Melatonin alleviates aluminum-induced growth inhibition by modulating carbon and nitrogen metabolism, and reestablishing redox homeostasis in Zea mays L.

https://doi.org/10.1016/j.jhazmat.2021.127159Get rights and content

Highlights

  • Melatonin decreases Al concentration in maize roots and leaves.

  • Melatonin application alleviates aluminum-induced growth inhibition in maize plants.

  • Exogenous supply of melatonin promotes higher steady-state levels of C and N metabolism.

  • Melatonin mitigates Al-induced oxidative stress by increasing antioxidant defence.

Abstract

Melatonin, a regulatory molecule, performs pleiotropic functions in plants, including aluminum (Al) stress mitigation. Here, we conducted transcriptomic and physiological analyses to identify metabolic processes associated with the alleviated Al-induced growth inhibition of the melatonin-treated (MT) maize (Zea mays L.) seedlings. Melatonin decreased Al concentration in maize roots and leaves under Al stress. Al stress reduced the total dry weight (DW) by 41.2% after 7 days of treatment. By contrast, the total DW was decreased by only 19.4% in MT plants. According to RNA-Seq, enzyme activity, and metabolite content data, MT plants exhibited a higher level of relatively stable carbon and nitrogen metabolism than non-treated (NT) plants. Under Al stress, MT plants showed higher photosynthetic rate and sucrose content by 29.9% and 20.5% than NT plants, respectively. Similarly, the nitrate reductase activity and protein content of MT plants were 34.0% and 15.0% higher than those of NT plants, respectively. Furthermore, exogenous supply of melatonin mitigated Al-induced oxidative stress. Overall, our results suggest that melatonin alleviates aluminum-induced growth inhibition through modulating carbon and nitrogen metabolism, and reestablishing redox homeostasis in maize.

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Introduction

Aluminum (Al) toxicity adversely impacts crop production in acid soils. As the soil pH drops below 5, toxic forms of Al become soluble into the soil solution, triggering various physiological and metabolic changes, such as the disruption of carbohydrate metabolism, degradation of proteins, and peroxidation of lipids, causing a inhibition of root growth and function and thus reducing crop yields (Maron et al., 2008, Dai et al., 2019). Given that as much as 30% of the world’s total lands are acidic, and approximately 50% of the world’s potentially arable land area consists of acid soils, Al toxicity is one of the most important limiting factors for global agricultural production (Shetty et al., 2021, Wang et al., 2015). Maize (Zea mays L.) is a major food crop in the tropics and subtropics, where acid soils are prevalent (Maron et al., 2013). Therefore, how to alleviate the Al-induced growth inhibition in maize is an urgent problem to be solved.

Melatonin is a pleiotropic regulatory molecule present in almost every living organism, ranging from prokaryotes to eukaryotes (Tan et al., 2012). Melatonin was first found in morning glory (Pharbitis nil) in 1993. Since then, many studies have been conducted on melatonin, revealing its positive role in plants (Wang et al., 2013b, Wang et al., 2013a). Evidence shows that melatonin mediates various physiological responses, including rooting, seed germination, photosynthesis, flowering, and aging (Back et al., 2016; Arnao et al., 2019; Wang et al., 2019). More importantly, endogenously induced or exogenously applied melatonin increases plant tolerance to numerous abiotic stresses, such as salt, drought, nutrient deficiency, heat, cold, heavy metal toxicity, and ultraviolet-B irradiation (Shi et al., 2014; Antoniou et al., 2017; Chen et al., 2018; Zhang et al., 2019). Melatonin increases heavy metal stress tolerance in plants mainly by improving the activities of antioxidant enzymes and vacuolar sequestration of toxic metals, and by modulating polyamine metabolism and phytochelatin biosynthesis (Hasan et al., 2015, Wang et al., 2019, Shah et al., 2020). Additionally, studies indicate that melatonin is linked to a feedback mechanism in plants that comprises different regulatory elements of the redox network, such as reactive oxygen species (ROS) and reactive nitrogen species (RNS), particularly through the action of H2O2 and nitric oxide (NO), respectively (Arnao and Hernández, Ruiz, 2019). Nevertheless, whether melatonin could mitigate the inhibitory effects of Al stress on maize growth and the underlying mechanism remain poorly unclear, and this is the focus of this study.

The maintenance of carbon (C) and nitrogen (N) assimilation is essential for improving stress tolerance and ensuring sink strength without yield penalties (Li et al., 2018). The interactions between C and N metabolism are important for plant growth and development, and intricate mechanisms operate in the plant for coordinating C assimilation with N metabolism (Masclaux-Daubresse et al., 2010). Carbohydrates produced via photosynthesis provide an energy source and basic C skeletons for a variety of biological processes, such as N assimilation. However, C fixation via photosynthesis is easily affected by external environmental factors, including N availability (Coruzzi and Zhou, 2001, Zhang et al., 2018). C and N metabolites regulate the activity of enzymes and transporters, which control C and N fluxes, thereby regulating the response of plants to environmental signals and changing source–sink relationships (Nunes-Nesi et al., 2010). Hence, the maintenance of higher steady-state levels of C and N assimilation is essential for improving plant growth and crop yield during Al stress conditions.

