Glutamate receptors are well characterized channels that mediate cell-to-cell communication during neurotransmission in animals, but their functional role in organisms without a nervous system remains unclear. In plants, genes of the GLUTAMATE RECEPTOR-LIKE (GLR) family have been implicated in defence against pathogens, reproduction, control of stomata aperture and light signal transduction. However, the large number of GLR genes present in angiosperm genomes (20 to 70) has prevented the observation of strong phenotypes in loss-of-function mutants. Here we show that in the basal land plant Physcomitrella patens, mutation of the GLR genes GLR1 and GLR2 causes failure of sperm cells to target the female reproductive organs. In addition, we show that GLR genes encode non-selective Ca-permeable channels that can regulate cytoplasmic Ca and are needed to induce the expression of a BELL1-like transcription factor essential for zygote development. Our work reveals functions for GLR channels in sperm chemotaxis and transcriptional regulation. Sperm chemotaxis is essential for fertilization in both animals and early land plants such as bryophytes and pteridophytes. Therefore, our results suggest that ionotropic glutamate receptors may have been conserved throughout plant evolution to mediate cell-to-cell communication during sexual reproduction.

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The phytohormone ethylene has numerous effects on plant growth and development. Its immediate precursor, 1-aminocyclopropane-1-carboxylic acid (ACC), is a non-proteinogenic amino acid produced by ACC SYNTHASE (ACS). ACC is often used to induce ethylene responses. Here, we demonstrate that ACC exhibits ethylene-independent signaling in Arabidopsis thaliana reproduction. By analyzing an acs octuple mutant with reduced seed set, we find that ACC signaling in ovular sporophytic tissue is involved in pollen tube attraction, and promotes secretion of the pollen tube chemoattractant LURE1.2. ACC activates Ca 2+-containing ion currents via GLUTAMATE RECEPTOR-LIKE (GLR) channels in root protoplasts. In COS-7 cells expressing moss PpGLR1, ACC induces the highest cytosolic Ca 2+ elevation compared to all twenty proteinogenic amino acids. In ovules, ACC stimulates transient Ca 2+ elevation, and Ca 2+ influx in octuple mutant ovules rescues LURE1.2 secretion. These findings uncover a novel ACC function and provide insights for unraveling new physiological implications of ACC in plants.

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Plant glutamate receptor-like (GLR) genes encode ion channels with demonstrated roles in electrical and calcium (Ca2+) signaling. The expansion of the GLR family along the lineage of land plants, culminating in the appearance of a multiclade system among flowering plants, has been a topic of interest since their discovery nearly 25 years ago. GLRs are involved in many physiological processes, from wound signaling to transcriptional regulation to sexual reproduction. Emerging evidence supports the notion that their fundamental functions are conserved among different groups of plants as well. In this review, we update the physiological and genetic evidence for GLRs, establishing their role in signaling and cell–cell communication. Special emphasis is given to the recent discussion of GLRs’ atomic structures. Along with functional assays, a structural view of GLRs’ molecular organization presents a window for novel hypotheses regarding the molecular mechanisms underpinning signaling associated with the ionic fluxes that GLRs regulate. Newly uncovered transcriptional regulations associated with GLRs—which propose the involvement of genes from all clades of Arabidopsis thaliana in ways not previously observed—are discussed in the context of the broader impacts of GLR activity. We posit that the functions of GLRs in plant biology are probably much broader than anticipated, but describing their widespread involvement will only be possible with ( a) a comprehensive understanding of the channel's properties at the molecular and structural levels, including protein–protein interactions, and ( b ) the design of new genetic approaches to explore stress and pathogen responses where precise transcriptional control may result in more precise testable hypotheses to overcome their apparent functional redundancies. Expected final online publication date for the Annual Review of Plant Biology, Volume 74 is May 2023. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

This article comments on: https://doi.org/10.1111/pce.13759

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