Response of phenolic metabolism to cadmium and phenanthrene and its influence on pollutant translocations in the mangrove plant Aegiceras corniculatum (L.) Blanco (Ac)

https://doi.org/10.1016/j.ecoenv.2017.03.041Get rights and content

Highlights

  • Response of mangrove phenolic metabolism to cadmium and phenanthrene was studied.

  • Contents of total phenols, tannins and lignin in leaves and roots were increased.

  • Accumulation of phenolic compounds decreased the pollutant translocation factor.

Abstract

Polyphenolic compounds are abundant in mangrove plants, playing a pivotal role in the detoxification of pollutants extruded from surrounding environments into plant tissues. The present study aimed to examine the variations of phenolic compounds, namely total polyphenolics, soluble tannins, condensed tannins and lignin, in the mangrove plant Aegiceras corniculatum (L.) due to the presence of exogenous cadmium and phenanthrene and to explore the influence of phenolic metabolism on biological translocation of these pollutants from roots to leaves. After a 6-week exposure to cadmium and phenanthrene, significant accumulations of both pollutants were observed. All determined phenolic compounds in both leaves and roots at high dosage levels were enhanced compared to the uncontaminated plant. Elevations of polyphenols in both treatments are possibly a result of stimulation in the activity of phenylalanine ammonia-lyase (PAL) and the enrichment of soluble sugar. Additionally, a significantly positive dosage relationship between polyphenolic metabolism intensity and phenanthrene contamination levels was found, while the trend observed in cadmium treatment was weak since cadmium at high levels inhibited phenolic production. The enrichment of polyphenols led to a decline in the biological translocation of these pollutants from roots to leaves. The immobilization of pollutants in the plant roots is possibly linked to the adsorption potential of polyphenols. These results will improve the understanding of the tolerance of mangrove plants to exogenous pollutants and will guide the selection of plants in phytoremediation because of the variability of polyphenol concentrations among species.

Introduction

Mangroves are shrubs or trees with a wide distribution along coasts and estuaries in tropical and sub-tropical regions, covering latitudes of 30°N to 37°S (Feller et al., 2010). Mangrove forests are highly productive; therefore they are one of the most important wetland ecosystems worldwide, providing a wide range of ecological and economic benefits to humans, such as a nursing ground for aquaculture, a source of herbs and protection of banks from erosion (Lee et al., 2014). However, due to intensive human activities in coastal belts, mangroves are subject to a large variety of anthropogenic contaminants, namely trace elements and persistent organic pollutants (Bayen, 2012). Mangrove plants have an extensive root system with a large biomass (Feller et al., 2010). This invasive sediment-root interface may result in a rapid transfer of pollutants from sediment matrix into mangrove tissues, which likely triggers inhibitions of germination, declines of photosynthesis, alterations of mineral nutrition and loss of water balance in plant cells (Kummerová and Kmentová, 2004, Hasan et al., 2009). These biological impacts possibly lead to shrinkage of mangrove coverage and therefore triggering replacement of the dominant species from mangroves to opportunity species, such as cordgrass, in mangrove ecosystems (Yu et al., 2015). Consequently, the biological response of mangrove plants to accumulations of anthropogenic pollutants has received much interest from the scientific community in recent years (Huang and Wang, 2010, Sodré et al., 2013, Zhang et al., 2014b, Jiang et al., 2016).

Plant phenolic compounds are important metabolites with complex structures and large molecular weights, usually ranging from 500 to 3000 Da (Wang et al., 2014), comprising simple phenols, coumarin, lignin, lignan, condensed and hydrolyzable tannins, and flavonoids (Khoddami et al., 2013). These are assumed to actively respond to ecological and physiological stresses, such as pathogen and insect attacks, UV radiation and wounding (Khoddami et al., 2013). Phenolic compounds also play an important role in the detoxification of pollutants extruded from surrounding environments into plant tissues. Specifically, studies revealed that the uptake of cadmium and nickel in plant roots can be significantly influenced by phenolic acids (Kováčik et al., 2011). In addition, as reviewed by Kraus et al. (2003), phenols can chelate toxic metal ions with hydroxyl and carboxyl groups and consequently influence the transfer of metals in plant tissues. In terms of their effects on organic pollutants, enzymes, such as lignin peroxidase and manganese peroxidase, involved in the metabolism of phenolic compounds are also assumed to actively participate in the degradation of organic pollutants (Chroma et al., 2002). The adsorption capability of phenols to organic pollutants (e.g., PAHs) via a π–π electron-donor–acceptor interaction may also influence the biological translocation and toxicity of organic contaminants in plants (Zhang et al., 2014a). Polyphenols are also well known for their antioxidant activity, which can be involved in the scavenging of hydrogen peroxides introduced by inorganic/organic pollutants in plant cells (Michalak, 2006, Wang et al., 2014).

