Elsevier

Scientia Horticulturae

Volume 181, 2 January 2015, Pages 18-25
Scientia Horticulturae

Sodic alkaline stress mitigation with exogenous melatonin involves reactive oxygen metabolism and ion homeostasis in tomato

https://doi.org/10.1016/j.scienta.2014.10.049Get rights and content

Highlights

  • Exogenous melatonin alleviated the inhibited growth of tomato by NaHCO3.

  • Exogenous melatonin decreased oxidative stress in tomato induced by NaHCO3.

  • Exogenous melatonin improved the AsA–GSH cycle of tomato under NaHCO3 stress.

  • Exogenous melatonin maintained the balance of Na+ and K+ in tomato leaves under NaHCO3 stress

Abstract

Melatonin, as an indoleamine molecule, is involved in multiple physiological processes in plants. In this study, the effects of exogenous melatonin on plant growth, reactive oxygen metabolism and ion homeostasis in alkaline-treated tomato seedlings were investigated. Alkaline stress caused much lower level in maximum photochemistry efficiency of PSII (Fv/Fm), chlorophyll content, the activity of antioxidant enzymes and biomass accumulation of tomato plants, accompanied by the reactive oxygen species (ROS) burst, lipid peroxidation and membrane damage. The exogenous melatonin could increase tomato plants tolerance to sodic alkaline stress, and the effect depended on the concentration. In the experiment, treatment with 0.5 μM melatonin showed the strongest powerful effect on promoting tomato plant growth under alkaline stress and reducing oxidative stress via inducing activities of antioxidant enzymes and accumulations of ascorbic acid (AsA) and glutathione (GSH), which could be partly responsible for protecting chlorophyll from degradation and keeping higher Fv/Fm. Furthermore, we found that melatonin treatment decreased Na+ content and increased K+ content in tomato leaves under alkaline stress, which showed the ion homeostasis maintenance by melatonin also played important role in enhancing tomato tolerance to alkaline stress

Introduction

Plants grow and reproduce in an intricate environment composed of a multitude of abiotic chemical and physical factors. Soil alkalinity, as an adverse environmental condition, has greatly limited plant growth and enormously reduced crop productivity globally. In the whole world, there are 434 million hectares of soils suffering from sodic alkaline accumulation (Jin et al., 2008). In those areas, alkalization of soil due to Na2CO3 or NaHCO3 may be the most serious problem. Sodic alkaline stress certifies as three main conditions injurious to plant growth and development: high soil pH, osmotic stress, ion-specific effects resulting from the excessive accumulation of sodium (Gong et al., 2014a). A high pH of rhizosphere directly causes Ca2+, Mg2+ and H2PO4 to precipitate, and may inhibit ion absorption as well as perturb the ion homeostasis in plants (Li et al., 2009). Osmotic stress results in water deficits, causing cell dehydration and the inhibition of cell expansion. And, the excessive accumulation of Na+ can cause K+ deficiency and other nutrient imbalances (Gong et al., 2014a).

Alkaline stress can also influence several physiological processes, from seed germination to plant development. Metabolic pathways are sensitive to hostile environments and metabolic imbalances can cause an oxidative stress in cells by boosting the generation and accumulation of reactive oxygen species (ROS) which will lead to oxidative damage to nucleic acids, proteins and lipids (Apel and Hirt, 2004). Furthermore, alkali stress can intensely reduce photosystem II efficiency and damage photosynthesis along with chlorophyll degradation. However, plants have utilized various physiological and biochemical mechanisms to battle with alkali stresses, including selective buildup, ion compartmentalization, alteration to the pathway of photosynthesis, the synthesis and accumulation of osmotic adjustment, stimulation of antioxidative enzymes (Suzuki et al., 2012). In the recent years, an increasing attention has been given to the research of the physiological mechanism and molecular basis of plant responses to sodic alkaline condition.

