2-Hydroxymelatonin, Rather Than Melatonin, Is Responsible for RBOH-Dependent Reactive Oxygen Species Production Leading to Premature Senescence in Plants.

Hyoung Yool Lee,Kyoungwhan Back

doi:10.3390/antiox10111728

Abstract

Unlike animals, plants amply convert melatonin into 2-hydroxymelatonin (2-OHM) and cyclic 3-hydroxymelatonin (3-OHM) through the action of melatonin 2-hydroxylase (M2H) and melatonin 3-hydroxylase (M3H), respectively. Thus, the effects of exogenous melatonin treatment in plants may be caused by melatonin, 2-OHM, or 3-OHM, or some combination of these compounds. Indeed, studies of melatonin’s effects on reactive oxygen species (ROS) production have reported conflicting results. In this study, we demonstrated that 2-OHM treatment induced ROS production, whereas melatonin did not. ROS production from 2-OHM treatment occurred in old arabidopsis leaves in darkness, consistent with an ethylene-mediated senescence mechanism. Transgenic tobacco plants containing overexpressed rice M2H exhibited dwarfism and leaf necrosis of the upper leaves and early senescence of the lower leaves. We also demonstrated that 2-OHM-mediated ROS production is respiratory burst NADPH oxidase (RBOH)-dependent and that 2-OHM-induced senescence genes require ethylene and the abscisic acid (ABA) signaling pathway in arabidopsis. In contrast to melatonin, 2-OHM treatment induced senescence symptoms such as leaf chlorosis and increased ion leakage in arabidopsis. Senescence induction is known to begin with decreased levels of proteins involved in chloroplast maintenance, including Lhcb1 and ClpR1. Together, these results show that 2-OHM acts as a senescence-inducing factor by inducing ROS production in plants.

Highlights

In plants, melatonin is a multifunctional molecule that displays a diverse set of physiological functions in plant growth and development ranging from seed germination to seed longevity and post-harvest preservation [1,2,3,4]
From 14 independent T1 transgenic tobacco plants, we further selected three homozygous tobacco plants. These T2 tobacco transgenic plants were grown to maturity (12 weeks) and showed a retarded growth phenotype compared to the wild type (WT) (Figure 1A)
2-OHM accept the mitogen-activated protein kinase (MPK) pathway as an integrated mediator to activate their own distinctive signaling. These findings suggest that the reactive oxygen species (ROS) RBOHD/F acts upstream of MPK3/6 signaling when arabidopsis leaves are exogenously treated with 2-OHM

Summary

Introduction

Melatonin is a multifunctional molecule that displays a diverse set of physiological functions in plant growth and development ranging from seed germination to seed longevity and post-harvest preservation [1,2,3,4]. The mechanisms by which melatonin plays these physiological roles are closely dependent on its intrinsic antioxidant activity and its function as a signaling molecule in association with its receptor and downstream signaling cascades [7,8]. In both animals and plants, melatonin is synthesized from tryptophan in a process requiring four enzymes [9]. In contrast to conserved melatonin biosynthesis, melatonin catabolism differs greatly between animals and plants, mainly in that it is almost an end product in animals, but a precursor for further metabolites in plants These melatonin metabolites are 2-hydroxymelatonin (2-OHM) and cyclic 3-hydroxymelatonin (3-OHM), both are produced nonenzymatically in animals as degradation products [11]

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Discussion

Conclusion