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First published online May 13, 2009; 10.1104/pp.109.138552 Plant Physiology 150:1380-1393 (2009) © 2009 American Society of Plant Biologists OPEN ACCESS ARTICLE
Senescence-Induced Serotonin Biosynthesis and Its Role in Delaying Senescence in Rice Leaves1,[C],[W],[OA]Department of Biotechnology, Interdisciplinary Program for Bioenergy and Biomaterials of Graduate School, Agricultural Plant Stress Research Center, Chonnam National University, Gwangju 500–757, South Korea
Serotonin, which is well known as a pineal hormone in mammals, plays a key role in conditions such as mood, eating disorders, and alcoholism. In plants, although serotonin has been suggested to be involved in several physiological roles, including flowering, morphogenesis, and adaptation to environmental changes, its regulation and functional roles are as yet not characterized at the molecular level. In this study, we found that serotonin is greatly accumulated in rice (Oryza sativa) leaves undergoing senescence induced by either nutrient deprivation or detachment, and its synthesis is closely coupled with transcriptional and enzymatic induction of the tryptophan biosynthetic genes as well as tryptophan decarboxylase (TDC). Transgenic rice plants that overexpressed TDC accumulated higher levels of serotonin than the wild type and showed delayed senescence of rice leaves. However, transgenic rice plants, in which expression of TDC was suppressed through an RNA interference (RNAi) system, produced less serotonin and senesced faster than the wild type, suggesting that serotonin is involved in attenuating leaf senescence. The senescence-retarding activity of serotonin is associated with its high antioxidant activity compared to either tryptophan or chlorogenic acid. Results of TDC overexpression and TDC RNAi plants suggest that TDC plays a rate-limiting role for serotonin accumulation, but the synthesis of serotonin depends on an absolute amount of tryptophan accumulation by the coordinate induction of the tryptophan biosynthetic genes. In addition, immunolocalization analysis revealed that serotonin was abundant in the vascular parenchyma cells, including companion cells and xylem-parenchyma cells, suggestive of its involvement in maintaining the cellular integrity of these cells for facilitating efficient nutrient recycling from senescing leaves to sink tissues during senescence.
Serotonin (5-hydroxytryptamine) is a ubiquitous monoamine that plays multiple roles as a neurotransmitter, hormone, and mitogenic factor and mediates a series of activities in various animal cells (Frazer and Hensler, 1999  ). In plants, serotonin has been found in a wide range of plant species (Roshchina, 2001) since its discovery was first reported in the fruit of the cowhage (Mucuna pruriens) plant (Bowden et al., 1954). Similar to the multiple roles played by serotonin in animal cells, serotonin has also been implicated in an array of physiological functions in plants that are purportedly related to growth regulation, flowering, xylem sap exudation, ion permeability, and plant morphogenesis (Csaba and Pal, 1982; Odjakova and Hadjiivanova, 1997; Murch et al., 2001; Roshchina, 2001).
Serotonin is predominantly distributed in reproductive as opposed to vegetative organs. For example, Griffonia simplicifolia leaves were found to contain 0.007 µg/g fresh weight (FW) serotonin, but seeds harbored 2,000 µg/g seeds (Fellows and Bell, 1970
One interesting study on serotonin synthesis and its possible biological function was reported for walnut (Juglans regia) seeds, in which serotonin is mainly accumulated during the process of fruit abscission (Bergmann et al., 1970
Serotonin biosynthesis occurs via two enzymatic steps (Fig. 1A
). The first committed enzyme is tryptophan decarboxylase (TDC), which catalyzes the conversion of Trp into tryptamine. The terminal enzyme is tryptamine 5-hydroxylase (T5H), which hydroxylates the C-5 position of tryptamine to form serotonin (Kang et al., 2007a
Although an exact role for serotonin in plants remains to be elucidated, it is tempting, by way of extrapolation, to think that serotonin synthesis is closely associated either with ripening or maturation of plant organs or with the accumulation of ammonia, which occurs predominantly during the process of plant senescence (Peeters and Van Laere, 1992 ). One approach to testing this possibility is to examine the levels of serotonin upon senescence in rice plants because they are known to harbor at least two functional TDC genes of which TDC1 is functionally implicated in synthesizing serotonin (Kang et al., 2007b). In contrast to the previous reports showing the predominant production of serotonin in reproductive organs, this report describes the enormous induction of serotonin synthesis in senescing rice leaves, which is characterized by chlorophyll loss, membrane lipid peroxidation, increased reactive oxygen species (ROS), and induced senescence-related genes. It further shows that the induction of serotonin accumulation is coordinately regulated with the induction of the entire set of Trp biosynthetic mRNAs and is proportional to the induction of TDC protein. Furthermore, the accumulation of serotonin is believed to play a protective role against ROS, leading to a delay in the process of senescence as demonstrated by analyses of transgenic rice plants, such as TDC overexpression and TDC RNA interference (RNAi) lines.
