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Plant function and evolutionary biology
RESEARCH ARTICLE

Glutamate and NMDA affect cell excitability and action potential dynamics of single cell of macrophyte Nitellopsis obtusa

Indre Lapeikaite https://orcid.org/0000-0001-7323-1721 A B , Vilmantas Pupkis A , Vladas Neniskis A , Osvaldas Ruksenas A and Vilma Kisnieriene A
+ Author Affiliations
- Author Affiliations

A Institute of Biosciences, Life Sciences Centre, Vilnius University, Sauletekio Avenue. 7, LT-10257 Vilnius, Lithuania.

B Corresponding author. Email: pinivija@gmail.com

Functional Plant Biology 47(12) 1032-1040 https://doi.org/10.1071/FP20074
Submitted: 19 March 2020  Accepted: 11 May 2020   Published: 23 June 2020

Abstract

The effect of glutamate and N-methyl-d-aspartate (NMDA) on electrical signalling – action potentials (AP) and excitation current transients – was studied in intact macrophyte Nitellopsis obtusa (Characeaen) internodal cell. Intracellular glass electrode recordings of single cell in current clamp and two-electrode voltage clamp modes indicate that glutamate (Glu, 0.1–1.0 mM) and NMDA (0.01–1.0 mM) increase electrically induced AP amplitude by hyperpolarising excitation threshold potential (Eth) and prolong AP fast repolarisation phase. Amplitude of Cl current transient, as well as its activation and inactivation durations were also increased. Both Glu and NMDA act in a dose-dependent manner. The effect of NMDA exceeds that of Glu. Ionotropic glutamate receptor inhibitors AP-5 (NMDA-type receptors) and DNQX (AMPA/Kainate-type) have no effect on Nitellopsis cell electrical signalling per se, yet robustly inhibit excitatory effect of NMDA. This study reinforces NMDA as an active component in glutamatergic signalling at least in some plants and stresses the elaborate fine-tuning of electrical signalling.

Additional keywords: amino acids, Characeaen, electrophysiology, voltage-clamp.


References

Beilby MJ (1986) Potassium channels and different states of Chara plasmalemma. Journal of Membrane Biology 89, 241–249.
Potassium channels and different states of Chara plasmalemma.Crossref | GoogleScholarGoogle Scholar |

Beilby MJ (2007) Action potential in Charophytes. International Review of Cytology 257, 43–82.
Action potential in Charophytes.Crossref | GoogleScholarGoogle Scholar | 17280895PubMed |

Beilby MJ, Al Khazaaly S (2016) Re-modeling Chara action potential: I. from Thiel model of Ca2+ transient to action potential form. AIMS Biophysics 3, 431–449.
Re-modeling Chara action potential: I. from Thiel model of Ca2+ transient to action potential form.Crossref | GoogleScholarGoogle Scholar |

Beilby MJ, Casanova MT (2014) ‘The physiology of Characean cells.’ (Springer: Berlin, Germany)

Berestovsky GN, Kataev AA (2005) Voltage-gated calcium and Ca2+-activated chloride channels and Ca2+ transients: voltage-clamp studies of perfused and intact cells of Chara. European Biophysics Journal 34, 973–986.
Voltage-gated calcium and Ca2+-activated chloride channels and Ca2+ transients: voltage-clamp studies of perfused and intact cells of Chara.Crossref | GoogleScholarGoogle Scholar | 15971063PubMed |

Chiu JC, Brenner ED, DeSalle R, Nitabach MN, Holmes TC, Coruzzi GM (2002) Phylogenetic and expression analysis of the glutamate-receptor-like gene family in Arabidopsis thaliana. Molecular Biology and Evolution 19, 1066–1082.
Phylogenetic and expression analysis of the glutamate-receptor-like gene family in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 12082126PubMed |

Choi WG, Miller G, Wallace I, Harper J, Mittler R, Gilroy S (2017) Orchestrating rapid long-distance signalling in plants with Ca2+, ROS and electrical signals. The Plant Journal 90, 698–707.
Orchestrating rapid long-distance signalling in plants with Ca2+, ROS and electrical signals.Crossref | GoogleScholarGoogle Scholar | 28112437PubMed |

