Mechanical stimulation Mechanical damage

Fungal infection Agrobacterium infection Rhizobium infection Cold stress

Heat stress Oxygen deficiency

Cytosolic acidification

Water stress

Phytohormones Carbon dioxide enrichment

UV stress Oxygen deficiency

Cold stress

Heat or water stress UV stress

Soybean leaves and hypocotyl tissue Soybean and tobacco leaves

Alfalfa and tomato phloem exudate Tomato cell apoplast Arabidopsis tumors

Legume nodule Soybean and Arabidopsis leaves

Asparagus mesophyll cells Barley and wheat seedlings Cowpea cell cultures Arabidopsis jfeaves Rice roots

Tea leaves, soybean sprouts, tobacco and Arabidopsis leaves

Medicago seedlings Rice cotyledons

Broccoli florets Asparagus mesophyll cells Carrot cell suspensions Tomato roots and leaves Soybean nodules and xylem sap

Wheat seedlings Arabidopsis leaves Datura root cultures Cherimoya fruit Broccoli florets Arabidopsis plants Tea leaves, soybean sprouts, tobacco and Arabidopsis leaves Arabidopsis leaves

Arabidopsis leaves Arabidopsis plants

Wallace et al. (1984); Bown and Zhang (2000) Ramputh and Bown (1996); Bown et al. (2002); Hall et al. (2004) Girousse et al. (1996); Valle et al. (1998) Solomon and Oliver (2001) Deeken et al. (2006)

Vance and Heichel (1991) Wallace et al. (1984); Kaplan et al. (2007); Allan et al. (2008) Cholewa et al. (1997) Mazzucotelli et al. (2006) Mayer et al. (1990) Allan et al. (2008) Reggiani et al. (1988);

Aurisano et al. (1995) Tsishida and Murai (1987); Allan et al. (2003); Breitkreuz et al. (2003); Allan et al. (2008) Ricoult et al. (2005) Kato-Noguchi and Ohashi (2006) Hansen et al. (2001) Crawford et al. (1994) Carroll et al. (1994) Bolarin et al. (1995) Serraj et al. (1998)

Bartyzel et al., (2003-2004) Allan et al. (2008) Ford et al. (1996) Merodio et al. (1998) Hansen et al. (2001) Fait et al. (2005) Allan et al. (2003, 2008); Breitkreuz et al. (2003)

Kaplan et al. (2007); Allan et al. (2008) Allan et al. (2008) Fait et al. (2005)_

stress conditions that should increase the cellular NADH:NAD+ ratio and decrease the adenylate energy charge, thereby inhibiting SSADH activity and diverting carbon from succinate (Shelp et al. 1995, 1999; Busch et al. 1999; Breitkreuz et al. 2003; Allan et al. 2008) . Other work revealed that: (1) ssadh mutant Arabidopsis plants grown under high UV light have five times the normal level of GHB and high levels of ROS (Fait et al. 2005), and; (2) the pattern of GHB in cold-acclimated Arabidopsis plants is consistent with the rise and fall of GABA (Kaplan et al. 2007). Together, these data indicate that the accumulation of GHB in plants, as well as GABA, is a general response to abiotic stress.

4 GABA and GHB Signaling Between Plants and Other Organisms

Several papers demonstrate that plant-derived extracellular GABA and possibly GHB mediate communications between plants and animals, fungi, bacteria and other plants. (1) Chemosensory recognition of GABA-mimetic molecules uniquely associated with the surface of crustose red algae induces the motile planktonic larvae of the large red abalone of the eastern Pacific to settle, attach to substrata and metamorphose into benthic juveniles, which feed nondestructively on the algal surface (Morse et al. 1979; Morse and Morse 1984; Trapido-Rosenthal and Morse 1986). (2) The ingestion of elevated GABA concentrations, either in synthetic diets or in transgenic tobacco plants overexpressing GAD, interferes with physiological and developmental processes of several invertebrate pests (Ramputh and Bown 1996; MacGregor et al. 2003; McLean et al. 2003), a result attributed to activation by excess GABA of chloride channels at neuromuscular junctions (Bown et al. 2006). (3) Elevated GABA concentrations in the apoplast of tomato cells infected with the fungus Cladosporium fulvum are associated with the induction of the fungal GABA-T and SSADH, indicating that the GABA is being utilized as a nutrient source (Solomon and Oliver 2001, 2002; Oliver and Solomon 2004) . (4) High GABA levels are present in Rhizobium-induced nodules (see review by Vance and Heichel 1991), as well as in Rhizobium bacteroids (Miller et al. 1991) which exhibit active GABA metabolism during symbiosis (Prell et al. 2002). (5) Elevated GABA concentrations in tobacco GAD overexpression mutants, wounded tomato stems or culture solution enters Agrobacterium tumefaciens cells via the GABA transporter Bra and controls the level of the quorum-sensing signal, thereby resulting in a decline in Agrobacterium virulence (Chevrot et al. 2006). It is noteworthy that the level of the quorum-sensing signal is also modulated by GHB (Carlier et al. 2004; Chai et al. 2007), suggesting that plant-derived extracellular GHB might be effective in controlling Agrobacterium virulence; however, further research is required to test this hypothesis. (6) A GABA-T-mediated gradient of GABA through apoplastic spaces within the Arabidopsis pistil to the female gametophyte is required to guide the pollen tube (Palanivelu et al. 2003), providing evidence for the role of GABA in cell-to-cell communication within plants (Bouché et al. 2003b; Palanivelu et al.

