Role of acetylcholine and acetylcholinesterase in improving abiotic stress resistance/tolerance

Figures & data

Figure 1. The illustration presents mechanisms and responses linked to the interaction of ACh-AChE with different phytohormones and genes for improving plant growth and enhancing stress tolerance to various abiotic stimuli. IAA, indole-3-acetic acid; CKs, cytokines; ABA, abscisic acid; GAs, gibberellic acids; SOD, superoxide dismutase; CAT, catalase; APX, Ascorbate peroxidase; POD, peroxidase; LeEXPA2, tomato expansin gene; HEMA1, glutamyl-tRNA reductase; ZmKAO, Ent-kaurenoic acid oxidase; CHLH, Mg-chelatase; CAO, Chlorophyllide-a-Oxygenase and POR, protochlorophyllide oxidoreductase.

Table 1. An overview of ACh-AChE activity and defense mechanisms in plants under abiotic stresses.

Involvement of ACh
Abiotic stress	Species	Effect	Suggested mechanism	References
Osmotic stress	Vicia faba	Reduced endogenous ACh level in the abaxial epidermis of leaves, xylem sap, and root tips	The reduction in ACh content at the root tips led to a drop in ACh transport from root to shoot causing a decrease in stomatal opening and transpiration rate	[13]
Salinity stress	Nicotiana benthamiana	Reduced lipid peroxidation, Na/K ratio. Increased production of cell wall synthesizing genes and triggered pathways associated with phytohormones. Also improved gas-exchange parameters, relative water content, and photosynthesis	Amelioration of chlorophyll biosynthetic intermediates like protoporphyrin-IX, Mg-photoporphyrin-IX and protochlorophyllide, upregulation of HEMA1, CHLH, CAO and POR genes, modulations in SOD and POD activity, maintain ion homeostasis, hydraulic conductivity and water balance	[10,78]
Salinity stress	Zea mays	Increased plant growth and germination	Antioxidants, upregulation of α-amylase and β-galactosidase activity and ZmKAO (involved in gibberellin signaling), downregulation of ZmNCED3 (involved in ABA signaling)	[11]
Osmotic stress	Glycine max (L.) Merrill	Increased germination, growth and dry weight	ACh combined with auxin increased transcription of the expansin LeEXPA2 gene	[8]
Osmotic stress	Glycine max	Improved water use efficiency and photosynthesis	Antioxidants, reduced ABA2 gene expression,	[79]
Osmotic stress	Nicotiana benthamiana	Increased osmoregulation in the leaf and root cells, decreased membrane lipid peroxidation and enhanced photosynthesis	Regulate stomatal movement, increased PSII and RUBISCO activity, and upregulation of antioxidants	[80]
Metal stress	Nicotiana benthamiana	Restored normal chlorophyll synthesis pathway	Improved photosystem II activity, antioxidants, declined Cd accumulation, weakened Mg-chelatase gene expression	[81]
Heat stress	Vigna sinensis	Reduced endogenous ACh content in leaf, stem and secondary pulvinus	ACh hydrolysis may control the recovery of ions	[82]
	Raphanus sativus
	Cucumis sativus
Involvement of AChE
Salinity stress	Salicornia Europaea	High AChE activity observed in lower stem and roots	Ion transportation and exclude excess NaCl from roots	[83]
Heat stress	Zea mays	Increased AChE activity in the endodermal cells of the node	Opening and closing of channels in plasma membrane	[84,85]
Heat stress	Vigna sinensis	Observed high AChE activity in roots, nodes, and pulvini	Differences in ion conductivity and channel opening in cells	[86]
	Raphanus sativus
	Cucumis sativus
Involvement of ACh-AChE
Heat stress	Macroptilium atropurpureum	In both primary and secondary pulvini, AChE activity was increased reduced endogenous ACh content with improved leaf recovery	ACh may control ion or hormone fluxes by regulating the opening of ion channels	[87]
Salinity stress	Solanum lycopersicum	Increased AChE activity with reduced endogenous ACh content	Ion transportation and exclude excess NaCl from roots	[88]

Table

Year	Number of publications (Research/ Review/Book)	References
2013	4	[99], [71], [100], [101],
2014	5	[102], [103], [104], [51], [105]
2015	4	[50], [15], [58], [106]
2016	6	[49], [107], [108], [59], [109], [110]
2017	1	[111],
2018	3	[112], [113], [114]
2019	3	[10], [115], [116]
2020	2	[96], [81], [92]
2021	1	[78]
2022	1	[4]
2023	4	[52], [65], [93], [117]

