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

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.

SUBMITTER: Hu Z

PROVIDER: S-EPMC7261800 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Jasmonate is an essential phytohormone involved in plant development and stress responses. Jasmonate perception occurs through the COI nuclear receptor allowing to target the JAZs repressors for degradation by the 26S proteasome. Consequently, repressed transcription factors are released and expression of JA-responsive genes is induced. In rice, three OsCOI genes have been identified, OsCOI1a and the closely related OsCOI1b homolog, and OsCOI2. While a role for OsCOI-1a and -1b genes was previously established in plant defense or leaf senescence, evidence for an important role of OsCOI2 in plant development, jasmonate-signaling and defence emerged only recently. To decipher the role of OsCOI2 in regulating jasmonate responses, we used rice mutant lines, edited both in the OsCOI1a and OsCOI1b genes, or in the OsCOI2 gene. Rice roots from WT and oscoi lines were treated by jasmonate to establish the molecular responses of each line, at the transcriptomic and metabolomic levels. RNA-seq data indicate that OsCOI2 is the main actor of the large transcriptional reprogramming observed after a JA challenge in rice roots. A series of transcription factors with an OsCOI2-dependent expression was identified, including transcription factors known to have a role in root development or stress response. An OsCOI2-dependent expression was detected for genes involved in specific processes or pathways such as photosynthesis, cell-growth and secondary metabolite biosynthesis (phenylpropanoids and diterpene phytoalexins). Functional redundancy between OsCOI1a/b and OsCOI2 can be shown for some genes, even if a lower response usually occurred in oscoi2 plants compared to oscoi1ab plants. Metabolic data revealed a shift from the primary metabolism to the secondary metabolism that is mainly OsCOI2-dependent. Differential accumulation of oryzalexins was also observed in oscoi lines.These data validate the major role of OsCOI2 in JA responses in rice roots. OsCOI2 is the major regulator of specialized metabolic pathways related to development and production of secondary metabolites. This study suggests that OsCOI2 controls the growth-defense trade-off in response to JA.

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

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