Cellular and Molecular Life Sciences

, Volume 74, Issue 9, pp 1577–1603 | Cite as

γ-Aminobutyric acid (GABA) signalling in plants

  • Sunita A. Ramesh
  • Stephen D. Tyerman
  • Matthew Gilliham
  • Bo Xu
Review

Abstract

The role of γ-aminobutyric acid (GABA) as a signal in animals has been documented for over 60 years. In contrast, evidence that GABA is a signal in plants has only emerged in the last 15 years, and it was not until last year that a mechanism by which this could occur was identified—a plant ‘GABA receptor’ that inhibits anion passage through the aluminium-activated malate transporter family of proteins (ALMTs). ALMTs are multigenic, expressed in different organs and present on different membranes. We propose GABA regulation of ALMT activity could function as a signal that modulates plant growth, development, and stress response. In this review, we compare and contrast the plant ‘GABA receptor’ with mammalian GABAA receptors in terms of their molecular identity, predicted topology, mode of action, and signalling roles. We also explore the implications of the discovery that GABA modulates anion flux in plants, its role in signal transduction for the regulation of plant physiology, and predict the possibility that there are other GABA interaction sites in the N termini of ALMT proteins through in silico evolutionary coupling analysis; we also explore the potential interactions between GABA and other signalling molecules.

Keywords

γ-Aminobutyric acid Aluminium-activated malate transporters GABAA receptors Signalling GABA metabolism Carbon–nitrogen balance Stress response Topology Pharmacology 

