Abstract
In human, acetylcholinesterase (AChE) is a cholinergic enzyme involved in the hydrolysis of neurotransmitter acetylcholine (ACh) into its constituents, choline, and acetate. In plants, the biological functions of AChE are lacking and its existence has been recognized by indirect evidence of its activity. Therefore, in the present investigation, a systematic analysis of the AChE gene family in tomato was performed by integrating structural features, phylogenetic analysis, and its enzyme activity. Using the computational approach, we have identified 87 SlAChE genes containing GDSL lipase/acylhydrolase domain in tomato. In silico expression analysis of SlAChE genes showed up-and down regulation under salinity stress condition. The activity of the AChE enzyme was further confirmed using Ellman assay. Promoter analysis of SlAChE genes using PlantCARE showed the presence of several cis-acting elements including abiotic stress, light, and hormone regulatory elements. In silico screening indicated that tomato AChE homologs are widely distributed in plants. Syntenic analysis revealed several gene pairs between tomato and other species. Interestingly, the deduced amino acid sequence of human AChE showed no similarity with that of tomato AChE sequence. However, the binding energy of SlAChE enzyme to agonists and antagonists was almost identical to that of human AChE. This preliminary study of ChE-like activity in plants may open the way for additional research in non-neuronal role in plants. The studies provide a theoretical basis for further elucidating the functions of the AChE gene family at the molecular level.
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References
Ahammed GJ, Li X (2023) Dopamine-induced abiotic stress tolerance in horticultural plants. Sci Hortic 307:111506. https://doi.org/10.1016/j.scienta.2022.111506
Akoh CC, Lee GC, Liaw YC, Huang TH, Shaw JF (2004) GDSL family of serine esterases/lipases. Prog Lipid Res 43(6):534–552. https://doi.org/10.1016/j.plipres.2004.09.002
Altaf MA, Shahid R, Kumar R, Altaf MM, Kumar A, Khan LU, Saqib M, Nawaz MA, Saddiq B, Bahadur S, Tiwari RK (2022) Phytohormones mediated modulation of abiotic stress tolerance and potential crosstalk in horticultural crops. J Plant Growth Regul 42(8):4724–4750. https://doi.org/10.1007/s00344-022-10812-0
Bamel K, Gupta SC, Gupta R (2007) Acetylcholine causes rooting in leaf explants of in vitro raised tomato (Lycopersicon esculentum Miller) seedlings. Life Sci 80(24–25):2393–2396. https://doi.org/10.1016/j.lfs.2007.01.039
Bamel K, Gupta R, Gupta SC (2016) 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 11(6):e1187355. https://doi.org/10.1080/15592324.2016.1187355
Barlow RB, Dixon RO (1973) Choline acetyltransferase in the nettle Urtica dioica L. Biochem J 132(1):15–18. https://doi.org/10.1042/bj1320015
Birhanie ZM, Yang D, Luan M, Xiao A, Liu L, Zhang C, Biswas A, Dey S, Deng Y, Li D (2022) Salt Stress induces changes in physiological characteristics, bioactive constituents, and antioxidants in Kenaf (Hibiscus cannabinus L.). Antioxidants 11(10):2005. https://doi.org/10.3390/antiox11102005
Bita CE, Gerats T (2013) Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress-tolerant crops. Front Plant Sci 4:273. https://doi.org/10.3389/fpls.2013.00273
Braga I, Pissolato MD, Souza GM (2017) Mitigating effects of acetylcholine supply on soybean seed germination under osmotic stress. Braz J Bot 40(3):617–624. https://doi.org/10.1007/s40415-017-0367-2
Brenner ED, Stahlberg R, Mancuso S, Vivanco J, Baluška F, Van Volkenburgh E (2006) Plant neurobiology: an integrated view of plant signaling. Trends Plant Sci 11(8):413–419. https://doi.org/10.1016/j.tplants.2006.06.009