High-throughput transcriptome sequencing has been extensively applied to diverse plant species to analyze transcriptional changes in genes in response to Al stress, and numerous candidate genes (such as heavy metal transporter) or pathways (such as the glutathione and diterpenoid pathway), involved in the regulation of Al tolerance, have been identified (Singh et al., 2015, Liu et al., 2021). However, enzymes and transcription factors acting downstream of these genes and pathways also play essential roles in biological processes in higher plants. To adapt to abiotic stress environments, plants have evolved various sophisticated and effective strategies, such as gene expression reprogramming, epigenetic plasticity, physiological and metabolic reconstruction, and lipid remodeling (Zhu et al., 2018, Zenda et al., 2019). Thus, the combined transcriptomic and physiological analyses may enhance our understanding of the underlying mechanism by which melatonin alleviates the inhibitory effects of Al stress on maize growth.

Previous studies have focused on the roles of melatonin in reducing the Al concentration and in enhancing the antioxidant capacity (Sami et al., 2020, Sun et al., 2020). In contrast, the metabolic processes associated with the alleviated Al-induced growth inhibition of the melatonin-treated maize seedlings have not paid enough attention. Indeed, plant growth is a biomass accumulation process relying on the interplay between multiple metabolic pathways, mainly the interactions between C and N metabolism (Li et al., 2018; Erdal et al., 2019). Exogenous melatonin has been shown to alleviate the growth inhibition of wheat/rice under the heavy metal stress (Ni et al., 2018, Kaya et al., 2019, Bao et al., 2021). Additionally, the role of melatonin in improving plant photosynthetic efficiency has been confirmed under heavy metal stress conditions (Wang et al., 2019, Li et al., 2021). Here, we hypothesized that melatonin could mitigate the inhibitory effect of Al stress on C/N metabolism through decreasing the Al concentration in maize roots and leaves, and as a result could alleviate the growth inhibition. Photosynthetic activity, enzyme activities, metabolite contents, and gene expression levels were analyzed in maize plants under Al stress with or without melatonin supplementation. Moreover, the role of melatonin in mitigating oxidative stress in maize plants was also investigated.

Section snippets

Plant growth and Al and melatonin treatments

Seeds of maize (Zea mays L.) cultivar TY363 (Al sensitive) were disinfected with 1% sodium hypochlorite (v/v) for 10 min and then rinsed with distilled water. The sterilized seeds were placed on a wet filter paper and incubated at 25 °C for 3 days in the dark to induce germination. Seedlings were then transplanted into plastic containers containing 6 L full nutrient solution at pH 4.0 as previously described (Piñeros et al., 2002). 14-d-old maize seedlings were treated with 0 or 50 μM

Effects of melatonin application on Al concentration and plant growth in maize

Under Al stress, melatonin application decreased Al concentration in both maize roots and leaves (Fig. 1A and B). In the absence of Al, no significant difference was detected in total DW between melatonin-treated (MT) and non-treated (NT) maize plants. The total DW was reduced by 41.2% in NT plants at the end of the Al stress treatment. By contrast, the total DW was decreased by only 19.4% in MT plants (Fig. 1E). Similarly, MT plants showed higher total leaf area and root vigor than NT plants (

Discussion

In plants, excess Al3+ can interfere with many physiological and metabolic processes, leading to a reduction in crop productivity. Accordingly, reducing the accumulation of Al in plants is highly desirable and urgent to improve crop yield under Al stress (Dai et al., 2019, Shetty et al., 2021). Sun et al. (2020) confirmed that exogenous application of melatonin significantly decreasing the amount of cell wall polysaccharides, thereby enhancing aluminum exclusion and promoting wheat root growth.

Conclusions

Aluminum (Al) stress adversely affects plant physiological and biochemical processes, leading to a reduction in crop productivity. Melatonin has been extensively validated as a regulator of plant growth and development, as well as of Al stress responses. Under Al stress, MT plants maintained higher photosynthetic rate and SPS gene expression, and resulting in higher sucrose content, than NT plants. Increased carbon assimilation in MT plants was well correlated with higher NO3- level, NR

CRediT authorship contribution statement

J. Zhao, Z. Yang and J. Ren: conceived and designed the experiments. J. Ren, X. Yang, N. Zhang, C. Ma and Y. Wang: performed the experiments. J. Ren, X. Yang and L. Feng: analyzed the data. J. Zhao, Z. Yang and J. Ren: wrote the paper.

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgments

This work was supported by the “National Millet and Sorghum Industry Technical System” Project (CARS-06-13.5-A28), National Key Technology R&D Program of China (2015BAD23B04-2), Shanxi Agricultural Valley Construction Scientific Research Program (SXNGJSKYZX201704), Key Research and Development General Project in Shanxi Province (201603D221003-2), and the National Natural Science Foundation of China (31101113).

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