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Annual Review of Plant Biology

Volume 74, 2023

Merging Signaling with Structure: Functions and Mechanisms of Plant Glutamate Receptor Ion Channels

Abstract

Plant glutamate receptor-like (GLR) genes encode ion channels with demonstrated roles in electrical and calcium (Ca2+) signaling. The expansion of the GLR family along the lineage of land plants, culminating in the appearance of a multiclade system among flowering plants, has been a topic of interest since their discovery nearly 25 years ago. GLRs are involved in many physiological processes, from wound signaling to transcriptional regulation to sexual reproduction. Emerging evidence supports the notion that their fundamental functions are conserved among different groups of plants as well. In this review, we update the physiological and genetic evidence for GLRs, establishing their role in signaling and cell–cell communication. Special emphasis is given to the recent discussion of GLRs’ atomic structures. Along with functional assays, a structural view of GLRs’ molecular organization presents a window for novel hypotheses regarding the molecular mechanisms underpinning signaling associated with the ionic fluxes that GLRs regulate. Newly uncovered transcriptional regulations associated with GLRs—which propose the involvement of genes from all clades of in ways not previously observed—are discussed in the context of the broader impacts of GLR activity. We posit that the functions of GLRs in plant biology are probably much broader than anticipated, but describing their widespread involvement will only be possible with () a comprehensive understanding of the channel's properties at the molecular and structural levels, including protein–protein interactions, and () the design of new genetic approaches to explore stress and pathogen responses where precise transcriptional control may result in more precise testable hypotheses to overcome their apparent functional redundancies.

Keyword(s): action potential, amino acid signaling, calcium signaling, calcium transport, cell–cell communication, electric signaling, excitability, GLR, glutathione, ion channels, plant glutamate receptor
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/content/journals/10.1146/annurev-arplant-070522-033255
2023-05-22
2024-04-29
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Literature Cited

  1. 1.
    Acher FC, Bertrand HO. 2005. Amino acid recognition by Venus flytrap domains is encoded in an 8-residue motif. Biopolymers 80:357–66
     [Google Scholar]
  2. 2.
    Alfieri A, Doccula FG, Pederzoli R, Grenzi M, Bonza MC et al. 2020. The structural bases for agonist diversity in an Arabidopsis thaliana glutamate receptor-like channel. PNAS 117:752–60First structural determination of GLR LBDs bound to amino acids.
     [Google Scholar]
  3. 3.
    Amin JB, Leng X, Gochman A, Zhou H-X, Wollmuth LP. 2018. A conserved glycine harboring disease-associated mutations permits NMDA receptor slow deactivation and high Ca2+ permeability. Nat. Commun. 9:3748
     [Google Scholar]
  4. 4.
    Aouini A, Matsukura C, Ezura H, Asamizu E. 2012. Characterisation of 13 glutamate receptor-like genes encoded in the tomato genome by structure, phylogeny and expression profiles. Gene 493:36–43
     [Google Scholar]
  5. 5.
    Barbier-Brygoo H, Vinauger M, Colcombet J, Ephritikhine G, Frachisse JM, Maurel C. 2000. Anion channels in higher plants: functional characterization, molecular structure and physiological role. Biochim. Biophys. Acta Biomembr. 1465:199–218
     [Google Scholar]
  6. 6.
    Beilby MJ. 2007. Action potential in charophytes. Int. Rev. Cytol. 257:43–82
     [Google Scholar]
  7. 7.
    Bjornson M, Pimprikar P, Nurnberger T, Zipfel C. 2021. The transcriptional landscape of Arabidopsis thaliana pattern-triggered immunity. Nat. Plants 7:579–86Transcriptomic analysis reporting core immunity genes including breakthrough characterization of clade 2 GLRs (GLR2.7, GLR2.8, GLR2.9).
     [Google Scholar]
  8. 8.
    Brenner ED, Martinez-Barboza N, Clark AP, Liang QS, Stevenson DW, Coruzzi G. 2000. Arabidopsis mutants resistant to S(+)-β-methyl-α, β-diaminopropionic acid, a cycad-derived glutamate receptor agonist. Plant Physiol. 124:1615–24
     [Google Scholar]
  9. 9.
    Brockie PJ, Jensen M, Mellem JE, Jensen E, Yamasaki T et al. 2013. Cornichons control ER export of AMPA receptors to regulate synaptic excitability. Neuron 80:129–42
     [Google Scholar]
  10. 10.
    Brown PMGE, McGuire H, Bowie D. 2018. Stargazin and cornichon-3 relieve polyamine block of AMPA receptors by enhancing blocker permeation. J. Gen. Physiol. 150:67–82
     [Google Scholar]
  11. 11.
    Burada AP, Vinnakota R, Kumar J. 2020. The architecture of GluD2 ionotropic delta glutamate receptor elucidated by cryo-EM. J. Struct. Biol. 211:107546
     [Google Scholar]
  12. 12.
    Burada AP, Vinnakota R, Kumar J. 2020. Cryo-EM structures of the ionotropic glutamate receptor GluD1 reveal a non-swapped architecture. Nat. Struct. Mol. Biol. 27:84–91
     [Google Scholar]
  13. 13.
    Burnashev N, Schoepfer R, Monyer H, Ruppersberg JP, Günther W et al. 1992. Control by asparagine residues of calcium permeability and magnesium blockade in the NMDA receptor. Science 257:1415–19
     [Google Scholar]
  14. 14.
    Burnashev N, Villarroel A, Sakmann B. 1996. Dimensions and ion selectivity of recombinant AMPA and kainate receptor channels and their dependence on Q/R site residues. J. Physiol. 496:165–73
     [Google Scholar]
  15. 15.
    Carbone AL, Plested AJR. 2016. Superactivation of AMPA receptors by auxiliary proteins. Nat. Commun. 7:10178
     [Google Scholar]
  16. 16.
