Abstract
Serotonin is a well-known pineal hormone that in mammals plays a key role in mood. In plants, serotonin is implicated in several physiological roles such as flowering, morphogenesis, and adaptation to environmental changes. However, its biosynthetic enzyme in plants has not been characterized. Therefore, we measured the serotonin content and enzyme activity responsible for serotonin biosynthesis in rice seedlings. Tryptamine 5-hydroxylase (T5H), which converts tryptamine into serotonin, was found as a soluble enzyme that had maximal activity in the roots. The maximal activity of T5H was closely associated with the enriched synthesis of serotonin in roots. Tetrahydropterine-dependent T5H activity was inhibited by tyramine, tryptophan, 5-OH-tryptophan, and octopamine, but remained unaltered by dopamine in vitro. The tissues of rice seedlings grown in the presence of tryptamine exhibited a dose-dependent increase in serotonin in parallel with enhanced T5H enzyme activity. However, no significant increase in serotonin was observed in rice tissues grown in the presence of tryptophan, suggesting that tryptamine is a bottleneck intermediate substrate for serotonin synthesis.
Similar content being viewed by others
Abbreviations
- AADC:
-
Aromatic l-amino acid decarboxylase
- FW:
-
Fresh weight
- T5H:
-
Tryptamine 5-hydroxylase
- TDC:
-
Tryptophan decarboxylase
- TPH:
-
Tryptophan hydroxylase
- Trp:
-
Tryptophan
References
Badria FA (2002) Melatonin, serotonin, and tryptamine in some Egyptian food and medicinal plants. J Med Food 5:153–157
Bowden K, Brown BG, Batty JE (1954) 5-Hydroxytryptamine: its occurrence in cowhage. Nature 174:925–926
Csaba G, Pal K (1982) Effect of insulin triodothyronine and serotonin on plant seed development. Protoplasma 110:20–22
Facchini PJ, Huber-Allanach KL, Tari LW (2000) Plant aromatic l-amino acid decarboxylases: evolution, biochemistry, regulation, and metabolic engineering applications. Phytochemistry 54:121–138
Fellows LE, Bell EA (1970) 5-Hydroxy-l-tryptophan, 5-hydroxytryptamine and l-tryptophan-5-hydroxylase in Griffonia simplicifolia. Phytochemistry 9:2389–2396
Fitzpatrick PF (1999) Tetrahydropterin-dependent amino acid hydroxylases. Annu Rev Biochem 68:355–381
Groβe W (1982) Function of serotonin in seeds of walnuts. Phytochemistry 21:819–822
Hernandez-Ruiz J, Cano A, Arnao MB (2005) Melatonin acts as a growth-stimulating compound in some monocot species. J Pineal Res 39:137–142
Jang SM, Ishihara A, Back K (2004) Production of coumaroylserotonin and feruloylserotonin in transgenic rice expressing pepper hydroxycinnamoyl-coenzyme A:serotonin N-(hydroxycinnamoyl)transferase. Plant Physiol 135:346–356
Kang S, Back K (2006) Enriched production of N-hydroxycinnamic acid amides and biogenic amines in pepper (Capsicum annuum) flowers. Sci Hortic 108:337–341
Koyama N, Kuribayashi K, Seki T, Kobayashi K, Furuhata Y, Suzuki K, Arisaka H, Nakano T, Amino Y, Ishii K (2006) Serotonin derivatives, major safflower (Carthamus tinctorius L.) seed antioxidants, inhibit low-density lipoprotein (LDL) oxidation and atherosclerosis in apolipoprotein E-deficient mice. J Agric Food Chem 54:4970–4976
Lee DE, Kang K, Lee SG, Back K (2007) Enhanced synthesis of feruloyltyramine and 4-coumaroyltyramine is associated with tyramine availability in transgenic rice expressing pepper tyramine N-hydroxycinnamoyltransferase. Plant Sci 172:57–63
Lesurtel M, Graf R, Aleil B, Walther DJ, Tian Y, Jochum W, Gachet C, Bader M, Clavien PA (2006) Platelet-derived serotonin mediates liver regeneration. Science 312:104–107
Murch SJ, KrishnaRaj S, Saxena PK (2000) 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 19:698–704
Murch SJ, Campbell SSB, Saxena PK (2001) 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 Biol Plant 37:786–793
Niaussat P, Laborit H, Dubolis C, Hiaussat M (1958) Action de la serotonine sur la croissance des jeunes plantules d’Avoine. Compt Rend Soc Biol 152:945–947
Odjakova M, Hadjiivanova C (1997) Animal neurotransmitter substances in plants. Bulg J Plant Physiol 23:94–102
RadWanski ER, Last RL (1995) Tryptophan biosynthesis and metabolism: biochemical and molecular genetics. Plant Cell 7:921–934
Roshchina VV (2001) Neurotransmitters in plant life. Science Publishers, Enfield, pp 4–81
Roshchina VV, Melnikova EV (1998) Allelopathy and plant reproductive cells: participation of acetylcholine and histamine in signaling in the interactions of pollen and pistil. Allelopathy J 5:171–182
Schröder P, Abele C, Gohr P, Stuhlfauth-Roisch U, Grosse W (1999) Latest on the enzymology of serotonin biosynthesis in walnut seeds. Adv Exp Med Biol 467:637–644
Tanaka E, Tanaka C, Mori N, Kuwahara Y, Tsuda M (2003) Phenylpropanoid amides of serotonin accumulate in witches’ broom diseased bamboo. Phytochemistry 64:965–969
Tsai FY, Brotherton JE, Widholm JM (2005) Overexpression of the feedback-insensitive anthranilate synthase gene in tobacco causes tryptophan accumulation. Plant Cell Rep 23:548–556
Ueno M, Shibata H, Kihara J, Honda Y, Arase S (2003) Increased tryptophan decarboxylase and monoamine oxidase activities induce Sekiguchi lesion formation in rice infected with Magnaporthe grisea. Plant J 36:215–228
Veenstra-VanderWeele J, Anderson GM, Cook EH (2000) Pharmacogenetics and the serotonin system: initial studies and future directions. Eur J Pharmacol 410:165–181
Vrana SL, Dworkin SI, Vrana KE (1993) Radioenzymatic assay for tryptophan hydroxylase: 3HH2O release assessed by charcoal adsorption. J Neurosci Methods 48:123–129
Yao K, De Luca V, Brisson N (1995) Creation of a metabolic sink for tryptophan alters the phenylpropanoid pathway and the susceptibility of potato to Phytophthora infestans. Plant Cell 7:1787–1799
Acknowledgments
This study was supported by the SRC program from the Korea Science and Engineering Foundation (KOSEF) through the Agricultural Plant Stress Research Center Program grant no. R11-2001-09203001-0.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by D. Somers.
Rights and permissions
About this article
Cite this article
Kang, S., Kang, K., Lee, K. et al. Characterization of tryptamine 5-hydroxylase and serotonin synthesis in rice plants. Plant Cell Rep 26, 2009–2015 (2007). https://doi.org/10.1007/s00299-007-0405-9
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00299-007-0405-9