Abstract
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.
Highlights
Serotonin, which is well known as a pineal hormone in mammals, plays a key role in conditions such as mood, eating disorders, and alcoholism
tryptophan decarboxylase (TDC) serves as a bottleneck point regulating serotonin biosynthesis since TDC expression is very low or negligible, while tryptamine 5-hydroxylase (T5H) is constitutively expressed in healthy rice (Oryza sativa) plants
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
Summary
Serotonin, which is well known as a pineal hormone in mammals, plays a key role in conditions such as mood, eating disorders, and alcoholism. 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. 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) This abscission period is accompanied by proteolysis and deamination of amino acids giving rise to ammonium accumulation in walnut seeds. Due to the low expression of TDC in rice plants, serotonin levels in leaves and seeds were reported to be around 0.3 mg/g FW and 0.12 mg/g seeds, respectively, whereas transgenic rice plants overexpressing TDC produced 25- and 11-fold higher serotonin in the leaves and seeds, respectively, than the wild type (Kang et al, 2007b)
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