    Carrillo E, Gonzalez CU, Berka V, Jayaraman V. 2021. Delta glutamate receptors are functional glycine- and d-serine–gated cation channels in situ. Sci. Adv. 7:eabk2200
     [Google Scholar]
  17. 17.
    Castro-Rodriguez V, Kleist TJ, Gappel NM, Atanjaoui F, Okumoto S et al. 2022. Sponging of glutamate at the outer plasma membrane surface reveals roles for glutamate in development. Plant J. 109:664–74
     [Google Scholar]
  18. 18.
    Chen G-Q, Cui C, Mayer ML, Gouaux E. 1999. Functional characterization of a potassium-selective prokaryotic glutamate receptor. Nature 402:817–21
     [Google Scholar]
  19. 19.
    Chen S, Zhao Y, Wang Y, Shekhar M, Tajkhorshid E, Gouaux E. 2017. Activation and desensitization mechanism of AMPA receptor-TARP complex by cryo-EM. Cell 170:1234–46.e14
     [Google Scholar]
  20. 20.
    Chiu J, Brenner ED, DeSalle R, Nitabach MN, Holmesm TC, Coruzzi GM. 2002. Phylogenetic and expression analysis of the glutamate-receptor–like gene family in Arabidopsis thaliana. Mol. Biol. Evol. 19:1066–82
     [Google Scholar]
  21. 21.
    Chiu J, 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. 16:826–38
     [Google Scholar]
  22. 22.
    Cho D, Kim SA, Murata Y, Lee S, Jae SK et al. 2009. De-regulated expression of the plant glutamate receptor homolog AtGLR3.1 impairs long-term Ca2+-programmed stomatal closure. Plant J. 58:437–49
     [Google Scholar]
  23. 23.
    Choi WG, Hilleary R, Swanson SJ, Kim SH, Gilroy S. 2016. Rapid, long-distance electrical and calcium signaling in plants. Annu. Rev. Plant Biol. 67:287–307
     [Google Scholar]
  24. 24.
    Coombs ID, Soto D, McGee TP, Gold MG, Farrant M, Cull-Candy SG. 2019. Homomeric GluA2(R) AMPA receptors can conduct when desensitized. Nat. Commun. 10:4312
     [Google Scholar]
  25. 25.
    Coombs ID, Soto D, Zonouzi M, Renzi M, Shelley C et al. 2012. Cornichons modify channel properties of recombinant and glial AMPA receptors. J. Neurosci. 32:9796–804
     [Google Scholar]
  26. 26.
    Cuin TA, Dreyer I, Michard E. 2018. The role of potassium channels in Arabidopsis thaliana long distance electrical signalling: AKT2 modulates tissue excitability while GORK shapes action potentials. Int. J. Mol. Sci. 19:926
     [Google Scholar]
  27. 27.
    Davenport R. 2002. Glutamate receptors in plants. Ann. Bot. 90:549–57
     [Google Scholar]
  28. 28.
    De Bortoli S, Teardo E, Szabo I, Morosinotto T, Alboresi A. 2016. Evolutionary insight into the ionotropic glutamate receptor superfamily of photosynthetic organisms. Biophys. Chem. 218:14–26
     [Google Scholar]
  29. 29.
    Demidchik V, Essah PA, Tester M. 2004. Glutamate activates cation currents in the plasma membrane of Arabidopsis root cells. Planta 219:167–75
     [Google Scholar]
  30. 30.
    Dennison KL, Spalding EP. 2000. Glutamate-gated calcium fluxes in Arabidopsis. Plant Physiol. 124:1511–14
     [Google Scholar]
  31. 31.
    Dietrich P, Anschutz U, Kugler A, Becker D. 2010. Physiology and biophysics of plant ligand-gated ion channels. Plant Biol. 12:80–93
     [Google Scholar]
  32. 32.
    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. 35:800–10
     [Google Scholar]
  33. 33.
    Edel KH, Kudla J. 2015. Increasing complexity and versatility: how the calcium signaling toolkit was shaped during plant land colonization. Cell Calcium 57:231–46
     [Google Scholar]
  34. 34.
    Edel KH, Marchadier E, Brownlee C, Kudla J, Hetherington AM. 2017. The evolution of calcium-based signalling in plants. Curr. Biol. 27:R667–79
     [Google Scholar]
  35. 35.
    Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792–97
     [Google Scholar]
  36. 36.
    Farmer EE, Gasperini D, Acosta IF. 2014. The squeeze cell hypothesis for the activation of jasmonate synthesis in response to wounding. New Phytol. 204:282–88
     [Google Scholar]
  37. 37.
    Fichman Y, Mittler R. 2021. Integration of electric, calcium, reactive oxygen species and hydraulic signals during rapid systemic signaling in plants. Plant J. 107:7–20
     [Google Scholar]
  38. 38.
    Fichman Y, Myers RJ Jr., Grant DG, Mittler R. 2021. Plasmodesmata-localized proteins and ROS orchestrate light-induced rapid systemic signaling in Arabidopsis. Sci. Signal. 14:eabf0322
     [Google Scholar]
  39. 39.
    Forde BG, Lea PJ. 2007. Glutamate in plants: metabolism, regulation, and signalling. J. Exp. Bot. 58:2339–58
     [Google Scholar]
  40. 40.
    Forde BG, Roberts MR. 2014. Glutamate receptor-like channels in plants: a role as amino acid sensors in plant defence?. F1000 Prime Rep. 6:37
     [Google Scholar]
  41. 41.
    Gaffey CT, Mullins LJ. 1958. Ion fluxes during the action potential in Chara. J. Physiol. 144:505–24
     [Google Scholar]
  42. 42.
    Gangwar SP, Green MN, Michard E, Simon AA, Feijó JA, Sobolevsky AI. 2021. Structure of the Arabidopsis glutamate receptor-like channel GLR3.2 ligand-binding domain. Structure 29:161–69.e4Report, using X-ray crystallography, of amino acid binding to AtGLR3.2.