Wang H, Zhang S, Wang X, et al. Role of acetylcholine on plant root-shoot signal transduction. Chinese Sci Bull. 2003;48(6):570–573. doi: 10.1360/03tb9121

 Google Scholar

Qin C, Su YY, Li BS, et al. Acetylcholine mechanism of action to enhance tolerance to salt stress in Nicotiana benthamiana. Photosynthetica. 2019;57(2):590–598. doi: 10.32615/ps.2019.084

 Web of Science ®Google Scholar

Qin C, Ahanger MA, Lin B, et al. Comparative transcriptome analysis reveals the regulatory effects of acetylcholine on salt tolerance of Nicotiana benthamiana. Phytochemistry. 2021;181:112582. doi: 10.1016/j.phytochem.2020.112582

 PubMed Web of Science ®Google Scholar

Shen J, Qin C, Qin Y, et al. Acetylcholine alleviates salt stress in Zea mays L. by promoting seed germination and regulating phytohormone level and antioxidant capacity. J Plant Growth Regul. 2024;43(1):341–352. doi: 10.1007/s00344-023-11089-7

 Web of Science ®Google Scholar

Braga I, Pissolato MD, Souza GM. Mitigating effects of acetylcholine supply on soybean seed germination under osmotic stress. Braz J Bot. 2017;40(3):617–624. doi: 10.1007/s40415-017-0367-2

 Web of Science ®Google Scholar

Braga-Reis I, Neris DM, Ribas AF, et al. Gamma-aminobutyric acid (GABA) and acetylcholine (ACh) alleviate water deficit effects in soybean: From gene expression up to growth performance. Environ Exp Bot. 2021;182:104303. doi: 10.1016/j.envexpbot.2020.104303

 Web of Science ®Google Scholar

Qi M, Zheng X, Niu G, et al. Supplementation of acetylcholine mediates physiological and biochemical changes in tobacco lead to alleviation of damaging effects of drought stress on growth and photosynthesis. J Plant Growth Regul. 2023;42(8):4616–4628. doi: 10.1007/s00344-022-10642-0

 Web of Science ®Google Scholar

Su Y, Qin C, Begum N, et al. Acetylcholine ameliorates the adverse effects of cadmium stress through mediating growth, photosynthetic activity and subcellular distribution of cadmium in tobacco (Nicotiana benthamiana). Ecotoxicol Environ Saf. 2020;198:110671. doi: 10.1016/j.ecoenv.2020.110671

 PubMed Web of Science ®Google Scholar

Momonoki YS, Momonoki T. Changes in acetylcholine levels following leaf wilting and leaf recovery by heat stress in plant cultivars. Jpn J Crop Sci. 1991;60(2):283–290.

 Google Scholar

Momonoki YS, Oguri S, Kato S, et al. Studies on the mechanism of salt tolerance in Salicornia europaea L.: III, Salt accumulation and ACh function. Jpn J Crop Sci. 1996;65(4):693–699.

 Google Scholar

Momonoki YS, Momonoki T, Whallon JH. Acetylcholine as a signaling system to environmental stimuli in plants: I. Contribution of Ca2+ in heat-stressed Zea mays seedlings. Jpn J Crop Sci. 1996;65(2):260–268.

 Google Scholar

Yamamoto K, Sakamoto H, Momonoki YS. Maize acetylcholinesterase is a positive regulator of heat tolerance in plants. J Plant Physiol. 2011;168(16):1987–1992. doi: 10.1016/j.jplph.2011.06.001

 Web of Science ®Google Scholar

Momonoki YS, Momonoki T. Changes in acetylcholine-hydrolyzing activity in heat-stressed plant cultivars. Jpn J Crop Sci. 1993;62(3):438–446.

 Google Scholar

Momonoki YS, Momonoki T. The influence of heat stress on acetylcholine content and its hydrolyzing activity in Macroptilium atropurpureum cv. Siratro. Jap J Crop Sci. 1992;61(1):112–118.

