Salinity alleviates the arsenic toxicity in the facultative halophyte Salvadora persica L. by the modulations of physiological, biochemical, and ROS scavenging attributes

https://doi.org/10.1016/j.jhazmat.2020.123368Get rights and content

Highlights

  • Halophyte S. persica is an As-hyperaccumulator and can withstand high salinity and arsenic.

  • The salinity tolerance index was > 99 and As tolerance index was > 70 in S. persica.

  • In-built As-salinity cross tolerance mechanisms confer tolerance to metal toxicity in S. persica.

  • Higher root phytochelatin suggest higher vacuolar sequestration of arsenic in root.

  • Modulations of ROS-scavenging attributes safeguard the plant from As-induced oxidative stress.

Abstract

Heavy metal(loid)s contamination in soil is a major environmental concern that limits agricultural yield and threatens human health worldwide. Arsenic (As) is the most toxic non-essential metalloid found in soil which comes from various natural as well as human activities. S. persica is a facultative halophyte found abundantly in dry, semiarid and saline areas. In the present study, growth, mineral nutrient homeostasis, MDA content, phytochelatin levels, and ROS-scavenging attributes were examined in S. persica imposed to solitary treatments of salinity (250 mM and 750 mM NaCl), solitary treatments of arsenic (200 μM and 600 μM As), and combined treatments of As with 250 mM NaCl with an aim to elucidate salinity and As tolerance mechanisms. The results demonstrated that S. persica plants sustained under high levels of As (600 μM As) as well as NaCl (750 mM). The activity of superoxide dismutase, catalase, peroxidase, and glutathione reductase were either elevated or unaffected under salt or As stress. However, ascorbate peroxidase activity declined under both solitary and combination of As with NaCl. Furthermore, the cellular redox status measured in terms of reduced ascorbate/dehydroascorbate, and reduced glutathione/oxidized glutathione ratios also either increased or remained unaffected in seedlings treated with both solitary and combined treatments of As + NaCl. Significant accumulation of various oxidative stress indicators (H2O2 and O2radical dot) were observed under high As stress condition. However, presence of salt with high As significantly reduced the levels of ROS. Furthermore, exogenous salt improved As tolerance index (Ti) under high As stress condition. The values of translocation factor (Tf) and As bioaccumulation factor (BF) were >1 in all the treatments. From this study, it can be concluded that the facultative halophyte S. persica is a potential As accumulator and may find application for phytoextraction of arsenic-contaminated saline soil.

Introduction

Rapid urbanization and industrialization have lead to the widespread contamination of heavy metal(loid) with incessant adding of organic as well as inorganic wastes in the environment. Metalloids are elements with physico-chemical properties that are intermediate between those of metals and nonmetals, and they are also known as semimetals. The commonly recognized metalloids include boron, arsenic, silicon, selenium, tellurium, germanium and antimony. Among them boron, silicon, and selenium are essential to plant and required in minor amounts whereas, arsenic, germanium, tellurium and antimony are non-essential to the plants even at minute concentrations (Gene et al., 2019). From the soil, heavy metal(loid)s are transferred to various parts of the plant and through biomagnification, directly or indirectly involved in the food chain. Heavy metal(loid)s pollution in the soil due to various natural and anthropogenic activities pose a critical global threat to the human health. Heavy metal(loid)s influence the physiology of plants in a multiple-way by limiting seed germination, growth, and ultimately the yield (Guala et al., 2010). Moreover, they can reduce the uptake of essential nutrients and affect several metabolic processes in different cell organelles. Heavy metal(loid)s limit the process of photosynthesis by disturbing the structure and permeability of the chloroplast membrane, interrupting electron transfer chain of photosystem II (PSII), and reducing the biosynthesis of chlorophyll (Qadir et al., 2004). Alteration in mineral status induced by the heavy metal contamination causes toxicity in plants. In addition, heavy metals also affect the plant water status and induce oxidative stress (Sghaier et al., 2015). Among the heavy metal(loid)s, arsenic (As) is a highly toxic metalloid found in soil which comes from various natural as well as human processes like smelting, mining, and use of As-containing herbicides, pesticides, paints, dyes, soaps, and drugs (Zhao et al., 2010). The inorganic arsenic usually found as As(V), As(III), As(0) and As(-III) in the environment (Jang et al., 2016). Among them As (V) and As (III) are predominantly transported by the plants via various phosphate transporters and aquaporin NIPs channels respectively and are known to interfere with several metabolic processes in plants. Moreover, As(V) is an analogue of inorganic phosphate (Pi) and this analogue nature of As(V) known to alter the Pi metabolism in plants (Fitz and Wenzel, 2002). Exposure of the plants to arsenic stress causes decrease in net photosynthesis rate (PN), degradation of chlorophyll, disintegration of membrane structure, reduce fresh and dry biomass accumulation and yield, production of ROS, and lipid peroxidation (Panda et al., 2017). Apart from this, arsenic can directly react with the thiol group of enzymes and interferes various metabolic reactions. Being phosphate analogue, arsenic hampers various vital cellular processes like electron transport chain and ATP synthesis (Tripathi et al., 2007). Plants evolved different mechanisms to battle the deleterious effects of As. One of the strategy is synthesis of phytochelatins which are heavy metal binding cysteine-rich peptide for detoxification of arsenic. PCs are produced from GSH by phytochelatin synthase (Vromman et al., 2016). The synthesis of PCs depends on the heavy metal’s occurrence in plants because the synthesizing enzyme requires metal as a cofactor for their activity. Since, As(V) has no affinity for sulfhydryl group of PCs, As(III) binds with PCs and/or glutathione and facilitate the vacuolar sequestration of As-PCs complex through ATP binding cassette (ABC) transporter (Panda et al., 2017). In this way, plant reduces free arsenic concentration in the cytoplasm as well as the arsenic toxicity. High salinity deleteriously affects plant growth and decrease crop production worldwide. Salinity has negative influences on plants in many ways such as reduction in water uptake due to increased osmotic pressure, accumulation of toxic ions like Na+ and Cl, mineral deficiency, reduced photosynthesis, and generation of osmotic stress (Rangani et al., 2016). However, to protect from salinity stress plants have developed several physiological and biochemical mechanisms like control of water flux, compartmentalization of ions, biosynthesis of organic osmolytes, and activation of various antioxidants (Ahanger et al., 2020). The antioxidant system and several metabolites in plants play vital roles in adaptation under stress conditions. Salinity and arsenic induced oxidative damage to the plants trigger the generation of ROS, leading to the peroxidation of membrane lipid, and degradation of nucleic acids, proteins, enzymes and chloroplastic pigments (Bankaji et al., 2016; Ahmad et al., 2020). Plants have antioxidant defense mechanisms to survive against stress-induced oxidative damage, which neutralize, remove, and scavenge the stress-induced ROS. The antioxidant system includes some key enzymes like SOD, CAT, APX, GR, DHAR, MDHAR, and GPX and non-enzymatic antioxidants such as ascorbate, glutathione, carotenoids, and α-tocopherol which also detoxify ROS (Verma and Dubey, 2003; Panda et al., 2017; Kaya et al., 2020).