     [Google Scholar]
  43. 43.
    Ger M-F, Rendon G, Tilson JL, Jakobsson E. 2010. Domain-based identification and analysis of glutamate receptor ion channels and their relatives in prokaryotes. PLOS ONE 5:e12827
     [Google Scholar]
  44. 44.
    Gilliham M, Campbell M, Dubos C, Becker D, Davenport R 2006. The Arabidopsis thaliana glutamate-like receptor family (AtGLR). Communication in Plants F Baluska, S Mancuso, D Volkmann 187–204. Berlin/Heidelberg: Springer
     [Google Scholar]
  45. 45.
    Green MN, Gangwar SP, Michard E, Simon AA, Portes MT et al. 2021. Structure of the Arabidopsis thaliana glutamate receptor-like channel GLR3.4. Mol. Cell 81:3216–26.e8First structural determination of a full-length GLR using cryo-EM.
     [Google Scholar]
  46. 46.
    Greger IH, Watson JF, Cull-Candy SG. 2017. Structural and functional architecture of AMPA-type glutamate receptors and their auxiliary proteins. Neuron 94:713–30
     [Google Scholar]
  47. 47.
    Grenzi M, Bonza MC, Alfieri A, Costa A 2021. Structural insights into long-distance signal transduction pathways mediated by plant glutamate receptor-like channels. New Phytol. 229:1261–67
     [Google Scholar]
  48. 48.
    Grenzi M, Bonza MC, Costa A 2022. Signaling by plant glutamate receptor-like channels: What else!. Curr. Opin. Plant Biol. 68:102253
     [Google Scholar]
  49. 49.
    Gutiérrez RA, Stokes TL, Thum K, Xu X, Obertello M et al. 2008. Systems approach identifies an organic nitrogen-responsive gene network that is regulated by the master clock control gene CCA1. PNAS 105:4939–44
     [Google Scholar]
  50. 50.
    Hansen KB, Wollmuth LP, Bowie D, Furukawa H, Menniti FS et al. 2021. Structure, function, and pharmacology of glutamate receptor ion channels. Pharmacol. Rev. 73:1469–658
     [Google Scholar]
  51. 51.
    Hansen KB, Yi F, Perszyk RE, Furukawa H, Wollmuth LP et al. 2018. Structure, function, and allosteric modulation of NMDA receptors. J. Gen. Physiol. 150:1081–105
     [Google Scholar]
  52. 52.
    Hedrich R, Fukushima K. 2021. On the origin of carnivory: molecular physiology and evolution of plants on an animal diet. Annu. Rev. Plant Biol. 72:133–53
     [Google Scholar]
  53. 53.
    Hedrich R, Salvador-Recatala V, Dreyer I. 2016. Electrical wiring and long-distance plant communication. Trends Plant Sci. 21:376–87
     [Google Scholar]
  54. 54.
    Helliwell KE, Chrachri A, Koester JA, Wharam S, Verret F et al. 2019. Alternative mechanisms for fast Na+/Ca2+ signaling in eukaryotes via a novel class of single-domain voltage-gated channels. Curr. Biol. 29:1503–11.e6
     [Google Scholar]
  55. 55.
    Hernandez-Coronado M, Dias Araujo PC, Ip PL, Nunes CO, Rahni R et al. 2022. Plant glutamate receptors mediate a bet-hedging strategy between regeneration and defense. Dev. Cell 57:451–65.e6Comprehensive analysis of GLRs’ genetic reprogramming in roots following injury.
     [Google Scholar]
  56. 56.
    Hollmann M, O'Shea-Greenfield A, Rogers SW, Heinemann S 1989. Cloning by functional expression of a member of the glutamate receptor family. Nature 342:643–48
     [Google Scholar]
  57. 57.
    Homann U, Thiel G. 1994. CI− and K+ channel currents during the action potential in Chara. Simultaneous recording of membrane voltage and patch currents. J. Membrane Biol. 141:297–309
     [Google Scholar]
  58. 58.
    Huettner JE. 2015. Glutamate receptor pores. J. Physiol. 593:49–59
     [Google Scholar]
  59. 59.
    Hunt E, Gattolin S, Newbury HJ, Bale JS, Tseng H-M et al. 2010. A mutation in amino acid permease AAP6 reduces the amino acid content of the Arabidopsis sieve elements but leaves aphid herbivores unaffected. J. Exp. Bot. 61:55–64
     [Google Scholar]
  60. 60.
    Inanobe A, Furukawa H, Gouaux E. 2005. Mechanism of partial agonist action at the NR1 subunit of NMDA receptors. Neuron 47:71–84
     [Google Scholar]
  61. 61.
    Iosip AL, Bohm J, Scherzer S, Al-Rasheid KAS, Dreyer I et al. 2020. The Venus flytrap trigger hair–specific potassium channel KDM1 can reestablish the K+ gradient required for hapto-electric signaling. PLOS Biol. 18:e3000964
     [Google Scholar]
  62. 62.
    Iwano M, Ito K, Fujii S, Kakita M, Asano-Shimosato H et al. 2015. Calcium signalling mediates self-incompatibility response in the Brassicaceae. Nat. Plants 1:15128
     [Google Scholar]
  63. 63.
    Jalali-Yazdi F, Chowdhury S, Yoshioka C, Gouaux E. 2018. Mechanisms for zinc and proton inhibition of the GluN1/GluN2A NMDA receptor. Cell 175:1520–32.e15
     [Google Scholar]
  64. 64.
    Janovjak H, Sandoz G, Isacoff EY. 2011. A modern ionotropic glutamate receptor with a K+ selectivity signature sequence. Nat. Commun. 2:232
     [Google Scholar]
  65. 65.
