Evidence for GABA-Induced Systemic GABA Accumulation in Arabidopsis upon Wounding

The non-proteinogenic amino acid γ-aminobutyric acid (GABA) is present in all plant species analyzed so far. Its synthesis is stimulated by either acidic conditions occurring after tissue disruption or higher cytosolic calcium level. In mammals, GABA acts as inhibitory neurotransmitter but its function in plants is still not well understood. Besides its involvement in abiotic stress resistance, GABA has a role in the jasmonate-independent defense against invertebrate pests. While the biochemical basis for GABA accumulation in wounded leaves is obvious, the underlying mechanisms for wounding-induced GABA accumulation in systemic leaves remained unclear. Here, the Arabidopsis thaliana knock-out mutant lines pop2-5, unable to degrade GABA, and tpc1-2, lacking a wounding-induced systemic cytosolic calcium elevation, were employed for a comprehensive investigation of systemic GABA accumulation. A wounding-induced systemic GABA accumulation was detected in tpc1-2 plants demonstrating that an increased calcium level was not involved. Similarly, after both mechanical wounding and Spodoptera littoralis feeding, GABA accumulation in pop2-5 plants was significantly higher in local and systemic leaves, compared to wild-type plants. Consequently, larvae feeding on these GABA-enriched mutant plants grew significantly less. Upon exogenous application of a D2-labeled GABA to wounded leaves of pop2-5 plants, its uptake but no translocation to unwounded leaves was detected. In contrast, an accumulation of endogenous GABA was observed in vascular connected systemic leaves. These results suggest that the systemic accumulation of GABA upon wounding does not depend on the translocation of GABA or on an increase in cytosolic calcium.

[1]  Bingru Huang,et al.  Metabolic pathways regulated by abscisic acid, salicylic acid and γ-aminobutyric acid in association with improved drought tolerance in creeping bentgrass (Agrostis stolonifera). , 2017, Physiologia plantarum.

[2]  A. Bown,et al.  Plant GABA: Not Just a Metabolite. , 2016, Trends in plant science.

[3]  Nobuhiro Suzuki,et al.  ROS, Calcium, and Electric Signals: Key Mediators of Rapid Systemic Signaling in Plants1[OPEN] , 2016, Plant Physiology.

[4]  U. Flügge,et al.  Gamma-aminobutyric acid depletion affects stomata closure and drought tolerance of Arabidopsis thaliana. , 2016, Plant science : an international journal of experimental plant biology.

[5]  A. Mithöfer,et al.  Herbivore-Triggered Electrophysiological Reactions: Candidates for Systemic Signals in Higher Plants and the Challenge of Their Identification1 , 2016, Plant Physiology.

[6]  M. Reichelt,et al.  Insect Herbivory-Elicited GABA Accumulation in Plants is a Wound-Induced, Direct, Systemic, and Jasmonate-Independent Defense Response , 2015, Front. Plant Sci..

[7]  M. Reichelt,et al.  Synthesis, metabolism and systemic transport of a fluorinated mimic of the endogenous jasmonate precursor OPC-8:0. , 2015, Biochimica et biophysica acta.

[8]  E. Peiter,et al.  Systemic cytosolic Ca(2+) elevation is activated upon wounding and herbivory in Arabidopsis. , 2015, The New phytologist.

[9]  J. T. Puthur,et al.  γ-Aminobutyric acid (GABA) priming enhances the osmotic stress tolerance in Piper nigrum Linn. plants subjected to PEG-induced stress , 2015, Plant Growth Regulation.

[10]  P. Malekzadeh,et al.  Alleviating effects of exogenous Gamma-aminobutiric acid on tomato seedling under chilling stress , 2013, Physiology and Molecular Biology of Plants.

[11]  H. Nayyar,et al.  γ-Aminobutyric Acid (GABA) Imparts Partial Protection from Heat Stress Injury to Rice Seedlings by Improving Leaf Turgor and Upregulating Osmoprotectants and Antioxidants , 2013, Journal of Plant Growth Regulation.

[12]  E. Farmer,et al.  Leaf numbering for experiments on long distance signalling in Arabidopsis , 2013 .

[13]  E. Farmer,et al.  GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signalling , 2013, Nature.

[14]  M. Knight,et al.  Calcium signatures are decoded by plants to give specific gene responses. , 2013, The New phytologist.

[15]  B. Shelp.  Does long-distance GABA signaling via the phloem really occur? , 2012 .

[16]  J. ShelpBarry,et al.  Strategies and tools for studying the metabolism and function of γ-aminobutyrate in plants. II. Integrated analysis , 2012 .

[17]  M. Reichelt,et al.  CML42-Mediated Calcium Signaling Coordinates Responses to Spodoptera Herbivory and Abiotic Stresses in Arabidopsis1[W][OA] , 2012, Plant Physiology.

[18]  Prisca Viehoever,et al.  GABI-Kat SimpleSearch: new features of the Arabidopsis thaliana T-DNA mutant database , 2011, Nucleic Acids Res..

[19]  J. Renou,et al.  GABA accumulation causes cell elongation defects and a decrease in expression of genes encoding secreted and cell wall-related proteins in Arabidopsis thaliana. , 2011, Plant & cell physiology.

