Transcriptomic and metabolomic analyses reveal that melatonin promotes melon root development under copper stress by inhibiting jasmonic acid biosynthesis

Zhicheng Hu,Jing Zheng,Qiushi Fu,Aiai Zhang,Huaisong Wang

doi:10.1038/s41438-020-0293-5

Abstract

Melatonin has been shown to alleviate the effects of abiotic stress and to regulate plant development. Copper, a common heavy metal and soil pollutant, can suppress plant growth and development. In this work, we explored the protective effects of exogenous melatonin on lateral root formation in response to copper stress using melon seeds subjected to three germination treatments: CK1 (control), CK2 (300 μmol/L CuSO4), and MT3 (300 μmol/L melatonin + 300 μmol/L CuSO4). Melatonin pretreatment increased the antioxidant enzyme activities and root vigor, and decreased the proline and malondialdehyde (MDA) contents in the roots of copper-stressed melon seedlings. We then used transcriptomic and metabolomic analyses to explore the mechanisms by which exogenous melatonin protects against copper stress. There were 70 significant differentially expressed genes (DEGs) (28 upregulated, 42 downregulated) and 318 significantly differentially expressed metabolites (DEMs) (168 upregulated, 150 downregulated) between the MT3 and CK2 treatments. Melatonin pretreatment altered the expression of genes related to redox and cell wall formation processes. In addition, we found that members of the AP2/ERF, BBR/BPC, GRAS, and HD-ZIP transcription factor families may have vital roles in lateral root development. Melatonin also increased the level of Glutathione (GSH), which chelates excess Cu2+. The combined transcriptomic and metabolomic analysis revealed DEGs and DEMs involved in jasmonic acid (JA) biosynthesis, including four lipoxygenase-related genes and two metabolites (linoleic acid and lecithin) related to melatonin’s alleviation effect on copper toxicity. This research elucidated the molecular mechanisms of melatonin’s protective effects in copper-stressed melon.

Highlights

Melatonin (N-acetyl-5-methoxytryptamine) is an indoleamine ubiquitous in the plant kingdom[1], and a modulator of multiple developmental processes and stresses[2,3]
Shi et al.[30] found that exogenous melatonin improved the resistance of bermudagrass to drought, salt, and cold stress by enhancing antioxidative enzyme activities (i.e., POD, superoxide dismutase (SOD), and CAT) and alleviating the reactive oxygen species burst
And 2, copper toxicity decreased CAT, SOD, and POD activities; increased the MDA content; and inhibited lateral root development. These results indicated that copper harmed melon root systems

Summary

Introduction

Melatonin (N-acetyl-5-methoxytryptamine) is an indoleamine ubiquitous in the plant kingdom[1], and a modulator of multiple developmental processes and stresses[2,3]. Various types of research have demonstrated that melatonin can alleviate the effects of biotic and abiotic stresses, such as fungal, salt, and heavy metal stresses[4,5,6]. In copper-stressed Arabidopsis thaliana, root and shoot lengths and chlorophyll content levels decreased, whereas the anthocyanin content increased[11]. High copper concentrations inhibited root and stem growth in Arabidopsis and reduced cell elongation, division, and expansion[12]. Some research has suggested that the application of exogenous melatonin was able to protect plants from copper stress toxicity

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