Cantalapiedra CP, Hernández-Plaza A, Letunic I, Bork P, Huerta-Cepas J (2021) eggNOG-mapper v2: functional annotation, orthology assignments, and domain prediction at the metagenomic scale. Mol Biol Evol 38:5825–5829. https://doi.org/10.1093/molbev/msab293
Chepyshko H, Lai CP, Huang LM, Liu JH, Shaw JF (2012) Multifunctionality and diversity of GDSL esterase/lipase gene family in rice (Oryza sativa L. japonica) genome: new insights from bioinformatics analysis. BMC Genomics 13:1–19. https://doi.org/10.1186/1471-2164-13-309
Dai X, Zhao PX (2011) psRNATarget: a plant small RNA target analysis server. Nucleic Acids Res 39(2):W155–W159. https://doi.org/10.1093/nar/gkr319
Di Sansebastiano GP, Fornaciari S, Barozzi F, Piro G, Arru L (2014) New insights on plant cell elongation: a role for acetylcholine. Int J Mol Sci 15(3):4565–4582. https://doi.org/10.3390/ijms15034565
Ding LN, Li M, Wang WJ, Cao J, Wang Z, Zhu KM, Yang YH, Li YL, Tan XL (2019) Advances in plant GDSL lipases: from sequences to functional mechanisms. Acta Physiol Plant 41:1–11. https://doi.org/10.1007/s11738-019-2944-4
Ellman GL, Courtney KD, Andres V Jr, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7(2):88–95. https://doi.org/10.1016/0006-2952(61)90145-9
Finn RD, Mistry J, Schuster-Böckler B, Griffiths-Jones S, Hollich V, Lassmann T, Moxon S, Marshall M, Khanna A, Durbin R, Eddy SR (2006) Pfam: clans, web tools and services. Nucleic Acids Res 34(1):D247–D251. https://doi.org/10.1093/nar/gkj149
Finn RD, Clements J, Eddy SR (2011) HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 39(2):W29–W37. https://doi.org/10.1093/nar/gkr367
Ge SX, Jung D, Yao R (2020) ShinyGO: a graphical gene-set enrichment tool for animals and plants. Bioinformatics 36(8):2628–2629. https://doi.org/10.1093/bioinformatics/btz931
Gupta A, Gupta R (1997) A survey of plants for presence of cholinesterase activity. Phytochemistry 46(5):827–831. https://doi.org/10.1016/S0031-9422(97)00393-2
Hartmann E, Gupta R (1989) Acetylcholine as a signaling system in plants. In: Boss WE, Morré JD (eds) Second messengers in plant growth and development. Liss AR Inc., New York, pp 257–287
Hassan AH, Alkhalifah DH, Al Yousef SA, Beemster GT, Mousa AS, Hozzein WN, AbdElgawad H (2020) Salinity stress enhances the antioxidant capacity of Bacillus and Planococcus species isolated from saline lake environment. Front Microbiol 11:561816. https://doi.org/10.3389/fmicb.2020.561816
Hestrin S (1950) Acylation reactions mediated by purified acetylcholine esterase II. Biochem Biophys Acta 4:310–321. https://doi.org/10.1016/0006-3002(50)90037-0
Horiuchi Y, Kimura R, Kato N, Fujii T, Seki M, Endo T, Kato T, Kawashima K (2003) Evolutional study on acetylcholine expression. Life Sci 72(15):1745–1756. https://doi.org/10.1016/S0024-3205(02)02478-5
Huerta-Cepas J, Szklarczyk D, Heller D, Hernández-Plaza A, Forslund SK, Cook H, Mende DR, Letunic I, Rattei T, Jensen LJ, von Mering C (2019) EggNOG 5.0: a hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses. Nucleic Acids Res 47(D1):D309–D314. https://doi.org/10.1093/nar/gky1085
Islam W, Waheed A, Naveed H, Zeng F (2022) MicroRNAs mediated plant responses to salt stress. Cells 11(18):2806. https://doi.org/10.3390/cells11182806
Jami SK, Clark GB, Ayele BT, Ashe P, Kirti PB (2012) Genome-wide comparative analysis of annexin superfamily in plants. PLoS ONE 7(11):e47801. https://doi.org/10.1371/journal.pone.0047801
Jiang Y, Chen R, Dong J, Xu Z, Gao X (2012) Analysis of GDSL lipase (GLIP) family genes in rice (Oryza sativa). Plant Omics 5(4):351–358. https://doi.org/10.3316/informit.672714403539805