Cuin TA, Dreyer I, Michard E (2018) The role of potassium channels in Arabidopsis thaliana long distance electrical signalling: AKT2 modulates tissue excitability while GORK shapes action potentials. International Journal of Molecular Sciences 19, 926
The role of potassium channels in Arabidopsis thaliana long distance electrical signalling: AKT2 modulates tissue excitability while GORK shapes action potentials.Crossref | GoogleScholarGoogle Scholar |

De Bortoli S, Teardo E, Szabò I, Morosinotto T, Alboresi A (2016) Evolutionary insight into the ionotropic glutamate receptor superfamily of photosynthetic organisms. Biophysical Chemistry 218, 14–26.
Evolutionary insight into the ionotropic glutamate receptor superfamily of photosynthetic organisms.Crossref | GoogleScholarGoogle Scholar | 27586818PubMed |

Demidchik V, Essah PA, Tester M (2004) Glutamate activates cation currents in the plasma membrane of Arabidopsis root cells. Planta 219, 167–175.
Glutamate activates cation currents in the plasma membrane of Arabidopsis root cells.Crossref | GoogleScholarGoogle Scholar | 14767768PubMed |

Demidchik V, Shabala S, Isayenkov S, Cuin TA, Pottosin I (2018) Calcium transport across plant membranes: mechanisms and functions. New Phytologist 220, 49–69.
Calcium transport across plant membranes: mechanisms and functions.Crossref | GoogleScholarGoogle Scholar | 29916203PubMed |

Dennison KL, Spalding EP (2000) Glutamate-gated calcium fluxes in Arabidopsis. Plant Physiology 124, 1511–1514.
Glutamate-gated calcium fluxes in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 11115867PubMed |

Felle HH, Zimmermann MR (2007) Systemic signalling in barley through action potentials. Planta 226, 203–214.
Systemic signalling in barley through action potentials.Crossref | GoogleScholarGoogle Scholar | 17226028PubMed |

Feng W, Liu S, Li C, Li X, Song F, Wang B, Chen H, Wu F (2019) Algal uptake of hydrophilic and hydrophobic dissolved organic nitrogen in the eutrophic lakes. Chemosphere 214, 295–302.
Algal uptake of hydrophilic and hydrophobic dissolved organic nitrogen in the eutrophic lakes.Crossref | GoogleScholarGoogle Scholar | 30265937PubMed |

Fisahn J, Herde O, Willmitzer L, Peña-Cortés H (2004) Analysis of the transient increase in cytosolic Ca2+ during the action potential of higher plants with high temporal resolution: requirement of Ca2+ transients for induction of jasmonic acid biosynthesis and PINII gene expression. Plant & Cell Physiology 45, 456–459.
Analysis of the transient increase in cytosolic Ca2+ during the action potential of higher plants with high temporal resolution: requirement of Ca2+ transients for induction of jasmonic acid biosynthesis and PINII gene expression.Crossref | GoogleScholarGoogle Scholar |

Fromm J, Lautner S (2007) Electrical signals and their physiological significance in plants. Plant, Cell & Environment 30, 249–257.
Electrical signals and their physiological significance in plants.Crossref | GoogleScholarGoogle Scholar |

Kang J, Mehta S, Turano FJ (2004) The putative glutamate receptor 1.1 (AtGLR1.1) in Arabidopsis thaliana regulates abscisic acid biosynthesis and signalling to control development and water loss. Plant & Cell Physiology 45, 1380–1389.
The putative glutamate receptor 1.1 (AtGLR1.1) in Arabidopsis thaliana regulates abscisic acid biosynthesis and signalling to control development and water loss.Crossref | GoogleScholarGoogle Scholar |

Kisnieriene V, Lapeikaite I, Pupkis V (2018) Electrical signalling in Nitellopsis obtusa: potential biomarkers of biologically active compounds. Functional Plant Biology 45, 132–142.
Electrical signalling in Nitellopsis obtusa: potential biomarkers of biologically active compounds.Crossref | GoogleScholarGoogle Scholar | 32291027PubMed |

