Plant and animal cells live in different ionic milieus and evolved different electrical membrane properties. As membrane transport in plants and animals has diversified through the population of ion channels to tailor signaling strategies, the glutamate receptor superfamily has emerged to conserve a prominent role in Ca2+ and electrical signaling. Ionotropic glutamate receptors (iGluRs) in the mammalian central nervous system are ligand-gated cation channels. Their specificity for glutamate as a ligand required to promote ion channel opening is critical to fast excitatory synaptic transmission and is indispensable for higher cognitive function. Plant glutamate receptor-like channels (GLRs) are also involved in Ca2+ and electrical signaling for a breadth of biotic and abiotic stress responses, sexual reproduction, and cell-cell communication events as determined by genetic analysis. However, the biophysical underpinnings to GLR’s role in cell signaling have only begun to emerge. We addressed the evolutionary conservations of function within the glutamate receptor superfamily and their specialization for plant membrane transport by means of genetics and an electrophysiological characterization of GLR1 encoded by the moss Physcomitrium patens (PpGLR1) using whole-cell patch clamp and Ca2+ imaging. We present a role of PpGLR1 in moss development as a homomeric ion channel involved in light signal transduction that suggests a conservation of function with GLRs found in angiosperms at the physiological level. At the molecular level, we identify the extracellular ligand binding domain of plant GLRs retains structural homology to iGluRs—without the glutamate specificity— while CORNICHON homolog proteins (CNIHs) also have a conserved role in glutamate receptor gating. We further establish distinctive properties of GLRs in ion channel gating and ion selectivity derive from the transmembrane channel pore. The pore works as a direct gate and co-opts the ion selectivity necessary for a membrane depolarization in plant cells by yielding a strong anion permeability with weak mono-cation and Ca2+ permeability. By targeted-mutagenesis, the PpGLR1 selectivity filter was swapped out for the mammalian GluA2 (Q-form) selectivity filter converting a predominantly anion-selective channel poorly responsive to ligands into a primarily cationic channel significantly potentiated by the ligand ACC (1-aminocyclopropane-1-carboxylic acid). These results map the molecular evolution of glutamate receptors shaping the ion channel properties conserving plant GLR’s role in Ca2+ and electrical signaling.