[20]  Yuting Cai,et al.  Effect of exogenous γ-aminobutyric acid treatment on proline accumulation and chilling injury in peach fruit after long-term cold storage. , 2011, Journal of agricultural and food chemistry.

[21]  Xiaomei Sun,et al.  Effects of exogenous GABA on gene expression of Caragana intermedia roots under NaCl stress: regulatory roles for H2O2 and ethylene production. , 2010, Plant, cell & environment.

[22]  R. Mullen,et al.  Subcellular localization and expression of multiple tomato γ-aminobutyrate transaminases that utilize both pyruvate and glyoxylate , 2009, Journal of experimental botany.

[23]  Hubert H. Felle,et al.  System Potentials, a Novel Electrical Long-Distance Apoplastic Signal in Plants, Induced by Wounding1 , 2009, Plant Physiology.

[24]  D. Faure,et al.  Role of g -Aminobutyrate and g -Hydroxybutyrate in Plant Communication , 2009 .

[25]  Han Rauwerda,et al.  The Arabidopsis her1 mutant implicates GABA in E-2-hexenal responsiveness. , 2007, The Plant journal : for cell and molecular biology.

[26]  Robert W. Gereau,et al.  The Glutamate Receptors , 2008 .

[27]  A. Fernie,et al.  Highway or byway: the metabolic role of the GABA shunt in plants. , 2008, Trends in plant science.

[28]  A. Good,et al.  Contribution of the GABA shunt to hypoxia-induced alanine accumulation in roots of Arabidopsis thaliana. , 2008, Plant & cell physiology.

[29]  J. Whisstock,et al.  GABA production by glutamic acid decarboxylase is regulated by a dynamic catalytic loop , 2007, Nature Structural &Molecular Biology.

[30]  Hubert H. Felle,et al.  Systemic signalling in barley through action potentials , 2007, Planta.

[31]  N. Dengler.  The shoot apical meristem and development of vascular architecture , 2006 .

[32]  A. Bown,et al.  Gamma-aminobutyrate: defense against invertebrate pests? , 2006, Trends in plant science.

[33]  W. Boland,et al.  Effects of Feeding Spodoptera littoralis on Lima Bean Leaves. II. Continuous Mechanical Wounding Resembling Insect Feeding Is Sufficient to Elicit Herbivory-Related Volatile Emission , 2005, Plant Physiology.

[34]  Rainer Bergomaz.  A SIMPLE INSTANT DIET FOR REARING ARCTIIDAE AND OTHER MOTHS , 2005 .

[35]  H. Fromm,et al.  GABA in plants: just a metabolite? , 2004, Trends in plant science.

[36]  A. Bown,et al.  Overexpression of Glutamate Decarboxylase in Transgenic Tobacco Plants Deters Feeding by Phytophagous Insect Larvae , 2003, Journal of Chemical Ecology.

[37]  D. Preuss,et al.  Pollen Tube Growth and Guidance Is Regulated by POP2, an Arabidopsis Gene that Controls GABA Levels , 2003, Cell.

[38]  Dawn E. Hall,et al.  Insect Footsteps on Leaves Stimulate the Accumulation of 4-Aminobutyrate and Can Be Visualized through Increased Chlorophyll Fluorescence and Superoxide Production1 , 2002, Plant Physiology.

[39]  F. Turano,et al.  Gamma Aminobutyric Acid (GABA) and Plant Responses to Stress , 2000 .

[40]  A. Bown,et al.  The Metabolism and Functions of [gamma]-Aminobutyric Acid , 1997, Trends in plant science.

[41]  A. Trewavas,et al.  Calcium signalling in Arabidopsis thaliana responding to drought and salinity. , 1997, The Plant journal : for cell and molecular biology.

[42]  A. Bown,et al.  Rapid [gamma]-Aminobutyric Acid Synthesis and the Inhibition of the Growth and Development of Oblique-Banded Leaf-Roller Larvae , 1996, Plant physiology.

[43]  A. Trewavas,et al.  Cold calcium signaling in Arabidopsis involves two cellular pools and a change in calcium signature after acclimation. , 1996, The Plant cell.

[44]  W. Snedden,et al.  Calcium/Calmodulin Activation of Soybean Glutamate Decarboxylase , 1995, Plant physiology.

[45]  A. Carroll,et al.  Ammonium Assimilation and the Role of [gamma]-Aminobutyric Acid in pH Homeostasis in Carrot Cell Suspensions , 1994, Plant physiology.

[46]  M Kamermans,et al.  GABA-mediated positive autofeedback loop controls horizontal cell kinetics in tiger salamander retina , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[47]  S. Lummis,et al.  GABA receptors in insects. , 1990, Comparative biochemistry and physiology. C, Comparative pharmacology and toxicology.

[48]  W. Wallace,et al.  Rapid Accumulation of gamma-Aminobutyric Acid and Alanine in Soybean Leaves in Response to an Abrupt Transfer to Lower Temperature, Darkness, or Mechanical Manipulation. , 1984, Plant physiology.

[49]  P. O'brien.  [47] Superoxide production , 1984 .

[50]  Sze Py.  L-Glutamate decarboxylase. , 1979, Advances in experimental medicine and biology.