Kapoor N, Pande V (2015) Effect of salt stress on growth parameters, moisture content, relative water content and photosynthetic pigments of fenugreek variety RMt-1. J Plant Sci 10(6):210–221. https://doi.org/10.3923/jps.2015.210.221
Kasturi R, Vasantharajan VN (1976) Properties of acetylcholinesterase from Pisum sativum. Phytochemistry 15(9):1345–1347
Kawashima K, Misawa H, Moriwaki Y, Fujii YX, Fujii T, Horiuchi Y, Yamada T, Imanaka T, Kamekura M (2007) Ubiquitous expression of acetylcholine and its biological functions in life forms without nervous systems. Life Sci 80(24–25):2206–2209. https://doi.org/10.1016/j.lfs.2007.01.059
Khatri D, Chhetri SB (2020) Reducing sugar, total phenolic content, and antioxidant potential of nepalese plants. Biomed Res Int 2020:7296859. https://doi.org/10.1155/2020/7296859
Kram BW, Bainbridge EA, Perera MA, Carter C (2008) Identification, cloning and characterization of a GDSL lipase secreted into the nectar of Jacaranda mimosifolia. Plant Mol Biol 68:173–183. https://doi.org/10.1007/s11103-008-9361-1
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35(6):1547. https://doi.org/10.1093/molbev/msy096
Lai CP, Huang LM, Chen LF, Chan MT, Shaw JF (2017) Genome-wide analysis of GDSL-type esterases/lipases in Arabidopsis. Plant Mol Biol 95:181–197. https://doi.org/10.1007/s11103-017-0648-y
Lee DS, Kim BK, Kwon SJ, Jin HC, Park OK (2009) Arabidopsis GDSL lipase 2 plays a role in pathogen defense via negative regulation of auxin signaling. Biochem Biophys Res Commun 379(4):1038–1042. https://doi.org/10.1016/j.bbrc.2009.01.006
Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouzé P, Rombauts S (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30(1):325–327. https://doi.org/10.1093/nar/30.1.325
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods 25(4):402–408. https://doi.org/10.1006/meth.2001.1262
Massoulié J, Pezzementi L, Bon S, Krejci E, Vallette FM (1993) Molecular and cellular biology of cholinesterases. Prog Neurobiol 41(1):31–91. https://doi.org/10.1016/0301-0082(93)90040-Y
Mittal D, Sharma N, Sharma V, Sopory SK, Sanan-Mishra N (2016) Role of microRNAs in rice plant under salt stress. Ann Appl Biol 168(1):2–18. https://doi.org/10.1111/aab.12241
Momonoki YS, Momonoki T (1992) The influence of heat stress on acetylcholine content and its hydrolyzing activity in Macroptilium atropurpureum cv. Siratro Jpn J Crop Sci 61(1):112–118. https://doi.org/10.1626/jcs.61.112
Nachmansohn DA, Machado AL (1943) The formation of acetylcholine. A new enzyme:" choline acetylase. J Neurophysiol 6(5):397–403. https://doi.org/10.1152/jn.1943.6.5.397
Nakai K, Horton P (2007) Computational prediction of subcellular localization. Protein Target Protoc. https://doi.org/10.1007/978-1-59745-466-7_29
Naranjo MA, Forment J, Roldan M, Serrano R, Vicente O (2006) Overexpression of Arabidopsis thaliana LTL1, a salt-induced gene encoding a GDSL-motif lipase, increases salt tolerance in yeast and transgenic plants. Plant Cell Environ 29(10):1890–1900. https://doi.org/10.1111/j.1365-3040.2006.01565.x
Nerdy N, Manurung K (2018) Spectrophotometric method for antioxidant activity test and total phenolic determination of red dragon fruit leaves and white dragon fruit leaves. Rasayan J Chem 11(3):1183–1192
Pierleoni A, Martelli PL, Fariselli P, Casadio R (2006) BaCelLo: a balanced subcellular localization predictor. Bioinformatics 22(14):e408–e416. https://doi.org/10.1093/bioinformatics/btl222