    Johannes E, Ermolayeva E, Sanders D. 1996. Red light–induced membrane potential transients in the moss Physcomitrella patens: ion channel interaction in phytochrome signalling. J. Exp. Bot. 48:599–608
     [Google Scholar]
  66. 66.
    Ju C, Van de Poel B, Cooper ED, Thierer JH, Gibbons TR et al. 2015. Conservation of ethylene as a plant hormone over 450 million years of evolution. Nat. Plants 1:14004
     [Google Scholar]
  67. 67.
    Jumper J, Evans R, Pritzel A, Green T, Figurnov M et al. 2021. Highly accurate protein structure prediction with AlphaFold. Nature 596:583–89
     [Google Scholar]
  68. 68.
    Jung H, Tschaplinski T, Wang L, Glazebrook J, Greenberg J. 2009. Priming in systemic plant immunity. Science 324:89–91
     [Google Scholar]
  69. 69.
    Kan C-C, Chung T-Y, Wu H-Y, Juo Y-A, Hsieh M-H 2017. Exogenous glutamate rapidly induces the expression of genes involved in metabolism and defense responses in rice roots. BMC Genom. 18:186
     [Google Scholar]
  70. 70.
    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. PNAS 100:6872–77
     [Google Scholar]
  71. 71.
    Kang S, Kim HB, Lee H, Choi JY, Heu S et al. 2006. Overexpression in Arabidopsis of a plasma membrane-targeting glutamate receptor from small radish increases glutamate-mediated Ca2+ influx and delays fungal infection. Mol. Cells 21:418–27
     [Google Scholar]
  72. 72.
    Kim SA, Kwak JM, Jae S-K, Wang M-H, Nam HG 2001. Overexpression of the AtGluR2 gene encoding an Arabidopsis homolog of mammalian glutamate receptors impairs calcium utilization and sensitivity to ionic stress in transgenic plants. Plant Cell Physiol. 42:74–84
     [Google Scholar]
  73. 73.
    Klein RM, Howe JR. 2004. Effects of the lurcher mutation on GluR1 desensitization and activation kinetics. J. Neurosci. 24:4941–51
     [Google Scholar]
  74. 74.
    Kleist TJ, Wudick MM. 2022. Shaping up: recent advances in the study of plant calcium channels. Curr. Opin. Cell Biol. 76:102080
     [Google Scholar]
  75. 75.
    Kong D, Hu H-C, Okuma E, Lee Y, Lee HS et al. 2016. L-Met activates Arabidopsis GLR Ca2+ channels upstream of ROS production and regulates stomatal movement. Cell Rep. 17:2553–61
     [Google Scholar]
  76. 76.
    Kong D, Ju C, Parihar A, Kim S, Cho D, Kwak JM. 2015. Arabidopsis glutamate receptor homolog 3.5 modulates cytosolic Ca2+ level to counteract effect of abscisic acid in seed germination. Plant Physiol. 167:1630–42
     [Google Scholar]
  77. 77.
    Koselski M, Trebacz K, Dziubinska H, Krol E. 2008. Light- and dark-induced action potentials in Physcomitrella patens. Plant Signal. Behav. 3:13–18
     [Google Scholar]
  78. 78.
    Krol E, Dziubinska H, Trebacz K, Koselski M, Stolarz M. 2007. The influence of glutamic and aminoacetic acids on the excitability of the liverwort Conocephalum conicum. J. Plant Physiol. 164:773–84
     [Google Scholar]
  79. 79.
    Kumari A, Chetelat A, Nguyen CT, Farmer EE. 2019. Arabidopsis H+-ATPase AHA1 controls slow wave potential duration and wound-response jasmonate pathway activation. PNAS 116:20226–31
     [Google Scholar]
  80. 80.
    Kuner T, Beck C, Sakmann B, Seeburg PH. 2001. Channel-lining residues of the AMPA receptor M2 segment: structural environment of the Q/R site and identification of the selectivity filter. J. Neurosci. 21:4162–72
     [Google Scholar]
  81. 81.
    Kuner T, Seeburg PH, Guy HR. 2003. A common architecture for K+ channels and ionotropic glutamate receptors?. TRENDS Neurosci. 26:27–32
     [Google Scholar]
  82. 82.
    Kurenda A, Nguyen CT, Chételat A, Stolz S, Farmer EE. 2019. Insect-damaged Arabidopsis moves like wounded Mimosa pudica. PNAS 116:26066–71
     [Google Scholar]
  83. 83.
    Kwaaitaal M, Huisman R, Maintz J, Reinstadler A, Panstruga R. 2011. Ionotropic glutamate receptor (iGluR)-like channels mediate MAMP-induced calcium influx in Arabidopsis thaliana. Biochem. J. 440:355–65
     [Google Scholar]
  84. 84.
    Lacombe B, Becker D, Hedrich R, DeSalle R, Hollmann M et al. 2001. The identity of plant glutamate receptors. Science 292:1486–87
     [Google Scholar]
  85. 85.
    Lam HM, Chiu J, Hsieh MH, Meisel L, Oliveira IC et al. 1998. Glutamate-receptor genes in plants. Nature 396:125–26Discovered genes in plants homologous to mammalian glutamate receptors.
     [Google Scholar]
  86. 86.
    Lew TTS, Koman VB, Silmore KS, Seo JS, Gordiichuk P et al. 2020. Real-time detection of wound-induced H2O2 signalling waves in plants with optical nanosensors. Nat. Plants 6:404–15
     [Google Scholar]
  87. 87.
    Li F, Wang J, Ma C, Zhao Y, Wang Y et al. 2013. Glutamate receptor-like channel 3.3 is involved in mediating glutathione-triggered cytosolic calcium transients, transcriptional changes, and innate immunity responses in Arabidopsis. Plant Physiol. 162:1497–509
     [Google Scholar]
  88. 88.