Kisnieriene V, Lapeikaite I, Pupkis V, Beilby MJ (2019) Modeling the action potential in Characeae Nitellopsis obtusa: effect of saline stress. Frontiers in Plant Science 10, 82
Modeling the action potential in Characeae Nitellopsis obtusa: effect of saline stress.Crossref | GoogleScholarGoogle Scholar | 30833949PubMed |

Kong D, Ju C, Parihar A, Kim S, Cho D, Kwak JM (2015) Arabidopsis glutamate receptor homolog3.5 modulates cytosolic Ca2+ level to counteract effect of abscisic acid in seed germination. Plant Physiology 167, 1630–1642.
Arabidopsis glutamate receptor homolog3.5 modulates cytosolic Ca2+ level to counteract effect of abscisic acid in seed germination.Crossref | GoogleScholarGoogle Scholar | 25681329PubMed |

Krol E, Dziubinska H, Trebacz K, Koselski M, Stolarz M (2007) The influence of glutamic and aminoacetic acids on the excitability of the liverwort Conocephalum conicum. Journal of Plant Physiology 164, 773–784.
The influence of glutamic and aminoacetic acids on the excitability of the liverwort Conocephalum conicum.Crossref | GoogleScholarGoogle Scholar | 16891034PubMed |

Kwaaitaal M, Huisman R, Maintz J, Reinstädler A, Panstruga R (2011) Ionotropic glutamate receptor (iGluR)-like channels mediate MAMP-induced calcium influx in Arabidopsis thaliana. The Biochemical Journal 440, 355–373.
Ionotropic glutamate receptor (iGluR)-like channels mediate MAMP-induced calcium influx in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 21848515PubMed |

Lapeikaite I, Dragunaite U, Pupkis V, Ruksenas O, Kisnieriene V (2019) Asparagine alters action potential parameters in single plant cell. Protoplasma 256, 511–519.
Asparagine alters action potential parameters in single plant cell.Crossref | GoogleScholarGoogle Scholar | 30291442PubMed |

Lewis LA, McCourt RM (2004) Green algae and the origin of land plants. American Journal of Botany 91, 1535–1556.
Green algae and the origin of land plants.Crossref | GoogleScholarGoogle Scholar | 21652308PubMed |

Lohaus G, Heldt HW (1997) Assimilation of gaseous ammonia and the transport of its products in barley and spinach leaves. Journal of Experimental Botany 48, 1779–1786.
Assimilation of gaseous ammonia and the transport of its products in barley and spinach leaves.Crossref | GoogleScholarGoogle Scholar |

Lunevsky VZ, Zherelova OM, Vostrikov IY, Berestovsky GN (1983) Excitation of Characeae cell membranes as a result of activation of calcium and chloride channels. Journal of Membrane Biology 72, 43–58.
Excitation of Characeae cell membranes as a result of activation of calcium and chloride channels.Crossref | GoogleScholarGoogle Scholar |

McAinsh MR, Pittman JK (2009) Shaping the calcium signature. New Phytologist 181, 275–294.
Shaping the calcium signature.Crossref | GoogleScholarGoogle Scholar | 19121028PubMed |

Medvedev SS (2018) Principles of calcium signal generation and transduction in plant cells. Russian Journal of Plant Physiology: a Comprehensive Russian Journal on Modern Phytophysiology 65, 771–783.
Principles of calcium signal generation and transduction in plant cells.Crossref | GoogleScholarGoogle Scholar |

Mousavi SAR, Chauvin A, Pascaud F, Kellenberger S, Farmer EE (2013) GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signalling. Nature 500, 422–426.
GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signalling.Crossref | GoogleScholarGoogle Scholar |

Munnik T, Vermeer JE (2010) Osmotic stress‐induced phosphoinositide and inositol phosphate signalling in plants. Plant, Cell & Environment 33, 655–669.
Osmotic stress‐induced phosphoinositide and inositol phosphate signalling in plants.Crossref | GoogleScholarGoogle Scholar |

