A role for glycine in the gating of plant NMDA‐like receptors

Abstract

These authors contributed equally to this work. SummaryThe amino acid glycine has a well-established role in signalling in the mammalian central nervous system. For example, glycine acts synergistically with the major excitatory neurotransmitter, glutamate, to regulate the in¯ux of ions such as calcium, through N-methyl-D-aspartate (NMDA) receptors. Plants possess NMDAlike receptors, generically referred to as glutamate receptors (GLRs), named on the basis of their presumed ligand, glutamate. Previously, glycine has not been implicated in plant GLR activity or any other aspect of plant signalling. Using transgenic Arabidopsis seedlings expressing aequorin to monitor ligand-mediated changes in the cytosolic concentration of Ca 2 ([Ca 2 ] cyt ), the data presented herein show that glutamate and glycine act synergistically to control ligand-mediated gating of calcium in plants. Glutamate and glycine synergism also regulates hypocotyl elongation. Transient increases in [Ca 2 ] cyt mediated by glutamate and glycine, as well as hypocotyl elongation, were inhibited by 6,7-dinitroquinoxaline-2,3 dione (DNQX), a competitive inhibitor of animal GLRs. Using a multiscale docking algorithm in combination with a molecular model of the ligand-binding domain of plant GLRs, evidence is provided indicating that glycine, and not glutamate, is likely to be the natural ligand for most plant GLR subunits. These ®ndings uncover a hitherto unconsidered role for glycine signalling in plants, and suggest that the synergistic action of glutamate and glycine at NMDA-like receptors predates the divergence of plants and animals.

Glutamate Receptor Subtypes Evidenced by Differences in Desensitization and Dependence on theGLR3.3andGLR3.4Genes

“…The Ca 21 rise triggered by Gly in isolated hypocotyl segments ( Fig. 1C) was also similar to the Ca 21 response measured in whole seedlings (Dennison and Spalding, 2000;Dubos et al, 2003) and roots (Qi et al, 2006). Hypocotyl cells depolarized similarly to the same six amino acids as roots, namely, Ala, Asn, Cys, Glu, Gly, and Ser, and, as in roots, the response depended strongly on the GLR3.3 Glu receptor (Fig.…”

“…These roles include regulation of hypocotyl elongation (Lam et al, 1998;Dubos et al, 2003), sensing of mineral nutrient status (Kim et al, 2001), regulating carbon/nitrogen balance (Kang and Turano, 2003), resisting aluminum toxicity (Sivaguru et al, 2003) and cold (Meyerhoff et al, 2005), root meristem function (Li et al, 2006;Walch-Liu et al, 2006), as well as jasmonate-mediated defense mechanisms (Kang et al, 2006).…”

A Rice Glutamate Receptor–Like Gene Is Critical for the Division and Survival of Individual Cells in the Root Apical Meristem

“…The identification of the putative iGluR genes in plants has given rise to the hypothesis that a primitive signaling mechanism involving excitatory amino acids or related small molecules existed before the divergence of plants and animals (Chiu et al, 2002). After the discovery of the plant GLRs, indirect evidence for the participation of those putative receptors in Glu-mediated calcium signaling was reported (Dennison and Spalding, 2000;Dubos et al, 2003). By means of molecular modeling and applying different iGluR agonists in combination with a pH-homeostasis mutant, det3, some characteristics of the N-methyl-D-aspartate family of iGluRs were reported in Arabidopsis (Dubos et al, 2003(Dubos et al, , 2005 and implicated in the redistribution of carbon (Dubos et al, 2005).…”

“…After the discovery of the plant GLRs, indirect evidence for the participation of those putative receptors in Glu-mediated calcium signaling was reported (Dennison and Spalding, 2000;Dubos et al, 2003). By means of molecular modeling and applying different iGluR agonists in combination with a pH-homeostasis mutant, det3, some characteristics of the N-methyl-D-aspartate family of iGluRs were reported in Arabidopsis (Dubos et al, 2003(Dubos et al, , 2005 and implicated in the redistribution of carbon (Dubos et al, 2005). The functional properties of these proteins and their roles in plant physiology and development, however, remain elusive because of a shortage of genetic studies.…”

Glutamate Receptor-Like Channel3.3 Is Involved in Mediating Glutathione-Triggered Cytosolic Calcium Transients, Transcriptional Changes, and Innate Immunity Responses in Arabidopsis

“…The predicted protein structure of AtGLRs includes conserved transmembrane and extracellular ligand binding domains of iGLRs and G protein-coupled receptors (GPCRs; Chiu et al, 1999;Turano et al, 2001). Different plant GLR members are suggested to play roles in various physiological processes, including mineral nutrient homeostasis (Kim et al, 2001;Dubos et al, 2003;Kang et al, 2006;Aouini et al, 2012), carbon/nitrogen balance (Kang and Turano, 2003), root development (Li et al, 2006), stomata movement (Cho et al, 2009), abscisic acid sensing (Kang et al, 2004), gravitropism sensing (Miller et al, 2010), and pollen tube elongation (Michard et al, 2011). Recently, pharmacological approaches produced evidence that AtGLRs could be involved in innate immunity response in Arabidopsis seedlings (Kwaaitaal et al, 2011(Kwaaitaal et al, , 2012.…”