    Li J, Zhu S, Song X, Shen Y, Chen H et al. 2006. A rice glutamate receptor-like gene is critical for the division and survival of individual cells in the root apical meristem. Plant Cell 18:340–49
     [Google Scholar]
  89. 89.
    Liu S, Zhang X, Xiao S, Ma J, Shi W et al. 2021. A single-nucleotide mutation in a GLUTAMATE RECEPTOR-LIKE gene confers resistance to fusarium wilt in Gossypium hirsutum. Adv. Sci. 8:2002723
     [Google Scholar]
  90. 90.
    Llinás R, Steinberg IZ, Walton K 1981. Relationship between presynaptic calcium current and postsynaptic potential in squid giant synapse. Biophys. J. 33:323–52
     [Google Scholar]
  91. 91.
    Lohaus G, Pennewiss K, Sattelmacher B, Hussmann M, Muehling KH. 2001. Is the infiltration-centrifugation technique appropriate for the isolation of apoplastic fluid? A critical evaluation with different plant species. Physiol. Plant. 111:457–65
     [Google Scholar]
  92. 92.
    Lomash S, Chittori S, Brown P, Mayer ML. 2013. Anions mediate ligand binding in Adineta vaga glutamate receptor ion channels. Structure 21:414–25
     [Google Scholar]
  93. 93.
    Lu W, Du J, Goehring A, Gouaux E. 2017. Cryo-EM structures of the triheteromeric NMDA receptor and its allosteric modulation. Science 355:eaal3729
     [Google Scholar]
  94. 94.
    Lu W, Shi Y, Jackson AC, Bjorgan K, During MJ et al. 2009. Subunit composition of synaptic AMPA receptors revealed by a single-cell genetic approach. Neuron 62:254–68
     [Google Scholar]
  95. 95.
    Lunevsky VZ, Zherelova OM, Vostrikov IY, Berestovsky GN. 1983. Excitation of Characeae cell membranes as a result of activation of calcium and chloride channels. J. Membrane Biol. 72:43–58
     [Google Scholar]
  96. 96.
    Luo J, Wang Y, Yasuda RP, Dunah AW, Wolfe BB. 1996. The majority of N-methyl-d-aspartate receptor complexes in adult rat cerebral cortex contain at least three different subunits (NR1/NR2A/NR2B). Mol. Pharmacol. 51:79–86
     [Google Scholar]
  97. 97.
    Manzoor H, Kelloniemi J, Chiltz A, Wendehenne D, Pugin A et al. 2013. Involvement of the glutamate receptor AtGLR3.3 in plant defense signaling and resistance to Hyaloperonospora arabidopsidis. Plant J. 76:466–80
     [Google Scholar]
  98. 98.
    Marhavý P, Kurenda A, Siddique S, Dénervaud Tendon V, Zhou F et al. 2019. Single-cell damage elicits regional, nematode-restricting ethylene responses in roots. EMBO J. 38:e100972
     [Google Scholar]
  99. 99.
    Maricq AV, Peckol E, Driscoll M, Bargmann CI. 1995. Mechanosensory signalling in C. elegans mediated by the GLR-1 glutamate receptor. Nature 378:78–81
     [Google Scholar]
  100. 100.
    Martiniere A, Gibrat R, Sentenac H, Dumont X, Gaillard I, Paris N. 2018. Uncovering pH at both sides of the root plasma membrane interface using noninvasive imaging. PNAS 115:6488–93
     [Google Scholar]
  101. 101.
    Marvin JS, Borghuis BG, Tian L, Cichon J, Harnett MT et al. 2013. An optimized fluorescent probe for visualizing glutamate neurotransmission. Nat. Methods 10:162–70
     [Google Scholar]
  102. 102.
    Meyerhoff O, Muller K, Roelfsema MR, Latz A, Lacombe B et al. 2005. AtGLR3.4, a glutamate receptor channel-like gene is sensitive to touch and cold. Planta 222:418–27
     [Google Scholar]
  103. 103.
    Meyerson JR, Kumar J, Chittori S, Rao P, Pierson J et al. 2014. Structural mechanism of glutamate receptor activation and desensitization. Nature 514:328–34
     [Google Scholar]
  104. 104.
    Michard E, Lima PT, Borges F, Silva AC, Portes MT et al. 2011. Glutamate receptor–like genes form Ca2+ channels in pollen tubes and are regulated by pistil d-serine. Science 332:434–37First study implying GLRs’ ionotropic function and role in plant reproduction and the involvement of d-Ser.
     [Google Scholar]
  105. 105.
    Moe-Lange J, Gappel NM, Machado M, Wudick MM, Sies CSA et al. 2021. Interdependence of a mechanosensitive anion channel and glutamate receptors in distal wound signaling. Sci. Adv. 7:eabg4298
     [Google Scholar]
  106. 106.
    Mou W, Kao Y-T, Michard E, Simon AA, Li D et al. 2020. Ethylene-independent signaling by the ethylene precursor ACC in Arabidopsis ovular pollen tube attraction. Nat. Commun. 11:4082
     [Google Scholar]
  107. 107.
    Mousavi SA, Chauvin A, Pascaud F, Kellenberger S, Farmer EE. 2013. GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signalling. Nature 500:422–26Use of surface-potential measurements to demonstrate the involvement of GLR3.3 and GLR3.6 in long-distance electrical signaling.
     [Google Scholar]
  108. 108.
    Nadler V, Kloog Y, Sokolovsky M. 1988. 1-Aminocyclopropane-1-carboxylic acid (ACC) mimics the effects of glycine on the NMDA receptor ion channel. Eur. J. Pharmacol. 157:115–16
     [Google Scholar]
  109. 109.
    Nahum-Levy R, Fossom LH, Skolnick P, Benveniste M 1999. Putative partial agonist 1-aminocyclopropanecarboxylic acid acts concurrently as a glycine-site agonist and a glutamate-site antagonist at N-methyl-d-aspartate receptors. Mol. Pharamacol. 56:1207–18
     [Google Scholar]
  110. 110.