2003) and between plants (Shelp et al. 2006). For further discussion of these papers, refer to a recent review by Shelp et al. (2006).

5 Conclusions and Future Prospects

The neurotransmitters GABA and GHB are found in virtually all prokaryotic and eukaryotic organisms. Recent studies suggest that GABA receptors exist in plants and that GABA serves as a signaling molecule within plants. The physiological roles of GABA and GHB in plants are not yet clear, but both metabolites readily accumulate in response to stress by a combination of biochemical and transcriptional processes. GABA accumulation has been associated with the appearance of extracellular GABA, and evidence is available for a role of extracellular GABA in communications between plants and animals, fungi, bacteria or other plants, although the mechanisms by which GABA functions in communication appear to be diverse. There is no evidence from plants of GHB receptors, GHB signaling or extracellular GHB yet, although the level of the quorum-sensing signalin Agrobacterium is known to be modulated by GHB. Future studies should attempt to address these issues and to uncover further examples and the mechanisms by which extracellular GABA is employed to mediate plant communication with other organisms.

Acknowledgments The authors acknowledge research support from the Natural Science and Engineering Research Council of Canada and the Ontario Ministry of Agriculture and Food to B.J.S., and the Centre National de la Recherche Scientifique to D.F.


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 58:2699-2707 Allan WL, Peiris C, Bown AW, Shelp BJ (2003) Gamma-hydroxybutyrate accumulates in green tea leaves and soybean sprouts in response to oxygen deficiency. Can J Plant Sci 83:951-953 Allan WL, Simpson JP, Clark SM, Shelp BJ (2008) g-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):2545-2554 Ansari MI, Lee RH, Chen RG (2005) A novel senescence-associated gene encoding g-aminobutyric acid (GABA): pyruvate transaminase is upregulated during rice leaf senescence. Physiol Plant 123:1-8

Aurisano N, Bertani A, Regianni R (1995) Anaerobic accumulation of 4-aminobutyrate in rice seedlings: causes and significance. Phytochemistry 38:1147-1150 Bartyzel I, Pelczar K, Paskowski A (2003/4) Functioning of the g-aminobutyrate pathway in wheat seedlings affected by osmotic stress. Biol Plant 47:221-225 Beuve N, Rispail N, Laine P, Cliquet J-B, Ourry A, Le Deunff E (2004) Putative role of g-ami-nobutyric acid as a long-distance signal in up-regulation of nitrate uptake in Brassica napus L. Plant Cell Environ 27:1035-1046

Bolarin MC, Santa-Cruz A, Cayuela E, Perez-Alfocea F (1995) Short-term solute changes in leaves and roots of cultivated and wil tomato seedlings under salinity. J Plant Physiol 147:463-468 Bouché N, Fait A, Bouchez D, Moller SG, Fromm H (2003a) Mitochondrial succinic-semialdehyde dehydrogenase of the gamma-aminobutyrate shunt is required to restrict levels of reactive oxygen intermediates in plants. Proc Natl Acad Sci USA 100:6843-6848 Bouché N, Lacomb B, Fromm H (2003b) GABA signalling: a conserved and ubiquitous mechanism.

Trends Cell Biol 13:607-610 Bown AW, Shelp BJ (1989) The metabolism and physiological roles of 4-aminobutyric acid.

