Melatonin in Plants - Diversity of Levels and Multiplicity of Functions

Abstract

Melatonin has been detected in numerous plant species. A particularly surprising finding concerns the highly divergent levels of melatonin that vary between species, organs and environmental conditions, from a few pg/g to over 20 μg/g, reportedly up to 200 μg/g. Highest values have been determined in oily seeds and in plant organs exposed to high UV radiation. The divergency of melatonin concentrations is discussed under various functional aspects and focused on several open questions. This comprises differences in precursor availability, catabolism, the relative contribution of isoenzymes of the melatonin biosynthetic pathway, and differences in rate limitation by either serotonin N-acetyltransferase or N-acetylserotonin O-methyltransferase. Other differences are related to the remarkable pleiotropy of melatonin, which exhibits properties as a growth regulator and morphogenetic factor, actually debated in terms of auxin-like effects, and as a signaling molecule that modulates pathways of ethylene, abscisic, jasmonic and salicylic acids and is involved in stress tolerance, pathogen defense and delay of senescence. In the context of high light/UV intensities, elevated melatonin levels exceed those required for signaling via stress-related phytohormones and may comprise direct antioxidant and photoprotectant properties, perhaps with a contribution of its oxidatively formed metabolites, such as N (1)-acetyl-N (2)-formyl-5-methoxykynuramine and its secondary products. High melatonin levels in seeds may also serve antioxidative protection and have been shown to promote seed viability and germination capacity.

Keywords: antioxidant; auxin-like; circadian; photoprotection; seeds; senescence; stress.

FIGURE 1

Overview of ubiquitous primary metabolic reactions of melatonin. All hydroxylation reactions are nonenzymatically possible by interaction with free radicals, e.g., by consecutive reactions with two ⋅OH. By contrast with animals, enzymatic 6-hydroxylation by CYP monooxygenases does not seem to play a substantial role in plants. Instead, 2-hydroxylation by M2H enzymes, which belong to the family of 2-oxoglutarate-dependent dioxygenases (2-ODDs), has been shown to be of quantitative importance. 2-Hydroxymelatonin is in a tautomeric equilibrium with 3-acetamidoethyl-5-methoxyindolin-2-one. 2,3-Dioxygenation is enzymatically possible, e.g., by peroxidases and other heme enzymes, as well as nonenzymatically by some photocatalysts, hemin, free radicals and singlet oxygen. AFMK is also formed from cyclic 3-hydroxymelatonin, e.g., by two ⋅OH. AFMK can be further metabolized to numerous other compounds not depicted because of lacking documentation in plants. N-nitrosation has been shown to occur by interaction with ⋅NO, other NO congeners or via transnitrosation from organic nitroso compounds. Additional reactions known from animals, such as deacetylation or demethylation, have not been sufficiently studied in plants.

FIGURE 2

Increases in melatonin (A) and their consequences for protection and stress tolerance (B). Bold arrows: particularly strong accumulations of melatonin. Dotted arrows: secondary effects via antioxidative protection. ^∗Melatonin may be more strongly taken up than synthesized on-site. HSP, heat shock protein; LMW, low-molecular weight. Some actions may be species-specific or conditional.