    Navarro-Retamal C, Schott-Verdugo S, Gohlke H, Dreyer I. 2021. Computational analyses of the AtTPC1 (Arabidopsis two-pore channel 1) permeation pathway. Int. J. Mol. Sci. 22:10345
     [Google Scholar]
  111. 111.
    Nguyen CT, Kurenda A, Stolz S, Chetelat A, Farmer EE. 2018. Identification of cell populations necessary for leaf-to-leaf electrical signaling in a wounded plant. PNAS 115:10178–83Genetic analysis reporting GLR-dependent phenotypes in long-distance electrical signaling with Ca2+ signaling simultaneously.
     [Google Scholar]
  112. 112.
    Ni J, Yu Z, Du G, Zhang Y, Taylor JL et al. 2016. Heterologous expression and functional analysis of rice GLUTAMATE RECEPTOR-LIKE family indicates its role in glutamate triggered calcium flux in rice roots. Rice 9:9
     [Google Scholar]
  113. 113.
    Nishiyama T, Sakayama H, de Vries J, Buschmann H, Saint-Marcoux D et al. 2018. The Chara genome: secondary complexity and implications for plant terrestrialization. Cell 174:448–64.e24
     [Google Scholar]
  114. 114.
    Noctor G, Foyer CH. 2016. Intracellular redox compartmentation and ROS-related communication in regulation and signaling. Plant Physiol. 171:1581–92
     [Google Scholar]
  115. 115.
    Ortiz-Ramírez C, Michard E, Simon AA, Damineli DSC, Hernández-Coronado M et al. 2017. GLUTAMATE RECEPTOR-LIKE channels are essential for chemotaxis and reproduction in mosses. Nature 549:91–95Genetic and electrophysiological characterization of P. patens GLR1/GLR2 in reproduction and transcriptional regulation.
     [Google Scholar]
  116. 116.
    Pérez-Otaño I, Larsen RS, Wesseling JF. 2016. Emerging roles of GluN3-containing NMDA receptors in the CNS. Nat. Rev. Neurosci. 17:623–35
     [Google Scholar]
  117. 117.
    Plieth C, Sattelmacher B, Hansen U, Thiel G. 1998. The action potential in Chara: Ca2+ release from internal stores visualized by Mn2+-induced quenching of fura-dextran. Plant J. 13:167–75
     [Google Scholar]
  118. 118.
    Price MB, Jelesko J, Okumoto S. 2012. Glutamate receptor homologs in plants: functions and evolutionary origins. Front. Plant Sci. 3:235
     [Google Scholar]
  119. 119.
    Price MB, Kong D, Okumoto S. 2013. Inter-subunit interactions between glutamate-like receptors in Arabidopsis. Plant Signal. Behav. 8:e27034
     [Google Scholar]
  120. 120.
    Qi Z, Stephens NR, Spalding EP. 2006. Calcium entry mediated by GLR3.3, an Arabidopsis glutamate receptor with a broad agonist profile. Plant Physiol. 142:963–71
     [Google Scholar]
  121. 121.
    Qiu XM, Sun YY, Ye XY, Li ZG. 2019. Signaling role of glutamate in plants. Front. Plant Sci. 10:1743
     [Google Scholar]
  122. 122.
    Ramos-Vicente D, Ji J, Gratacós-Batlle E, Gou G, Reig-Viader R et al. 2018. Metazoan evolution of glutamate receptors reveals unreported phylogenetic groups and divergent lineage-specific events. eLife 7:e35774
     [Google Scholar]
  123. 123.
    Riva I, Eibl C, Volkmer R, Carbone AL, Plested AJ. 2017. Control of AMPA receptor activity by the extracellular loops of auxiliary proteins. eLife 6:e28680
     [Google Scholar]
  124. 124.
    Roy BC, Mukherjee A. 2017. Computational analysis of the glutamate receptor gene family of Arabidopsis thaliana. J. Biomol. Struct. Dyn. 35:2454–74
     [Google Scholar]
  125. 125.
    Roy SJ, Gilliham M, Berger B, Essah PA, Cheffings C et al. 2008. Investigating glutamate receptor-like gene co-expression in Arabidopsis thaliana. Plant Cell Environ. 31:861–71
     [Google Scholar]
  126. 126.
    Saitou N, Nei M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4:406–25
     [Google Scholar]
  127. 127.
    Salvador-Recatalá V. 2016. New roles for the GLUTAMATE RECEPTOR-LIKE 3.3, 3.5, and 3.6 genes as on/off switches of wound-induced systemic electrical signals. Plant Signal. Behav. 11:e1161879
     [Google Scholar]
  128. 128.
    Salvador-Recatalá V, Tjallingii WF, Farmer EE. 2014. Real-time, in vivo intracellular recordings of caterpillar-induced depolarization waves in sieve elements using aphid electrodes. New Phytol. 203:674–84
     [Google Scholar]
  129. 129.
    Scherzer S, Böhm J, Huang S, Iosip AL, Kreuzer I et al. 2022. A unique inventory of ion transporters poises the Venus flytrap to fast-propagating action potentials and calcium waves. Curr. Biol. 32:4255–63.e5
     [Google Scholar]
  130. 130.
    Scherzer S, Huang S, Iosip A, Kreuzer I, Yokawa K et al. 2022. Ether anesthetics prevents touch-induced trigger hair calcium-electrical signals excite the Venus flytrap. Sci. Rep. 12:2851
     [Google Scholar]
  131. 131.
    Schneggenburger R. 1998. Altered voltage dependence of fractional Ca2+ current in N-methyl-d-aspartate channel pore mutants with a decreased Ca2+ permeability. Biophys. J. 74:1790–94
     [Google Scholar]
  132. 132.
