Skip to main content
SpringerLink
Log in

Receptor modifiers indicate that 4-aminobutyric acid (GABA) is a potential modulator of ion transport in plants

  • Published:
Plant Growth Regulation Aims and scope Submit manuscript

Abstract

GABA (4-aminobutyric acid) is a ubiquitousnon-protein amino acid that accumulates rapidly inplants in response to stress. GABA was firstidentified in plants (potato tubers) and animals(brain tissue) 50 years ago. Although GABA is nowrecognized as the most important inhibitoryneurotransmitter in the mammalian central nervoussystem (CNS), the role of GABA in plants remainsunclear. Studies were performed using Lemna toinvestigate the possibility that GABA elicits aresponse in plants that may be related to that of asignaling molecule as described for GABA effects onthe CNS. Lemna growth was increased 2 to 3-foldby 5 mM GABA, but growth was strongly inhibited by 0.5mM of the isomers 3-aminobutyric acid and2-aminobutyric acid. Growth promotion by GABA wasrapidly terminated by addition of 2-aminobutyric acidto the culture medium, but inhibitory effects of2-aminobutyric acid were not reversed by GABAregardless of amounts added. Promotion of Lemnagrowth by GABA was associated with an increase inmineral content of treated plants in a dose dependentmanner. Results support the hypothesis that GABAactivity in plants involves an effect on ion transportand an interaction with a receptor. Evidence for GABAreceptors in Lemna was obtained from experimentswith pharmacological agents that have been used toidentify GABA receptors in animals. GABA mediatedpromotion of Lemna growth was inhibited bybicuculline and picrotoxin, which are respectivelycompetitive and non-competitive antagonists of GABAreceptors in the CNS. Growth inhibition bybicuculline was not relieved by increasing the amountsof GABA in the medium, indicating that the alkaloid isnot acting, as in the CNS, by competitive antagonismof GABA at GABA receptor sites. Baclofen, a GABAagonist that promotes GABA activity in animalssignificantly increased GABA mediated promotion ofLemna growth. These findings and the knownaction of GABA in regulating ion channels in animalssuggests a way that GABA could amplify the stressresponse in plants.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Aurisano N, Bertani A and Reggiani R (1995) Anerobic accumulation of 4-aminobyutyrate in rice seedlings; causes and significance. Phytochemistry 38: 1147–1150

    Google Scholar 

  2. Babcock, DF, Herrington J and Goodwin, PC (1997) Mitochondrial participation in the Intracellular Ca2+ network. J Cell Biol 136: 833–834

    Google Scholar 

  3. Baum G, Lev-Yadun S, Fridmann Y, Arazi T, Katsnelson H, Zik M and Fromm H (1996) Calmodulin binding to glutamate decarboxylase is required for regulation of glutamate and GABA metabolism and normal development in plants. EMBO Journal 15: 2988–2996

    Google Scholar 

  4. Bowery NG and Brown DA (1997) The cloning of GABAB receptors. Nature 386: 223–224

    Google Scholar 

  5. Bown AW and Shelp BJ (1997) The metabolism and functions of γ-aminobutyric acid. Plant Physiol 115: 1–5

    Google Scholar 

  6. Chen Y, Baum G and Fromm H (1994) The 58-kilodalton calmodulin-binding glutamate decarboxylase is a ubiquitous protein in petunia organs and its expression is developmentally regulated. Plant Physiol 106: 1381–1387

    Google Scholar 

  7. Cohen Y, Nidermann T, Mödninger E and Fluhr R (1994) γ-aminobutyric acid induces the accumulation of pathogenesisrelated proteins in tomato (Lycopersicon escuentum L.) Plants and resistance to late blight infection caused by Phytophthora infestans. Plant Physiol 104: 59–66

    Google Scholar 

  8. Cross JW (1999) The Charms of Duckweed, Poster #8, P32. Baltimore, MD: Plant Biology' 99, American Society of Plant Physiologists

    Google Scholar 

  9. Curtis DR, Duggan AW, Felix D and Johnston GAR (1971) Bicuculline, an antagonist of GABA and synaptic inhibition in the spinal cord. Brain Research 32: 69–96

    Google Scholar 

  10. Deisz RA (1997) Electrophysiology of GABAB receptors. In: Enna SJ and Bowery NG (eds) The GABA Receptors, 2nd edn. Totowa, New Jersey: Humana Press, pp 157–207

    Google Scholar 

  11. Hanower P and Brzowoska (1975) Influence d'un choc osmotique sur la composition des deuilles de cotonnier en acides amines libres. Phytochemistry 14: 1691–1694

    Google Scholar 

  12. Hansteen B (1899) Ñber einweissynthese in grünen phanerogamen. Jahrb Wiss Bot 33: 417–486

    Google Scholar 

  13. Hillman WS (1961) The lemnaceae or duckweeds. A review of the descriptive and experimental literature. Bot Rev 27: 221–287

    Google Scholar 

  14. Ichas F, Jouaville LS and Mazat JP (1997) Mitochondria are excitable organelles capable of generating and conveying electrical and calcium signals. Cell 89: 1145–1153

    Google Scholar 

  15. Johnston GAR (1997) Molecular biology, pharmacology and physiology of GABAC receptors. In: Enna SJ and Bowery NG (eds) The GABA Receptors, 2nd edn. Totowa, New Jersey: Humana Press, pp 297–323

    Google Scholar 

  16. Kathiresan A, Miranda J, Chinnappa CC and Reid DM (1998) γ-aminobutyric acid promotes stem elongation in Stellaria longipes: The role of ethylene. Plant Growth Regulation 26: 131–137

    Google Scholar 

  17. Kinnersley AM(1998) Bioactivity of AuxiGroTM Plant Metabolic Primer, a formulation containing GABA and glutamic acid. Proceedings of 25th Annual Meeting Plant Growth Regulation Society of America, July 7–10, pp 89–94.