Abbreviations

3-MPA

3-Mercaptopropionic acid

ALMT

Aluminium (Al3+)-activated malate transporter

C/Cys

Cysteine

EC50

Half-maximal response

F/Phe

Phenylalanine

GABA

γ-aminobutyric acid

GABA-T

GABA transaminase

GABP

GABA permease

GAD

Glutamate decarboxylase

GAT

GABA transporter

GDH

Glutamate dehydrogenase

E/Glu

Glutamic acid

I/Ile

Isoleucine

SSA

Succinic semialdehyde

SSADH

Succinic semialdehyde dehydrogenase

T/Thr

Threonine

D/Asp

Aspartic acid

V/Val

Valine

Y/Tyr

Tyrosine

Q/Gln

Glutamine

L/Leu

Leucine

R/Arg

Arginine

TMDs

Transmembrane domains

K/Lys

Lysine

S/Ser

Serine

G/Gly

Glycine

References

  1. 1.
    Steward F, Thompson J, Dent C (1949) γ-Aminobutyric acid, a constituent of the potato tuber. Science 110:439–440Google Scholar
  2. 2.
    Roberts E, Frankel S (1950) γ-Aminobutyric acid in brain: its formation from glutamic acid. J Biol Chem 187:55–63PubMedGoogle Scholar
  3. 3.
    Awapara J, Landua AJ, Fuerst R, Seale B (1950) Free γ-aminobutyric acid in brain. J Biol Chem 187:35–39PubMedGoogle Scholar
  4. 4.
    Elliott K, Jasper HH (1959) Gamma-aminobutyric acid. Physiol Rev 39(2):383–406PubMedGoogle Scholar
  5. 5.
    Bloom F, Iversen L (1971) Localizing 3H-GABA in nerve terminals of rat cerebral cortex by electron microscopic autoradiography. Nature 229:628–630PubMedCrossRefGoogle Scholar
  6. 6.
    Palacios JM, Wamsley JK, Kuhar MJ (1981) High affinity GABA receptors—autoradiographic localization. Brain Res 222(2):285–307PubMedCrossRefGoogle Scholar
  7. 7.
    Watanabe M, Fukuda A (2015) Development and regulation of chloride homeostasis in the central nervous system. Front Cell Neurosci 9:14. doi:10.3389/fncel.2015.00371 CrossRefGoogle Scholar
  8. 8.
    Cooper P, Selman I (1974) An analysis of the effects of tobacco mosaic virus on growth and the changes in the free amino compounds in young tomato plants. Ann Bot 38:625–638CrossRefGoogle Scholar
  9. 9.
    Ben-Ari Y, Gaiarsa J-L, Tyzio R, Khazipov R (2007) GABA: a pioneer transmitter that excites immature neurons and generates primitive oscillations. Physiol Rev 87(4):1215–1284PubMedCrossRefGoogle Scholar
  10. 10.
    Li K, Xu E (2008) The role and the mechanism of γ-aminobutyric acid during central nervous system development. Neurosci Bull 24(3):195–200PubMedCrossRefGoogle Scholar
  11. 11.
    Erdö SL, De Vincentis G, Amenta F (1990) Autoradiographic localization of [3 H] muscimol binding sites in rat stomach: evidence for mucosal GABAA receptors. Eur J Pharmacol 175(3):351–354PubMedCrossRefGoogle Scholar
  12. 12.
    Barragan A, Weidner JM, Jin Z, Korpi E, Birnir B (2015) GABAergic signalling in the immune system. Acta Physiol 213(4):819–827CrossRefGoogle Scholar
  13. 13.
    Owens DF, Kriegstein AR (2002) Is there more to GABA than synaptic inhibition? Nat Rev Neurosci 3(9):715–727PubMedCrossRefGoogle Scholar
  14. 14.
    Shelp BJ, Bown AW, McLean MD (1999) Metabolism and functions of gamma-aminobutyric acid. Trends Plant Sci 4(11):446–452PubMedCrossRefGoogle Scholar
  15. 15.
    Bouché N, Fait A, Bouchez D, Møller SG, Fromm H (2003) Mitochondrial succinic-semialdehyde dehydrogenase of the γ-aminobutyrate shunt is required to restrict levels of reactive oxygen intermediates in plants. Proc Natl Acad Sci USA 100(11):6843–6848PubMedPubMedCentralCrossRefGoogle Scholar
  16. 16.
    Bouche N, Fromm H (2004) GABA in plants: just a metabolite? Trends Plant Sci 9(3):110–115. doi:10.1016/j.tplants.2004.01.006 PubMedCrossRefGoogle Scholar
  17. 17.
    Bown A, Shelp B (1997) The metabolism and functions of γ-aminobutyric acid. Plant Physiol Biochem 115:1–5Google Scholar
  18. 18.
    Ramesh SA, Tyerman SD, Xu B, Bose J, Kaur S, Conn V, Domingos P, Ullah S, Wege S, Shabala S, Feijo JA, Ryan PR, Gilliham M (2015) GABA signalling modulates plant growth by directly regulating the activity of plant-specific anion transporters. Nat Commun. doi:10.1038/ncomms8879 Google Scholar
  19. 19.
    Palanivelu R, Brass L, Edlund AF, Preuss D (2003) Pollen tube growth and guidance is regulated by POP2, an Arabidopsis gene that controls GABA levels. Cell 114(1):47–59PubMedCrossRefGoogle Scholar
  20. 20.
    Yue X, Gao XQ, Wang F, Dong Y, Li X, Zhang XS (2014) Transcriptional evidence for inferred pattern of pollen tube-stigma metabolic coupling during pollination. PLoS One 9(9):e107046. doi:10.1371/journal.pone.0107046 PubMedPubMedCentralCrossRefGoogle Scholar
  21. 21.
    Shelp BJ, Mullen RT, Waller JC (2012) Compartmentation of GABA metabolism raises intriguing questions. Trends Plant Sci 17(2):57–59. doi:10.1016/j.tplants.2011.12.006 PubMedCrossRefGoogle Scholar
  22. 22.
    Kinnersley AM, Turano FJ (2000) Gamma aminobutyric acid (GABA) and plant responses to stress. Crit Rev Plant Sci 19(6):479–509. doi:10.1080/07352680091139277 CrossRefGoogle Scholar
  23. 23.
    Kinnersley AM (1999) Physiological evidence for GABA receptors in plants. Plant Biol 1999:153Google Scholar
  24. 24.
    Bouche N, Lacombe B, Fromm H (2003) GABA signaling: a conserved and ubiquitous mechanism. Trends Cell Biol 13(12):607–610PubMedCrossRefGoogle Scholar
  25. 25.
    Shelp BJ, Bozzo GG, Trobacher CP, Zarei A, Deyman KL, Brikis CJ (2012) Hypothesis/review: contribution of putrescine to 4-aminobutyrate (GABA) production in response to abiotic stress. Plant Sci 193–194:130–135. doi:10.1016/j.plantsci.2012.06.001 PubMedCrossRefGoogle Scholar
  26. 26.
    Bown AW, Shelp BJ (2016) Plant GABA: not just a metabolite. Trend Plant SciGoogle Scholar
  27. 27.
    Gilliham M, Tyerman SD (2015) Linking metabolism to membrane signaling: the GABA—malate connection. Trends Plant SciGoogle Scholar
  28. 28.
    Žárský V (2015) Signal transduction: GABA receptor found in plants. Nat Plants 1:15115PubMedCrossRefGoogle Scholar
  29. 29.
    Yin YG, Tominaga T, Iijima Y, Aoki K, Shibata D, Ashihara H, Nishimura S, Ezura H, Matsukura C (2010) Metabolic alterations in organic acids and gamma-aminobutyric acid in developing tomato (Solanum lycopersicum L.) fruits. Plant Cell Physiol 51(8):1300–1314. doi:10.1093/pcp/pcq090 PubMedCrossRefGoogle Scholar
  30. 30.
    Code RA, Burd GD, Rubel EW (1989) Development of GABA immunoreactivity in brainstem auditory nuclei of the chick: ontogeny of gradients in terminal staining. J Comp Neurol 284(4):504–518PubMedCrossRefGoogle Scholar
  31. 31.
    Johnston GA (1996) GABAC receptors: relatively simple transmitter-gated ion channels? Trends Pharmacol Sci 17(9):319–323PubMedCrossRefGoogle Scholar
  32. 32.
    Zhang W, Ryan P, Sasaki T, Yamamoto Y, Sullivan W, Tyerman S (2008) Characterisation of the TaALMT1 protein as an Al3+-activated anion channel in transformed tobacco (Nicotiana tabacum L.) cells. Plant Cell Physiol 49:1316–1330PubMedCrossRefGoogle Scholar
  33. 33.
    Pineros MA, Cançado GM, Kochian LV (2008) Novel properties of the wheat aluminum tolerance organic acid transporter (TaALMT1) revealed by electrophysiological characterization in Xenopus oocytes: functional and structural implications. Plant Physiol 147(4):2131–2146PubMedPubMedCentralCrossRefGoogle Scholar
  34. 34.
    Meyer S, Mumm P, Imes D, Endler A, Weder B, Al-Rasheid KAS, Geiger D, Marten I, Martinoia E, Hedrich R (2010) AtALMT12 represents an R-type anion channel required for stomatal movement in Arabidopsis guard cells. Plant J 63(6):1054–1062. doi:10.1111/j.1365-313X.2010.04302.x PubMedCrossRefGoogle Scholar
  35. 35.
    Cho MH, Spalding EP (1996) An anion channel in Arabidopsis hypocotyls activated by blue light. Proc Natl Acad Sci USA 93(15):8134–8138PubMedPubMedCentralCrossRefGoogle Scholar
  36. 36.
    Thomine S, Lelièvre F, Boufflet M, Guern J, Barbier-Brygoo H (1997) Anion-channel blockers interfere with auxin responses in dark-grown Arabidopsis hypocotyls. Plant Physiol 115(2):533–542PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    Colcombet J, Mathieu Y, Peyronnet R, Agier N, Lelièvre F, Barbier-Brygoo H, Frachisse J-M (2009) R-type anion channel activation is an essential step for ROS-dependent innate immune response in Arabidopsis suspension cells. Funct Plant Biol 36(9):832–843CrossRefGoogle Scholar
  38. 38.
    Barbier-Brygoo H, De Angeli A, Filleur S, Frachisse JM, Gambale F, Thomine S, Wege S (2011) Anion channels/transporters in plants: from molecular bases to regulatory networks. Annu Rev Plant Biol 62:25–51. doi:10.1146/annurev-arplant-042110-103741 PubMedCrossRefGoogle Scholar
  39. 39.
    Kollist H, Jossier M, Laanemets K, Thomine S (2011) Anion channels in plant cells. FEBS J 278(22):4277–4292PubMedCrossRefGoogle Scholar
  40. 40.
    Bormann J (1988) Electrophysiology of GABAA and GABAB receptor subtypes. Trends Neurosci 11(3):112–116PubMedCrossRefGoogle Scholar
  41. 41.
    Bowery NG, Doble A, Hill DR, Hudson AL, Shaw JS, Turnbull MJ, Warrington R (1981) Bicuculline-insensitive GABA receptors on peripheral autonomic nerve terminals. Eur J Pharmacol 71(1):53–70PubMedCrossRefGoogle Scholar
  42. 42.
    Ben-Ari Y, Khazipov R, Leinekugel X, Caillard O, Gaiarsa J-L (1997) GABAA, NMDA and AMPA receptors: a developmentally regulatedménage à trois’. Trends Neurosci 20(11):523–529PubMedCrossRefGoogle Scholar
  43. 43.
    Ben-Ari Y (2002) Excitatory actions of GABA during development: the nature of the nurture. Nat Rev Neurosci 3(9):728–739PubMedCrossRefGoogle Scholar
  44. 44.
    Bouche N, Fait A, Zik M, Fromm H (2004) The root-specific glutamate decarboxylase (GAD1) is essential for sustaining GABA levels in Arabidopsis. Plant Mol Biol 55(3):315–325. doi:10.1007/s11103-004-0650-z PubMedCrossRefGoogle Scholar
  45. 45.
    Lam H-M, Chiu J, Hsieh M-H, Meisel L, Oliveira IC, Shin M, Coruzzi G (1998) Glutamate-receptor genes in plants. Nature 396(6707):125–126PubMedCrossRefGoogle Scholar
  46. 46.
    Lacombe B, Becker D, Hedrich R, DeSalle R, Hollmann M, Kwak JM, Schroeder JI, Le Novère N, Nam HG, Spalding EP (2001) The identity of plant glutamate receptors. Science 292(5521):1486PubMedCrossRefGoogle Scholar
  47. 47.
    Turano FJ, Panta GR, Allard MW, van Berkum P (2001) The putative glutamate receptors from plants are related to two superfamilies of animal neurotransmitter receptors via distinct evolutionary mechanisms. Mol Biol Evol 18(7):1417–1420PubMedCrossRefGoogle Scholar
