A Plant Homolog of Animal Glutamate Receptors Is an Ion Channel Gated by Multiple Hydrophobic Amino Acids

Hydrophobic amino acids, rather than glutamate, activate the Arabidopsis glutamate receptor homolog AtGLR1.4. Ionotropic Amino Acid Sensor Sequence similarity suggests that there are plant homologs of animal ionotropic glutamate receptors, which are ligand-gated, glutamate-activated ion channels. Tapken et al. showed that the Arabidopsis homolog AtGLR1.4 behaved as anything but a glutamate-activated channel. Of the 20 amino acids tested on AtGLR1.4 expressed in Xenopus oocytes, methionine was the most effective and potent of the seven amino acids that activated the channel, arginine was the most effective competitive antagonist of methionine-activated current, and glutamate did not affect channel activity. Electrophysiological analysis showed that AtGLR1.4 was a nonselective cation channel. Analysis of leaves from knockout plants indicated that AtGLR1.4 mediated membrane depolarization in response to methionine but not glutamate. Thus, to call these glutamate receptors in plants is a misnomer. Ionotropic glutamate receptors (iGluRs) are ligand-gated cation channels that mediate neurotransmission in animal nervous systems. Homologous proteins in plants have been implicated in root development, ion transport, and several metabolic and signaling pathways. AtGLR3.4, a plant iGluR homolog from Arabidopsis thaliana, has ion channel activity and is gated by asparagine, serine, and glycine. Using heterologous expression in Xenopus oocytes, we found that another Arabidopsis iGluR homolog, AtGLR1.4, functioned as a ligand-gated, nonselective, Ca2+-permeable cation channel that responded to an even broader range of amino acids, none of which are agonists of animal iGluRs. Seven of the 20 standard amino acids—mainly hydrophobic ones—acted as agonists, with methionine being most effective and most potent. Nine amino acids were antagonists, and four, including glutamate and glycine, had no effect on channel activity. We constructed a model of this previously uncharacterized ligand specificity and used knockout mutants to show that AtGLR1.4 accounts for methionine-induced membrane depolarization in Arabidopsis leaves.

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