Review
Functional biology of halophytes in the phytoremediation of heavy metal contaminated soils

https://doi.org/10.1016/j.envexpbot.2014.11.010Get rights and content

Highlights

  • Halophytes are important plants for both saline agriculture and phytoremediation.

  • Halophyte adaptive mechanisms may confer tolerance to ions beyond sodium and chloride.

  • Further research should explore the relationship salt/metal tolerance in these species.

Abstract

Halophytic plants are characterized by their ability to survive, even thrive, at concentrations of sodium and chloride ions that would be toxic to most crop species. Given the diminishing prospects for the availability of fresh water for agriculture, halophytes represent an important resource for both our understanding of the fundamental physiological mechanisms in salt stress adaptation and utilization of saline waters for agriculture. Mechanisms of adaptation that allow halophytes to survive high salt concentrations may be not exclusive to sodium and chloride and may confer tolerance to other toxic ions, including the loosely defined family of heavy metals. It has been recently shown that a number of these halophytes do indeed have ability to accumulate heavy metals or tolerate high levels of toxic ions in the environment. These abilities make some halophytes excellent candidates for phytoextraction and phytostabilization of heavy metals in contaminated soils. This review addresses the general deleterious effects of heavy metals in plants, present known mechanisms of adaptation to heavy metal stress in halophytes and discusses the potential of halophytes for phytoremediation of contaminated soils. Considering the multifaceted potential of halophytes for biomass production in marginal and/or extreme environments, their potential role in the broader context of agriculture and food security should be further explored.

Introduction

Halophytic plants represent a tremendous resource in biology to study the mechanisms of adaptation and evolution to/in hyperosmotic environments. Halophytes have evolved to adapt to harsh conditions such as high salinity, xerothermic environments, and cold seasonal temperatures (Flowers et al., 2010) and they typically tolerate the presence of toxic ions, mainly in the form of sodium and chloride (Flowers and Colmer, 2008). Sensitivity and tolerance can vary greatly within a single genus where optimal concentrations for growth and development may range from 20 to 500 mM (Cheeseman, 2013). Significant advances have been made in understanding how halophytes have adapted to high salinity (Flowers et al., 2010, Bressan et al., 2013). Moreover, halophytes have received particular attention in past few years not just as model species in salt tolerance research, but as potential forage, fibre, and biomass crops as well as platforms for developing crop systems that use saline water and/or ameliorate salinized soils (Abdelly et al., 2006, Fedoroff et al., 2010, Shabala, 2013). It is estimated that 20% of all agricultural land and 50% of cropland throughout the world is salt affected (Flowers and Yeo, 1995, Shabala, 2012). In addition, as water availability for agricultural uses becomes limited, utilization of semi-saline and saline waters becomes an alternative source of water but soil salinization remains a potential risk (Letey et al., 2011). The application of halophytes that bioaccumulate Na+ and Cl presents a means of reducing salt content in soil where leaching and mechanical extraction is not economical (Qadir et al., 2003, Qadir et al., 2005). Sodium bioaccumulating species can be grown on saline soils and harvested on a regular basis. Addition of water and fertilizer can accelerate the bioremediation process (Keiffer and Ungar, 2002). Several studies on the use of halophytes in soil desalination have been reported in the literature. The obligate halophyte, Sesuvium portulacastrum L., for example, proved successful in desalinating soils with the potential to remove up to 1 t Na+ ha−1 through sequestration in roots and shoots (Rabhi et al., 2008, Rabhi et al., 2010). Also Suaeda maritima and S. portulacastrum have been shown to bioaccumulate salts in their tissues and reduce soil salinity (Ravindran et al., 2007, Rabhi et al., 2009). Similarly, the halophyte Sulla carnosa Desf. demonstrated the ability to desalinize soils moderately, 0.3 t Na+ ha−1, and showed potential as a forage crop (Jlassi et al., 2013). Deep rooted halophytes like Atriplex lentiformis have been used to absorb salt from mildly saline effluent from waste-water treatment facilities with the intent to protect aquifers in urban environments (Glenn et al., 2009).

Despite these and further examples on the practical use of halophytes to recover salinized soils/waters, their ability to withstand other adverse conditions and/or adapt to agriculture-unfavourable or extreme environments at large has been extensively explored. In some cases, halophyte adaptive mechanisms confer tolerance to other ions beyond sodium and chloride. Evidence suggests that the evolutionary adaptations present in halophytes can also confer tolerance to other toxic elements (Flowers et al., 2010). Therefore, the enormous potential halophytes present to plant biology and agriculture is not just limited to salt tolerance. As momentum builds within the research community studying halophytes and salt tolerance, understanding how these species interact with other abiotic stresses will become more important (Huchzermeyer and Flowers, 2013, Wang et al., 2014). Many of the physiological and molecular mechanisms that contribute to salt tolerance in halophytes, including the ability to limit entry of ions into the transpiration stream, ions compartmentalization, synthesis of organic solutes (Flowers and Colmer, 2008, Manousaki and Kalogerakis, 2011) and a robust antioxidative system (Freeman et al., 2006) are also found in heavy metal tolerant species. Therefore, it has been proposed that heavy metal plants and halophytes share a number of processes in common (Shevyakova et al., 2003).

In this review we summarize the main features of halophytic plants in relationship to their potential in phytoremediation of heavy metals contaminated soils. Although we have predominantly focused on the dual tolerance of halophytes to NaCl and heavy metals and possible interactions between underlying physiological and molecular mechanisms, we also refer to glycophytes when necessary, since for this group of plants heavy metals tolerance has been better documented. In the very last section of this review, we attempted to contextualize the role of halophytes in three important agricultural systems to demonstrate that further research on halophytes could ultimately contribute to recover contaminated soils, improve food security and decrease competition for arable land.

Section snippets

Heavy metals accumulation in plants and their environment

Heavy metals represent a significant environmental pollutant and can have serious effects on soil and water quality, plant and animal nutrition, as well as human health (Schwarzenbach et al., 2010, Jomova and Valko, 2011, Alloway, 2013). The generic term of “heavy metals” refers to elements that demonstrate metallic properties (transition metals, metalloids, lanthanides, and actinides), have a high specific gravity, 5.0 or greater, and are toxic, even at low concentrations. The definition of

Specificities of some halophytes

In recent years significant progress in understanding the links between NaCl and heavy metal responses has been made with species in the Poaceae family. The genus Spartina includes C4 perennial grasses often found in coastal area or inland salt marshes. Redondo-Gómez, (2013) reviewed a number of these species and their ability to tolerate and accumulate heavy metals. Spartina argentinensis, S. densiflora, S. maritima all have been shown to accumulate heavy metals. In particular, S. densiflora

Concluding remarks and a look forward

Although a number of plants are currently being considered for use in the phytoextraction of heavy metals from contaminated soils (Table 1), several unsolved issues remain. For phytoextraction to be a viable solution, plants need to possess the ability to uptake specific ions and accumulate them at high concentrations while not suffering deleterious effects due to their toxicity. Moreover, as the goal of phytoextraction is to remove a contaminant from the environment, hyperaccumulators must be

Acknowledgements

This work was supported by Italian “Ministero dell'Istruzione, dell'Università e della Ricerca” through the PON Research and Competivity 2007–2013 (ENERBIOCHEM- PON01_01966).

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