Galanthamine, an anti-cholinesterase drug, effects plant growth and development in Artemisia tridentata Nutt. Via modulation of auxin and neurotransmitter signaling

Plant Signaling and Behavior

Volumn 9, Issue 4, 2014, Pages

  Turi, Christina E ^a   Axwik, Katarina E ^a   Smith, Anderson ^a   Jones, A Maxwell P ^b   Saxena, Praveen K ^b   Murch, Susan J ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF GUELPH   (Canada)

Author keywords

Acetylcholine; Artemisia tridentata; Auxin; Cholinergic signalling; Galanthamine; Melatonin; Metabolomics

Indexed keywords

ARTEMISIA TRIDENTATA;

ACETYLCHOLINE; ACETYLCHOLINESTERASE; CHOLINESTERASE INHIBITOR; GALANTAMINE; INDOLEACETIC ACID DERIVATIVE; MELATONIN; SEROTONIN;

ARTEMISIA; CELL CULTURE TECHNIQUE; DRUG EFFECTS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; OXIDATIVE STRESS; PLANT DEVELOPMENT;

ACETYLCHOLINE; ACETYLCHOLINESTERASE; ARTEMISIA; CHOLINESTERASE INHIBITORS; CULTURE TECHNIQUES; GALANTAMINE; INDOLEACETIC ACIDS; MELATONIN; OXIDATIVE STRESS; PLANT DEVELOPMENT; SEROTONIN;

EID: 84924095094     PISSN: 15592316     EISSN: 15592324     Source Type: Journal    
DOI: 10.4161/psb.28645     Document Type: Article

References (66)