  48. 48.
    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(6):800–810PubMedCrossRefGoogle Scholar
  49. 49.
    Michard E, Lima PT, Borges F, Silva AC, Portes MT, Carvalho JE, Gilliham M, Liu LH, Obermeyer G, Feijo JA (2011) Glutamate receptor-like genes form Ca2+ channels in pollen tubes and are regulated by pistil D-serine. Science 332(6028):434–437. doi:10.1126/science.1201101 PubMedCrossRefGoogle Scholar
  50. 50.
    Kim SA, Kwak J, Jae S-K, Wang M-H, Nam H (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(1):74–84PubMedCrossRefGoogle Scholar
  51. 51.
    Demidchik V, Essah PA, Tester M (2004) Glutamate activates cation currents in the plasma membrane of Arabidopsis root cells. Planta 219(1):167–175PubMedCrossRefGoogle Scholar
  52. 52.
    Dennison KL, Spalding EP (2000) Glutamate-gated calcium fluxes in Arabidopsis. Plant Physiol 124(4):1511–1514PubMedPubMedCentralCrossRefGoogle Scholar
  53. 53.
    Lancien M, Roberts MR (2006) Regulation of Arabidopsis thaliana 14-3-3 gene expression by gamma-aminobutyric acid. Plant Cell Environ 29(7):1430–1436. doi:10.1111/j.1365-3040.2006.01526.x PubMedCrossRefGoogle Scholar
  54. 54.
    Laha KT, Tran PN (2013) Multiple tyrosine residues at the GABA binding pocket influence surface expression and mediate kinetics of the GABAA receptor. J Neurochem 124(2):200–209. doi:10.1111/jnc.12083 PubMedCrossRefGoogle Scholar
  55. 55.
    Sanders D, Pelloux J, Brownlee C, Harper JF (2002) Calcium at the crossroads of signaling. Plant Cell 14:S401–S417PubMedPubMedCentralGoogle Scholar
  56. 56.
    Kovermann P, Meyer S, Hortensteiner S, Picco C, Scholz-Starke J, Ravera S, Lee YEM (2007) The Arabidopsis vacuolar malate channel is a member of the ALMT family. Plant J 52:1169–1180PubMedCrossRefGoogle Scholar
  57. 57.
    De Angeli A, Zhang J, Meyer S, Martinoia E (2013) AtALMT9 is a malate-activated vacuolar chloride channel required for stomatal opening in Arabidopsis. Nat Commun 4:1804PubMedPubMedCentralCrossRefGoogle Scholar
  58. 58.
    Dreyer I, Gomez-Porras JL, Riaño-Pachón DM, Hedrich R, Geiger D (2013) Molecular evolution of slow and quick anion channels (SLACs and QUACs/ALMTs). Front Plant Sci:97Google Scholar
  59. 59.
    Hedrich R (2012) Ion channels in plants. Physiol Rev 92(4):1777–1811PubMedCrossRefGoogle Scholar
  60. 60.
    Gutermuth T, Lassig R, Portes M-T, Maierhofer T, Romeis T, Borst J-W, Hedrich R, Feijó JA, Konrad KR (2013) Pollen tube growth regulation by free anions depends on the interaction between the anion channel SLAH3 and calcium-dependent protein kinases CPK2 and CPK20. Plant Cell 25(11):4525–4543PubMedPubMedCentralCrossRefGoogle Scholar
  61. 61.
    De Angeli A, Baetz U, Francisco R, Zhang J, Chaves MM, Regalado A (2013) The vacuolar channel VvALMT9 mediates malate and tartrate accumulation in berries of Vitis vinifera. Planta 238(2):283–291PubMedCrossRefGoogle Scholar
  62. 62.
    Shelp BJ, Bozzo GG, Zarei A, Simpson JP, Trobacher CP, Allan WL (2012) Strategies and tools for studying the metabolism and function of γ-aminobutyrate in plants. II. Integrated analysis. Botany 90(9):781–793CrossRefGoogle Scholar
  63. 63.
    Cully DF, Vassilatis DK, Liu KK, Paress PS, Van der Ploeg L, Schaeffer JM, Arena JP (1994) Cloning of an avermectin-sensitive glutamate-gated chloride channel from Caenorhabditis elegans. Nature 371(6499):707–711PubMedCrossRefGoogle Scholar
  64. 64.
    Hilf RJ, Dutzler R (2009) Structure of a potentially open state of a proton-activated pentameric ligand-gated ion channel. Nature 457(7225):115–118PubMedCrossRefGoogle Scholar
  65. 65.
    Miller PS, Aricescu AR (2014) Crystal structure of a human GABAA receptor. Nature 512(7514):270–275PubMedPubMedCentralCrossRefGoogle Scholar
  66. 66.
    Schofield PR, Darlison MG, Fujita N, Burt DR, Stephenson FA, Rodriguez H, Rhee LM, Ramachandran J, Reale V, Glencorse TA (1987) Sequence and functional expression of the GABAA receptor shows a ligand-gated receptor super-family. Nature 328:221–227. doi:10.1038/328221a0 PubMedCrossRefGoogle Scholar
  67. 67.
    Sieghart W, Fuchs K, Tretter V, Ebert V, Jechlinger M, Höger H, Adamiker D (1999) Structure and subunit composition of GABAA receptors. Neurochem Int 34(5):379–385PubMedCrossRefGoogle Scholar
  68. 68.
    Sieghart W (2006) Structure, pharmacology, and function of GABAA receptor subtypes. Adv Pharmacol 54:231PubMedCrossRefGoogle Scholar
  69. 69.
    Smith GB, Olsen RW (1995) Functional domains of GABAA receptors. Trends Pharmacol Sci 16(5):162–168PubMedCrossRefGoogle Scholar
  70. 70.
    Cromer BA, Morton CJ, Parker MW (2002) Anxiety over GABAA receptor structure relieved by AChBP. Trends Biochem Sci 27(6):280–287PubMedCrossRefGoogle Scholar
  71. 71.
    Sieghart W, Sperk G (2002) Subunit composition, distribution and function of GABAA receptor subtypes. Curr Top Med Chem 2(8):795–816PubMedCrossRefGoogle Scholar
  72. 72.
    Whiting P (1999) The GABAA receptor gene family: new targets for therapeutic intervention. Neurochem Int 34(5):387–390PubMedCrossRefGoogle Scholar
  73. 73.
    Sieghart W, Fuchs K, Tretter V, Ebert V, Jechlinger W, Hoger H, Adamiker D (1999) Structure and subunit composition of GABAA receptors. Neurochem Int 34:379–385PubMedCrossRefGoogle Scholar
  74. 74.
    Brickley S, Farrant M, Swanson G, Cull-Candy S (2001) CNQX increases GABA-mediated synaptic transmission in the cerebellum by an AMPA/kainate receptor-independent mechanism. Neuropharmacol 41(6):730–736CrossRefGoogle Scholar
  75. 75.
    Stell BM, Brickley SG, Tang C, Farrant M, Mody I (2003) Neuroactive steroids reduce neuronal excitability by selectively enhancing tonic inhibition mediated by δ subunit-containing GABAA receptors. Proc Natl Acad Sci USA 100(24):14439–14444PubMedPubMedCentralCrossRefGoogle Scholar
  76. 76.
    Farrant M, Nusser Z (2005) Variations on an inhibitory theme: phasic and tonic activation of GABAA receptors. Nat Rev Neurosci 6(3):215–229PubMedCrossRefGoogle Scholar
  77. 77.
    Horenstein J, Wagner DA, Czajkowski C, Akabas MH (2001) Protein mobility and GABA-induced conformational changes in GABAA receptor pore-lining M2 segment. Nat Neurosci 4(5):477–485PubMedGoogle Scholar
  78. 78.
    Chang Y, Weiss DS (2002) Site-specific fluorescence reveals distinct structural changes with GABA receptor activation and antagonism. Nat Neurosci 5(11):1163–1168PubMedCrossRefGoogle Scholar
  79. 79.
    Amin J, Dickerson I, Weiss DS (1994) The agonist binding site of the gamma-aminobutyric acid type A channel is not formed by the extracellular cysteine loop. Mol Pharmacol 45(2):317–323PubMedGoogle Scholar
  80. 80.
    Sumikawa K, Gehle VM (1992) Assembly of mutant subunits of the nicotinic acetylcholine receptor lacking the conserved disulfide loop structure. J Biol Chem 267(9):6286–6290PubMedGoogle Scholar
  81. 81.
    Vandenberg RJ, Rajendra S, French CR, Barry PH, Schofield PR (1993) The extracellular disulfide loop motif of the inhibitory glycine receptor does not form the agonist binding site. Mol Pharm 44(1):198–203Google Scholar
  82. 82.
    Miller SM, Piasecki CC, Peabody MF, Lonstein JS (2010) GABAA receptor antagonism in the ventrocaudal periaqueductal gray increases anxiety in the anxiety-resistant postpartum rat. Pharmacol Biochem Behav 95(4):457–465PubMedCrossRefGoogle Scholar
  83. 83.
    Macdonald RL, Olsen RW (1994) GABAA receptor channels. Annu Rev Neurosci 17(1):569–602PubMedCrossRefGoogle Scholar
  84. 84.
    Rabow LE, Russek SJ, Farb DH (1995) From ion currents to genomic analysis: recent advances in GABAA receptor research. Synapse 21(3):189–274PubMedCrossRefGoogle Scholar
  85. 85.
    Chen ZW, Olsen RW (2007) GABAA receptor associated proteins: a key factor regulating GABAA receptor function. J Neurochem 100(2):279–294PubMedCrossRefGoogle Scholar
  86. 86.
    Jacob TC, Moss SJ, Jurd R (2008) GABAA receptor trafficking and its role in the dynamic modulation of neuronal inhibition. Nat Rev Neurosci 9(5):331–343PubMedPubMedCentralCrossRefGoogle Scholar
  87. 87.
    Boileau AJ, Evers AR, Davis AF, Czajkowski C (1999) Mapping the agonist binding site of the GABAA receptor: evidence for a β-strand. J Neurosci 19(12):4847–4854PubMedGoogle Scholar
  88. 88.
    Motoda H, Sasaki T, Kano Y, Ryan PR, Delhaize E, Matsumoto H, Yamamoto Y (2007) The membrane topology of ALMT1, an aluminum-activated malate transport protein in wheat (Triticum aestivum). Plant Signal Behav 2(6):467–472PubMedPubMedCentralCrossRefGoogle Scholar
  89. 89.
    Mumm P, Imes D, Martinoia E, Al-Rasheid KA, Geiger D, Marten I, Hedrich R (2013) C-terminus-mediated voltage gating of Arabidopsis guard cell anion channel QUAC1. Mol Plant 6(5):1550–1563PubMedCrossRefGoogle Scholar
  90. 90.
    Zhang J, Baetz U, Krügel U, Martinoia E, De Angeli A (2013) Identification of a probable pore-forming domain in the multimeric vacuolar anion channel AtALMT9. Plant Physiol 163(2):830–843PubMedPubMedCentralCrossRefGoogle Scholar
  91. 91.
    Smith GB, Olsen RW (1994) Identification of a [3H] muscimol photoaffinity substrate in the bovine gamma-aminobutyric acid A receptor alpha subunit. J Biol Chem 269(32):20380–20387PubMedGoogle Scholar
  92. 92.
    Sigel E, Baur R, Kellenberger S, Malherbe P (1992) Point mutations affecting antagonist affinity and agonist dependent gating of GABAA receptor channels. EMBO J 11(6):2017PubMedPubMedCentralGoogle Scholar
  93. 93.
    Szczot M, Kisiel M, Czyzewska MM, Mozrzymas JW (2014) α1F64 Residue at GABAA receptor binding site is involved in gating by influencing the receptor flipping transitions. J Neurosci 34(9):3193–3209PubMedCrossRefGoogle Scholar
  94. 94.
    de Ruijter NC, Malhó R (2000) F-box proteins in Arabidopsis. Cell 5(11):1360–1385. doi:10.1016/S1360-1385(00)01769-6 Google Scholar
  95. 95.
    Lamberti G, Gügel IL, Meurer J, Soll J, Schwenkert S (2011) The cytosolic kinases STY8, STY17, and STY46 are involved in chloroplast differentiation in Arabidopsis. Plant Physiol 157(1):70–85PubMedPubMedCentralCrossRefGoogle Scholar
  96. 96.
    Marks DS, Colwell LJ, Sheridan R, Hopf TA, Pagnani A, Zecchina R, Sander C (2011) Protein 3D structure computed from evolutionary sequence variation. PLoS One 6(12):e28766PubMedPubMedCentralCrossRefGoogle Scholar