  18. Kinnersley AM (1993) The role of phytochelates in plant growth and productivity. Plant Growth Regulation 12: 207–219

    Google Scholar 

  19. Kinnersley AM, Scott TC III, Whitten GH and Yopp JH (1990) Promotion of plant growth by polymers of lactic acid. Plant Growth Regulation 9: 137–146

    Google Scholar 

  20. Krogsgaard-Larsen P, Frolund B and Ebert B (1997) GABAA receptor agonists, partial agonists, and antagonists. In: Enna SJ and Bowery HG (eds) The GABA Receptors, 2nd edn. Totowa, New Jersey: Humana Press, pp 37–81

    Google Scholar 

  21. Kuriyama K and Hirouchi M (1997) Biochemical and molecular properties of GABAB receptors. In: Enna SJ and Bowery GG (eds) The GABA Recepters. Totawa, NJ: Humana Press, pp 259–269

    Google Scholar 

  22. Lam HM, Chiu J, Hsieh MH, Meisel L, Oliveira IC, Shin M and Corruzzi G (1998) Glutamate-receptor genes in plants. Nature 396: 125–126

    Google Scholar 

  23. Lotan T and Fluhr R (1990) Xylanase, a novel elicitor of pathogenesis-related proteins in tobacco, uses a non-ethylene pathway of induction. Plant Physiol 93: 811–817

    Google Scholar 

  24. Malho R, Moutinho A, van der Luit A and Trewavas AJ (1998) Spatial characteristics of calcium signaling: The calcium wave as a basic unit in plant cell calcium signaling. Philos Trans R Soc Lond B 353: 1463–1473

    Google Scholar 

  25. Martell AE and Smith RM (1977) Critical Stability Constants. Volume 1: Amino Acids. New York: Plenum Press

    Google Scholar 

  26. Mayer RR Cherry JL and Rhodes D (1990) Effects of heat shock on amino acid metabolism of cowpea cells. Phytochemistry 94: 796–810

    Google Scholar 

  27. Mizusaki S, Noguchi M and Tamaki E (1964) Studies on nitrogen metabolism in tobacco plants VI. Metabolism of glutamic acid γ-aminobutyric acid and proline in tobacco leaves. Arch Biochem Biophys 105: 599

    Google Scholar 

  28. Parola AL, Yamamura HI and Laird II HE (1993) Minireview. Peripheral-type benzodiazepine receptors. Life Sciences 52: 1329–1342

    Google Scholar 

  29. Qian H and Dowling JE (1994) Pharmacology of novel GABA receptors found on rod horizontal cells of the white perch retina. J Neurosci 14: 4299–4307

    Google Scholar 

  30. Roberts E (1988) The establishment of GABA as a neurotransmitter. In: Squires RF (ed) GABA and Benzodiazepine Receptors. Boca Raton, Florida: CRC Press, pp 1–21

    Google Scholar 

  31. Sanders D, Brownlee C and Harper JF (1999) Communicating with calcium. The Plant Cell 11: 691–706

    Google Scholar 

  32. Satya Narayan V and Nair PM (1990) Metabolism, enzymology and possible roles of 4-aminobutyric acid in higher plants. Phytochemistry 29: 367–375

    Google Scholar 

  33. Sprengel R and Seeburg PH (1995) Ionotropic glutamate receptors. In: North RA (ed) Ligand and Voltage-Gated Ion Channels. Boca Raton, Florida: CRC Press, pp 213–263

    Google Scholar 

  34. Steward FC, Thompson JF and Dent CE (1949) γ-aminobutyric acid, a constituent of the potato tuber Science 110: 439–440

    Google Scholar 

  35. Subbaiah CC, Bush DS and Sachs MM (1998) Mitochondrial contribution to the anoxic Ca2+ signal in maize suspension-cultured cells. Plant Physiol 118: 759–771

    Google Scholar 

  36. Tyndale RF, Olsen RW and Tobin AJ (1995) GABAA receptors. In: North RA (ed) Ligand and Voltage-Gated Ion Channels. Boca Raton, Florida: CRC Press, pp 265–290

    Google Scholar 

  37. Wallace W, Secor J and Schrader LE (1984) Rapid accumulation of-aminobutyric acid and alanine in soybean leaves in response to an abrupt transfer to lower temperature, darkness, or mechanical manipulation. Plant Physiol 75: 170–175

    Google Scholar 

  38. Young AB and Penney JB (1991) Benzodiazepine, GABA and glutamate receptors in cerebral centex, hippociampus, basal ganglia, and cerebellum. In: Mendelsohn FAO and Paxines G (eds) Receptors in the Human Bervous System. Academic Press, pp 9

  39. Zielinski RE (1998) Calmodulin and calmodulin-binding proteins in plants. Ann Rev Plant Physiol Plant Mol Biol 49: 497–725

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Auxein Corporation, 3125 Sovereign Drive, Suite B, Lansing, MI, 48911

    Alan M. Kinnersley

  2. Auxein Corporation, 3125 Sovereign Drive, Suite B, Lansing, MI, 48911

    Fang Lin

Authors
  1. Alan M. Kinnersley
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fang Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kinnersley, A.M., Lin, F. Receptor modifiers indicate that 4-aminobutyric acid (GABA) is a potential modulator of ion transport in plants. Plant Growth Regulation 32, 65–76 (2000). https://doi.org/10.1023/A:1006305120202

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1006305120202

Search

Navigation