1. Skoog F, Miller CO. Chemical regulation of growth and organ formation in plant tissues cultured in vitro. Symp Soc Exp Biol 1957; 11:118-30; . PMID:13486467 6.
2. Murch SJ, Saxena PK, Journey of a Single Cell to a Plant. Enfield, NH, ed. Science Publishers, Inc:2005.
3. Murch SJ, Saxena PK. Melatonin: A potential 7 regulator of plant growth and development? In Vitro Cell Dev Pl 2002; 38:531-536; http://dx.doi.org/10.1079/IVP2002333 8.
4. Murch SJ, Saxena PK. Role of indoleamines in regulation of morphogenesis in in vitro cultures of St. John’s Wort (Hypericum perforatum L.) Future for Medicinal and Aromatic Plants 2004:425-432.
5. Cao J, Cole IB, Murch SJ. Neurotransmitters, neu- 9. roregulators and neurotoxins in the life of plants.Can J Plant Sci 2006; 86:1183-8; http://dx.doi.org/10.4141/P06-034.
6. Stanton DJ, McArthur ED, Freeman DC, Golenberg EM. No genetic substructuring in Artemisia subgenus Tridentatae despite strong ecotypic subspecies selection. Biochem Syst Ecol 2002; 30:579-93; http://dx.doi.org/10.1016/S0305-1978(01)00118-1.
7. Douglas, GW., Stanley, GB., Meidinger, D., Pojar, J. Illustrated flora of British Columbia, gymnosperms and dicotyledons, Vol 1. British Columbia; 1998.
8. Moerman DE. Native American Ethnobotany. Portland, OR: Timber Press, Inc, 2009.
9. Turi CE, Shipley PR, Murch SJ. North American Artemisia species from the sub genus Tridentatae (Sagebrush): a phytochemical, botanical and pharmacological review. Phytochemistry 2014; 98:926; PMID:24359634; http://dx.doi.org/10.1016/.phytochem.2013.11.016.
10. Turi CE, Axwik KE, Murch SJ. In vitro conservation, phytochemistry, and medicinal activity of Artemisia tridentata nutt: Metabolomics as a hypothesis-generating tool for plant tissue culture. Plant Growth Regul 2014; Forthcoming http://dx.doi.org/10.1007/s10725-014-9915-y.
11. Murch SJ. Krishna Raj S, Saxena PK. Tryptophan is a precursor for melatonin and serotonin biosynthesis in in vitro regenerated St. John’s Wort (Hypericum perforatum L. cv. anthos) plants. Plant Cell Rep 2000; 19:698-704; http://dx.doi.org/10.1007/s002990000206.
12. Murch SJ, Campbell S, Saxena PK. The role of serotonin and melatonin in plant morphogenesis: Regulation of auxin-induced root organogenesis in in vitro-cultured explants of St. John’s Wort (Hypericum perforatum L.). In Vitro Cell Dev Pl 2001; 37:786-793; http://dx.doi.org/10.1007/s11627-001-0130-y.
13. Jones MPA, Cao J, O’Brien R, Murch SJ, Saxena PK. The mode of action of thidiazuron: auxins, indoleamines, and ion channels in the regeneration of Echinacea purpurea L. Plant Cell Rep 2007; 26:1481-90; PMID:17483954; http://dx.doi.org/10.1007/s00299-007-0357-0.
14. Cole IB, Cao J, Alan AR, Saxena PK, Murch SJ. Comparisons of Scutellaria baicalensis, Scutellaria lateriflora and Scutellaria racemosa: genome size, antioxidant potential and phytochemistry. Planta Med 2008; 74:474-81; PMID:18484546; http://dx.doi.org/10.1055/s-2008-1034358.
15. Park S, Byeon Y, Back K. Functional analyses of three ASMT gene family members in rice plants. J Pineal Res 2013; 55:409-15; PMID:24033370.
16. Lazar D, Murch SJ, Beilby MJ, Al Khazaaly S. Exogenous melatonin affects photosynthesis in characeae Chara australis. Plant Signal Behav 2013; 8:e23279; PMID:23299331; http://dx.doi.org/10.4161/psb.23279.
17. Murch SJ, Alan AR, Cao J, Saxena PK. Melatonin and serotonin in flowers and fruits of Datura metel L. J Pineal Res 2009; 47:277-83; PMID:19732299; http://dx.doi.org/10.1111/j.1600-079X.2009.00711.x.