  97. 97.
    Hopf TA, Colwell LJ, Sheridan R, Rost B, Sander C, Marks DS (2012) Three-dimensional structures of membrane proteins from genomic sequencing. Cell 149(7):1607–1621PubMedPubMedCentralCrossRefGoogle Scholar
  98. 98.
    Marks DS, Hopf TA, Sander C (2012) Protein structure prediction from sequence variation. Nat Biotechnol 30(11):1072–1080PubMedPubMedCentralCrossRefGoogle Scholar
  99. 99.
    Meier J, Vannier C, Serge A, Triller A, Choquet D (2001) Fast and reversible trapping of surface glycine receptors by gephyrin. Nat Neurosci 4(3):253–260PubMedCrossRefGoogle Scholar
  100. 100.
    Borgdorff AJ, Choquet D (2002) Regulation of AMPA receptor lateral movements. Nature 417(6889):649–653PubMedCrossRefGoogle Scholar
  101. 101.
    Perez-Velazquez JL, Angelides KJ (1993) Assembly of GABAA receptor subunits determines sorting and localization in polarized cells. Nature 361:457–460. doi:10.1038/361457a0 PubMedCrossRefGoogle Scholar
  102. 102.
    Barnes EM (2000) Intracellular trafficking of GABAA receptors. Life Sci 66(12):1063–1070PubMedCrossRefGoogle Scholar
  103. 103.
    Kittler JT, Moss SJ (2003) Modulation of GABAA receptor activity by phosphorylation and receptor trafficking: implications for the efficacy of synaptic inhibition. Curr Opin Chem Biol 13(3):341–347Google Scholar
  104. 104.
    Jalilian Tehrani MH, Barnes EM (1993) Identification of GABAA/benzodiazepine receptors on clathrin-coated vesicles from rat rrain. J Neurochem 60(5):1755–1761CrossRefGoogle Scholar
  105. 105.
    Kittler JT, Delmas P, Jovanovic JN, Brown DA, Smart TG, Moss SJ (2000) Constitutive endocytosis of GABAA receptors by an association with the adaptin AP2 complex modulates inhibitory synaptic currents in hippocampal neurons. J Neurosci 20(21):7972–7977PubMedGoogle Scholar
  106. 106.
    Herring D, Huang R, Singh M, Robinson LC, Dillon GH, Leidenheimer NJ (2003) Constitutive GABAA receptor endocytosis is dynamin-mediated and dependent on a dileucine AP2 adaptin-binding motif within the β2 subunit of the receptor. J Biol Chem 278(26):24046–24052PubMedCrossRefGoogle Scholar
  107. 107.
    Tehrani MHJ, Barnes EM (1991) Agonist-dependent internalization of γ-aminobutyric acid A/benzodiazepine receptors in chick cortical neurons. J Neurochem 57(4):1307–1312PubMedCrossRefGoogle Scholar
  108. 108.
    Calkin PA, Baumgartner BJ, Barnes EM (1994) Agonist administration in ovo down-regulates cerebellar GABAA receptors in the chick embryo. Mol Brain Res 26(1):18–25PubMedCrossRefGoogle Scholar
  109. 109.
    Johnston GA (1996) GABAA receptor pharmacology. Pharmacol Ther 69(3):173–198PubMedCrossRefGoogle Scholar
  110. 110.
    Johnston GA, Hanrahan JR, Chebib M, Duke RK, Mewett KN (2006) Modulation of ionotropic GABA receptors by natural products of plant origin. Adv Pharmacol 54:285PubMedCrossRefGoogle Scholar
  111. 111.
    Grant SM, Heel RC (1991) Vigabatrin. Drugs 41(6):889–926PubMedCrossRefGoogle Scholar
  112. 112.
    Katoh J, Taniguchi H, Ogura M, Kasuga M, Okada Y (1995) A convulsant, 3-mercaptopropionic acid, decreases the level of GABA and GAD in rat pancreatic islets and brain. Experientia 51(3):217–219PubMedCrossRefGoogle Scholar
  113. 113.
    Barker JL, Mathers DA (1981) GABA analogues activate channels of different duration on cultured mouse spinal neurons. Science 212(4492):358–361PubMedCrossRefGoogle Scholar
  114. 114.
    Jackson MB, Lecar H, Mathers DA, Barker JL (1982) Single channel currents activated by gamma-aminobutyric acid, muscimol, and (−)-pentobarbital in cultured mouse spinal neurons. J Neurosci 2(7):889–894PubMedGoogle Scholar
  115. 115.
    Khawaled R, Bruening-Wright A, Adelman JP, Maylie J (1999) Bicuculline block of small-conductance calcium-activated potassium channels. Pflügers Archiv 438(3):314–321PubMedCrossRefGoogle Scholar
  116. 116.
    Barker J, McBurney R, Mathers D (1983) Convulsant-induced depression of amino acid responses in cultured mouse spinal neurones studied under voltage clamp. Br J Pharmacol 80(4):619–629PubMedPubMedCentralCrossRefGoogle Scholar
  117. 117.
    Crawley J, Goodwin FK (1980) Preliminary report of a simple animal behavior model for the anxiolytic effects of benzodiazepines. Pharmacol Biochem Behav 13(2):167–170PubMedCrossRefGoogle Scholar
  118. 118.
    Hoffman E, Warren E (1993) Flumazenil: a benzodiazepine antagonist. Clin Pharm 12(9):641–656 (quiz 699–701) PubMedGoogle Scholar
  119. 119.
    Bowden K, Drysdale A (1965) A novel constituent of Amanitamuscaria. Tetrahedron Lett 6(12):727–728CrossRefGoogle Scholar
  120. 120.
    Nayak P, Chatterjee A (2001) Effects of aluminium exposure on brain glutamate and GABA systems: an experimental study in rats. Food Chem Toxicol 39(12):1285–1289PubMedCrossRefGoogle Scholar
  121. 121.
    Flaten TP, Alfrey AC, Birchall JD, Savory J, Yokel RA (1996) Status and future concerns of clinical and environmental aluminum toxicology. J Toxicol Environ Health A 48(6):527–542CrossRefGoogle Scholar
  122. 122.
    Organisation WH (1997) Environment health criteria 194. Aluminium. WHO, GenevaGoogle Scholar
  123. 123.
    Kochian LV (1995) Cellular mechanisms of aluminum toxicity and resistance in plants. Annu Rev Plant Biol 46(1):237–260CrossRefGoogle Scholar
  124. 124.
    Delhaize E, Ryan PR (1995) Aluminum toxicity and tolerance in plants. Plant Physiol 107(2):315PubMedPubMedCentralCrossRefGoogle Scholar
  125. 125.
    Kochian LV, Pineros MA, Hoekenga OA (2005) The physiology, genetics and molecular biology of plant aluminum resistance and toxicity. Root physiology: from gene to function. Springer, New York, pp 175–195CrossRefGoogle Scholar
  126. 126.
    Alfrey AC, LeGendre GR, Kaehny WD (1976) The dialysis encephalopathy syndrome: possible aluminum intoxication. N Engl J Med 294(4):184–188PubMedCrossRefGoogle Scholar
  127. 127.
    Berlyne G (1989) Dialysis in the third world. Nephron 53(1):1CrossRefGoogle Scholar
  128. 128.
    Bolla KI, Briefel G, Spector D, Schwartz BS, Wieler L, Herron J, Gimenez L (1992) Neurocognitive effects of aluminum. Arch Neurol 49(10):1021–1026PubMedCrossRefGoogle Scholar
  129. 129.
    Trombley PQ (1998) Selective modulation of GABAA receptors by aluminum. J Neurophysiol 80(2):755–761PubMedGoogle Scholar
  130. 130.
    Horst W, Wagner A, Marschner H (1983) Effect of aluminium on root growth, cell-division rate and mineral element contents in roots of Vigna unguiculata genotypes. Zeitschrift für Pflanzenphysiologie 109(2):95–103CrossRefGoogle Scholar
  131. 131.
    Ryan P, Delhaize E, Jones D (2001) Function and mechanism of organic anion exudation from plant roots. Annu Rev Plant Biol 52(1):527–560CrossRefGoogle Scholar
  132. 132.
    Čiamporová M (2002) Morphological and structural responses of plant roots to aluminium at organ, tissue, and cellular levels. Biol Plantarum 45(2):161–171CrossRefGoogle Scholar
  133. 133.
    Platt B, Büsselberg D (1994) Actions of aluminum on voltage-activated calcium channel currents. Cell Mol Neurobiol 14(6):819–829PubMedCrossRefGoogle Scholar
  134. 134.
    Platt B, Haas H, Büsselberg D (1994) Aluminium reduces glutamate-activated currents of rat hippocampal neurones. NeuroReport 5(17):2329–2332PubMedCrossRefGoogle Scholar
  135. 135.
    Candy J, Klinowski J, Perry R, Perry E, Fairbairn A, Oakley A, Carpenter T, Atack J, Blessed G, Edwardson J (1986) Aluminosilicates and senile plaque formation in Alzheimer’s disease. Lancet 327(8477):354–356CrossRefGoogle Scholar
  136. 136.
    Perl DP, Gajdusek DC, Garruto RM, Yanagihara RT, Gibbs CJ (1982) Intraneuronal aluminum accumulation in amyotrophic lateral sclerosis and Parkinsonism-dementia of Guam. Science 217(4564):1053–1055PubMedCrossRefGoogle Scholar
  137. 137.
    El-Rahman SSA (2003) Neuropathology of aluminum toxicity in rats (glutamate and GABA impairment). Pharmacol Res 47(3):189–194PubMedCrossRefGoogle Scholar
  138. 138.
    Ma JF, Ryan PR, Delhaize E (2001) Aluminium tolerance in plants and the complexing role of organic acids. Trends Plant Sci 6(6):273–278PubMedCrossRefGoogle Scholar
  139. 139.
    Ryan PR, Tyerman SD, Sasaki T, Furuichi T, Yamamoto Y, Zhang W, Delhaize E (2011) The identification of aluminium-resistance genes provides opportunities for enhancing crop production on acid soils. J Exp Bot 62(1):9–20PubMedCrossRefGoogle Scholar
  140. 140.
    Michaeli S, Fait A, Lagor K, Nunes-Nesi A, Grillich N, Yellin A, Bar D, Khan M, Fernie AR, Turano FJ (2011) A mitochondrial GABA permease connects the GABA shunt and the TCA cycle, and is essential for normal carbon metabolism. Plant J 67(3):485–498PubMedCrossRefGoogle Scholar
  141. 141.
    Meyer A, Eskandari S, Grallath S, Rentsch D (2006) AtGAT1, a high affinity transporter for γ-aminobutyric acid in Arabidopsis thaliana. J Biol Chem 281(11):7197–7204PubMedPubMedCentralCrossRefGoogle Scholar
  142. 142.
    Cordeiro J, Silva V, Oliveira C, Goncalves P (2003) Aluminium-induced impairment of Ca2+ modulatory action on GABA transport in brain cortex nerve terminals. J Inorg Biochem 97(1):132–142PubMedCrossRefGoogle Scholar
  143. 143.
    Ohta T (1989) Role of gene duplication in evolution. Genome 31(1):304–310PubMedCrossRefGoogle Scholar
  144. 144.
    Otto SP, Whitton J (2000) Polyploid incidence and evolution. Annu Rev Genet 34(1):401–437PubMedCrossRefGoogle Scholar
  145. 145.
    Taylor JS, Raes J (2004) Duplication and divergence: the evolution of new genes and old ideas. Annu Rev Genet 38:615–643PubMedCrossRefGoogle Scholar
  146. 146.
    Shimeld SM, Holland PW (2000) Vertebrate innovations. Proc Natl Acad Sci USA 97(9):4449–4452PubMedPubMedCentralCrossRefGoogle Scholar
  147. 147.
    Ortells MO, Lunt GG (1995) Evolutionary history of the ligand-gated ion-channel superfamily of receptors. Trends Neurosci 18(3):121–127PubMedCrossRefGoogle Scholar
  148. 148.
    Russek SJ (1999) Evolution of GABA A receptor diversity in the human genome. Gene 227(2):213–222PubMedCrossRefGoogle Scholar
  149. 149.
    Darlison MG, Pahal I, Thode C (2005) Consequences of the evolution of the GABAA receptor gene family. Cell Mol Neurobiol 25(3–4):607–624PubMedCrossRefGoogle Scholar
  150. 150.