Biochemistry (Life Sci Adv) 8:21-25 Bown AW, Zhang G (2000) Mechanical stimulation, 4-aminobutyric acid (GABA) synthesis, and growth inhibition in soybean hypocotyl tissue. Can J Bot 78:119-1123 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 129:1430-1434 Bown AW, MacGregor KB, Shelp BJ (2006) Gamma-aminobutyrate: defense against invertebrate pests?. Trends Plant Sci 11:424-427 Breitkreuz KE, Allan WL, Van Cauwenberghe OR, Jakobs C, Talibi D, Andre B, Shelp BJ (2003) A novel gamma-hydroxybutyrate dehydrogenase: identification and expression of an Arabidopsis cDNA and potential role under oxygen deficiency. J Biol Chem 278:41552-41556 Busch KB , Fromm H (1999) Plant sucinic semialdehyde dehydrogenase. Cloning, purification, localization in mitochondria, and regulation by adenine nucleotides. Plant Physiol 121:589-597 Carlier A, Chevrot R, Dessaux Y, Faure D (2004) The assimilation of g-butyrolactone in Agrobacterium tumfaciens C58 interferes with the accumulation of the A-acyl-homoserine lactone signal. Mol Plant Microbe Interact 17:951-957 Carroll AD, Fox GC, Laurie S, Phillips R, Ratcliffe RG, Stewart GR (1994) Ammonium assimilation and the role of g-aminobutyric acid in pH homeostasis in carrot cell suspensions. Plant Physiol 106:513-520

Chai Y, Tsai CS, Cho H, Winans SC (2007) Reconstitution of the biochemical activities ofthe AttJ repressor and the AttK, AttL, and AttM catabolic enzymes of Agrobacterium tumefaciens. J Bacteriol 189:3674-3679 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 103:7460-7464

Cholewa E, Cholewinski A J, Shelp BJ, Snedden WA, Bown AW (1997) Cold shock-stimulated g-aminobutyric acid synthesis is mediated by an increase in cytosolic Ca2+, not by an increase in cytosolic H+. Can J Bot 75:375-382 Chung I, Bown AW, Shelp BJ (1992) The production and efflux of 4-aminobutyrate in isolated mesophyll cells. Plant Physiol 99:659-664 Cramer GR, Ergül A, Grimplet J, Tillett RL, Tattersall EAR, Bohlman MC, Vincent D, Sonderegger J, Evans J, Osborne C, Quilici D, Schlauch KA, Schooley DA, Cushman JC (2007) Water and salinity stress in grapevines: early and late changes in transcript and metabolite profiles. Funct Integr Genomics 7:111-134 Crawford LA, Bown AW, Breitkreuz KE, Guinel F (1994) The synthesis of g-aminobutyric acid in response to treatments reducing cytosolic pH. Plant Physiol 104:865-871 Deeken R, Engelmann JC, Efetova M, Czirjak T, Müller T, Kaiser WM, Tietz O, Krischke M, Mueller MJ , Palme K , Dandekar T, Hedrich R (2006) An integrated view of gene expression and solute profiles of Arabidopsis tumors: a genome-wide approach. Plant Cell 18:3617-3634 Fait A, Yellin A, Fromm H (2005) GABA shunt deficiencies and accumulation of reactive oxygen intermediates: insight from Arabidopsis mutants. FEBS Lett 579:415-420 Ford Y-Y, Ratcliffe RG, Robins RJ (1996) Phytohormone-induced GABA production in transformed root cultures of Datura strammonium: an in vivo 15N NMR study. J Exp Bot 47:865-871 Girousse C , Bournoville R , Bonnemain J-L (1996) Water deficit-induced changes in concentrations of proline and some other amino acids in the phloem sap of alfalfa. Plant Physiol 111: 109-113

Hall DE, MacGregor KB, Nijisse J, Bown AW (2004) Footsteps from insect larvae damage leaf surfaces and initiate rapid responses. Eur J Plant Pathol 110:441-447 Hansen ME, Sorensen H, Cantwell M (2001) Changes in acetaldehyde, ethanol and amino acids in broccoli florets during aire and controlled atmosphere storage. Postharv Biol Technol 22:227-237 Hoover GJ , Van Cauwenberghe OR , Breitkreuz KE , Clark SM , Merrill AR , Shelp BJ (2007a) Characteristics of an Arabidopsis glyoxylate reductase: general biochemical properties and substrate specificity for the recombinant protein, and developmental expression and implications for glyoxylate and succinic semialdehyde metabolism in planta. Can J Bot 85:883-895 Hoover GJ, Prentice GA, Merrill AR, Shelp BJ (2007b) Kinetic mechanism of an Arabidopsis glyoxylate reductase: studies of initial velocity, dead-end inhibition and product inhibition. Can J Bot 95:896-902