Tomato (Solanum lycopersicum L.) is the most considerable vegetable crop in the world, and is moderately sensitive to salt and alkaline stress. Its physiology mechanism of salt tolerance has been studied extensively; however, little research has focused on alkaline tolerance of tomato. Recently, Gong et al. (2013) compared the impacts of NaCl and NaHCO3 stress on photosynthetic parameters, the antioxidant system and nutrient metabolism in tomato leaves. They concluded that alkaline stress had more destructive effects on tomato relative to salt stress when both of them were the same concentration. So, the research on how to improve the alkalinity resistance of tomato has a great significance.

Melatonin (N-acetyl-5-methoxytryptamine), a well-known animal compound, is also a ubiquitous and highly conserved molecule in plants. Dubbels et al. (1995) and Hattori et al. (1995) first independently discovered melatonin in vascular plants. Later, melatonin has been detected in a lot of plants especially in aromatic plants, and there were more abundant in leaves than in seeds (Arnao, 2014). In the past several years, an increasing number of researches have been reported on the physiological functions of melatonin in plants. One of its most significant functions is acting as the first line of fight against internal and external oxidative stress (Tan et al., 2012). This indoleamine has many properties which make it a perfect antioxidant, for it can be regenerated after radical quenching (Galano et al., 2011) and that it is low-molecular-weight, lipophilic highly and hydrophilic partly. It is also a broad-spectrum scavenger and able to transport across various cell membranes easily (Venegas et al., 2012). As an antioxidative molecule, melatonin plays a significant role in scavenging free radicals, especially reactive oxygen and nitrogen species (ROS/RNS). In fact, plants are able to produce high levels of melatonin to defend against the massive oxidative stress (Arnao and Hernández-Ruiz, 2013a, Arnao and Hernández-Ruiz, 2013b). The detrimental environments can also induce the melatonin synthesis and increase endogenous melatonin level (Arnao and Hernández-Ruiz, 2009a, Arnao and Hernández-Ruiz, 2014, Zhang et al., 2014).

As a hormone, melatonin also participates in many physiological processes in plants, such as flowering (Kolář et al., 2003), lateral root generation (Arnao and Hernández-Ruiz, 2007, Zhang et al., 2012) and seed germination (Posmyk et al., 2009). Exogenous melatonin application affected the early stages of photoperiodic flower induction in the short-day plant Chenopodium rubrum (Kolář et al., 2003). Similar to indole-3-acetic acid, melatonin was shown as root promoter according to Arnao and Hernández-Ruiz (2007). Exposure to chilling stress, applying melatonin significantly enhanced the germination of cucumber seeds (Posmyk et al., 2009).

Increasing number of reports showed the capacity of melatonin to relief the effects of detrimental environmental conditions, including drought (Zhang et al., 2012), cold (Bajwa et al., 2014), high temperature (Zhao et al., 2013) and salinity stress (Li et al., 2012). Exogenous melatonin can also delay the senescence of plant leaves (Arnao and Hernández-Ruiz, 2009b). Its alleviating effects seemed to relying on the following factors: inhibiting the degradation of chlorophyll, improving the capacity of photosynthesis, enhancing the activities of antioxidant enzymes, directly scavenging free radical and regulating the AsA–GSH cycle.

So far, the role of melatonin in alkali stress has not been reported. The purposes of the present study were to determine if melatonin has the protective role in tomato under alkali stress and to define its possible physiological mechanism of alkalinity resistance in tomato plants.

Section snippets

Plant materials and treatments

Tomato seeds were surface-sterilized in 2.5% NaClO, washed with distilled water, soaked for 8 h at 28 °C and then germinated on moisture filter paper in the dark at 28 °C. Seeds were sown in vermiculite. Seedlings with three true leaves, were transplanted into plastic container filled with 5 L of half-strength Hoagland nutrient solution: 2 mM Ca(NO3)3, 3 mM KNO3, 1 mM MgSO4, 0.5 mM NH4H2PO4, 40 μM Fe-EDTA, 23.3 μM H3BO3, 4.75 μM MnSO4, 0.4 μM ZnSO4, 0.15 μM CuSO4 and 0.01 μM (NH4)6Mo7O24. Plants were