18. Zhao Y, Qi LW, Wang WM, Saxena PK, Liu CZ. Melatonin improves the survival of cryopre- served callus of Rhodiola crenulata. J Pineal Res 2011; 50:83-8; PMID:21073518; http://dx.doi.org/10.1111/j.1600-079X.2010.00817.x.
19. Uchendu EE, Shukla MR, Reed BM, Saxena PK. Melatonin enhances the recovery of cryopreserved shoot tips of American elm (Ulmus americana L.). J Pineal Res 2013; 55:435-42; PMID:24117864.
20. Hartmann E, Gupta R. Acetylcholine as a signaling system in plants. In: Second Messengers in Plant Growth and Development. Boss W, Marre D, eds. New York: Alan R Liss, 1989:257-288.
21. Hartmann E, Kilbinger H. Occurrence of light-dependent acetylcholine concentrations in higher plants. Experientia 1974; 30:13978; PMID:4442525; http://dx.doi.org/10.1007/BF01919649.
22. Tretyn A, Kendrick R. Acetylcholine in plants - presence, metabolism and mechanism of action. Bot Rev 1991; 57:33-73; http://dx.doi.org/10.1007/BF02858764.
23. Roshchina VV. Neurotransmitters in Plant Life. Science Publishers: 2001.
24. Jaffe MJ. Evidence for the regulation of phytochrome-mediated processes in bean roots by the neurohumor, acetylcholine. Plant Physiol 1970; 46:768-77; PMID:5500205; http://dx.doi.org/10.1104/pp.46.6.768.
25. Mehta M, Malik M, Khurana J, Maheshwari S. Phytochrome modulation of calcium fluxes in wheat (Triticum aestivum L) protoplasts. Plant Growth Regul 1993; 12:293-302; http://dx.doi.org/10.1007/BF00027211.
26. Bamel K, Gupta SC, Gupta R. Acetylcholine causes rooting in leaf explants of in vitro raised tomato (Lycopersicon esculentum Miller) seedlings. Life Sci 2007; 80:2393-6; PMID:17328922; http://dx.doi.org/10.1016/j.lfs.2007.01.039.
27. Yang C, Zhai Z, Guo Y, Gao P. Effects of acetylcholine, cytochalasin B and amiprophosmethyl on phloem transport in radish (Raphanus sativas). J Integr Plant Biol 2007; 49:550-5; http://dx.doi.org/10.1111/j.1744-7909.2007.00434.x.
28. Tezuka T, Akita I, Yoshino N, Suzuki Y. Regulation of self-incompatibility by acetylcholine and cAMP in Lilium longiflorum. J Plant Physiol 2007; 164:87885; PMID: 16882455; http://dx.doi.org/10.1016/j. jplph.2006.05.013.
29. Heinrich M, Lee Teoh H. Galanthamine from snowdrop--the development of a modern drug against Alzheimer’s disease from local Caucasian knowledge. J Ethnopharmacol 2004; 92:147-62; PMID:15137996; http://dx.doi.org/10.1016/j. jep.2004.02.012.
30. Ago Y, Koda K, Takuma K, Matsuda T. Pharmacological aspects of the acetylcholinesterase inhibitor galantamine. J Pharmacol Sci 2011; 116:617; PMID:21498956; http://dx.doi.org/10.1254/jphs.11R01CR.
31. Horiuchi Y, Kimura R, Kato N, Fujii T, Seki M, Endo T, Kato T, Kawashima K. Evolutional study on acetylcholine expression. Life Sci 2003; 72:174556; PMID:12559395; http://dx.doi.org/10.1016/S0024-3205(02)02478-5.
32. Wessler I, Kirkpatrick CJ, Racke K. The cholinergic ‘pitfall’: acetylcholine, a universal cell molecule in biological systems, including humans. Clin Exp Pharmacol Physiol 1999; 26:198-205; PMID:10081614; http://dx.doi.org/10.1046/j.1440-1681.1999.03016.x.
33. Grando SA, Kawashima K, Kirkpatrick CJ, Meurs H, Wessler I. The non-neuronal cholinergic system: basic science, therapeutic implications and new perspectives. Life Sci 2012; 91:969-72; PMID:23141771; http://dx.doi.org/10.1016/j.lfs.2012.10.004.
34. Paredes SD, Korkmaz A, Manchester LC, Tan DX, Reiter RJ. Phytomelatonin: a review. J Exp Bot 2009; 60:57-69; PMID:19033551; http://dx.doi.org/10.1093/jxb/ern284.
