Comparing plant and animal glutamate receptors: common traits but different fates?

Abstract

Animal ionotropic glutamate receptors (iGluRs) are ligand-gated channels whose evolution is intimately linked to the one of the nervous system, where the agonist glutamate and co-agonists glycine/D-serine act as neuro-transmitters or -modulators. While iGluRs are specialized in neuronal communication, plant glutamate receptor-like (GLR) homologues have evolved many plant-specific physiological functions, such as sperm signaling in moss, pollen tube growth, root meristem proliferation, innate immune and wound responses. GLRs have been associated with Ca2+ signaling by directly channeling its extracellular influx into the cytosol. Nevertheless, very limited information on functional properties of GLRs is available, and we mostly rely on structure/function data obtained for animal iGluRs to interpret experimental results obtained for plant GLRs. Yet, a deeper characterization and better understanding of plant GLRs is progressively unveiling original and different mode of functions when compared to their mammalian counterparts. Here, we review the function of plant GLRs comparing their predicted structure and physiological roles to the well-documented ones of iGluRs. We conclude that interpreting GLR function based on comparison to their animal counterparts calls for caution, especially when presuming physiological roles and mode of action for plant GLRs from comparison to iGluRs in peripheral, non-neuronal tissues.

Structure of the Glutamate-Like Receptor GLR3.2 ligand-binding domain

“…Overall, the ligand-binding pocket of GLR3.2 is shaped to universally bind differently sized amino acids (for example, glycine versus methionine) by exploiting the same interactions for binding the conserved amino acid core and adjusting the fit of the side chain into the corresponding biding pocket cavity with water. This explains a diverse range of ligand specificity previously observed for GLRs, with at least 12 of the 20 proteinogenic amino acids and D-Serine serving as agonists for the most studied AtGLR1.2, AtGLR1.4, AtGLR3.3, AtGLR3.4, and AtGLR3.5 (Forde and Roberts, 2014;Kong et al, 2016;Michard et al, 2011;Tapken et al, 2013;Vincill et al, 2012;Vincill et al, 2013;Wudick et al, 2018a). Such promiscuity has never been observed in iGluRs.…”

“…Different number of GLRs are found in genomes of plants, including 20 for Arabidopsis thaliana, 2 for moss, 9 for ginkgo, 40 for pine and, 13 for tomato (Aouini et al, 2012;De Bortoli et al, 2016;Ortiz-Ramirez et al, 2017;Price et al, 2012;Wudick et al, 2018b). Arabidopsis thaliana GLRs (AtGLRs) are phylogenetically divided into 3 different clades (Chiu et al, 2002;Lacombe et al, 2001;Wudick et al, 2018a). AtGLR3.2, a representative of the third clade, was found localized in the plasma membrane (Vincill et al, 2013).…”

‘Calcium is life’

“…Unified representation of Ca 2+ signaling in the plant cell, with different types of organization color coded by quadrant of the ‘textbook’ diagram. Moving clockwise: (i) structures—mitochondria ( Costa et al , 2018 ), pollen tubes ( Wudick et al , 2018 ), and guard cells ( Konrad et al , 2018 ); (ii) processes —ion homeostasis and salt stress tolerance ( Manishankar et al , 2018 ), and nodulation ( Charpentier, 2018 ).…”

“…Multiple functions have been attributed to GLRs, but the field was shaken by the demonstration that they may be involved in the conductance of long-range electrical signaling in response both to herbivore ( Mousavi et al , 2013 ) and aphid ( Vincent et al , 2017 ) feeding. Wudick et al (2018) take a different perspective, and rather focus on the point that given the current uncertainties on regulation by oligomerization, ligand gating, ion specificity and association with other proteins, data from this kind of screening will always be difficult to interpret in terms of channel function. Further structural and evolutionary arguments are raised to make the case that elucidation of the molecular properties of these channels is needed for full understanding of their biological function, as GLRs stand as a good example of the limitations inherent to strictly translating mammalian knowledge of function and regulation.…”

Marine Excitatory Amino Acids: Structure, Properties, Biosynthesis and Recent Approaches to Their Syntheses

“…These receptors are associated with many plant-specific physiological functions, such as sperm signaling in moss, pollen tube growth, root meristem proliferation, and innate immune and wound responses. It should be taken into account that the main physiological roles and modes of action of plant GluRs, in contrast to those in animals, are performed in peripheral, non-neuronal tissues [35].…”