Melatonin-induced tomato tolerance to NaHCO3 stress

After 10 days of treatment, the growth of tomato seedlings was significantly reduced by NaHCO3 stress (Fig. 1A) (P < 0.05). The addition of 0.25–0.75 μM melatonin noticeably mitigated this detrimental response, especially in the treatment of 0.5 μM melatonin application. Apparent leaf wilting was observed under NaHCO3 stress, and the wilting was obviously decreased by application of melatonin. The pseudocolored Fv/Fm images and values showed NaHCO3 stress imposed significantly negative effects on

Discussion

The mitigation of NaCl stress on plant by exogenous substances has been widely investigated, in fact, compared to 397 million hectares of neutral saline soil, 434 million hectares of soils were affected by sodic salinity in the world (Jin et al., 2008). In our previous study, it was found that NaHCO3 (sodic alkaline salt) stress showed more obviously inhibited effects on tomato plant growth than NaCl (neutral salt) stress (Gong et al., 2013), and among a total of 313 proteins in tomato roots

Conclusions

In our knowledge, this is the first research to investigate the influence of exogenous melatonin on tomato seedlings tolerance to sodic alkaline. Here, application of 0.5 μM melatonin showed a marked mitigation of alkalinity-treated inhibition of plant growth, and a slowed decline in chlorophyll contents and the maximum photochemistry efficiency of PSII (Fv/Fm). The application of this compound also alleviated lipid peroxidation and reduced oxidative damage in tomato seedlings under alkaline

Acknowledgments

This work was supported by the National Natural Science Foundation of China (No. 31372059), the China Agriculture Research System (CARS-25-D) and Shandong Agriculture Research System (SDAIT-02-022-08).

References (47)

  • J.K. Zhu

    Regulation of ion homeostasis under salt stress

    Curr. Opin. Plant Biol.

    (2003)
  • G.M. Abogadallah

    Antioxidative defense under salt stress

    Plant Signal. Behav.

    (2010)
  • K. Apel et al.

    Reactive oxygen species: metabolism, oxidative stress, and signal transduction

    Annu. Rev. Plant Biol.

    (2004)
  • M.B. Arnao et al.

    Melatonin promotes adventitious- and lateral root regeneration in etiolated hypocotyls of Lupinus albus L

    J. Pineal Res.

    (2007)
  • M.B. Arnao et al.

    Chemical stress by different agents affects the melatonin content of barley roots

    J. Pineal Res.

    (2009)
  • M.B. Arnao et al.

    Protective effect of melatonin against chlorophyll degradation during the senescence of barley leaves

    J. Pineal Res.

    (2009)
  • M.B. Arnao et al.

    Growth conditions determine different melatonin levels in Lupinus albus L

    J. Pineal Res.

    (2013)
  • M.B. Arnao et al.

    Melatonin: plant growth regulator and/or biostimulator during stress?

    Trends Plant Sci.

    (2014)
  • M.B. Arnao

    Phytomelatonin: discovery, content, and role in plants

    Adv. Bot.

    (2014)
  • V.S. Bajwa et al.

    Role of melatonin in alleviating cold stress in a Arabidopsis thaliana

    J. Pineal Res.

    (2014)
  • R. Dubbels et al.

    Melatonin in edible plants identified by radioimmunoassay and by high performance liquid chromatography–mass spectrometry

    J. Pineal Res.

    (1995)
  • C.H. Foyer et al.

    The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism

    Planta

    (1976)
  • A. Galano et al.

    Melatonin as a natural ally against oxidative stress: a physicochemical examination

    J. Pineal Res.

    (2011)
  • Cited by (104)

    • Heterologous overexpression of HIOMT alleviates alkaline stress in apple plants by increasing melatonin concentration

      2023, Scientia Horticulturae
      Citation Excerpt :

      Spraying of melatonin on apple leaves under long-term drought stress could improve the efficiency of leaf light energy conversion and carbon assimilation (Wang et al., 2013). Similarly, exogenous addition of 0.5 µmol·L−1 melatonin can significantly increase the biomass of tomato seedlings under alkaline salt stress, protect the photosynthetic mechanism (Liu et al., 2015). The main regulatory mechanism is that melatonin increases CO2 availability by protecting chloroplast integrity, and in the Calvin cycle, melatonin can regulate the expression of Rubisco element and other enzymes. (

    View all citing articles on Scopus
    View full text