35. Galano A, Tan DX, Reiter RJ. Melatonin as a natural ally against oxidative stress: a physicochemical examination. J Pineal Res 2011; 51:1-16; PMID:21752095; http://dx.doi.org/10.1111/j.1600-079X.2011.00916.x.
36. Park WJ. Melatonin as an endogenous plant regulatory signal: Debates and perspectives. J Plant Biol 2011; 54:143-9; http://dx.doi.org/10.1007/s12374-011-9159-6.
37. Grobe W. Function of serotonin in seeds of walnut. Phytochem 1982; 21:819-22; http://dx.doi.org/10.1016/0031-9422(82)80071-X.
38. Matsukawa M, Ogawa M, Nakadate K, Maeshima T, Ichitani Y, Kawai N, Okado N. Serotonin and acetylcholine are crucial to maintain hippocampal synapses and memory acquisition in rats. Neurosci Lett 1997; 230:13-6; PMID:9259452; http://dx.doi.org/10.1016/S0304-3940(97)00460-6.
39. Terry AV Jr., Buccafusco JJ, Wilson C. Cognitive dysfunction in neuropsychiatric disorders: selected serotonin receptor subtypes as therapeutic targets. Behav Brain Res 2008; 195:30-8; PMID:18241938; http://dx.doi.org/10.1016/j.bbr.2007.12.006.
40. Yuliana ND, Khatib A, Choi YH, Verpoorte R. Metabolomics for bioactivity assessment of natural products. Phytother Res 2011; 25:157-69; PMID:20658470.
41. Verpoorte R, Choi YH, Kim HK. Metabolomics: will it stay? Phytochem Anal 2010; 21:2-3; PMID:20013869; http://dx.doi.org/10.1002/pca.1191.
42. Sanchez DH, Schwabe F, Erban A, Udvardi MK, Kopka J. Comparative metabolomics of drought acclimation in model and forage legumes. Plant Cell Environ 2012; 35:136-49; PMID:21902697; http://dx.doi.org/10.1111/j.1365-3040.2011.02423.x.
43. Obata T, Fernie AR. The use of metabolomics to dissect plant responses to abiotic stresses. Cell Mol Life Sci 2012; 69:3225-43; PMID:22885821; http://dx.doi.org/10.1007/s00018-012-1091-5.
44. Kral’ova K, Jampilek J, Ostrovsky I. Metabolomics - useful tool for study of plant responses to abiotic stresses. Ecol Chem Eng S 2012; 19:133-61.
45. Arbona V, Manzi M, Ollas Cd, Gomez-Cadenas A. Metabolomics as a tool to investigate abiotic stress tolerance in plants. Int J Mol Sci 2013; 14:4885911; PMID:23455464; http://dx.doi.org/10.3390/ijms14034885.
46. Rasmussen S, Parsons AJ, Jones CS. Metabolomics of forage plants: a review. Ann Bot 2012; 110:1281-90; PMID:22351485; http://dx.doi.org/10.1093/aob/mcs023.
47. Davis MC, Fiehn O, Durnford DG. Metabolic acclimation to excess light intensity in Chlamydomonas reinhardtii. Plant Cell Environ 2013; 36:1391405; PMID:23346954; http://dx.doi.org/10.1111/pce.12071.
48. Brady SM, Provart NJ. Web-queryable large-scale data sets for hypothesis generation in plant biology. Plant Cell 2009; 21:1034-51; PMID:19401381; http://dx.doi.org/10.1105/tpc.109.066050.
49. Brown PN, Turi CE, Shipley PR, Murch SJ. Comparisons of large (Vaccinium macrocarpon Ait.) and small (Vaccinium oxycoccos L., Vaccinium vitis- idaea L.) cranberry in British Columbia by phytochemical determination, antioxidant potential, and metabolomic profiling with chemometric analysis. Planta Med 2012; 78:630-40; PMID:22337317; http://dx.doi.org/10.1055/s-0031-1298239.
50. Gnonlonfin GJB, Sanni A, Brimer L. Review sco- poletin - A coumarin phytoalexin with medicinal properties. Crit Rev Plant Sci 2012; 31:47-56; http://dx.doi.org/10.1080/07352689.2011.616039.
51. Wilt FM, Geddes JD, Tamma RV, Miller GC, Everett RL. Interspecific variation of phenolic concentrations in persistent leaves among 6 taxa from subgenus Tridentatae of Artemisia (Asteraceae). Biochem Syst Ecol 1992; 20:41-52; http://dx.doi.org/10.1016/0305-1978(92)90071-K.