Kaplan F, Kopka J, Sung DY, Zhao W, Popp W, Porat R, Guy CL (2007) Transcript and metabolite profiling during cold acclimation of Arabidopsis reveals an intricate relationship of cold-regulated gene expression with modifications in metabolite content. Plant J 50:967-981 Kathiresan A, Miranda J, Chinnapa CC, Reid DD (1998) g-Aminobutyric acid promotes elongation in Stellaria longipes: the role of ethylene. Plant Growth Regul 26:131-137 Kato-Noguchi H, Ohashi C (2006) Effects of anoxia on amino acid levels in rice cotyledons. Plant Prod Sci 9:383-387

Kinnersley AM , Lin F (2000) Receptor modifiers indicate that 4-aminobutyric acid (GABA) is a potential modulator of ion transport in plants. Plant Growth Regul 32:65-76 Kisaka H, Kida T, Miwa T (2006) Antisense suppression of glutamate decarboxylase in tomato (Lycopersicon esculentum L.) results in accumulation of glutamate in transgenic tomato fruits. Plant Biotech 23:267-274 Klok EJ, Wilson IW, Wilson D, Chapman, SC, Ewing RM, Somerville SC, Peacock WJ, Dolferus R, Dennis ES (2002) Expression profile analysis of the low-oxygen response in Arabidopsis root cultures. Plant Cell 14:2481-2494 Lacombe B , Becker D , Hedrich R , DeSalle R , Hollmann M , Kwak JM , Schroeder JI , Le Novere N, Nam HG, Spalding EP, Tester M, Turano FJ, Chiu J, Coruzzi (2001) The identity of plant glutamate receptors. Science 292:1486-1487 Lancien M , Roberts MR (2006) Regulation of Arabidopsis thaliana 14-3-3 gene expression by g-aminobutyric acid. Plant Cell Environ 29:1430-1436 MacGregor KB, Shelp BJ, Peiris SE, Bown AW (2003) Overexpression of glutamate decar-boxylase in transgenic tobacco deters feeding by phytophagous insect larvae. J Chem Ecol 29:2177-2182

Mamelak M (1989) Gammahydroxybutyrate: an endogenous regulator of energy metabolism .

Neurosci Biobehav Rev 13:187-197 Mayer R, Cheery J, Rhodes D (1990) Effect of heat shock on amino acid metabolism. Plant Physiol 94:796-810

Mazzucotelli E , Tartari A , Cattivelli L , Forlani G (2006) Metabolism of g-aminobutyric acid during cold acclimation and freezing and its relationship to frost tolerance in barley and wheat. J Exp Bot 57:3755-3766

McLean MD , Yevtushenko DP, Deschene D , 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 11:277-285 Merodio C, Muñoz MT, Del Cure B, Buitrango D, Escribano MI (1998) Effect ofhigh CO2 on the titres of g-aminobutyric acid, total polyamines and some pathogenesis-related proteins in cherimoya fruit stored at low temperature. J Exp Bot 49:1339-1347 Meyer A, Eskandari S, Grallath S, Rentsch D (2006) AtGAT1, a high affinity transporter for g-aminobutyric acid in Arabidopsis thaliana. J Biol Chem 281:7197-7204 Miller RW, McRae DG , Joy K (1991) Glutamate and g-aminobutyrate metabolism in isolated

Rhizobium meliloti bacteroids. Mol Plant Microbes Interact 4:37-45 Mirabella R, Rauwerda H, Struys EA, Jakobs C, Triantaphylides C, Haring MA, Schuurink RC (2008) The Arabidopsis herl mutant implicates GABA in £"-2-hexanal responsiveness. Plant J 53:197-213

Miyashita Y, Good AG (2008) Contribution of the GABA shunt to hypoxia-induced alanine accumulation in roots of Arabidopsis thaliana. Plant Cell Physiol 49:92-102 Morse DE, Hooker N, Duncan H, Jensen L (1979) g-aminobutyric acid, a neurotransmitter, induces planktonic abalone larvae to settle and begin metamorphosis. Science 204:407-410 Morse ANC, Morse DE (1984) Recruitment and metamorphosis of Haliotis larvae induced by molecules uniquely available at the surface of crustose red algae . J Exp Mar Biol Ecol 75:191-215