Qi M, Zheng X, Niu G, Ye A, Rather SA, Ahmed N, Mustafad NS, Wang P, Siddiqui MH, Kimar R, Zhang L (2022) 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 30:1–3. https://doi.org/10.1007/s00344-022-10642-0
Qin C, Ahanger MA, Zhou J, Ahmed N, Wei C, Yuan S, Ashraf M, Zhang L (2020) Beneficial role of acetylcholine in chlorophyll metabolism and photosynthetic gas exchange in Nicotiana benthamiana seedlings under salinity stress. Plant Biol (stuttg) 22(3):357–365. https://doi.org/10.1111/plb.13079
Raza A, Salehi H, Rahman MA, Zahid Z, Madadkar Haghjou M, Najafi-Kakavand S, Charagh S, Osman HS, Albaqami M, Zhuang Y, Siddique KH (2022a) Plant hormones and neurotransmitter interactions mediate antioxidant defenses under induced oxidative stress in plants. Front Plant Sci. https://doi.org/10.3389/fpls.2022.961872
Raza A, Sharif Y, Chen K, Wang L, Fu H, Zhuang Y, Chitikineni A, Chen H, Zhang C, Varshney RK, Zhuang W (2022b) Genome-wide characterization of ascorbate peroxidase gene family in peanut (Arachis hypogea L.) revealed their crucial role in growth and multiple stress tolerance. Front Plant Sci 13:962182. https://doi.org/10.3389/fpls.2022.962182
Raza A, Tabassum J, Fakhar AZ, Sharif R, Chen H, Zhang C, Ju L, Fotopoulos V, Siddique KH, Singh RK, Zhuang W (2022c) Smart reprograming of plants against salinity stress using modern biotechnological tools. Crit Rev Biotechnol. https://doi.org/10.1080/073885512093695
Raza A, Charagh S, Najafi-Kakavand S, Abbas S, Shoaib Y, Anwar S, Sharifi S, Lu G, Siddique KH (2023) Role of phytohormones in regulating cold stress tolerance: physiological and molecular approaches for developing cold-smart crop plants. Plant Stress. https://doi.org/10.1016/j.stress.2023.100152
Rehmsmeier M, Steffen P, Höchsmann M, Giegerich R (2004) Fast and effective prediction of microRNA/target duplexes. RNA 10(10):1507–1517. https://doi.org/10.1261/rna.5248604
Riov J, Jaffe MJ (1973) Cholinesterases from plant tissues: I. Purification and characterization of a cholinesterase from mung bean roots. Plant Physiol 51(3):520–528. https://doi.org/10.1104/pp.51.3.520
Roshchina VV (2001) Neurotransmitters in plant life. CRC Press. https://doi.org/10.1201/9781482279856
Roy SW, Penny D (2007) Patterns of intron loss and gain in plants: intron loss–dominated evolution and genome-wide comparison of O. sativa and A. thaliana. Mol Biol Evol 24(1):171–181. https://doi.org/10.1093/molbev/msl159
Roychoudhury A (2020) Neurotransmitter acetylcholine comes to the plant rescue. J Mol Cell Biol Forecast 3(1):1019. https://doi.org/10.1104/pp.105.062927
Sagane Y, Nakagawa T, Yamamoto K, Michikawa S, Oguri S, Momonoki YS (2005) Molecular characterization of maize acetylcholinesterase. A novel enzyme family in the plant kingdom. Plant Physiol 138(3):1359–1371
Sharma M, Kumar P, Verma V, Sharma R, Bhargava B, Irfan M (2022) Understanding plant stress memory response for abiotic stress resilience: molecular insights and prospects. Plant Physiol Biochem 179:10–24. https://doi.org/10.1016/j.plaphy.2022.03.004
Shen G, Sun W, Chen Z, Shi L, Hong J, Shi J (2022) Plant GDSL esterases/lipases: evolutionary physiological and molecular functions in plant development. Plants (basel). https://doi.org/10.3390/plants11040468
Su S, Zhou Y, Qin JG, Yao W, Ma Z (2010) Optimization of the method for chlorophyll extraction in aquatic plants. J Freshw Ecol 25(4):531–538. https://doi.org/10.1080/02705060.2010.9664402
Su Y, Qin C, Begum N, Ashraf M, Zhang L (2020) 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 198:110671. https://doi.org/10.1016/j.ecoenv.2020.110671