In mangrove plants, total phenolic compounds may comprise as much as 5–40% dry weight in leaf and bark tissues (Wei et al., 2010, Wang et al., 2014). The majority of phenols in their tissues is hydrolysable and condensed tannins with a strong antioxidant activity and free radical scavenging potential (Wang et al., 2014), which is possibly linked to the uptake and biological translocation of anthropogenic pollutants in mangroves. Currently, the research literature with regard to systematic and comprehensive studies of the variations of total polyphenolic compounds in mangrove plants due to stresses of metals and organic pollutants are limited. To fill this knowledge gap, in the present study, the role of phenolic metabolism in mangrove plants against inorganic and organic contamination stresses was investigated. Aegiceras corniculatum (L.) Blanco (Ac) (hereafter A. corniculatum) was selected as the model plant in the current research because of (1) the wide distribution along coastal and estuarine areas in China (Chen et al., 2009), (2) the active production of polyphenols in mangrove tissues (Wang et al., 2014) and (3) a great tolerance to exogenous pollutants, especially metals (Li et al., 2013). Phenanthrene (Phe), a three-ring polycyclic aromatic hydrocarbon (PAH) compound, was applied as the contamination source of the organic pollutants and cadmium (Cd), a typical trace element in mangrove sediments, was used as the source of metals. The selection was based on the known toxic effects and frequency of occurrence in mangrove swamps. The research aimed to determine (1) dosage response of phenolic compounds and metabolisms to both pollutants and potential differences in response; and (2) the relationship between enrichments of phenols and the biological translocation of these pollutants in mangrove plants.

Section snippets

Exposure experiments

Undamaged propagules of A. corniculatum with intact testa were collected from the Caoputou Mangrove Reserve (24°29′N, 117°55′E), Jiulong River Estuary, Fujian Province, China. Afterwards, they were planted in rubber pots. Each pot contained three propagules. The propagules/seedlings were irrigated by Hoagland solution modified for mangrove growth (Xie et al., 2013). The salinity of the culture solution was adjusted by NaCl to 13 PSU (practical salinity units), which is similar with the

Cd and Phe in A. corniculatum

After the 6-week incubation, no phytotoxicity symptoms, such as dark spots or dehydration, were observed in leaves among all treatments while the mangrove roots had turned a slight yellow/brown color. By contrast, accumulations of Cd and Phe residues in A. corniculatum were observed (Fig. 1A and Fig. 1B). In the control group, the Cd content in leaves and roots (i.e., roots and iron plate) was 2.6 and 43.4 μg g−1 (mean concentration), respectively. In the Cd dosed plants, residue concentration of

Discussion

Mangrove plants are frequently in contact with metals and persistent organic pollutants derived from multiple input sources, such as surface loading, coastal groundwater discharge and precipitation (Bayen, 2012). As a direct result, accumulation of pollutants within mangrove plants is ubiquitous. In the control group, the presence of Cd and Phe in both leaves and roots was observed, though the plants were irrigated with the artificial nutrient solution. This may be due to the atmospheric

Conclusions

The response of phenol metabolism in A. corniculatum to Cd and Phe was studied. Significant enhancements in concentrations of polyphenolics, such as total phenols and condensed tannins were observed in the majority of dosed groups, which may result from promoted phenol production rate, as evidenced by increased PAL activity and soluble sugar content. In addition, high levels of treatments led to a significantly increased accumulation of lignin in roots, indicating that A. corniculatum roots

Acknowledgements

This work was kindly funded by National Natural Science Foundation of China (31530008), Ministry of Science and Technology of the People's Republic of China (2013CB956504) and National Natural Science Foundation of China (31370516). The authors would like to thank Mr Zengfeng Song, Ms Jing Huang, Dr Feng Xie, Dr Junyi Yu, and Dr Jingna Du for their great assistant in both field campaigns and laboratory analysis. Thanks are due to Prof. John Merefield at Exeter University and Dr Tara Kelly at

References (43)

  • D.E. Nixon et al.

    Routine clinical determination of lead, arsenic, cadmium, and thallium in urine and whole blood by inductively coupled plasma mass spectrometry

    Spectrochim. Acta Part B

    (1996)
  • L.J. Porter et al.

    The conversion of procyanidins and prodelphinidins to cyanidin and delphinidin

    Phytochemistry

    (1985)
  • A.A. Rahim et al.

    Mangrove tannins and their flavanoid monomers as alternative steel corrosion inhibitors in acidic medium

    Corros. Sci.

    (2007)
  • V. Sodré et al.

    Physiological aspects of mangrove (Laguncularia racemosa) grown in microcosms with oil-degrading bacteria and oil contaminated sediment

    Environ. Pollut.

    (2013)
  • F.Q. Zhang et al.

    Effect of heavy metal stress on antioxidative enzymes and lipid peroxidation in leaves and roots of two mangrove plant seedlings (Kandelia candel and Bruguiera gymnorrhiza)

    Chemosphere

    (2007)
  • G.J. Ahammed et al.

    Brassinosteroid regulates secondary metabolism in tomato towards enhanced tolerance to phenanthrene

    Biol. Plant.

    (2013)
  • S.A. Brown et al.

    Shikimic acid as a precursor in lignin biosynthesis

    Nature

    (1955)
  • L. Chen et al.

    Recent progresses in mangrove conservation, restoration and research in China

    J. Plant Ecol.

    (2009)
  • P.S. Chow et al.

    A method for routine measurements of total sugar and starch content in woody plant tissues

    Tree Physiol.

    (2004)
  • L. Chroma et al.

    Enzymes in plant metabolism of PCBs and PAHs

    Acta Biotechnol.

    (2002)
  • L.P. Dai et al.

    Cadmium induced changes in pigments, total phenolics, and phenylalanine ammonia lyase activity in fronds of Azolla imbricata

    Environ. Toxicol.

    (2006)
  • Cited by (38)

    View all citing articles on Scopus
    View full text