Nishiyama T, Sakayama H, de Vries J, Buschmann H, Saint-Marcoux D, Ullrich KK, Haas FB, Vanderstraeten L, Becker D, Lang D, Vosolsobě S, Rombauts S, Wilhelmsson PKI, Janitza P, Kern R, Heyl A, Rümpler F, Villalobos LIAC, Clay JM, Skokan R, Toyoda A, Suzuki Y, Kagoshima H, Schijlen E, Tajeshwar N, Catarino B, Hetherington AJ, Saltykova A, Bonnot C, Breuninger H, Symeonidi A, Radhakrishnan GV, Van Nieuwerburgh F, Deforce D, Chang C, Karol KG, Hedrich R, Ulvskov P, Glöckner G, Delwiche CF, Petrášek J, Van de Peer Y, Friml J, Beilby M, Dolan L, Kohara Y, Sugano S, Fujiyama A, Delaux P-M, Quint M, Theißen G, Hagemann M, Harholt J, Dunand C, Zachgo S, Langdale J, Maumus F, Van Der Straeten D, Gould SB, Rensing SA (2018) The Chara genome: secondary complexity and implications for plant terrestrialization. Cell 174, 448–464.e24.
The Chara genome: secondary complexity and implications for plant terrestrialization.Crossref | GoogleScholarGoogle Scholar | 30007417PubMed |

Philippe F, Verdu I, Morère-Le Paven MC, Limami AM, Planchet E (2019) Involvement of Medicago truncatula glutamate receptor-like channels in nitric oxide production under short-term water deficit stress. Journal of Plant Physiology 236, 1–6.
Involvement of Medicago truncatula glutamate receptor-like channels in nitric oxide production under short-term water deficit stress.Crossref | GoogleScholarGoogle Scholar | 30836205PubMed |

Qi Z, Stephens NR, Spalding EP (2006) Calcium entry mediated by GLR3.3, an Arabidopsis glutamate receptor with a broad agonist profile. Plant Physiology 142, 963–971.
Calcium entry mediated by GLR3.3, an Arabidopsis glutamate receptor with a broad agonist profile.Crossref | GoogleScholarGoogle Scholar | 17012403PubMed |

Sakano K, Tazawa M (1984) Intracellular distribution of free amino acids between the vacuolar and extravacuolar compartments in internodal cells of Chara australis. Plant & Cell Physiology 25, 1477–1486.
Intracellular distribution of free amino acids between the vacuolar and extravacuolar compartments in internodal cells of Chara australis.Crossref | GoogleScholarGoogle Scholar |

Sandström J, Pettersson J (1994) Amino acid composition of phloem sap and the relation to intraspecific variation in pea aphid (Acyrthosiphon pisum) performance. Journal of Insect Physiology 40, 947–955.
Amino acid composition of phloem sap and the relation to intraspecific variation in pea aphid (Acyrthosiphon pisum) performance.Crossref | GoogleScholarGoogle Scholar |

Shepherd VA, Beilby MJ, Al Khazaaly SA, Shimmen T (2008) Mechano-perception in Chara cells: the influence of salinity and calcium on touch-activated receptor potentials, action potentials and ion transport. Plant, Cell & Environment 31, 1575–1591.
Mechano-perception in Chara cells: the influence of salinity and calcium on touch-activated receptor potentials, action potentials and ion transport.Crossref | GoogleScholarGoogle Scholar |

Shimmen T (1996) Studies on mechano-perception in characean cells: development of a monitoring apparatus. Plant & Cell Physiology 37, 591–597.
Studies on mechano-perception in characean cells: development of a monitoring apparatus.Crossref | GoogleScholarGoogle Scholar |

Sivaguru M, Pike S, Gassmann W, Baskin TI (2003) Aluminum rapidly depolymerizes cortical microtubules and depolarizes the plasma membrane: evidence that these responses are mediated by a glutamate receptor. Plant & Cell Physiology 44, 667–675.
Aluminum rapidly depolymerizes cortical microtubules and depolarizes the plasma membrane: evidence that these responses are mediated by a glutamate receptor.Crossref | GoogleScholarGoogle Scholar |