    Martyniuk CJ, Aris-Brosou S, Drouin G, Cahn J, Trudeau VL (2007) Early evolution of ionotropic GABA receptors and selective regimes acting on the mammalian-specific theta and epsilon subunits. PLoS One 2(9):e894PubMedPubMedCentralCrossRefGoogle Scholar
  151. 151.
    Wendel JF (2000) Genome evolution in polyploids. Plant molecular evolution. Springer, New York, pp 225–249CrossRefGoogle Scholar
  152. 152.
    Ku H-M, Vision T, Liu J, Tanksley SD (2000) Comparing sequenced segments of the tomato and Arabidopsis genomes: large-scale duplication followed by selective gene loss creates a network of synteny. Proc Natl Acad Sci USA 97(16):9121–9126PubMedPubMedCentralCrossRefGoogle Scholar
  153. 153.
    Vision TJ, Brown DG, Tanksley SD (2000) The origins of genomic duplications in Arabidopsis. Science 290(5499):2114–2117PubMedCrossRefGoogle Scholar
  154. 154.
    Bowers JE, Chapman BA, Rong J, Paterson AH (2003) Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events. Nature 422(6930):433–438PubMedCrossRefGoogle Scholar
  155. 155.
    Soltis DE, Soltis PS, Endress PK, Chase MW (2005) Phylogeny and evolution of angiosperms. Sinauer Associates IncorporatedGoogle Scholar
  156. 156.
    Blanc G, Agarkova I, Grimwood J, Kuo A, Brueggeman A, Dunigan DD, Gurnon J, Ladunga I, Lindquist E, Lucas S (2012) The genome of the polar eukaryotic microalga Coccomyxa subellipsoidea reveals traits of cold adaptation. Genome Biol 13(5):R39PubMedPubMedCentralCrossRefGoogle Scholar
  157. 157.
    Marchler-Bauer A, Derbyshire MK, Gonzales NR, Lu S, Chitsaz F, Geer LY, Geer RC, He J, Gwadz M, Hurwitz DI (2014) CDD: NCBI’s conserved domain database. Nucleic Acids Res:gku1221Google Scholar
  158. 158.
    Baum G, Lev-Yadun S, Fridmann Y, Arazi T, Katsnelson H, Zik M, Fromm H (1996) Calmodulin binding to glutamate decarboxylase is required for regulation of glutamate and GABA metabolism and normal development in plants. EMBO J 15(12):2988–2996PubMedPubMedCentralGoogle Scholar
  159. 159.
    Bown AW, Zhang G (2000) Mechanical stimulation, 4-aminobutyric acid (GABA) synthesis, and growth inhibition in soybean hypocotyl tissue. Can J Bot 78(1):119–123Google Scholar
  160. 160.
    Kathiresan A, Tung P, Chinnappa CC, Reid DM (1997) gamma-aminobutyric acid stimulates ethylene biosynthesis in sunflower. Plant Physiol 115(1):129–135. doi:10.1104/pp.115.1.129 PubMedPubMedCentralCrossRefGoogle Scholar
  161. 161.
    Renault H, Roussel V, El Amrani A, Arzel M, Renault D, Bouchereau A, Deleu C (2010) The Arabidopsis pop2-1 mutant reveals the involvement of GABA transaminase in salt stress tolerance. BMC Plant Biol 10(1):20PubMedPubMedCentralCrossRefGoogle Scholar
  162. 162.
    Renault H, El Amrani A, Palanivelu R, Updegraff EP, Yu A, Renou JP, Preuss D, Bouchereau A, Deleu C (2011) GABA accumulation causes cell elongation defects and a decrease in expression of genes encoding secreted and cell wall-related proteins in Arabidopsis thaliana. Plant Cell Physiol 52(5):894–908. doi:10.1093/pcp/pcr041 PubMedPubMedCentralCrossRefGoogle Scholar
  163. 163.
    Michaeli S, Fromm H (2015) Closing the loop on the GABA shunt in plants: are GABA metabolism and signaling entwined? Front Plant Sci 6Google Scholar
  164. 164.
    Beuve N, Rispail N, Laine P, Cliquet JB, Ourry A, Le Deunff E (2004) Putative role of γ-aminobutyric acid (GABA) as a long-distance signal in up-regulation of nitrate uptake in Brassica napus L. Plant Cell Environ 27(8):1035–1046CrossRefGoogle Scholar
  165. 165.
    Barbosa JM, Singh NK, Cherry JH, Locy RD (2000) GABA increases the rate of nitrate uptake and utilization in Arabidopsis roots. Plant Biol 2000:133Google Scholar
  166. 166.
    Barbosa JM, Singh NK, Cherry JH, Locy RD (2010) Nitrate uptake and utilization is modulated by exogenous gamma-aminobutyric acid in Arabidopsis thaliana seedlings. Plant Physiol Biochem 48(6):443–450. doi:10.1016/j.plaphy.2010.01.020 PubMedCrossRefGoogle Scholar
  167. 167.
    Jin H, Dilworth M, Glenn A (1990) 4-Aminobutyrate is not available to bacteroids of cowpea Rhizobium MNF2030 in snake bean nodules. Arch Microbiol 153(5):455–462CrossRefGoogle Scholar
  168. 168.
    Miller R, McRae D, Joy K (1991) Glutamate and gamma-aminobutyrate metabolism in isolated Rhizobium meliloti bacteroids. Mol Plant-Microbe Interact 4:37–45CrossRefGoogle Scholar
  169. 169.
    Sulieman S (2011) Does GABA increase the efficiency of symbiotic N2 fixation in legumes? Plant Signal Behav 6(1):32–36PubMedPubMedCentralCrossRefGoogle Scholar
  170. 170.
    Diaz C, Lemaître T, Christ A, Azzopardi M, Kato Y, Sato F, Morot-Gaudry J-F, Le Dily F, Masclaux-Daubresse C (2008) Nitrogen recycling and remobilization are differentially controlled by leaf senescence and development stage in Arabidopsis under low nitrogen nutrition. Plant Physiol 147(3):1437–1449PubMedPubMedCentralCrossRefGoogle Scholar
  171. 171.
    Allan WL, Shelp BJ (2006) A potential role for gamma-hydroxybuty rate production in redox homeostasis. Plant Biol 2006:219Google Scholar
  172. 172.
    Ling Y, Chen T, Jing Y, Fan L, Wan Y, Lin J (2013) γ-Aminobutyric acid (GABA) homeostasis regulates pollen germination and polarized growth in Picea wilsonii. Planta 238(5):831–843PubMedCrossRefGoogle Scholar
  173. 173.
    Frietsch S, Wang Y-F, Sladek C, Poulsen LR, Romanowsky SM, Schroeder JI, Harper JF (2007) A cyclic nucleotide-gated channel is essential for polarized tip growth of pollen. Proc Natl Acad Sci USA 104(36):14531–14536PubMedPubMedCentralCrossRefGoogle Scholar
  174. 174.
    Schiøtt M, Romanowsky SM, Bækgaard L, Jakobsen MK, Palmgren MG, Harper JF (2004) A plant plasma membrane Ca2+ pump is required for normal pollen tube growth and fertilization. Proc Natl Acad Sci USA 101(25):9502–9507PubMedPubMedCentralCrossRefGoogle Scholar
  175. 175.
    Song L-F, Zou J-J, Zhang W-Z, Wu W-H, Wang Y (2009) Ion transporters involved in pollen germination and pollen tube tip-growth. Plant Signal Behav 4(12):1193–1195PubMedPubMedCentralCrossRefGoogle Scholar
  176. 176.
    Saikusa T, Horino T, Mori Y (1994) Distribution of free amino acids in the rice kernel and kernel fractions and the effect of water soaking on the distribution. J Agric Food Chem 42(5):1122–1125CrossRefGoogle Scholar
  177. 177.
    Dluzniewska P, Gessler A, Kopriva S, Strnad M, Novak O, Dietrich H, Rennenberg H (2006) Exogenous supply of glutamine and active cytokinin to the roots reduces NO3 uptake rates in poplar. Plant Cell Environ 29(7):1284–1297PubMedCrossRefGoogle Scholar
  178. 178.
    Mazzucotelli E, Tartari A, Cattivelli L, Forlani G (2006) Metabolism of gamma-aminobutyric acid during cold acclimation and freezing and its relationship to frost tolerance in barley and wheat. J Exp Bot 57(14):3755–3766. doi:10.1093/jxb/erl141 PubMedCrossRefGoogle Scholar
  179. 179.
    Vannini C, Iriti M, Bracale M, Locatelli F, Faoro F, Croce P, Pirona R, Di Maro A, Coraggio I, Genga A (2006) The ectopic expression of the rice Osmyb4 gene in Arabidopsis increases tolerance to abiotic, environmental and biotic stresses. Physiol Mol Plant Pathol 69(1):26–42CrossRefGoogle Scholar
  180. 180.
    Xing SG, Jun YB, Hau ZW, Liang LY (2007) Higher accumulation of γ-aminobutyric acid induced by salt stress through stimulating the activity of diamine oxidases in Glycine max (L.) Merr. roots. Plant Physiol Biochem 45(8):560–566PubMedCrossRefGoogle Scholar
  181. 181.
    Bor M, Seckin B, Ozgur R, Yilmaz O, Ozdemir F, Turkan I (2009) Comparative effects of drought, salt, heavy metal and heat stresses on gamma-aminobutryric acid levels of sesame (Sesamum indicum L.). Acta Physiol Plant 31(3):655–659. doi:10.1007/s11738-008-0255-2 CrossRefGoogle Scholar
  182. 182.
    Patterson JH, Newbigin E, Tester M, Bacic A, Roessner U (2009) Metabolic responses to salt stress of barley (Hordeum vulgare L.) cultivars, Sahara and Clipper, which differ in salinity tolerance. J Exp Bot:erp243Google Scholar
  183. 183.
    Al-Quraan NA, Locy RD, Singh NK (2011) Implications of paraquat and hydrogen peroxide-induced oxidative stress treatments on the GABA shunt pathway in Arabidopsis thaliana calmodulin mutants. Plant Biotechnol Rep 5(3):225–234CrossRefGoogle Scholar
  184. 184.
    Akçay N, Bor M, Karabudak T, Özdemir F, Türkan I (2012) Contribution of gamma amino butyric acid (GABA) to salt stress responses of Nicotiana sylvestris CMSII mutant and wild type plants. J Plant Physiol 169(5):452–458PubMedCrossRefGoogle Scholar
  185. 185.
    Guo Y, Yang R, Chen H, Song Y, Gu Z (2012) Accumulation of γ-aminobutyric acid in germinated soybean (Glycine max L.) in relation to glutamate decarboxylase and diamine oxidase activity induced by additives under hypoxia. Eur Food Res Technol 234(4):679–687Google Scholar
  186. 186.
    Vergara R, Parada F, Rubio S, Perez FJ (2012) Hypoxia induces H2O2 production and activates antioxidant defence system in grapevine buds through mediation of H2O2 and ethylene. J Exp Bot 63(11):4123–4131. doi:10.1093/jxb/ers094 PubMedPubMedCentralCrossRefGoogle Scholar
  187. 187.
    Nayyar H, Kaur R, Kaur S, Singh R (2014) γ-Aminobutyric acid (GABA) imparts partial protection from heat stress injury to rice seedlings by improving leaf turgor and upregulating osmoprotectants and antioxidants. J Plant Growth Reg 33(2):408–419CrossRefGoogle Scholar
  188. 188.
    Mekonnen DW, Flügge U-I, Ludewig F (2016) Gamma-aminobutyric acid depletion affects stomata closure and drought tolerance of Arabidopsis thaliana. Plant Sci 245:25–34PubMedCrossRefGoogle Scholar
  189. 189.
    Fougere F, Le Rudulier D, Streeter JG (1991) Effects of salt stress on amino acid, organic acid, and carbohydrate composition of roots, bacteroids, and cytosol of alfalfa (Medicago sativa L.). Plant Physiol 96(4):1228–1236PubMedPubMedCentralCrossRefGoogle Scholar
  190. 190.
    Bolarín MC, Santa-Cruz A, Cayuela E, Perez-Alfocea F (1995) Short-term solute changes in leaves and roots of cultivated and wild tomato seedlings under salinity. J Plant Physiol 147(3):463–468CrossRefGoogle Scholar
  191. 191.
    Widodo, Patterson JH, Newbigin E, Tester M, Bacic A, Roessner U (2009) Metabolic responses to salt stress of barley (Hordeum vulgare L.) cultivars, Sahara and Clipper, which differ in salinity tolerance. J Exp Bot 60(14):4089–4103. doi:10.1093/jxb/erp243Google Scholar
