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. 2008 Jun;3(6):389–390. doi: 10.4161/psb.3.6.5401

Enzymatic features of serotonin biosynthetic enzymes and serotonin biosynthesis in plants

Kiyoon Kang 1, Sei Kang 1, Kyungjin Lee 1, Munyoung Park 1, Kyoungwhan Back 1,✉
PMCID: PMC2634310  PMID: 19704574

Abstract

Serotonin, a pineal hormone in mammals, is found in a wide range of plant species at detection levels from a few nanograms to a few milligrams, and has been implicated in several physiological roles, such as flowering, morphogenesis and adaptation to environmental changes. Serotonin synthesis requires two enzymes, tryptophan decarboxylase (TDC) and tryptamine 5-hydroxylase (T5H), with TDC serving as a rate-limiting step because of its high Km relation to the substrate tryptophan (690 µM) and its undetectable expression level in control plants. However, T5H and downstream enzymes, such as serotonin N-hydroxycinnamoyl transferase (SHT), have low Km values with corresponding substrates. This suggests that the biosynthesis of serotonin or serotonin-derived secondary metabolites is restricted to cellular stages when high tryptophan levels are present.

Key words: feruloylserotonin, serotonin, tryptamine, tryptamine 5-hydroxylase, tryptophan, tryptophan biosynthesis, tryptophan decarboxylase

Serotonin is found in a broad range of plants and is abundant in reproductive organs, such as fruits and seeds.1–3 Even though many physiological roles for serotonin in plants have been proposed,2–7 its actual roles have yet to be examined in detail using molecular, biochemical and genetic approaches. In plants, serotonin is synthesized by two enzymes: tryptophan decarboxylase (TDC) and tryptamine 5-hydroxylase (T5H). TDC decarboxylates tryptophan into tryptamine, after which T5H hydroxylates tryptamine into serotonin.8–10 TDC expresses at an undetectable level in rice leaves, whereas T5H expresses constitutively.11,12

Enzymatic Features of Serotonin Biosynthetic Enzymes

TDC from Catharanthus roseus has a low Km for tryptophan (0.072 mM), but the Km of other TDC enzymes isolated from tomato,13 Ophiorrhiza pumila14 and rice10 is at least tenfold higher than that of C. roseus. In particular, the Km of tomato TDC is 3 mM. Unlike TDC, all downstream enzymes after TDC have low Km values for corresponding substrates. For example, for the stub-strate tryptamine, the Km of T5H is 20 µM. The high Km values of TDC enzymes may suggest that TDC functions actively in cells with high tryptophan accumulations. Furthermore, recombinant rice TDC is slightly tolerant of high temperatures, with maximum TDC activity at 45°C and 50% enzyme activity at 55°C (Fig. 1A). In addition, TDC activity is greatest at high pH levels, with peak activity at pH 7.5–8.5, but rapidly decreases to 50% at pH 6.5 (Fig. 1B).

Figure 1.

Figure 1

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Effects of temperature (A) and pH (B) on the activity of purified recombinant rice TDC.

Regulation Between Tryptophan and Serotonin Biosynthesis

Tryptophan biosynthesis is tightly feedback-regulated by anthranilate synthase (AS), the first enzyme of the biosynthetic pathway. AS consists of two α-subunits and two β-subunits and plays a pivotal role in controlling the tryptophan level in plants.15 ASα exists as two isozymes: ASα2 is strongly feedback-inhibited by very low levels of tryptophan (2 µM), whereas ASα1 is insensitive to tryptophan.16 Thus, serotonin synthesis, which requires high levels of tryptophan as a substrate for TDC, is thought to occur via the tryptophan-insensitive ASα1 pathway, followed by the induction of TDC (Fig. 2).

Figure 2.

Figure 2

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Schematic diagram of the serotonin biosynthetic pathway. AS, anthranilate synthase; TDC, tryptophan decarboxylase; T5H, tryptamine 5-hydroxylase; SHT, serotonin N-hydroxycinnamoyl transferase.

This hypothesis is consistent with results showing that TDC overexpression in rice does not result in a massive increase of tryptamine, in contrast to the huge increase of tyramine in tyrosine decarboxylase (TYDC) overexpression.10 The small increase of tryptamine or/and serotonin in transgenic rice plants, despite the overexpression of TDC, has been ascribed to the absence of an increased tryptophan level. Therefore, serotonin synthesis seems to be regulated by two rate-limiting steps: tryptophan level and the induction of TDC in plants. The fact that a high level of tryptophan is required for serotonin synthesis may indicate that a high serotonin level is closely implicated in an increased pool of tryptophan in plants.

Addendum to: Kang S, Kang K, Lee K, Back K. Characterization of tryptamine 5-hydroxylase and serotonin synthesis in rice plants. Plant Cell Rep. 2007;26:2009–2015. doi: 10.1007/s00299-007-0405-9.

Footnotes

Previously published online as a Plant Signaling & Behavior E-publication: http://www.landesbioscience.com/journals/psb/article/5401

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