Synthesis of Serotonin in Attached Leaves of Rice Seedlings upon Senescence Induced by Nutrient Deprivation When 8-d-old rice seedlings were grown in water with no nutrients, the plants began to undergo the senescence process and turn yellow at 16 d. By day 26, most of the existing leaves had turned yellow and were dry and twisted, whereas most stems and roots remained healthy (Fig. 1B). In response to the process of senescence, a high level of serotonin accumulated in senescing rice leaves (Fig. 1C). In healthy leaves, serotonin levels were typically below 0.5 µg/g FW. However, as rice plants aged, serotonin synthesis began at 11 d (10 µg/g FW) in leaves and reached up to 75 µg/g FW at 16 d, at which time the leaves began to turn yellow. Serotonin continued to accumulate in leaves until day 26, at which time the serotonin content was around 350 µg/g FW. In roots, serotonin accumulated as the plants aged, but its level at 26 d was 9-fold less compared to that in leaves. Serotonin was also observed in stems and reached a peak level of 20 µg/g FW, which was 2-fold lower than that in roots. Although serotonin levels varied among tissues, serotonin was abundantly synthesized in senescent rice tissues, and the induced synthesis of serotonin was closely paralleled by the appearance of symptoms of senescence. In contrast, the rice seedlings grew without showing senescence symptoms and did not show any increases in serotonin synthesis in the leaves either in the presence of half-strength Murashige and Skoog solution without Suc or on soil-based compost (data not shown).
To examine whether rice seedlings exposed to nutrient-free water go through a typical senescence process, several biochemical and molecular indices related to the senescence syndrome were investigated (Fig. 2
). First, chlorophyll content gradually decreased over time. In 3 d, the leaf chlorophyll content decreased by 25% and remained at that level until 11 d later. Thereafter, the chlorophyll content dropped dramatically to 50% and 10% of that in the initial nonsenescent leaves at 21 and 26 d, respectively. In contrast, stem chlorophyll levels declined by 25% after 3 d, but this level of chlorophyll was maintained until 26 d, suggesting that no dramatic senescence had occurred in the stems compared to the leaves (Fig. 2A). Next, we measured ROS and malondialdehyde (MDA), which are characteristic symptomatic indicators of senescence in plants (Fig. 2, B and C). Upon senescence, ROS levels in leaves began to increase at 11 d and thereafter increased rapidly. Likewise, MDA levels in leaves increased in parallel with ROS levels. In contrast, stems and roots showed no significant increases in either ROS or MDA levels. To further confirm the senescence process at the molecular level in our in planta system, we performed northern-blot analysis using representative senescence-associated genes, such as Osl2 and Osl139, which were induced in rice leaves upon senescence (Lee et al., 2001
Induction of TDC in Parallel with Serotonin Accumulation
Serotonin is consecutively synthesized from Trp by two enzymes. TDC is the first committed enzyme, which catalyzes the conversion of Trp to tryptamine, followed by catalysis of tryptamine to produce serotonin by T5H (Kang et al., 2007a
TDC Protein Is Maximally Expressed in the Fully Senesced Leaves To examine the relative levels of the TDC1 protein in senescing leaves of rice seedlings, we took the 16-d-old senescing rice leaves induced by nutrient deprivation and dissected them into three parts: the tip (fully senesced), middle (partially senesced), and base (barely senesced) to measure the level of expression of the TDC1 protein and the level of serotonin. As shown in Figure 4 , expression of the TDC1 protein was highest in the fully senesced tip, followed by the middle and base. Although the polyclonal antibodies raised from TDC1 protein also show cross-reactivity to TDC2 protein, it is clear that the immune-reacted bands identified by the TDC1 antibodies predominantly correspond to TDC1 protein because the TDC2 mRNA was not significantly induced upon senescence (Fig. 3). The relative levels of the TDC protein