Stephens NR, Qi Z, Spalding EP (2008) Glutamate receptor subtypes evidenced by differences in desensitization and dependence on the GLR3.3 and GLR3.4 genes. Plant Physiology 146, 529–538.
Glutamate receptor subtypes evidenced by differences in desensitization and dependence on the GLR3.3 and GLR3.4 genes.Crossref | GoogleScholarGoogle Scholar | 18162597PubMed |

Stolarz M, Dziubinska H (2017) Osmotic and salt stresses modulate spontaneous and glutamate-induced action potentials and distinguish between growth and circumnutation in Helianthus annuus seedlings. Frontiers in Plant Science 8, 1766
Osmotic and salt stresses modulate spontaneous and glutamate-induced action potentials and distinguish between growth and circumnutation in Helianthus annuus seedlings.Crossref | GoogleScholarGoogle Scholar | 29093722PubMed |

Sukhov V, Sukhova E, Vodeneev V (2019) Long-distance electrical signals as a link between the local action of stressors and the systemic physiological responses in higher plants. Progress in Biophysics and Molecular Biology 146, 63–84.
Long-distance electrical signals as a link between the local action of stressors and the systemic physiological responses in higher plants.Crossref | GoogleScholarGoogle Scholar | 30508537PubMed |

Thiel G, Homann U, Plieth C (1997) Ion channel activity during the action potential in Chara: new insights with new techniques. Journal of Experimental Botany 48, 609–622.
Ion channel activity during the action potential in Chara: new insights with new techniques.Crossref | GoogleScholarGoogle Scholar | 21245235PubMed |

Toyota M, Spencer D, Sawai-Toyota S, Jiaqi W, Zhang T, Koo AJ, Howe GA, Gilroy S (2018) Glutamate triggers long-distance, calcium-based plant defense signalling. Science 361, 1112–1115.
Glutamate triggers long-distance, calcium-based plant defense signalling.Crossref | GoogleScholarGoogle Scholar | 30213912PubMed |

Vatsa P, Chiltz A, Bourque S, Wendehenne D, Garcia-Brugger A, Pugin A (2011) Involvement of putative glutamate receptors in plant defence signalling and NO production. Biochimie 93, 2095–2101.
Involvement of putative glutamate receptors in plant defence signalling and NO production.Crossref | GoogleScholarGoogle Scholar | 21524679PubMed |

Wacke M, Thiel G, Hütt MT (2003) Ca2+ dynamics during membrane excitation of green alga Chara: model simulations and experimental data. The Journal of Membrane Biology 191, 179–192.
Ca2+ dynamics during membrane excitation of green alga Chara: model simulations and experimental data.Crossref | GoogleScholarGoogle Scholar | 12571752PubMed |

Walch-Liu P, Liu LH, Remans T, Tester M, Forde BG (2006) Evidence that L-glutamate can act as an exogenous signal to modulate root growth and branching in Arabidopsis thaliana. Plant & Cell Physiology 47, 1045–1057.
Evidence that L-glutamate can act as an exogenous signal to modulate root growth and branching in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |

Weiland M, Mancuso S, Baluska F (2016) Signalling via glutamate and GLRs in Arabidopsis thaliana. Functional Plant Biology 43, 1–25.
Signalling via glutamate and GLRs in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |

Wudick MM, Michard E, Oliveira Nunes C, Feijó JA (2018) Comparing plant and animal glutamate receptors: common traits but different fates? Journal of Experimental Botany 69, 4151–4163.
Comparing plant and animal glutamate receptors: common traits but different fates?Crossref | GoogleScholarGoogle Scholar |

Yao X, Zhu G, Cai L, Zhu M, Zhao L, Gao G, Qin B (2012) Geochemical characteristics of amino acids in sediments of Lake Taihu, a large, shallow, eutrophic freshwater Lake of China. Aquatic Geochemistry 18, 263–280.
Geochemical characteristics of amino acids in sediments of Lake Taihu, a large, shallow, eutrophic freshwater Lake of China.Crossref | GoogleScholarGoogle Scholar |

Young VR, Ajami AM (2000) Glutamate: an amino acid of particular distinction. Journal of Nutrition 130, 892S–900S.
Glutamate: an amino acid of particular distinction.Crossref | GoogleScholarGoogle Scholar | 10736349PubMed |