  192. 192.
    Zhang J, Zhang Y, Du Y, Chen S, Tang H (2011) Dynamic metabonomic responses of tobacco (Nicotiana tabacum) plants to salt stress. J Proteome Res 10(4):1904–1914. doi:10.1021/pr101140n PubMedCrossRefGoogle Scholar
  193. 193.
    Renault H, El Amrani A, Berger A, Mouille G, Soubigou-Taconnat L, Bouchereau A, Deleu C (2013) gamma-Aminobutyric acid transaminase deficiency impairs central carbon metabolism and leads to cell wall defects during salt stress in Arabidopsis roots. Plant Cell Environ 36(5):1009–1018. doi:10.1111/pce.12033 PubMedCrossRefGoogle Scholar
  194. 194.
    Baetz U, Eisenach C, Tohge T, Martinoia E, De Angeli A (2016) Vacuolar chloride fluxes impact ion content and distribution during early salinity stress. Plant Physiol:00183.02016Google Scholar
  195. 195.
    Raggi V (1994) Changes in free amino acids and osmotic adjustment in leaves of water-stressed bean. Physiol Plant 91(3):427–434CrossRefGoogle Scholar
  196. 196.
    Serraj R, Shelp BJ, Sinclair TR (1998) Accumulation of gamma-aminobutyric acid in nodulated soybean in response to drought stress. Physiol Plant 102(1):79–86. doi:10.1034/j.1399-3054.1998.1020111.x CrossRefGoogle Scholar
  197. 197.
    Thompson JF, Stewart CR, Morris CJ (1966) Changes in amino acid content of excised leaves during incubation I. The effect of water content of leaves and atmospheric oxygen level. Plant Physiol 41(10):1578–1584PubMedPubMedCentralCrossRefGoogle Scholar
  198. 198.
    Scholz SS, Reichelt M, Mekonnen DW, Ludewig F, Mithöfer A (2015) Insect herbivory-elicited GABA accumulation in plants is a wound-induced, direct, systemic, and jasmonate-independent defense response. Front Plant Sci 6:1128. doi:10.3389/fpls.2015.01128 PubMedPubMedCentralCrossRefGoogle Scholar
  199. 199.
    Salvatierra A, Pimentel P, Almada R, Hinrichsen P (2016) Exogenous GABA application transiently improves the tolerance to root hypoxia on a sensitive genotype of Prunus rootstock. Environ Exp Bot 125:52–66CrossRefGoogle Scholar
  200. 200.
    Delhaize E, Craig S, Beaton CD, Bennet RJ, Jagadish VC, Randall PJ (1993) Aluminum tolerance in wheat (Triticum aestivum L.)(I. Uptake and distribution of aluminum in root apices). Plant Physiol 103(3):685–693PubMedPubMedCentralCrossRefGoogle Scholar
  201. 201.
    Delhaize E, Ryan PR, Randall PJ (1993) Aluminum tolerance in wheat (Triticum aestivum L.) (II. Aluminum-stimulated excretion of malic acid from root apices). Plant Physiol 103(3):695–702PubMedPubMedCentralCrossRefGoogle Scholar
  202. 202.
    Sasaki TYY, Ezaki B, Katsuhara M, Ahn SJ, Ryan PR, Delhaize E, Matsumoto H (2004) A wheat gene encoding an aluminium-activated malate transporter. Plant J 37:645–653PubMedCrossRefGoogle Scholar
  203. 203.
    Warren C (2015) Wheat roots efflux a diverse array of organic N compounds and are highly proficient at their recapture. Plant Soil. doi:10.1007/s11104-015-2612-4 Google Scholar
  204. 204.
    Badri DV, De-la-Peña C, Lei Z, Manter DK, Chaparro JM, Guimarães RL, Sumner LW, Vivanco JM (2012) Root secreted metabolites and proteins are involved in the early events of plant-plant recognition prior to competition. PLoS One 7(10):e46640PubMedPubMedCentralCrossRefGoogle Scholar
  205. 205.
    Fourcroy P, Sisó-Terraza P, Sudre D, Savirón M, Reyt G, Gaymard F, Abadía A, Abadia J, Álvarez-Fernández A, Briat JF (2014) Involvement of the ABCG37 transporter in secretion of scopoletin and derivatives by Arabidopsis roots in response to iron deficiency. New Phytol 201(1):155–167PubMedCrossRefGoogle Scholar
  206. 206.
    Solomon PS, Oliver RP (2001) The nitrogen content of the tomato leaf apoplast increases during infection by Cladosporium fulvum. Planta 213(2):241–249PubMedCrossRefGoogle Scholar
  207. 207.
    McLean MD, Yevtushenko DP, Deschene A, Van Cauwenberghe OR, Makhmoudova A, Potter JW, Bown AW, Shelp BJ (2003) Overexpression of glutamate decarboxylase in transgenic tobacco plants confers resistance to the northern root-knot nematode. Mol Breed 11(4):277–285CrossRefGoogle Scholar
  208. 208.
    Bown AW, MacGregor KB, Shelp BJ (2006) Gamma-aminobutyrate: defense against invertebrate pests? Trends Plant Sci 11(9):424–427PubMedCrossRefGoogle Scholar
  209. 209.
    Takahashi H, Matsumura H, Kawai-Yamada M, Uchimiya H (2008) The cell death factor, cell wall elicitor of rice blast fungus (Magnaporthe grisea) causes metabolic alterations including GABA shunt in rice cultured cells. Plant Signal Behav 3(11):945–953PubMedPubMedCentralCrossRefGoogle Scholar
  210. 210.
    Park DH, Mirabella R, Bronstein PA, Preston GM, Haring MA, Lim CK, Collmer A, Schuurink RC (2010) Mutations in gamma-aminobutyric acid (GABA) transaminase genes in plants or Pseudomonas syringae reduce bacterial virulence. Plant J 64(2):318–330. doi:10.1111/j.1365-313X.2010.04327.x PubMedCrossRefGoogle Scholar
  211. 211.
    Bown AW, Hall DE, MacGregor KB (2002) Insect footsteps on leaves stimulate the accumulation of 4-aminobutyrate and can be visualized through increased chlorophyll fluorescence and superoxide production. Plant Physiol 129(4):1430–1434PubMedPubMedCentralCrossRefGoogle Scholar
  212. 212.
    Irving S, Osborne M, Wilson R (1976) Virtual absence of L-glutamate from the haemoplasm of arthropod blood. Nature 263:431–433PubMedCrossRefGoogle Scholar
  213. 213.
    Irving S, Wilson R, Osborne M (1979) Studies on l-glutamate in insect haemolymph. Physiol Entomol 4:231–240CrossRefGoogle Scholar
  214. 214.
    Sattelle DB (1990) GABA receptors of insects. Adv Insect Physiol 22:1–113CrossRefGoogle Scholar
  215. 215.
    von Keyserlingk HC, Willis RJ (1992) The GABA activated Cl-channel in insects as target for insecticide action: a physiological study. Neurotox’91. Springer, New York, pp 79–104Google Scholar
  216. 216.
    Casida JE (1993) Insecticide action at the GABA-gated chloride channel: recognition, progress, and prospects. Arch Insect Biochem Physiol 22(1–2):13–23PubMedCrossRefGoogle Scholar
  217. 217.
    Seifi HS, Curvers K, De Vleesschauwer D, Delaere I, Aziz A, Hofte M (2013) Concurrent overactivation of the cytosolic glutamine synthetase and the GABA shunt in the ABA-deficient sitiens mutant of tomato leads to resistance against Botrytis cinerea. New Phytol 199(2):490–504. doi:10.1111/nph.12283 PubMedCrossRefGoogle Scholar
  218. 218.
    Chevrot R, Rosen R, Haudecoeur E, Cirou A, Shelp BJ, Ron E, Faure D (2006) GABA controls the level of quorum-sensing signal in Agrobacterium tumefaciens. Proc Natl Acad Sci USA 103(19):7460–7464. doi:10.1073/pnas.0600313103 PubMedPubMedCentralCrossRefGoogle Scholar
  219. 219.
    Yuan ZC, Haudecoeur E, Faure D, Kerr KF, Nester EW (2008) Comparative transcriptome analysis of Agrobacterium tumefaciens in response to plant signal salicylic acid, indole-3-acetic acid and gamma-amino butyric acid reveals signalling cross-talk and Agrobacterium-plant co-evolution. Cell Microbiol 10(11):2339–2354. doi:10.1111/j.1462-5822.2008.01215.x PubMedCrossRefGoogle Scholar
  220. 220.
    Planamente S, Mondy S, Hommais F, Vigouroux A, Morera S, Faure D (2012) Structural basis for selective GABA binding in bacterial pathogens. Mol Microbiol 86(5):1085–1099. doi:10.1111/mmi.12043 PubMedCrossRefGoogle Scholar
  221. 221.
    Planamente S, Vigouroux A, Mondy S, Nicaise M, Faure D, Moréra S (2010) A conserved mechanism of GABA binding and antagonism is revealed by structure-function analysis of the periplasmic binding protein Atu2422 in Agrobacterium tumefaciens. J Biol Chem 285(39):30294–30303PubMedPubMedCentralCrossRefGoogle Scholar
  222. 222.
    Busov V, Meilan R, Pearce DW, Rood SB, Ma CP, Tschaplinski TJ, Strauss SH (2006) Transgenic modification of gai or rgl1 causes dwarfing and alters gibberellins, root growth, and metabolite profiles in Populus. Planta 224(2):288–299. doi:10.1007/s00425-005-0213-9 PubMedCrossRefGoogle Scholar
  223. 223.
    Urano K, Maruyama K, Ogata Y, Morishita Y, Takeda M, Sakurai N, Suzuki H, Saito K, Shibata D, Kobayashi M, Yamaguchi-Shinozaki K, Shinozaki K (2009) Characterization of the ABA-regulated global responses to dehydration in Arabidopsis by metabolomics. Plant J 57(6):1065–1078. doi:10.1111/j.1365-313X.2008.03748.x PubMedCrossRefGoogle Scholar
  224. 224.
    Merewitz EB, Du H, Yu W, Liu Y, Gianfagna T, Huang B (2012) Elevated cytokinin content in ipt transgenic creeping bentgrass promotes drought tolerance through regulating metabolite accumulation. J Exp Bot 63(3):1315–1328. doi:10.1093/jxb/err372 PubMedCrossRefGoogle Scholar
  225. 225.
    Jespersen D, Yu JJ, Huang BR (2015) Metabolite responses to exogenous application of nitrogen, cytokinin, and ethylene inhibitors in relation to heat-induced senescence in Creeping Bentgrass. PLoS One. doi:10.1371/journal.pone.0123744 Google Scholar
  226. 226.
    Sweetlove LJ, Heazlewood JL, Herald V, Holtzapffel R, Day DA, Leaver CJ, Millar AH (2002) The impact of oxidative stress on Arabidopsis mitochondria. Plant J 32(6):891–904. doi:10.1046/j.1365-313X.2002.01474.x PubMedCrossRefGoogle Scholar
  227. 227.
    Luo F, Wang Q, Yin C, Ge Y, Hu F, Huang B, Zhou H, Bao G, Wang B, Lu R, Li Z (2015) Differential metabolic responses of Beauveria bassiana cultured in pupae extracts, root exudates and its interactions with insect and plant. J Invertebr Pathol 130:154–164. doi:10.1016/j.jip.2015.01.003 PubMedCrossRefGoogle Scholar
  228. 228.
    Janzen DJ, Allen LJ, MacGregor KB, Bown AW (2001) Cytosolic acidification and gamma-aminobutyric acid synthesis during the oxidative burst in isolated Asparagus sprengeri mesophyll cells. Can J Bot 79(4):438–443Google Scholar
  229. 229.
    Kathiresan A, Miranda J, Chinnappa CC, Reid DM (1998) gamma-aminobutyric acid promotes stem elongation in Stellaria longipes: the role of ethylene. Plant Growth Regul 26(2):131–137. doi:10.1023/a:1006107815064 CrossRefGoogle Scholar
  230. 230.
    Shi SQ, Shi Z, Jiang ZP, Qi LW, Sun XM, Li CX, Liu JF, Xiao WF, Zhang SG (2010) Effects of exogenous GABA on gene expression of Caragana intermedia roots under NaCl stress: regulatory roles for H2O2 and ethylene production. Plant Cell Environ 33(2):149–162. doi:10.1111/j.1365-3040.2009.02065.x PubMedCrossRefGoogle Scholar