were closely associated with the level of serotonin. The tip contained the highest level of serotonin at 270 µg/g FW, whereas the middle and base parts contained 152 and 30 µg/g FW, respectively. In particular, Trp, the substrate of the TDC enzyme, coordinately increased up to 400 µg/g FW in the fully senesced tip, which corresponded to a level 1.5-fold higher than serotonin. These data clearly suggested that TDC expression is abundant in the senesced tissues of rice leaves and is strongly induced in parallel with the high production of serotonin as well as Trp as the rice leaves undergo senescence. In addition, the effects of exogenous applications of serotonin on leaf senescence were investigated by measuring chlorophyll, ROS, and MDA. As shown in Supplemental Figure S1, treatment with 500 µM serotonin showed 2-fold higher chlorophyll content than the untreated leaves at 26 d. Both ROS and MDA levels decreased significantly in serotonin-treated leaves compared to untreated leaves. In addition, TDC enzyme activity was 3-fold lower in serotonin-treated leaves (500 µM) than in untreated leaves at 26 d, suggestive of retarded senescence caused by serotonin (Supplemental Fig. S2).
Accumulation of Serotonin and Plant Hormonal Effects upon Senescence of Detached Leaves of Rice In Figures 1 to 4, we show the course of serotonin synthesis as well as its effects on senescence (Supplemental Figs. S1 and S2) using an in planta system. To further verify the mechanisms of serotonin biosynthesis and its physiological roles and to simplify the experiment, we next used leaves detached from 4-week-old rice seedlings and measured the levels of serotonin in response to senescence. As shown in Figure 5 , serotonin began to be synthesized on day 4, produced 984 µg/g FW on day 6, and peaked on day 8 with 1,634 µg/g FW (Fig. 5A). The maximum level of serotonin in the detached leaves was 4.7-fold higher than that found in the attached leaves upon senescence, indicating that the detachment of the leaves had a more dramatic effect on serotonin synthesis than was observed for the attached leaves.
The effects of plant hormones, such as zeatin and abscisic acid (ABA), on serotonin synthesis in response to senescence were investigated. ABA treatment accelerated serotonin synthesis, producing 450 µg/g FW after 4 d, while control leaves produced only 16 µg/g FW serotonin and showed a maximum synthesis of serotonin (720 µg/g FW) at 6 d, followed by gradual decrease. In contrast to ABA, zeatin treatment delayed serotonin synthesis, and its levels were far lower compared to those of the untreated control leaves. These data on the changes in serotonin levels upon hormonal treatment were consistent with the known roles of zeatin and ABA, which play inhibitory and stimulatory roles in senescence, respectively. In addition, the Trp content also increased greatly in parallel with the serotonin levels upon senescence (Fig. 5B). The relative levels of Trp during the entire time course of senescence were higher in the ABA-treated leaves than in the untreated control. Similarly, zeatin-treated leaves showed lower levels of Trp synthesis than those detected in the untreated and ABA-treated leaves. The relative levels of serotonin in the detached leaves upon hormonal treatment were closely coupled with the relative levels of TDC protein expression (Fig. 5C). For example, the untreated control began to show a detectable level of TDC protein at 6 d and reached peak expression at 8 d, whereas the ABA-treated leaves showed a fast induction of TDC at 4 d and reached a maximum at 6 d. TDC expression levels were higher in the untreated control leaves relative to those of the ABA-treated leaves, accounting for the higher levels of serotonin synthesis in the untreated control leaves. Zeatin treatment suppressed the induced expression of the TDC protein and led to the low levels of serotonin synthesis compared to the untreated control. Taken together with the induced accumulation of serotonin upon senescence in the in planta system, these results clearly indicate that serotonin accumulation is directly associated with the process of senescence (Fig. 5D).
