Mechanical stimulation Mechanical damage
Fungal infection Agrobacterium infection Rhizobium infection Cold stress
Heat stress Oxygen deficiency
Phytohormones Carbon dioxide enrichment
UV stress Oxygen deficiency
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
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).
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.
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