 Google Scholar

Sarangle Y, Bamel K, Purty RS. Identification of acetylcholinesterase like gene family and its expression under salinity stress in Solanum lycopersicum. J Plant Growth Regul. 2024;43(3):940–960. doi: 10.1007/s00344-023-11152-3

 Web of Science ®Google Scholar

Bita CE, Gerats T. Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress-tolerant crops. Front Plant Sci. 2013;4:273. doi: 10.3389/fpls.2013.00273

 PubMed Web of Science ®Google Scholar

Muralidharan M, Buss K, Larrimore KE, et al. The Arabidopsis thaliana ortholog of a purported maize cholinesterase gene encodes a GDSL-lipase. Plant Mol Biol. 2013;81(6):565–576. doi: 10.1007/s11103-013-0021-8

 Web of Science ®Google Scholar

Roshchina V, Yashin V. Secreting cells of Saintpaulia as a model for studies of plant cholinergic system. Biologicheskie Membrany. 2013;30(5–6):454–461.

 Web of Science ®Google Scholar

Roshchina V, Yashin, VA, Švirst, NA, et al. Secreting cells as models to study the role of acetylcholine in signalling and communications of organisms. In: Zinchenko VP, Berezhnov AV, editors. The book of international conference “reception and intracellular signaling; 27–30 May 2013; EMA Pushchino; 2013. Vol. 2. p. 790–795

 Google Scholar

Roshchina VAV. Model systems to study the excretory function of higher plants. Springer Dordrecht: Springer; 2014.

 Google Scholar

Michelson MJ, Zeimal EV. Acetylcholine: an approach to the molecular mechanism of action. 1st ed. Oxford: Pergammon Press; 1973.

 Google Scholar

Kennedy DO. Plants and the human brain. USA: Oxford University Press; 2014.

 Google Scholar

Di Sansebastiano G-P, Fornaciari S, Barozzi F, et al. New insights on plant cell elongation: a role for acetylcholine. Int J Mol Sci. 2014;15(3):4565–4582. doi: 10.3390/ijms15034565

 Web of Science ®Google Scholar

Malik S. Cholinesterases in animals and Arabidopsis Thaliana. Int J Innovative Res Dev. 2014;3(2):280–281.

 Google Scholar

Bamel K, Gupta R, Gupta SC. Nicotine promotes rooting in leaf explants of in vitro raised seedlings of tomato, Lycopersicon esculentum Miller var. Pusa Ruby. Int Immunopharmacol. 2015;29(1):231–234. doi: 10.1016/j.intimp.2015.09.001

 Web of Science ®Google Scholar

Murata J, Watanabe T, Sugahara K, et al. High-resolution mass spectrometry for detecting Acetylcholine in Arabidopsis. Plant Signal Behav. 2015;10(10):e1074367. doi: 10.1080/15592324.2015.1074367

 Google Scholar

Yamamoto K, Shida S, Honda Y, et al. Overexpression of acetylcholinesterase gene in rice results in enhancement of shoot gravitropism. Biochem Biophys Res Commun. 2015;465(3):488–493. doi: 10.1016/j.bbrc.2015.08.044

 Web of Science ®Google Scholar

Wessler I, Michel-Schmidt R, Kirkpatrick CJ. pH-dependent hydrolysis of acetylcholine: Consequences for non-neuronal acetylcholine. Int Immunopharmacol. 2015;29(1):27–30. doi: 10.1016/j.intimp.2015.04.039

 Web of Science ®Google Scholar

Bamel K, Gupta R, Gupta SC. Acetylcholine suppresses shoot formation and callusing in leaf explants of in vitro raised seedlings of tomato, Lycopersicon esculentum Miller var. Pusa Ruby. Plant Signal Behav. 2016;11(6):e1187355. doi: 10.1080/15592324.2016.1187355

 Google Scholar

Roshchina VV. The fluorescence methods to study neurotransmitters (Biomediators) in plant cells. J Fluoresc. 2016;26(3):1029–1043. doi: 10.1007/s10895-016-1791-6

 Web of Science ®Google Scholar

Roshchina VV. New Trends and Perspectives in the Evolution of Neurotransmitters in Microbial, Plant, and Animal Cells. In: Lyte M, editor. Microbial Endocrinology: Interkingdom Signaling in Infectious Disease and Health. Advances in Experimental Medicine and Biology. Springer Cham: Springer; 2016. Vol. 874. p. 25–77.