The results from the detached leaves show that serotonin accumulation in response to senescence is accompanied by the induced accumulation of free Trp. To test whether Trp biosynthetic genes are induced upon senescence, five Trp biosynthetic genes were selected for characterization. Figure 6A
shows that the mRNAs encoding the enzymes anthranilate synthase (AS
Serotonin-Overproducing Transgenic Rice Leaves Lead to a Delay of Leaf Senescence
The role of serotonin in senescence was further investigated by performing a gain-of-function analysis. We used transgenic rice plants overexpressing the rice TDC1 gene under control of the maize (Zea mays) ubiquitin promoter. These TDC1 transgenic rice plants produced 25-fold higher serotonin in leaves than the wild type (Kang et al., 2007b
Suppression of TDC by RNAi Produces Low Serotonin and Promotes Senescence
To further examine the function of serotonin in vivo, we employed RNAi interference to silence the expression of TDC1, which is a rate-limiting enzyme for serotonin synthesis. A transgene TDC1 was controlled by a maize ubiquitin promoter, and 20 independent transgenic lines were generated through Agrobacterium tumefaciens-mediated transformation (Fig. 8).
Among them, two lines (RNAi-11 and RNAi-16) of T1 generation were further selected for examining the loss-of-function effects of TDC1 on serotonin synthesis. Four-week-old mature leaves of rice plants were detached and the levels of serotonin measured upon senescence. TDC1 RNAi lines showed that serotonin synthesis decreased markedly during senescence. For example, the wild type and vector control produced around 900 µg g–1 FW serotonin 6 d after senescence, whereas the RNAi lines (T1), such as RNAi-11 and RNAi-16, only produced 125 and 207 µg g–1 FW serotonin, respectively (Fig. 8B). Accordingly, these RNAi lines exhibited a rapid senescence relative to the wild type. Chlorophyll concentrations were 1.5-fold less in the RNAi lines than in the wild type after 8 d, confirming that serotonin itself plays a direct role in delaying senescence in rice leaves (Fig. 8D). In contrast to serotonin levels, Trp levels did not dramatically change in the RNAi lines, although the RNAi lines had lower levels of Trp than the wild type or vector control, especially after 6 d (Fig. 8C). Note that the RNAi lines (T1) were not different phenotypically from the wild type in both the vegetative and reproductive stages, suggesting that serotonin is not directly involved in primary metabolism, but rather in secondary metabolism acting as a metabolite to delay senescence. In rice plants, serotonin is further metabolized into serotonin derivatives, such as feruloylserotonin (FS) and 4-coumaroylserotonin (CS), in reactions catalyzed by serotonin N-hydroxycinnamoyl transferase (SHT). These serotonin derivatives are acknowledged to be strong antioxidant compounds. Thus, the role of these serotonin derivatives in delaying senescence could not be ruled out. In an attempt to verify the effects of serotonin derivatives on senescence, we used pepper (Capsicum annuum) SHT-overexpressing transgenic rice plants that produce high levels of serotonin derivatives (Jang et al., 2004
Immunohistochemical Localization of the TDC Protein and Serotonin in Senesced Leaves of Rice The spatial distribution of the TDC protein and serotonin in the cross section of rice leaves was examined by immunohistochemical localization using TDC and serotonin polyclonal antibodies (Fig. 10 ). TDC protein and serotonin were not stained in control leaves but were clearly observed 7 d after senescence, which was consistent with the results of previous analyses (Fig. 5). Although all of the mesophyll cells except the epidermal cells were thoroughly stained, signals for the TDC protein were abundant in vascular parenchyma cells, whereas bundle sheath cells and the metaxylem were not stained (Fig. 10, C and F). The companion cells were also clearly stained, but the signal intensity was not high compared to that in the xylem parenchyma cells. In contrast, serotonin was strongly stained in companion cells at a level of intensity similar to the vascular parenchyma cells (Fig. 10, D and G). These data suggest that serotonin may play an important role in maintaining the cellular integrity of vascular bundles with its high antioxidant activity during the process of senescence.
