subtype glutamate receptor.Nature 462, 745-756.
[41] Stephens NR, Qi Z, Spalding EP (2008). Glutamate re- ceptor subtypes evidenced by differences in desensitiza- tion and dependence on the GLR3.3 and GLR3.4 genes.Plant Physiol 146, 529-538.
[42] Tapken D, Anschütz U, Liu LH, Huelsken T, Seebohm G, Becker D, Hollmann M (2013). A plant homolog of animal glutamate receptors is an ion channel gated by multiple hydrophobic amino acids.Sci Signal 6, a47.
[43] Tapken D, Hollmann M (2008). Arabidopsis thaliana gluta- mate receptor ion channel function demonstrated by ion pore transplantation.J Mol Biol 383, 36-48.
[44] Teardo E, Carraretto L, Bortoli SD, Costa A, Behera S, Wagner R, Schiavo FL, Formentin E, Szabo I (2015). Alternative splicing-mediated targeting of the Arabidopsis GLUTAMATE RECEPTOR3.5 to mitochondria affects or- ganelle morphology1.Plant Physiol 167, 216-227.
[45] Teardo E, Formentin E, Segalla A, Giacometti GM, Marin O, Zanetti MA, Schiavo FL, Zoratti M, Szabò I (2011). Dual localization of plant glutamate receptor AtGLR3.4 to plastids and plasmamembrane.Biochim Biophys Acta 1807, 359-367.
[46] Teardo E, Segalla A, Formentin E, Zanetti M, Marin O, Giacometti GM, Schiavo FL, Zoratti M, Szabò I (2010). Characterization of a plant glutamate receptor activity.Cell Physiol Biochem 26, 253-262.
[47] Traynelis SF, Wollmuth LP, McBain CJ, Menniti FS, Vance KM, Ogden KK, Hansen KB, Yuan HJ, Myers SJ, Dingledine R (2010). Glutamate receptor ion chan- nels: structure, regulation, and function.Pharmacol Rev 62, 405-496.
[48] Turano FJ, Muhitch MJ, Felker FC, McMahon MB (2002). The putative glutamate receptor 3.2 from Arabidopsis thaliana (AtGLR3.2) is an integral membrane peptide that accumulates in rapidly growing tissues and persists in vascular-associated tissues.Plant Sci 163, 43-51.
[49] Turano FJ, Panta GR, Allard MW, Berkum PV (2001). The putative glutamate receptors from plants are related to two superfamilies of animal neurotransmitter receptors via distinct evolutionary mechanisms.Mol Biol Evol 18, 1417-1420.
[50] Ulbrich MH, Isacoff EY (2008). Rules of engagement for NMDA receptor subunits.Proc Natl Acad Sci USA 105, 14163-14168.
[51] Vatsa P, Chiltz A, Bourque S, Wendehenne D, Garcia- Brugger A, Pugin A (2011). Involvement of putative glutamate receptors in plant defence signaling and NO production.Biochimie 93, 2095-2101.
[52] Vincill ED, Bieck AM, Spalding EP (2012). Ca2+ conduction by an amino acid-gated ion channel related to glutamate receptors.Plant Physiol 159, 40-46.
[53] Vincill ED, Clarin AE, Molenda JN, Spalding EP (2013). Interacting glutamate receptor-like proteins in phloem re- gulate lateral root initiation in Arabidopsis.Plant Cell 25, 1304-1313.
[54] Walch-Liu P, Forde BG (2008). Nitrate signaling mediated by the NRT1.1 nitrate transporter antagonises L-gluta- mate-induced changes in root architecture.Plant J 54, 820-828.
[55] Walch-Liu P,Liu LH, Remans T, Tester M, Forde BG (2006). Evidence that L-glutamate can act as an exoge- nous signal to modulate root growth and branching in Arabidopsis thaliana.Plant Cell Physiol 47, 1045-1057.
No related articles found!
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed   
[1] 陈馥衡 范浚深. 新型切花保鲜剂氨氧基乙酸[J]. 植物学报, 1988, 5(02): 127 .
[2] 周广胜 邢雪荣 王辉民. 植被在全球气候变化中的作用[J]. 植物学报, 1995, 12(专辑2): 190 -194 .
[3] 周青 杨静 邵爱华 王雅玲. NaHSO3 对水稻幼苗根系生长及生理活性影响的研究[J]. 植物学报, 1998, 15(03): 51 -53 .
[4] 韩燕来 徐芳森 段海燕 石磊 王运华. 拟南芥养分离子转运蛋白研究进展[J]. 植物学报, 2003, 20(01): 23 -35 .
[5] 吴杰, 赵鑫, 宁伟. 东北地区蒲公英属瘦果微形态特征及其分类学意义[J]. 植物学报, 2011, 46(4): 437 -446 .
[6] 董淼, 黄越, 陈文铎, 徐涛, 郎秋蕾. 降解组测序技术在植物miRNA研究中的应用[J]. 植物学报, 2013, 48(3): 344 -353 .
[7] 种云霄, 于丹, 夏盛林, 康辉. 秦岭太白县水生—沼生植物区系地理的初步研究[J]. 植物生态学报, 1999, 23(199901): 28 -38 .
[8] 刘锺龄. 内蒙古的针茅草原[J]. 植物生态学报, 1963, (2): 156 -157 .
[9] 王琼, 廖咏梅. 林缘和荒草坡不同草本层盖度小生境中积雪草的等级可塑性[J]. 植物生态学报, 2007, 31(4): 576 -587 .
[10] 胡肄慧, 陈灵芝, 陈清郎, 孔繁志, 缪有贵. 几种树木枯叶分解速率的试验研究[J]. 植物生态学报, 1987, 11(2): 124 -132 .