 Google Scholar

Yamamoto K, Sakamoto H, Momonoki YS. Altered expression of acetylcholinesterase gene in rice results in enhancement or suppression of shoot gravitropism. Plant Signal Behav. 2016;11(4):e1163464. doi: 10.1080/15592324.2016.1163464

 Google Scholar

Fillafer C, Schneider MF. On the excitation of action potentials by protons and its potential implications for cholinergic transmission. Protoplasma. 2016;253(2):357–365. doi: 10.1007/s00709-015-0815-4

 Web of Science ®Google Scholar

Roshchina V, Shvirst N. Cholinesterase in contractile structures of plants and animals: histochemical experiments with azocompounds. In Biological Motility Ed Udaltsov SN Materials of International Symposium. Pushchino: SYNCHROBOOK; 2016. p. 198–202.

 Google Scholar

Amaroli A. Neurotransmitters or Biomediators. Cholinergic Syst Protozoa EC Microbiol. 2017;7:40–41.

 Google Scholar

Ramakrishna A, Roshchina VV. Neurotransmitters in plants: perspectives and applications. Boca Raton: CRC Press, Taylor & Francis; 2018. doi:10.1201/b22467

 Google Scholar

Roshchina V. Cholinesterase in secreting cells and isolated organelles of plants. Biologicheskie Membrany. 2018;35(2):143–149.

 Web of Science ®Google Scholar

Kurchii BA. Possible participation of acetylcholine in free-radical processes (redox reactions) in living cells. In: Ramakrishna A, Roshchina V, editors. Neurotransmitters in Plants: Perspectives and Applications. Boca Raton:: CRC Press, Taylor & Francis; 2018. p. 211–217.

 Google Scholar

Roshchina VV. Inter-and intracellular signaling in plant cells with participation of neurotransmitters (Biomediators). In: Ramakrishna A, and Roshchina V, editors. Neurotransmitters in Plants: perspectives and Applications. Boca Raton: CRC Press, Taylor & Francis; 2018. p. 147–180.

 Google Scholar

Roshchina V. Tools for microanalysis of the neurotransmitter location in plant cells. Neurotransmitters in plants, perspectives and applications. Boca Raton: CRC Press; 2018. p. 135–146.

 Google Scholar

Qin C, Ahanger MA, Zhou J, et al. Beneficial role of acetylcholine in chlorophyll metabolism and photosynthetic gas exchange in Nicotiana benthamiana seedlings under salinity stress. Plant Biol (Stuttg). 2020;22(3):357–365. doi: 10.1111/plb.13079

 Web of Science ®Google Scholar

Roychoudhury A. Neurotransmitter acetylcholine comes to the plant rescue. J Mol Cell Biol Forecast. 2020;3(1):1019.

 Google Scholar

Raza A, Salehi H, Rahman MA, et al. Plant hormones and neurotransmitter interactions mediate antioxidant defenses under induced oxidative stress in plants. Front Plant Sci. 2022;13:961872. doi: 10.3389/fpls.2022.961872

 PubMed Web of Science ®Google Scholar

Bamel K, Mondal N. In vitro culture using nicotine and d-tubocurarine and in silico analysis depict the presence of acetylcholine receptor (AChR) in tomato (Solanum lycopersicum L.). Vitro Cell Dev Biol Plant. 2023;59(1):39–48. doi: 10.1007/s11627-022-10324-2

 Web of Science ®Google Scholar

Sarangle Y, Bamel K, Purty RS. Identification of acetylcholinesterase like gene family and its expression under salinity stress in Solanum lycopersicum. J Plant Growth Regul. 2023;43(3):1–21. doi: 10.1007/s00344-023-11152-3

 Web of Science ®Google Scholar

Shen J, Qin C, Qin Y, et al. Acetylcholine alleviates salt stress in Zea mays L. by promoting seed germination and regulating phytohormone level and antioxidant capacity. J Plant Growth Regul. 2023;43(1):1–12. doi: 10.1007/s00344-023-11089-7

 Web of Science ®Google Scholar

Yang L, Ma X, Guo Y, et al. Acetylcholine (ACh) enhances Cd tolerance through transporting ACh in vesicles and modifying Cd absorption in duckweed (Lemna turionifera 5511). Environ Pollut. 2023;335:122305. doi: 10.1016/j.envpol.2023.122305

 Web of Science ®Google Scholar

Data availability statement

Data sharing is not applicable to this article as no new data were created or analyzed in this study.