This study characterized the mechanisms by which senescence triggers and coordinates serotonin synthesis through the biosynthetic machinery of the Trp pathway. Furthermore, we investigated the functional roles of serotonin during senescence via the analyses of serotonin-overproducing and -deficient transgenic rice plants. Senescence is a genetically controlled process that plays an important role in the recycling of nutrients from old leaves to young productive leaves and developing seeds. A myriad of developmental and environmental factors regulating senescence are characterized by a loss of chlorophyll and degradation of macromolecules, such as protein, lipids, and RNA (Kim et al., 2007 ).
While most genes are inactivated during senescence, particular sets of genes, referred to as senescence-related genes, are activated and participate in catabolic activities. The senescence-related genes include genes whose products are related to pathogen defense mechanisms. This indicates that defense-related genes play a role in leaf senescence as well as in pathogen infection. For example, microarray analyses have shown that many genes involved in the biosynthesis of secondary metabolites are up-regulated (Gregersen and Holm, 2007
During leaf senescence, the intensive breakdown of various macromolecules, such as proteins by the induction of proteases, is followed by an increase in free amino acids, such as Gln and Asn, which serve as long-distance transport forms of organic nitrogen (Hayashi and Chino, 1990
The report on Trp-overproducing transgenic rice demonstrated that Trp seems to be a stable primary metabolite suitable for either nutrient remobilization or storage in senescing plant tissues (Dubouzet et al., 2007
A representative secondary metabolite participating in scavenging ROS generated during senescence is tocopherol. As a strongly lipid-soluble antioxidant, tocopherol is known to be synthesized exclusively in chloroplasts and to protect the tissues from photosynthesis-derived ROS (Munné-Bosch, 2005
Furthermore, the preferential expression of TDC within these vascular cells in parallel with serotonin production may be coupled with the enriched Trp that was induced upon senescence, although Trp biosynthesis occurs in the plastids (Radwanski and Last, 1995
In Planta Senescence in Rice Seedlings Seeds of wild-type rice (Oryza sativa) were surface-sterilized and sown in half-strength Murashige and Skoog media in a plant growth room at 28°C with a 16-h-light/8-h-dark cycle for 8 d. A group of 10 seedlings was transferred into 50-mL polypropylene conical tubes with their roots exposed to water containing no nutrients. Senescence was visible after 16 d. Rice tissues were harvested at specified time points and subjected to further analysis. The data were analyzed by two to five replicates, and then the Duncan's multiple range was carried out to find the significant differences at P < 0.05.
Seeds of wild-type and transgenic rice were immersed in tap water for 2 d to induce germination and then potted in a tray filled with greenhouse compost (Boonong Soil). Seedlings were grown in a plant growth room at 28°C and 70% humidity in a 16-h-light/8-h-dark cycle at 150 µmol m–2 s–1 photosynthetic photon flux density for 4 weeks. The apical 15 cm of the third leaf was used in all experiments. A group of 10 segments was transferred into a 50-mL polypropylene conical tube containing 10 mL of water without nutrients and incubated under the same growth conditions mentioned above for specified time periods.
Chlorophyll content was spectrophotometrically determined according to the method of Lichtenthaler (1987)
Total RNA (10 µg) was isolated from leaves of transgenic or wild-type rice plants using TRI reagent (Sigma-Aldrich). Northern-blot analysis was performed as described previously (Kang et al., 2007b
Agrobacterium tumefaciens-mediated transformation was used to generate TDC1 RNAi transgenic rice plants. The rice TDC1 gene was amplified with the following primers: 5'-CTGGGTACCACTAGTATGACGCACTGGGCGAGC-3' (KpnI and SpeI sites underlined) and 5'-GGGATCCGAGCTCCCTGCATCGCCTCCAGCA-3' (BamHI and SacI sites underlined). The PCR product of 519 bp was digested with either SacI and SpeI or with KpnI and BamHI, gel purified, and ligated into the same restriction sites within the pTCK303 binary vector (a kind gift from Dr. Kang Chong of the Institute of Botany, Chinese Academy of Sciences, Beijing, China). The resulting TDC1 genes were now arranged in the order of an antisense TDC1, a rice intron, and sense TDC1 fragments between the maize (Zea mays) ubiquitin promoter and the nos 3'-terminator in the pTCK303 binary vector (Fig. 8A). After verifying the DNA sequence, the pTCK303-TDC RNAi binary vector was transformed into Agrobacterium LBA4404. Rice transformation was performed as previously described (Lee et al., 2000
A polyclonal mouse antiserum raised against the purified recombinant rice TDC1 protein was employed for immunoblot analysis (Peptron). Rice leaves (0.2 g) were homogenized in a mortar and pestle with 1 mL of homogenization buffer: 80 mM Tris-HCl (pH 7.0), 20% (w/v) glycerol, 10 mM sodium metabissulfate, 10 mM sodium ascorbate, 1% (w/v) polyvinyl pyrrolidone, 5 mM β-mercapthoethanol, and 2 mM EDTA for the extraction of total soluble proteins. After centrifuging for 10 min at 13,500g, the supernatant extracts were used as total soluble proteins. Proteins were separated by 11% SDS-PAGE and electroblotted onto polyvinylidene difluoride membranes. Immunodetection was performed according to standard procedures (Boehringer Mannheim).