  231. 231.
    Tian Q, Zhang X, Ramesh S, Gilliham M, Tyerman S, Zhang W (2014) Ethylene negatively regulates aluminium-induced malate efflux from wheat roots and tobacco cells transformed with TaALMT1. J Exp Bot 65(9):2415–2426. doi:10.1093/jxb/eru123 PubMedPubMedCentralCrossRefGoogle Scholar
  232. 232.
    Luchi S, Kobayashi M, Taji T, Naramoto M, Seki M, Kato T, Tabata S, Kakubari Y, Yamaguchi-Shinozaki K, Shinozaki K (2001) Regulation of drought tolerance by gene manipulation of 9-cis-epoxycarotenoid dioxygenase, a key enzyme in abscisci acid biosynthesis in Arabidopsis. Plant J 27:325–333CrossRefGoogle Scholar
  233. 233.
    Schwartz SH, LeonKloosterziel KM, Koornneef M, Zeevaart JAD (1997) Biochemical characterization of the aba2 and aba3 mutants in Arabidopsis thaliana. Plant Physiol 114(1):161–166. doi:10.1104/pp.114.1.161 PubMedPubMedCentralCrossRefGoogle Scholar
  234. 234.
    Cao S, Cai Y, Yang Z, Zheng Y (2012) MeJA induces chilling tolerance in loquat fruit by regulating proline and γ-aminobutyric acid contents. Food Chem Toxicol 133(4):1466–1470CrossRefGoogle Scholar
  235. 235.
    Scholz SS, Vadassery J, Heyer M, Reichelt M, Bender KW, Snedden WA, Boland W, Mithöfer A (2014) Mutation of the Arabidopsis calmodulin-like protein CML37 deregulates the jasmonate pathway and enhances susceptibility to herbivory. Mol Plant 7(12):1712–1726PubMedCrossRefGoogle Scholar
  236. 236.
    Fonseca S, Chini A, Hamberg M, Adie B, Porzel A, Kramell R, Miersch O, Wasternack C, Solano R (2009) (+)-7-iso-Jasmonoyl-l-isoleucine is the endogenous bioactive jasmonate. Nat Chem Biol 5(5):344–350. doi:10.1038/nchembio.161 PubMedCrossRefGoogle Scholar
  237. 237.
    Smith FA, Raven JA (1979) Intracellular pH and its regulation. Annu Rev Plant Physiol 30(1):289–311CrossRefGoogle Scholar
  238. 238.
    Crawford LA, Bown AW, Breitkreuz KE, Guinel FC (1994) The synthesis of γ-aminobutyric acid in response to treatments reducing cytosolic pH. Plant Physiol 104(3):865–871PubMedPubMedCentralCrossRefGoogle Scholar
  239. 239.
    Carroll AD, Fox GG, Laurie S, Phillips R, Ratcliffe RG, Stewart GR (1994) Ammonium assimilation and the role of γ-aminobutyric acid in pH homeostasis in carrot cell suspensions. Plant Physiol 106(2):513–520PubMedPubMedCentralCrossRefGoogle Scholar
  240. 240.
    Kader MA, Lindberg S (2010) Cytosolic calcium and pH signaling in plants under salinity stress. Plant Signal Behav 5(3):233–238PubMedPubMedCentralCrossRefGoogle Scholar
  241. 241.
    Tournaire-Roux C, Sutka M, Javot H, Gout E, Gerbeau P, Luu D-T, Bligny R, Maurel C (2003) Cytosolic pH regulates root water transport during anoxic stress through gating of aquaporins. Nature 425(6956):393–397PubMedCrossRefGoogle Scholar
  242. 242.
    Meyer S, Scholz-Starke J, De Angeli A, Kovermann P, Burla B, Gambale F, Martinoia E (2011) Malate transport by the vacuolar AtALMT6 channel in guard cells is subject to multiple regulation. Plant J 67(2):247–257PubMedCrossRefGoogle Scholar
  243. 243.
    Snowden CJ, Thomas B, Baxter CJ, Smith JAC, Sweetlove LJ (2015) A tonoplast Glu/Asp/GABA exchanger that affects tomato fruit amino acid composition. Plant J 81(5):651–660PubMedPubMedCentralCrossRefGoogle Scholar
  244. 244.
    Dinant S, Suárez-López P (2012) Multitude of long-distance signal molecules acting via phloem. In: Biocommunication of Plants. Springer, New York, pp 89–121Google Scholar
  245. 245.
    Notaguchi M, Okamoto S (2015) Dynamics of long-distance signaling via plant vascular tissues. Front Plant Sci 6:161PubMedPubMedCentralCrossRefGoogle Scholar
  246. 246.
    Frak E, Millard P, Le Roux X, Guillaumie S, Wendler R (2002) Coupling sap flow velocity and amino acid concentrations as an alternative method to (15)N labeling for quantifying nitrogen remobilization by walnut trees. Plant Physiol 130(2):1043–1053. doi:10.1104/pp.002139 PubMedPubMedCentralCrossRefGoogle Scholar
  247. 247.
    Queiroz HM, Sodek L, Haddad CRB (2012) Effect of salt on the growth and metabolism of Glycine max. Braz Arch Biol Techn 55(6):809–817CrossRefGoogle Scholar
  248. 248.
    Sulieman S, Schulze J (2010) Phloem-derived gamma-aminobutyric acid (GABA) is involved in upregulating nodule N2 fixation efficiency in the model legume Medicago truncatula. Plant, Cell Environ 33(12):2162–2172. doi:10.1111/j.1365-3040.2010.02214.x CrossRefGoogle Scholar
  249. 249.
    Shelp BJ (2012) Does long-distance GABA signaling via the phloem really occur? Botany 90(10):897–900CrossRefGoogle Scholar
  250. 250.
    Masharina A, Reymond L, Maurel D, Umezawa K, Johnsson K (2012) A fluorescent sensor for GABA and synthetic GABAB receptor ligands. J Am Chem Soc 134(46):19026–19034PubMedCrossRefGoogle Scholar
  251. 251.
    Erlander MG, Tillakaratne NJ, Feldblum S, Patel N, Tobin AJ (1991) Two genes encode distinct glutamate decarboxylases. Neuron 7(1):91–100PubMedCrossRefGoogle Scholar
  252. 252.
    Fon EA, Edwards RH (2001) Molecular mechanisms of neurotransmitter release. Muscle Nerve 24(5):581–601PubMedCrossRefGoogle Scholar
  253. 253.
    Cherubini E, Conti F (2001) Generating diversity at GABAergic synapses. Trends Neurosci 24(3):155–162PubMedCrossRefGoogle Scholar
  254. 254.
    Roberts E (1988) The establishment of GABA as a neurotransmitter. GABA and benzodiazepine receptors. CRC Press, Boca RatonGoogle Scholar
  255. 255.
    Corey JL, Guastella J, Davidson N, Lester HA (1994) GABA uptake and release by a mammalian cell line stably expressing a cloned rat brain GABA transporter. Mol Membr Biol 11(1):23–30PubMedCrossRefGoogle Scholar
  256. 256.
    Fenalti G, Law RH, Buckle AM, Langendorf C, Tuck K, Rosado CJ, Faux NG, Mahmood K, Hampe CS, Banga JP (2007) GABA production by glutamic acid decarboxylase is regulated by a dynamic catalytic loop. Nat Struct Mol Biol 14(4):280–286PubMedCrossRefGoogle Scholar
  257. 257.
    Akama K, Takaiwa F (2007) C-terminal extension of rice glutamate decarboxylase (OsGAD2) functions as an autoinhibitory domain and overexpression of a truncated mutant results in the accumulation of extremely high levels of GABA in plant cells. J Exp Bot 58(10):2699–2707. doi:10.1093/jxb/erm120 PubMedCrossRefGoogle Scholar
  258. 258.
    Yu GH, Zou J, Feng J, Peng XB, Wu JY, Wu YL, Palanivelu R, Sun MX (2014) Exogenous gamma-aminobutyric acid (GABA) affects pollen tube growth via modulating putative Ca2+-permeable membrane channels and is coupled to negative regulation on glutamate decarboxylase. J Exp Bot 65(12):3235–3248. doi:10.1093/jxb/eru171 PubMedPubMedCentralCrossRefGoogle Scholar
  259. 259.
    Espinoza C, Degenkolbe T, Caldana C, Zuther E, Leisse A, Willmitzer L, Hincha DK, Hannah MA (2010) Interaction with diurnal and circadian regulation results in dynamic metabolic and transcriptional changes during cold acclimation in Arabidopsis. PLoS One 5(11):e14101PubMedPubMedCentralCrossRefGoogle Scholar
  260. 260.
    Fait A, Fromm H, Walter D, Galili G, Fernie AR (2008) Highway or byway: the metabolic role of the GABA shunt in plants. Trends Plant Sci 13(1):14–19. doi:10.1016/j.tplants.2007.10.005 PubMedCrossRefGoogle Scholar
  261. 261.
    Miyashita Y, Good AG (2008) Contribution of the GABA shunt to hypoxia-induced alanine accumulation in roots of Arabidopsis thaliana. Plant Cell Physiol 49(1):92–102. doi:10.1093/pcp/pcm171 PubMedCrossRefGoogle Scholar
  262. 262.
    Fait A, Yellin A, Fromm H (2005) GABA shunt deficiencies and accumulation of reactive oxygen intermediates: insight from Arabidopsis mutants. FEBS Lett 579(2):415–420. doi:10.1016/j.febslet.2004.12.004 PubMedCrossRefGoogle Scholar
  263. 263.
    Brozoski TJ, Spires TJD, Bauer CA (2007) Vigabatrin, a GABA transaminase inhibitor, reversibly eliminates tinnitus in an animal model. J Assoc Res Otolaryngol 8(1):105–118PubMedPubMedCentralCrossRefGoogle Scholar
  264. 264.
    Ludewig F, Hüser A, Fromm H, Beauclair L, Bouché N (2008) Mutants of GABA transaminase (POP2) suppress the severe phenotype of succinic semialdehyde dehydrogenase (ssadh) mutants in Arabidopsis. PLoS ONE 3(10):e3383PubMedPubMedCentralCrossRefGoogle Scholar
  265. 265.
    Toyokura K, Watanabe K, Oiwaka A, Kusano M, Tameshige T, Tatematsu K, Matsumoto N, Tsugeki R, Saito K, Okada K (2011) Succinic semialdehyde dehydrogenase is involved in the robust patterning of Arabidopsis leaves along the adaxial-abaxial axis. Plant Cell Physiol 52(8):1340–1353. doi:10.1093/pcp/pcr079 PubMedCrossRefGoogle Scholar
  266. 266.
    Bao H, Chen XY, Lv SL, Jiang P, Feng JJ, Fan PX, Nie LL, Li YX (2015) Virus-induced gene silencing reveals control of reactive oxygen species accumulation and salt tolerance in tomato by gamma-aminobutyric acid metabolic pathway. Plant Cell Environ 38(3):600–613. doi:10.1111/pce.12419 PubMedCrossRefGoogle Scholar
  267. 267.
    Seher Y, Filiz O, Melike B (2013) Gamma-amino butyric acid, glutamate dehydrogenase and glutamate decarboxylase levels in phylogenetically divergent plants. Plant Syst Evol 299(2):403–412. doi:10.1007/s00606-012-0730-5 CrossRefGoogle Scholar
  268. 268.
    Batushansky A, Kirma M, Grillich N, Pham PA, Rentsch D, Galili G, Fernie AR, Fait A (2015) The transporter GAT1 plays an important role in GABA-mediated carbon–nitrogen interactions in Arabidopsis. Front Plant Sci 6:785. doi:10.3389/fpls.2015.00785
  269. 269.
    Batushansky A, Kirma M, Grillich N, Toubiana D, Pham PA, Balbo I, Fromm H, Galili G, Fernie AR, Fait A (2014) Combined transcriptomics and metabolomics of Arabidopsis thaliana seedlings exposed to exogenous GABA suggest its role in plants is predominantly metabolic. Mol Plant 7(6):1065–1068. doi:10.1093/mp/ssu017 PubMedCrossRefGoogle Scholar
  270. 270.
    Allan WL, Simpson JP, Clark SM, Shelp BJ (2008) γ-hydroxybutyrate accumulation in Arabidopsis and tobacco plants is a general response to abiotic stress: putative regulation by redox balance and glyoxylate reductase isoforms. J Exp Bot 59(9):2555–2564. doi:10.1093/jxb/ern122 PubMedPubMedCentralCrossRefGoogle Scholar
  271. 271.
    Mirabella R, Rauwerda H, Struys EA, Jakobs C, Triantaphylides C, Haring MA, Schuurink RC (2008) The Arabidopsis her1 mutant implicates GABA in E-2-hexenal responsiveness. Plant J 53(2):197–213. doi:10.1111/j.1365-313X.2007.03323.x PubMedCrossRefGoogle Scholar
