Abstract

Melatonin, a bioactive compound and an important signaling molecule produced in plants and animals, is involved in many biological processes. However, its function and synthetic pathways in fungi are poorly understood. Here, the samples from Tolypocladium guangdongense, a highly valued edible fungus with functional food properties, were collected under different experimental conditions to quantify the levels of melatonin and its intermediates. The results showed that the intracellular melatonin content was markedly improved by Congo red (CR), cold, and heat stresses; the levels of intracellular melatonin and its intermediates increased at the primordial (P) and fruiting body (FB) stages. However, the levels of most intermediates exhibited a notable decrease under CR stress. Several genes related to melatonin synthesis, excluding AADC (aromatic-L-amino-acid decarboxylase), were markedly upregulated at an early stage of CR stress but downregulated later. Compared to the mycelial stage, those genes were significantly upregulated at the P and FB stages. Additionally, exogenous melatonin promoted resistance to several abiotic stressors and P formation in T. guangdongense. This study is the first to report melatonin biosynthesis pathway in macro-fungi. Our results should help in studying the diversity of melatonin function and melatonin-synthesis pathways and provide a new viewpoint for melatonin applications in the edible-medicinal fungus.

Highlights

  • Melatonin [N-acetyl-3-(2-aminoethyl)-5-methoxyindole] is an indoleamine that was first reported as a neurohormone in the bovine pineal gland (Lerner et al, 1958)

  • In S. cerevisiae, a low temperature and low sugar level delayed the peaking of intracellular melatonin levels, whereas melatonin synthesis production was significantly promoted at 12°C (Wang et al, 2016; Morcillo-Parra et al, 2020a)

  • Compared to My stage, intracellular melatonin levels had approximate 16-fold and 28-fold increase at the P and FB stages, respectively (Figure 1B). These results suggested that intracellular melatonin may be involved in the primordial formation, fruiting body growth and the response of T. guangdongense to abiotic stresses, which need to be confirmed by further study

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Summary

Introduction

Melatonin [N-acetyl-3-(2-aminoethyl)-5-methoxyindole] is an indoleamine that was first reported as a neurohormone in the bovine pineal gland (Lerner et al, 1958). In 1960, Axelord et al first reported the classical pathway of melatonin biosynthesis in vertebrates. The melatonin-synthesis pathway in plants differs from that in vertebrates (Arnao and Hernández-Ruiz, 2017). Tryptamine is catalyzed into N-acetyltryptamine (NAT) and 5HT via serotonin N-acetyltransferase (SNAT) and tryptamine 5-hydroxylase (T5H), respectively, whereas 5HTryp is converted into serotonin by TDC. T5H and SNAT catalyze the conversion of NAT and 5HT, respectively, into N-acetylserotonin (NAS), whereas serotonin is converted into 5-methoxytryptamine (5MT) by acetylserotonin O-methyltransferase (ASMT) or caffeic acid O-methyltransferase (COMT). Muñiz-Calvo et al (2019) analyzed the melatonin-synthesis pathway in Saccharomyces cerevisiae by quantifying changes in the levels of melatonin and its biosynthetic intermediates in yeast cells at different growth stages. The synthesis pathway in yeast was similar to that in plants, except that NAT were not detected. The melatonin-synthesis pathway has not been elucidated in other fungi

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