Rice tissues (0.25 g) frozen with liquid nitrogen were homogenized to a fine powder using a mortar and pestle. Methanol was added to the powder, and the mixture was passed through a filter (Millex-LG; Millipore). Water (100 µL) was added to a 400-µL aliquot of the filtrate, and the mixture was passed through a Sep-pak Light C18 cartridge (Waters) that was equilibrated with 80% methanol. The cartridge was washed with 500 µL of 80% methanol and the effluent concentrated in a vacuum centrifuge. The resulting residue was dissolved in 40 µL of 50% methanol. This solution was analyzed by reversed-phase HPLC (Shimadzu) for quantification of serotonin and Trp. Compounds were separated on an Atlantis C18 column (3.9 x 150 mm; Waters) with an isocratic elution profile of 5% (v/v) methanol in water containing 0.3% trifluoroacetic acid at a flow rate of 0.8 mL/min. The elution of compounds was detected at 280 nm. The methanol extracts were passed through a Sep-Pak C18 cartridge (Waters) and further fractionated with a Sep-Pak Silica cartridge (Waters) for analysis of serotonin derivatives. The fraction eluted in chloroform:methanol (30:1) was evaporated to dryness and dissolved in 0.5 mL of methanol. Detection of serotonin derivatives was measured at 320 nm under the same HPLC conditions described above.
AS activity was measured as described previously (Bücker et al., 1995
The radical scavenging activity of a series of compounds, including Trp and serotonin, was measured using the 1,1-diphenyl-2-picrylhydrazyl (DPPH) method as described previously (Kang et al., 2005
For immunolocalization, rice leaves were fixed in 0.05% glutaraldehyde and 4% paraformaldehyde in 50 mM sodium phosphate buffer (pH 7.0), dehydrated in ethanol, and embedded in paraffin. Tissues were sliced into 7-µm-thick transverse sections. The deparaffinized sections were incubated with mouse antisera against rice TDC at a dilution of 1:7,000 or serotonin (Alpha Diagnostic) at a dilution of 1:100, respectively. According to the manufacturer's instructions, the primary antibodies were detected with the Dako LSAB 2 System (DakoCytomation) and colorized using 3-amino-9-ethylcarbazole for TDC or enhanced diamino benzidine for serotonin, respectively. Control experiments using preimmune sera were unreactive.
The following materials are available in the online version of this article.
We thank Dr. Kang Chong (Institute of Botany, Chinese Academy of Sciences, Beijing, China) for the pTCK303 RNAi binary vector and the National Institute of Agrobiological Sciences (http://www.rgrc.dna.affrc.go.jp/) for providing the Trp biosynthetic cDNAs. Received March 12, 2009; accepted May 7, 2009; published May 13, 2009.
1 This work was supported by the Science Research Center program of the Ministry of Science and Technology/Korea Science and Engineering Foundation to the Agricultural Plant Stress Research Center (R11–2001–09205001–0) of Chonnam National University.  The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Kyoungwhan Back (kback{at}chonnam.ac.kr).
[C] Some figures in this article are displayed in color online but in black and white in the print edition.
[W] The online version of this article contains Web-only data.
[OA] Open access articles can be viewed online without a subscription. www.plantphysiol.org/cgi/doi/10.1104/pp.109.138552 * Corresponding author; e-mail kback{at}chonnam.ac.kr.