Takahashi K, Shimada T, Kondo M, Tamai A, Mori M, Nishimura M, Hara-Nishimura I (2010) Ectopic expression of an esterase, which is a candidate for the unidentified plant cutinase, causes cuticular defects in Arabidopsis thaliana. Plant Cell Physiol 51(1):123–131. https://doi.org/10.1093/pcp/pcp173
Tanveer K, Gilani S, Hussain Z, Ishaq R, Adeel M, Ilyas N (2020) Effect of salt stress on tomato plant and the role of calcium. J Plant Nutr 43(1):28–35. https://doi.org/10.1080/01904167.2019.1659324
Tretyn A, Kendrick RE (1991) Acetylcholine in plants: presence, metabolism and mechanism of action. Bot Rev 57(1):33–73. https://doi.org/10.1007/BF02858764
Wang K, Durrett TP, Benning C (2019) Functional diversity of glycerolipid acylhydrolases in plant metabolism and physiology. Prog Lipid Res 75:100987. https://doi.org/10.1016/j.plipres.2019.100987
Wang W, Yamaguchi S, Suzuki A, Wagu N, Koyama M, Takahashi A, Takada R, Miyatake K, Nakamura K (2021) Investigation of the distribution and content of acetylcholine, a novel functional compound in eggplant. Foods 10(1):81. https://doi.org/10.3390/foods10010081
Waterhouse AM, Procter JB, Martin DM, Clamp M, Barton GJ (2009) Jalview version 2—a multiple sequence alignment editor and analysis workbench. Bioinformatics 25(9):1189–1191. https://doi.org/10.1093/bioinformatics/btp033
Wessler I, Kilbinger H, Bittinger F, Kirkpatrick CJ (2001) The non-neuronal cholinergic system the biological role of non-neuronal acetylcholine in plants and humans. Jpn J Pharmacol 85(1):2–10. https://doi.org/10.1254/jjp.85.2
Yamamoto K, Momonoki YS (2008) Subcellular localization of overexpressed maize AChE gene in rice plant. Plant Signal Behav 3(8):576–577. https://doi.org/10.4161/psb.3.8.5732
Yamamoto K, Oguri S, Chiba S, Momonoki YS (2009) Molecular cloning of acetylcholinesterase gene from Salicornia europaea L. Plant Signal Behav 4(5):361–366. https://doi.org/10.4161/psb.4.5.8360
Yao-guang SU, Yu-qing HE, He-xuan WA, Jing-bin JI, Huan-huan YA, Xiang-yang XU (2022) Genome-wide identification and expression analysis of GDSL esterase/lipase genes in tomato. J Integr Agric 21(2):389–406. https://doi.org/10.1016/S2095-3119(20)63461-X
Yu CS, Chen YC, Lu CH, Hwang JK (2006) Prediction of protein subcellular localization. Proteins Struct Funct Genet 64(3):643–651. https://doi.org/10.1002/prot.21018
Zandalinas SI, Mittler R (2022) Plant responses to multifactorial stress combination. New Phytol 234(4):1161–1167. https://doi.org/10.1111/nph.18087
Zhang Z, Yu J, Li D, Zhang Z, Liu F, Zhou X, Wang T, Ling Y, Su Z (2010) PMRD: plant microRNA database. Nucleic Acids Res 38(1):806–813. https://doi.org/10.1093/nar/gkp818
Zou M, Guo B, He S (2011) The roles and evolutionary patterns of intronless genes in deuterostomes. Comp Funct Genomics. https://doi.org/10.1155/2011/680673
Acknowledgements
YS like to thank Department of Biotechnology, India for granting DBT-Junior Research Fellowship 2020 (Grant No.: DBTHRDPMU/JRF/BET-20/1/2020/AL/119). We also thank GGS Indraprastha University, New Delhi and Department of Botany, Shivaji College (University of Delhi), Raja Garden, New Delh-110027 for encouragement.
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This investigation has been carried out under FRG Scheme received from GGS Indraprastha University, New Delhi, India (FRGS Grant No. GGSIPU/DRC/FRGS/2022/1223/20).
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Sarangle, Y., Bamel, K. & Purty, R.S. Identification of Acetylcholinesterase Like Gene Family and Its Expression Under Salinity Stress in Solanum lycopersicum. J Plant Growth Regul 43, 940–960 (2024). https://doi.org/10.1007/s00344-023-11152-3
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DOI: https://doi.org/10.1007/s00344-023-11152-3