Oliver RP, Solomon PS (2004) Does the oxidative stress used by plants for defence provide a source of nutrients for pathogenic fungi?. Trends Plant Sci 9:472-473 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 114:47-59 Pasentsis K, Falara V, Pateraki I, Gerasopoulos D, Kanellis AK (2007) Identification and expression profiling of low oxygen regulated genes from Citrus flavedo tissues using RT-PCR differential display. J Exp Bot 58:2203-2216 Prell J, Boesten B, Poole P, Priefer UB (2002) The Rhizobium leguminosarum bv. viciae VF39 g-aminobutyrate (GABA) aminotransferase gene (gabT) is induced by GABA and highly expressed in bacteroids. Microbiology 148:615-623 Ramputh A-I, Bown AW (1996) Rapid g-aminobutyric acid synthesis and the inhibition ofthe growth and development of oblique-banded leaf-roller larvae. Plant Physiol 111:1349-1352 Reggiani R, Cantu CA, Brimballa I, Britani A (1988) Accumulation and interconversion ofamino acids in rice roots under anoxia . Plant Cell Physiol 29 : 981 - 987 Ricoult C, Cliquet J-B, Limami AM (2005) Stimulation of alanine amino transferase (AlaAT) gene expression and alanine accumulation in embryo axis of the model legume Medicago truncatula contribute to anoxia stress tolerance. Physiol Plant 123:30-39 Secor J, Schrader LE (1985) Amino acid efflux from cells and leaf discs. In: Shibles R. (ed) World

Soybean Conference III: Proceedings. Westview Co. pp 749-758 Serraj R, Shelp BJ, Sinclair TR (1998) Accumulation of g-aminobutyric acid in nodulated soybean in response to drought stress. Physiol Plant 102:79-86 Shelp BJ, Walton CS, Snedden WA, Tuin LG, Oresnik IJ, Layzell DB (1995) GABA shunt in developing soybean seeds is associated with hypoxia. Physiol Plant 94:219-228 Shelp BJ, Bown AW, McLean MD (1999) Metabolism and functions of gamma-aminobutyric acid. Trends Plant Sci 4:446-452 Shelp BJ, Bown AW, Faure D (2006) Extracellular g-aminobutyrate mediates communication between plants and other organisms. Plant Physiol 142:1350-1352 Simpson JP, Di Leo R, Dhanoa PK, Allan WL, Makhmoudova A, Clark SM, Hoover GJ, Mullen RT, Shelp BJ (2008) Identification and characterization of a plastid-localized Arabidopsis glyoxylate reductase isoform: comparison with a cytosolic isoform and implications for cellular redox homeostasis and aldehyde detoxification. J Exp Bot 59(9):2545-2554 Solomon PS, Oliver RP (2001) The nitrogen content ofthe tomato leaf apoplast increases during infection by Cladosporium fulvum. Planta 213:241-249 Solomon PS, Oliver RP (2002) Evidence that g-aminobutyric acid is a major nitrogen source during

Cladosporium fulvum infection of tomato . Planta 214 : 414 - 420 Trapido-Rosenthal HG, Morse DE (1986) Availability of chemosensory receptors is down-regulated by habituation of larvae to a morphogenetic signal. Proc Natl Acad Sci USA 83:7658-7662 Tsishida T, Murai T (1987) Conversion of glutamic acid to g-aminobutyric acid in tea leaves under anaerobic conditions. Agric Biol Chem 51:2805-2871 Valle EM, Boggio SB, Heldt HW (1998) Free amino acid composition of phloem sap and growing fruit of Lycopersicon esculentum. Plant Cell Physiol 39:458-461 Van Cauwenberghe OR, Shelp BJ (1999) Biochemical characterization of partially purified

GABA: pyruvate transaminase from Nicotiana tabacum. Phytochemistry 52:575-581 Van Cauwenberghe OR , Makhmoudova A , McLean MD , Clark SM , Shelp BJ (2002) Plant pyruvate-dependent gamma-aminobutyrate transaminase: identification of an Arabidopsis cDNA and its expression in Escherichia coli. Can J Bot 80:933-941

Vance CP, Heichel GH (1991) Carbon in N2 fixation: limitation or exquisite adaptation. Annu Rev

Plant Physiol Plant Mol Biol 42:373-392 Wallace W, Secor J, Schrader LE (1984) Rapid accumulation of gamma-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 Wu C, Zhou S, Zhang Q, Zhao W, Peng Y (2006) Molecular cloning and differential expression of an g-aminobutyrate transaminase gene, OsGABA-T, in rice (Oryza sativa) leaves infected with blast fungus. J Plant Res 119:663-669 Yevtushenko D , McLean MD , Peiris SE , Van Cauwenberghe OR , Shelp BJ (2003) Calcium/ calmodulin activation of two divergent glutamate decarboxylases from tobacco . J Exp Bot 54:2001-2002

Yu G , Liang J , He Z , Sun M (2006) Quantum dot-mediated detection of g-aminobutyric acid binding sites on the surface of living pollen protoplasts in tobacco. Chem Biol 13:723-731

0 0

Post a comment