    Schneggenburger R, Neher E. 2000. Intracellular calcium dependence of transmitter release rates at a fast central synapse. Nature 406:889–93
     [Google Scholar]
  133. 133.
    Schuster CM, Ultsch A, Schloss P, Cox JA, Schmitt B, Betz H. 1991. Molecular cloning of an invertebrate glutamate receptor subunit expressed in Drosophila muscle. Science 254:112–14
     [Google Scholar]
  134. 134.
    Schwenk J, Harmel N, Zolles G, Bildl W, Kulik A et al. 2009. Functional proteomics identify cornichon proteins as auxiliary subunits of AMPA receptors. Science 323:1313–19
     [Google Scholar]
  135. 135.
    Shao Q, Gao Q, Lhamo D, Zhang H, Luan S. 2020. Two glutamate- and pH-regulated Ca2+ channels are required for systemic wound signaling in Arabidopsis. Sci. Signal. 13:eaba1453
     [Google Scholar]
  136. 136.
    Singh SK, Chien C-T, Chang I-F. 2016. The Arabidopsis glutamate receptor-like gene GLR3.6 controls root development by repressing the Kip-related protein gene KRP4. J. Exp. Bot. 67:1853–69
     [Google Scholar]
  137. 137.
    Stephens NR, Qi Z, Spalding EP. 2008. Glutamate receptor subtypes evidenced by differences in desensitization and dependence on the GLR3.3 and GLR3.4 genes. Plant Physiol. 146:529–38
     [Google Scholar]
  138. 138.
    Straub C, Tomita S. 2012. The regulation of glutamate receptor trafficking and function by TARPs and other transmembrane auxiliary subunits. Curr. Opin. Neurobiol. 22:488–95
     [Google Scholar]
  139. 139.
    Sze H, Li X, Palmgren MG. 1999. Energization of plant cell membranes by H+-pumping ATPases: regulation and biosynthesis. Plant Cell 11:677–89
     [Google Scholar]
  140. 140.
    Tapken D, Anschütz U, Liu L-H, Huelsken T, Seebohm G et al. 2013. A plant homolog of animal glutamate receptors is an ion channel gated by multiple hydrophobic amino acids. Sci. Signal. 6:ra47
     [Google Scholar]
  141. 141.
    Tapken D, Hollmann M. 2008. Arabidopsis thaliana glutamate receptor ion channel function demonstrated by ion pore transplantation. J. Mol. Biol. 383:36–48
     [Google Scholar]
  142. 142.
    Tazawa M, Shimmen T, Mimura T. 1987. Membrane control in the Characeae. Annu. Rev. Plant Physiol. 38:95–117
     [Google Scholar]
  143. 143.
    Teardo E, Carraretto L, De Bortoli S, Costa A, Behera S et al. 2015. Alternative splicing-mediated targeting of the Arabidopsis GLUTAMATE RECEPTOR3.5 to mitochondria affects organelle morphology. Plant Physiol. 167:216–27
     [Google Scholar]
  144. 144.
    Teardo E, Formentin E, Segalla A, Giacometti GM, Marin O et al. 2011. Dual localization of plant glutamate receptor AtGLR3.4 to plastids and plasmamembrane. Biochim. Biophys. Acta Bioenerg. 1807:359–67
     [Google Scholar]
  145. 145.
    Tehran DA, Kochlamazashvili G, Pampaloni NP, Sposini S, Shergill JK et al. 2022. Selective endocytosis of Ca2+-permeable AMPARs by the Alzheimer's disease risk factor CALM bidirectionally controls synaptic plasticity. Sci. Adv. 8:eabl5032
     [Google Scholar]
  146. 146.
    Toyota M, Spencer D, Sawai-Toyota S, Jiaqi W, Zhang T et al. 2018. Glutamate triggers long-distance, calcium-based plant defense signaling. Science 361:1112–15
     [Google Scholar]
  147. 147.
    Traynelis SF, Wollmuth LP, McBain CJ, Menniti FS, Vance KM et al. 2010. Glutamate receptor ion channels: structure, regulation, and function. Pharmacol. Rev. 62:405–96
     [Google Scholar]
  148. 148.
    Trebacz K, Simonis W, Schonknecht G. 1994. Cytoplasmic Ca2+, K+, Cl−, and activities in the liverwort Conocephalum conicum at rest and during action potentials. Plant Physiol. 106:1073–84
     [Google Scholar]
  149. 149.
    Twomey EC, Sobolevsky AI. 2018. Structural mechanisms of gating in ionotropic glutamate receptors. Biochemistry 57:267–76
     [Google Scholar]
  150. 150.
    Twomey EC, Yelshanskaya MV, Grassucci RA, Frank J, Sobolevsky AI. 2017. Channel opening and gating mechanism in AMPA-subtype glutamate receptors. Nature 549:60–65
     [Google Scholar]
  151. 151.
    Vincent TR, Avramova M, Canham J, Higgins P, Bilkey N et al. 2017. Interplay of plasma membrane and vacuolar ion channels, together with BAK1, elicits rapid cytosolic calcium elevations in Arabidopsis during aphid feeding. Plant Cell 29:1460–79Genetic analysis of GLR-dependent Ca2+ signaling under aphid attack.
     [Google Scholar]
  152. 152.
    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
     [Google Scholar]
  153. 153.
    Vincill ED, Clarin AE, Molenda JN, Spalding EP. 2013. Interacting glutamate receptor-like proteins in phloem regulate lateral root initiation in Arabidopsis. Plant Cell 25:1304–13
     [Google Scholar]
  154. 154.
    Walch-Liu P, Ivanov II, Filleur S, Gan Y, Remans T, Forde BG 2006. Nitrogen regulation of root branching. Ann. Bot. 97:875–81
     [Google Scholar]
  155. 155.