Barth C, Moeder W, Klessig DF, Conklin PL (2004) The timing of senescence and response to pathogens is altered in the ascorbate-deficient Arabidopsis mutant vitamin c-1. Plant Physiol 134: 1784–1792 Bergmann L, Grosse W, Ruppel HG (1970) Die Bildung von serotonin in Juglans regia L. Planta 94: 47–59[CrossRef][Web of Science] Bowden K, Brown BG, Batty JE (1954) 5-Hydroxytryptamine: its occurrence in cowhage. Nature 174: 925–926[CrossRef][Web of Science][Medline] Bücker C, Witte B, Windmüller U, Grambow J (1995) Anthranilate synthase and chorismate mutase activities in stem rust-inoculated and elicitor-treated resistant, moderately resistant, and susceptible near-isogenic wheat lines. Z Naturforsch [C] 50: 54–60 Cohen JD, Slovin JP, Hendrickson AM (2003) Two genetically discrete pathways convert tryptophan to auxin: more redundancy in auxin biosynthesis. Trends Plant Sci 8: 197–199[CrossRef][Web of Science][Medline] Collier HOJ, Chesher GB (1956) Identification of 5-hydroxytryptamine in the sting of the nettle (Urtica dioica). Br J Pharmacol 11: 186–189[Medline] Csaba G, Pal K (1982) Effect of insulin triodothyronine and serotonin on plant seed development. Protoplasma 110: 20–22[CrossRef][Web of Science] Dubouzet JG, Ishihara A, Matsuda F, Miyagawa H, Iwata H, Wakasa K (2007) Integrated metabolomic and transcriptomic analyses of high-tryptophan rice expressing a mutant anthranilate synthase alpha subunit. J Exp Bot 58: 3309–3321 Fellows LE, Bell EA (1970) 5-Hydroxy-L-tryptophan, 5-hydroxytryptamine and L-tryptophan 5-hydroxylase in Griffonia simplicifolia. Phytochemistry 9: 2389–2396[CrossRef][Web of Science] Foy JM, Parrat JR (1961) A note on the presence of noradrenaline and 5-hydroxytryptamine in plantain (Musa sapientum var. paradisiaca). J Pharm Pharmacol 12: 360–364[Web of Science] Frazer A, Hensler JG (1999) Understanding the neuroanatomical organization of serotonergic cells in brain provides insight into the functions of this neurotransmitter. In GJ Siegel, BW Agranoff, SK Fisher, RW Albers, MD Uhler, eds, Basic Neurochemistry. Lippincott Williams and Wilkins, Baltimore, pp 264–268 Gregersen PL, Holm PB (2007) Transcriptome analysis of senescence in the flag leaf of wheat (Triticum aestivum L.). Plant Biotechnol J 5: 192–206[CrossRef][Web of Science][Medline] Hayashi H, Chino M (1990) Chemical composition of phloem sap from the uppermost internode of the rice plant. Plant Cell Physiol 31: 247–251 Ishihara A, Hashimoto Y, Tanaka C, Dubouzet JG, Nakao T, Matsuda F, Nishioka T, Miyagawa H, Wakasa K (2008) The tryptophan pathway is involved in the defense responses of rice against pathogenic infection via serotonin production. Plant J 54: 481–495[CrossRef][Web of Science][Medline] 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 K, Jang SM, Kang S, Back K (2005) Enhanced neutraceutical serotonin derivatives of rice seed by hydroxycinnamoyl-CoA:serotonin N-(hydroxycinnamoyl)transferase. Plant Sci 168: 783–788[CrossRef][Web of Science] Kang S, Kang K, Lee K, Back K (2007a) Characterization of tryptamine 5-hydroxylase and serotonin synthesis in rice plants. Plant Cell Rep 26: 2009–2015[CrossRef][Web of Science][Medline] Kang S, Kang K, Lee K, Back K (2007b) Characterization of rice tryptophan decarboxylases and their direct involvement in serotonin biosynthesis in transgenic rice. Planta 227: 263–272[CrossRef][Web of Science][Medline] Kang K, Kang S, Lee K, Park M, Back K (2008) Enzymatic features of serotonin biosynthetic enzymes and serotonin biosynthesis in plants. Plant Signal Behav 3: 389–390 Kim HJ, Lim PO, Nam HG (2007) Molecular regulation of leaf senescence. In S Gan, ed, Senescence Processes in Plants. Blackwell Publishing, Ames, IA, pp 231–255 Lee HJ, Lee SB, Chung JS, Han SU, Han O, Guh JO, Jeon JS, An G, Back K (2000) Transgenic rice plants expressing a Bacillus subtilis protoporphyrinogen oxidase gene are resistant to diphenyl ether herbicide oxyfluorfen. Plant Cell Physiol 41: 743–749 Lee RH, Wang CH, Huang LT, Chen SCG (2001) Leaf senescence in rice plants: cloning and characterization of senescence up-regulated genes. J Exp Bot 52: 1117–1121 Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148: 350–382[CrossRef][Web of Science] Matsukawa T, Ishihara A, Iwamura H (2002) Induction of anthranilate synthase activity by elicitors in oats. Z Naturforsch [C] 57: 121–128[Medline] Munné-Bosch S (2005) The role of 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[CrossRef][Web of Science] Noh YS, Amasino RM (1999) Identification of a promoter region responsible for the senescence-specific expression of SAG12. Plant Mol Biol 41: 181–194[CrossRef][Web of Science][Medline] Odjakova M, Hadjiivanova C (1997) Animal neurotransmitter substances in plants. Bulg J Plant Physiol 23: 94–102 Peeters KMU, Van Laere AJ (1992) Ammonium and amino acid metabolism in excised leaves of wheat (Triticum aestivum) senescing in the dark. Physiol Plant 84: 243–249[CrossRef] Radwanski ER, Last RL (1995) Tryptophan biosynthesis and metabolism: biochemical and molecular genetics. Plant Cell 7: 921–934[CrossRef][Web of Science][Medline] Rice-Evans C, Miller NJ, Paganga G (1997) Antioxidant properties of phenolic compounds. Trends Plant Sci 2: 152–159[CrossRef][Web of Science] Rosenvasser S, Mayak S, Friedman H (2006) Increase in reactive oxygen species (ROS) and in senescence-associated gene transcript (SAG) levels during dark-induced senescence of Pelargonium cuttings, and the effect of gibberellic acid. Plant Sci 170: 873–879[CrossRef][Web of Science] Roshchina VV (2001) Neurotransmitters in Plant Life. Science Publishers, Enfield, NH, pp 4–81 Sakurai N, Hayakawa T, Nakamura T, Yamaya T (1996) Changes in the cellular localization of cytosolic glutamine synthetase in vascular bundles of rice leaves at various stages of development. Planta 200: 306–311[Web of Science] Soudry E, Ulitzur S, Gepstein S (2005) Accumulation and remobilization of amino acids during senescence of detached and attached leaves: in planta analysis of tryptophan levels by recombinant luminescent bacteria. J Exp Bot 56: 695–702 Takahama U, Oniki T (1997) A peroxidase/phenolics/ascorbate system can scavenge hydrogen peroxide in plant cells. Physiol Plant 101: 845–852[CrossRef] Tozawa Y, Hasrgawa H, Terakawa T, Wakasa K (2001) Characterization of rice anthranilate synthase Udenfriend S, Lovenberg W, Sjoerdsma A (1959) Physiologically active amines in common fruits and vegetables. Arch Biochem Biophys 85: 487–490[CrossRef][Web of Science][Medline] Ueno M, Shibata H, Kihara J, Hnda 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[CrossRef][Web of Science][Medline] Van Bel AJE (1993) Strategies of phloem loading. Annu Rev Plant Physiol Plant Mol Biol 44: 253–281[CrossRef][Web of Science] Zhao J, Last RL (1996) Coordinate regulation of the tryptophan biosynthetic pathway and indolic phytoalexin accumulation in Arabidopsis. Plant Cell 8: 2235–2244[Abstract] Related articles in Plant Physiol.:
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1 and ASβ2), phosphoribosylanthranilate transferase (PAT), indole-3-glycerolphosphate synthase (IGPS), and tryptophan synthase (TS
ex 340 nm/