Serotonin and Melatonin Biosynthesis in Plants: Genome-Wide Identification of the Genes and Their Expression Reveal a Conserved Role in Stress and Development

Abstract

Serotonin (Ser) and melatonin (Mel) serve as master regulators of plant growth and development by influencing diverse cellular processes. The enzymes namely, tryptophan decarboxylase (TDC) and tryptamine 5-hydroxylase (T5H) catalyse the formation of Ser from tryptophan. Subsequently, serotonin N-acetyl transferase (SNAT) and acetyl-serotonin methyltransferase (ASMT) form Mel from Ser. Plant genomes harbour multiple genes for each of these four enzymes, all of which have not been identified. Therefore, to delineate information regarding these four gene families, we carried out a genome-wide analysis of the genes involved in Ser and Mel biosynthesis in Arabidopsis, tomato, rice and sorghum. Phylogenetic analysis unravelled distinct evolutionary relationships among these genes from different plants. Interestingly, no gene family except ASMTs showed monocot- or dicot-specific clustering of respective proteins. Further, we observed tissue-specific, developmental and stress/hormone-mediated variations in the expression of the four gene families. The light/dark cycle also affected their expression in agreement with our quantitative reverse transcriptase-PCR (qRT-PCR) analysis. Importantly, we found that miRNAs (miR6249a and miR-1846e) regulated the expression of Ser and Mel biosynthesis under light and stress by influencing the expression of OsTDC5 and OsASMT18, respectively. Thus, this study may provide opportunities for functional characterization of suitable target genes of the Ser and Mel pathway to decipher their exact roles in plant physiology.

Melatonin induces drought tolerance by modulating lipoxygenase expression, redox homeostasis and photosynthetic efficiency in Arachis hypogaea L

“…This is further evident by an increase in the melatonin content in unprimed stressed plants of the tolerant variety. However, the decrease in melatonin content in tolerant primed stressed plants compared to unprimed stressed plants (Figure 2) signify the feedback inhibition, which is consistent with findings of Bhowal et al (2021). Further, down-regulated expression of T-5H and ASMT in this variety (Supplementary Figures 3B, D) also correlated to the decreased endogenous melatonin content.…”

Evidence that miR168a contributes to salinity tolerance of Brassica rapa L. via mediating melatonin biosynthesis

“…We only found one study regarding the role of miRNAs in regulating melatonin biosynthesis genes. Recently, Bhowal et al (2021) reported that miR6249a and miR1846e regulated the expression of serotonin and melatonin biosynthesis under heat, salinity, and drought stress by influencing the expression of TDC5 and ASMT18 , respectively. Our results provide evidence that partially sheds light on some attributes of this causal relationship.…”

Identification of Putative Markers of Non-infectious Bud Failure in Almond [Prunus dulcis (Mill.) D.A. Webb] Through Genome Wide DNA Methylation Profiling and Gene Expression Analysis in an Almond × Peach Hybrid Population

“…Its homologous gene in Arabidopsis (AT4G35160, or acetyl serotonin methyltransferase ASMT1 , Berardini et al, 2015 ) has been reported to be expressed in the epidermal L1 layer in the shoot apex. The melatonin biosynthesis pathway was recently shown to be associated with both abiotic ( Wang et al, 2021 ) and biotic ( Zhu et al, 2021 ) stress responses ( Bhowal et al, 2021 ). Members of the melatonin pathway have been shown to be involved in responses to osmotic, drought, and heat stresses ( Bhowal et al, 2021 ), and many of these genes are regulated through miRNAs.…”

“…The melatonin biosynthesis pathway was recently shown to be associated with both abiotic ( Wang et al, 2021 ) and biotic ( Zhu et al, 2021 ) stress responses ( Bhowal et al, 2021 ). Members of the melatonin pathway have been shown to be involved in responses to osmotic, drought, and heat stresses ( Bhowal et al, 2021 ), and many of these genes are regulated through miRNAs. In rice, induction of the homologous gene, OsASMT1 , occurred following exposure to the cytokinin benzylaminopurine ( Bhowal et al, 2021 ) which is known to stimulate cell division.…”

“…Members of the melatonin pathway have been shown to be involved in responses to osmotic, drought, and heat stresses ( Bhowal et al, 2021 ), and many of these genes are regulated through miRNAs. In rice, induction of the homologous gene, OsASMT1 , occurred following exposure to the cytokinin benzylaminopurine ( Bhowal et al, 2021 ) which is known to stimulate cell division. In tomato, melatonin enhances the expression of heat shock proteins following heat stress, improving thermotolerance ( Xu et al, 2016 ; Wang et al, 2018 ), while in grape, the role of ASMT1 was related to enhanced ozone tolerance in leaves ( Liu et al, 2021 ).…”