  272. 272.
    Clark SM, Di Leo R, Dhanoa PK, Van Cauwenberghe OR, Mullen RT, Shelp BJ (2009) Biochemical characterization, mitochondrial localization, expression, and potential functions for an Arabidopsis gamma-aminobutyrate transaminase that utilizes both pyruvate and glyoxylate. J Exp Bot 60(6):1743–1757. doi:10.1093/jxb/erp044 PubMedPubMedCentralCrossRefGoogle Scholar
  273. 273.
    Dimlioğlu G, Daş ZA, Bor M, Özdemir F, Türkan İ (2015) The impact of GABA in harpin-elicited biotic stress responses in Nicotiana tabaccum. J Plant Physiol 188:51–57PubMedCrossRefGoogle Scholar
  274. 274.
    Aurisano N, Bertani A, Reggiani R (1995) Involvement of calcium and calmodulin in protein and amino acid metabolism in rice roots under anoxia. Plant Cell Physiol 36(8):1525–1529Google Scholar
  275. 275.
    Reggiani R, Cantu CA, Brambilla I, Bertani A (1988) Accumulation and interconversion of amino acids in rice roots under anoxia. Plant Cell Physiol 29(6):981–987Google Scholar
  276. 276.
    Kim DW, Shibato J, Agrawal GK, Fujihara S, Iwahashi H, du Kim H, Shim Ie S, Rakwal R (2007) Gene transcription in the leaves of rice undergoing salt-induced morphological changes (Oryza sativa L.). Mol Cells 24(1):45–59PubMedGoogle Scholar
  277. 277.
    Shimajiri Y, Oonishi T, Ozaki K, Kainou K, Akama K (2013) Genetic manipulation of the gamma-aminobutyric acid (GABA) shunt in rice: overexpression of truncated glutamate decarboxylase (GAD2) and knockdown of gamma-aminobutyric acid transaminase (GABA-T) lead to sustained and high levels of GABA accumulation in rice kernels. Plant Biotechnol J 11(5):594–604. doi:10.1111/pbi.12050 PubMedCrossRefGoogle Scholar
  278. 278.
    Liu L, Zhai H, Wan J-M (2005) Accumulation of γ-aminobutyric acid in giant-embryo rice grain in relation to glutamate decarboxylase activity and its gene expression during water soaking. Cereal Chem 82(2):191–196CrossRefGoogle Scholar
  279. 279.
    Wallace W, Secor J, Schrader L (1984) Rapid accumulation of γ-aminobutyric acid and alanine in soybean leaves in response to an abrupt transfer to lower temperature, darkness, or mechanical manipulation. Plant Physiol 75:170–175PubMedPubMedCentralCrossRefGoogle Scholar
  280. 280.
    Ramputh A-I, Bown AW (1996) Rapid γ-aminobutyric acid synthesis and the inhibition of the growth and development of oblique-banded leaf-roller larvae. Plant Physiol 111(4):1349–1352PubMedPubMedCentralCrossRefGoogle Scholar
  281. 281.
    Akihiro T, Koike S, Tani R, Tominaga T, Watanabe S, Iijima Y, Aoki K, Shibata D, Ashihara H, Matsukura C (2008) Biochemical mechanism on GABA accumulation during fruit development in tomato. Plant Cell Physiol 49(9):1378–1389PubMedCrossRefGoogle Scholar
  282. 282.
    Deewatthanawong R, Rowell P, Watkins CB (2010) γ-Aminobutyric acid (GABA) metabolism in CO2 treated tomatoes. Postharvest Biol Technol 57(2):97–105CrossRefGoogle Scholar
  283. 283.
    Mae N, Makino Y, Oshita S, Kawagoe Y, Tanaka A, Aoki K, Kurabayashi A, Akihiro T, Akama K, Koike S, Takayama M, Matsukura C, Ezura H (2012) Accumulation mechanism of gamma-aminobutyric acid in tomatoes (Solanum lycopersicum L.) under low O2 with and without CO2. J Agric Food Chem 60(4):1013–1019. doi:10.1021/jf2046812 PubMedCrossRefGoogle Scholar
  284. 284.
    Bartyzel I, Pelczar K, Paszkowski A (2003) Functioning of the gamma-aminobutyrate pathway in wheat seedlings affected by osmotic stress. Biol Plantarum 47(2):221–225CrossRefGoogle Scholar
  285. 285.
    C-y Wang, J-r Li, Xia Q-p Wu, X-l Gao H-b (2014) Influence of exogenous gamma-aminobutyric acid (GABA) on GABA metabolism and amino acid contents in roots of melon seedling under hypoxia stress. J Appl Ecology 25(7):2011–2018Google Scholar
  286. 286.
    Yang R, Chen H, Gu Z (2011) Factors influencing diamine oxidase activity and gamma-aminobutyric acid content of fava bean (Vicia faba L.) during germination. J Agric Food Chem 59(21):11616–11620. doi:10.1021/jf202645p PubMedCrossRefGoogle Scholar
  287. 287.
    Martinez-Luscher J, Torres N, Hilbert G, Richard T, Sanchez-Diaz M, Delrot S, Aguirreolea J, Pascual I, Gomes E (2014) Ultraviolet-B radiation modifies the quantitative and qualitative profile of flavonoids and amino acids in grape berries. Phytochem 102:106–114. doi:10.1016/j.phytochem.2014.03.014 CrossRefGoogle Scholar
  288. 288.
    Allan W, Peiris C, Bown A, Shelp B (2003) Gamma-hydroxybutyrate accumulates in green tea and soybean sprouts in response to oxygen deficiency. Can J Plant Sci 83(4):951–953CrossRefGoogle Scholar
  289. 289.
    Scharff AM, Egsgaard H, Hansen PE, Rosendahl L (2003) Exploring symbiotic nitrogen fixation and assimilation in pea root nodules by in vivo 15N nuclear magnetic resonance spectroscopy and liquid chromatography-mass spectrometry. Plant Physiol 131(1):367–378PubMedPubMedCentralCrossRefGoogle Scholar
  290. 290.
    Johnston G, Chebib M, Duke R, Fernandez S, Hanrahan J, Hinton T, Mewett K (2009) Herbal products and GABA receptors. Encycl Neurosci  (4):1095-1101 Google Scholar
  291. 291.
    Johnston GA (2005) GABAA receptor channel pharmacology. Curr Pharm Des 11(15):1867–1885PubMedCrossRefGoogle Scholar
  292. 292.
    Johnston GA (1986) Multiplicity of GABA receptors. Benzodiazepine/GABA receptors and chloride channels: structural and functional propertiesGoogle Scholar
  293. 293.
    Ticku MK Drug modulation of GABAA-mediated transmission. In: Seminars in Neuroscience, 1991. vol 3. Elsevier, pp 211–218Google Scholar
  294. 294.
    Chebib M, Hanrahan JR, Mewett KN, Duke RK, Johnston GA (2004) Ionotropic GABA receptors as therapeutic targets for memory and sleep disorders. Annu Rep Med Chem 39:13–23CrossRefGoogle Scholar
  295. 295.
    Viola H, Wasowski C, De Stein ML, Wolfman C, Silveira R, Dajas F, Medina J, Paladini A (1995) Apigenin, a component of Matricaria recutita flowers, is a central benzodiazepine receptors-ligand with anxiolytic effects. Planta Med 61(03):213–216PubMedCrossRefGoogle Scholar
  296. 296.
    Patel D, Shukla S, Gupta S (2007) Apigenin and cancer chemoprevention: progress, potential and promise. Int J Oncol 30(1):233–246PubMedGoogle Scholar
  297. 297.
    Ruela-de-Sousa R, Fuhler G, Blom N, Ferreira C, Aoyama H, Peppelenbosch M (2010) Cytotoxicity of apigenin on leukemia cell lines: implications for prevention and therapy. Cell Death Dis 1(1):e19PubMedPubMedCentralCrossRefGoogle Scholar
  298. 298.
    Brogden RN, Goa KL (1991) Flumazenil. A reappraisal of its pharmacological properties and therapeutic efficacy as a benzodiazepine antagonist. Drugs 42(6):1061–1089PubMedCrossRefGoogle Scholar
  299. 299.
    Spivey WH (1991) Flumazenil and seizures: analysis of 43 cases. Clin Ther 14(2):292–305Google Scholar
  300. 300.
    Kavvadias D, Sand P, Youdim KA, Qaiser MZ, Rice-Evans C, Baur R, Sigel E, Rausch WD, Riederer P, Schreier P (2004) The flavone hispidulin, a benzodiazepine receptor ligand with positive allosteric properties, traverses the blood–brain barrier and exhibits anticonvulsive effects. Br J Pharmacol 142(5):811–820PubMedPubMedCentralCrossRefGoogle Scholar
  301. 301.
    Davidoff RA (1985) Antispasticity drugs: mechanisms of action. Ann Neurol 17(2):107–116PubMedCrossRefGoogle Scholar
  302. 302.
    Bucknam W (2007) Suppression of symptoms of alcohol dependence and craving using high-dose baclofen. Alcohol Alcohol 42(2):158–160PubMedCrossRefGoogle Scholar
  303. 303.
    Rando R (1977) Mechanism of the irreversible inhibition of γ-aminobutyric acid-α-ketoglutaric acid transaminase by the neurotoxin gabaculine. Biochem 16(21):4604–4610CrossRefGoogle Scholar
  304. 304.
    Rando RR, Bangerter F (1977) The in vivo inhibition of GABA-transaminase by gabaculine. Biochem Biophys Res Commun 76(4):1276–1281PubMedCrossRefGoogle Scholar
  305. 305.
    Ylinen A, Sivenius J, Pitkänen A, Halonen T, Partanen J, Mervaala E, Mumford J, Riekkinen P (1992) γ-Vinyl GABA (Vigabatrin) in Epilepsy: clinical, Neurochemical, and Neurophysiologic Monitoring in Epileptic Patients. Epilepsia 33(5):917–922PubMedCrossRefGoogle Scholar
  306. 306.
    Connelly J (1993) Vigabatrin. Ann Pharmacother 27(2):197–204PubMedGoogle Scholar
  307. 307.
    Mathivet P, Bernasconi R, De Barry J, Marescaux C, Bittiger H (1997) Binding characteristics of γ-hydroxybutyric acid as a weak but selective GABAB receptor agonist. Eur J Pharmacol 321(1):67–75PubMedCrossRefGoogle Scholar
  308. 308.
    Wong T, Guin C, Bottiglieri T, Snead OC (2003) GABA, γ-hydroxybutyric acid, and neurological disease. Ann Neurol 54(S6):S3–S12PubMedCrossRefGoogle Scholar
  309. 309.
    Wong CGT, Gibson KM, Snead OC (2004) From the street to the brain: neurobiology of the recreational drug γ-hydroxybutyric acid. Trends Pharmacol Sci 25(1):29–34PubMedCrossRefGoogle Scholar
  310. 310.
    Snead OC III, Gibson KM (2005) γ-Hydroxybutyric acid. N Engl J Med 352(26):2721–2732PubMedCrossRefGoogle Scholar
  311. 311.
    Olsen RW (1981) GABA-benzodiazepine-barbiturate receptor interactions. J Neurochem 37(1):1–13PubMedCrossRefGoogle Scholar
  312. 312.
    Olsen RW (1982) Drug interactions at the GABA receptor-ionophore complex. Annu Rev Pharmacol Toxicol 22(1):245–277PubMedCrossRefGoogle Scholar
  313. 313.
    Olson R (1987) The gamma-aminobutyric acid/benzodiazepine/barbiturate receptor-chloride ion channel complex of the mammalian brain. Synaptic function. Wiley, New YorkGoogle Scholar
  314. 314.
    Haefely W, Kulcsar A, Möhler H, Pieri L, Polc P, Schaffner R (1974) Possible involvement of GABA in the central actions of benzodiazepines. Adv Biochem Psychopharmacol 14:131–151Google Scholar
  315. 315.
    Hunkeler W, Möhler H, Pieri L, Polc P, Bonetti E, Cumin R, Schaffner R, Haefely W (1981) Selective antagonists of benzodiazepines. Nature 290:514–516PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing 2016

Authors and Affiliations

  1. 1.Plant Transport and Signalling Lab, ARC Centre of Excellence in Plant Energy Biology and School of Agriculture, Food and Wine, Waite Research InstituteUniversity of AdelaideGlen OsmondAustralia

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