52. Wilt FM, Miller GC. Seasonal-variation of coumarin and flavonoid concentrations in persistent leaves of Wyoming Big Sagebrush (Artemisia-tridentata ssp wyomingensis, asteraceae). Biochem Syst Ecol 1992; 20:53-67; http://dx.doi.org/10.1016/0305-1978(92)90072-L.
53. Sharan M, Taguchi G, Gonda K, Jouke T, Shimosaka M, Hayashida N, Okazaki M. Effects of methyl jasmonate and elicitor on the activation of phenylalanine ammonia-lyase and the accumulation of sco- poletin and scopolin in tobacco cell cultures. Plant Sci 1998; 132:13-9; http://dx.doi.org/10.1016/S0168-9452(97)00260-4.
54. Petit-Paly G, Franck T, Brisson L, Kevers C, Chenieux JC, Rideau M. Cytokinin modulates cata- lase activity and coumarin accumulation in in vitro cultures of tobacco. J Plant Physiol 1999; 155:9-15; http://dx.doi.org/10.1016/S0176-1617(99)80134-5.
55. Taguchi G, Yoshizawa K, Kodaira R, Hayashida N, Okazaki M. Plant hormone regulation on scopole- tin metabolism from culture medium into tobacco cells. Plant Sci 2001; 160:905-11; PMID:11297787; http://dx.doi.org/10.1016/S0168-9452(00)00464-7.
56. Darwin C. The Power of Movement in Plants. New York, USA: NYU Press, 1880.
57. Baluska F, Mancuso S. Plant neurobiology: from sensory biology, via plant communication, to social plant behavior. Cogn Process 2009; 10(Suppl 1):S3-7; PMID:18998182; http://dx.doi.org/10.1007/s10339-008-0239-6.
58. Murashige T, Skoog F. A revised medium for rapid growth and bio assays with Tobacco tissue cultures. Physiol Plant 1962; 15:473-97; http://dx.doi.org/10.1111/j.1399-3054.1962.tb08052.x.
59. Gamborg OL, Miller RA, Ojima K. Nutrient requirements of suspension cultures of soybean root cells. Exp Cell Res 1968; 50:151-8; PMID:5650857; http://dx.doi.org/10.1016/0014-4827(68)90403-5.
60. Mohanty JG, Jaffe JS, Schulman ES, Raible DG. A highly sensitive fluorescent micro-assay of H2O2 release from activated human leukocytes using a dihy- droxyphenoxazine derivative. J Immunol Methods 1997; 202:133-41; PMID:9107302; http://dx.doi.org/10.1016/S0022-1759(96)00244-X.
61. Zhou M, Diwu Z, Panchuk-Voloshina N, Haugland RP. A stable nonfluorescent derivative of resorufin for the fluorometric determination of trace hydrogen peroxide: applications in detecting the activity of phagocyte NADPH oxidase and other oxidases. Anal Biochem 1997; 253:162-8; PMID:9367498; http://dx.doi.org/10.1006/abio.1997.2391.
62. Ellman GL, Courtney KD, Andres V Jr., Feather- Stone RM. A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 1961; 7:88-95; PMID:13726518; http://dx.doi.org/10.1016/0006-2952(61)90145-9.
63. Sirois JC. Studies on growth regulators. I. Improved Avena coleoptile elongation test for auxin. Plant Physiol 1966; 41:1308-12; PMID:16656401; http://dx.doi.org/10.1104/pp.41.8.1308.
64. Turi CE, Murch SJ. Targeted and untargeted phytochemistry of Ligusticum canbyi: indoleam- ines, phthalides, antioxidant potential, and use of metabolomics as a hypothesis-generating technique for compound discovery. Planta Med 2013; 79:1370-9; PMID:23877920; http://dx.doi.org/10.1055/s-0033-1350618.
65. Brown PN, Murch SJ, Shipley PR. Phytochemical diversity of cranberry (Vaccinium macrocarpon Aiton) cultivars by anthocyanin determination and metabolo- mic profiling with chemometric analysis. J Agric Food Chem 2012; 60:261-71; PMID:22148867; http://dx.doi.org/10.1021/jf2033335.
66. Murch SJ, Rupasinghe HP, Goodenowe D, Saxena PK. A metabolomic analysis of medicinal diversity in Huang-qin (Scutellaria baicalensis Georgi) genotypes: discovery of novel compounds. Plant Cell Rep 2004; 23:419-25; PMID:15449017; http://dx.doi.org/10.1007/s00299-004-0862-3.