    Walch-Liu P, Liu L-H, Remans T, Tester M, Forde BG. 2006. Evidence that l-glutamate can act as an exogenous signal to modulate root growth and branching in Arabidopsis thaliana. Plant Cell Physiol. 47:1045–57
     [Google Scholar]
  156. 156.
    Wang G, Hu C, Zhou J, Liu Y, Cai J et al. 2019. Systemic root-shoot signaling drives jasmonate-based root defense against nematodes. Curr. Biol. 29:3430–38.e4
     [Google Scholar]
  157. 157.
    Wang PH, Lee CE, Lin YS, Lee MH, Chen PY et al. 2019. The glutamate receptor-like protein GLR3.7 interacts with 14-3-3ω and participates in salt stress response in Arabidopsis thaliana. Front. Plant Sci. 10:1169
     [Google Scholar]
  158. 158.
    Weiland M, Mancuso S, Baluska F. 2015. Signalling via glutamate and GLRs in Arabidopsis thaliana. Funct. Plant Biol. 43:1–25
     [Google Scholar]
  159. 159.
    Wen X, Zhang C, Ji Y, Zhao Q, He W et al. 2012. Activation of ethylene signaling is mediated by nuclear translocation of the cleaved EIN2 carboxyl terminus. Cell Res. 22:1613–16
     [Google Scholar]
  160. 160.
    Westphal L, Strehmel N, Eschen-Lippold L, Bauer N, Westermann B et al. 2019. pH effects on plant calcium fluxes: lessons from acidification-mediated calcium elevation induced by the γ-glutamyl-leucine dipeptide identified from Phytophthora infestans. Sci. Rep. 9:4733
     [Google Scholar]
  161. 161.
    Wildon DC, Thain JF, Minchin PEH, Gubb IR, Reilly AJ et al. 1992. Electrical signalling and systemic proteinase inhibitor induction in the wounded plant. Nature 36062–65Seminal study reporting that long-distance signaling is accomplished by electrical propagation.
  162. 162.
    Wo ZG, Oswald RE. 1995. Unraveling the modular design of glutamate-gated ion channels. Trends Neurosci. 18:161–68
     [Google Scholar]
  163. 163.
    Wood MW, VanDongen HM, VanDongen AM. 1995. Structural conservation of ion conduction pathways in K channels and glutamate receptors. PNAS 92:4882–86
     [Google Scholar]
  164. 164.
    Wu Q, Stolz S, Kumari A, Farmer EE. 2022. The carboxy-terminal tail of GLR3.3 is essential for wound-response electrical signaling. New Phytol. 236:2189–201
     [Google Scholar]
  165. 165.
    Wudick MM, Michard E, Oliveira Nunes C, Feijó JA 2018. Comparing plant and animal glutamate receptors: common traits but different fates?. J. Exp. Bot. 69:4151–63
     [Google Scholar]
  166. 166.
    Wudick MM, Portes MT, Michard E, Rosas-Santiago P, Lizzio MA et al. 2018. CORNICHON sorting and regulation of GLR channels underlie pollen tube Ca2+ homeostasis. Science 360:533–36Demonstration that GLR–CNIH interactions regulate Ca2+ homeostasis, likely through subcellular localization and channel gating.
     [Google Scholar]
  167. 167.
    Yelshanskaya MV, Patel DS, Kottke CM, Kurnikova MG, Sobolevsky AI. 2022. Opening of glutamate receptor channel to subconductance levels. Nature 605:172–78
     [Google Scholar]
  168. 168.
    Yu A, Salazar H, Plested AJR, Lau AY. 2018. Neurotransmitter funneling optimizes glutamate receptor kinetics. Neuron 97:139–49.e4
     [Google Scholar]
  169. 169.
    Yu B, Wu Q, Li X, Zeng R, Min Q, Huang J 2022. GLUTAMATE RECEPTOR-like gene OsGLR3.4 is required for plant growth and systemic wound signaling in rice (Oryza sativa). New Phytol. 233:1238–56Demonstration that systemic electrical signaling is conserved among GLRs from rice.
     [Google Scholar]
  170. 170.
    Yu J, Rao P, Clark S, Mitra J, Ha T, Gouaux E 2021. Hippocampal AMPA receptor assemblies and mechanism of allosteric inhibition. Nature 594:448–53
     [Google Scholar]
  171. 171.
    Zhang D, Watson JF, Matthews PM, Cais O, Greger IH. 2021. Gating and modulation of a hetero-octameric AMPA glutamate receptor. Nature 594:454–58
     [Google Scholar]
  172. 172.
    Zheng Y, Luo L, Wei J, Chen Q, Yang Y et al. 2018. The glutamate receptors AtGLR1.2 and AtGLR1.3 increase cold tolerance by regulating jasmonate signaling in Arabidopsis thaliana. Biochem. Biophys. Res. Commun. 506:895–900
     [Google Scholar]
  173. 173.
    Zuo J, De Jager PL, Takahashi KA, Jiang W, Linden DJ, Heintz N 1997. Neurodegeneration in Lurcher mice caused by mutation in δ2 glutamate receptor gene. Nature 388:769–73
     [Google Scholar]
  174. 174.
    Yoshida R, Mori IC, Kamizono N, Shichiri Y, Shimatani T et al 2016. Glutamate functions in stomatal closure in Arabidopsis and fava bean. J. Plant Res 129:39–49
     [Google Scholar]
  175. 175.
    Tsuruda T, Yoshida R 2023. L-Glutamate activates salicylic acid signaling to promote stomatal closure and PR1 expression in Arabidopsis. Physiol. Plant 175:e13858
     [Google Scholar]
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Merging Signaling with Structure: Functions and Mechanisms of Plant Glutamate Receptor Ion Channels
Annual Review of Plant Biology 74, 415 (2023); https://doi.org/10.1146/annurev-arplant-070522-033255
/content/journals/10.1146/annurev-arplant-070522-033255
/content/journals/10.1146/annurev-arplant-070522-033255
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