Salvadora persica L. is a facultative halophyte that grows in dry and semiarid regions from western India to Middle East and high saline lands along the coasts (Phulwaria et al., 2011). S. persica mainly grows as natural vegetation on saline soil and greatly adapted from sand dunes to heavy soil, dry region to marshy and waterlogged area, and non-saline to highly saline soil (Reddy et al., 2008). This species can tolerate frequent inundation by seawater and survive in intertidal and above tidal regions (Phulwaria et al., 2011). In harsh saline and desert condition, this species supports the wildlife and are important parts of the ecosystem. Contamination of arsenic is widespread in coastal areas of tropical littoral countries in Asia particularly India (coastal areas of Gujarat and West Bengal) due to the continuous release of industrial effluents, sewage discharge, and agriculture runoffs through the rivers into sea. The impacts of combine stress of salinity and heavy metals like Cd, Pb, Zn and Cu on growth, photosynthesis and antioxidant defense potential of the halophyte have been extensively studied in some halophytes (Manousaki and Kalogerakis (2009); Han et al., 2013; Mariem et al., 2014; Manousaki et al., 2014; Bankaji et al., 2015, 2016; Lutts et al., 2016). However, there are scanty reports demonstrating cross tolerance mechanisms of arsenic with salinity in some halophytes like Atriplex atacamensis (Vromman et al., 2016), Suaeda maritima (Panda et al., 2017), Tamarix gallica (Sghaier et al., 2015). Moreover, in these studies maximum salinity level reported in the halophytic species are up to 200 mM. In the present study, we have reported the salinity and arsenic cross tolerance mechanism in a high salt tolerant xero-halophyte S. persica that tolerate salinity level up to 750 mM NaCl by a comprehensive study including growth, nutrient homeostasis, osmotic adjustment, phytochelatin levels, antioxidative defense components, and phytoremediation potential. The growth, physiology, antioxidative responses, and metabolomic changes in response to salinity and drought have been reported earlier in S. persica by our group (Rangani et al., 2016; Kumari and Parida, 2018; Rangani et al., 2018). Being a salt and drought tolerant species, we assume that S. persica can grow in As contaminated area and can be a potential candidate for the phytoremediation of As. Thus far no significant attempt has been made to study the As tolerance mechanism of S. persica and role of NaCl in alleviating arsenic toxicity for exploring the phytoremediation potential of S. persica. In the present study, growth, ion homeostasis, levels of organic osmolytes, and ROS scavenging attributes were examined in S. persica exposed to single or combined stress of As and salt to assess the As tolerance mechanisms and phytoremediation potential of this halophyte.

Section snippets

Plant material and treatments

The seeds of Salvadora persica L. were obtained from the experimental salt farm area, CSMCRI, Bhavnagar, Gujarat, India. Seed disinfection and germination were carried out as previously described (Rangani et al., 2018). After germination, two months old seedlings were acclimatized for 14 d under hydroponic culture condition in Hoagland’s nutrient medium in a culture room (14 h d−1 photoperiod, 500 μmol m−2 s−2 photosynthetic active radiation, and 25 ± 2 °C). Thereafter, treatments of salinity

S. persica is capable to manage high salinity and As in external medium by maintaining plant water status

The seedlings of S. persica exposed to salt, arsenic and combine treatment of both did not show any morphologically visible phytotoxic symptoms like chlorosis and necrosis (Fig.1). Alterations in growth of S. persica under arsenic and salinity treatments were examined by measuring fresh and dry biomass of leaf, stem and root, shoot and root length, and leaf area of seedlings (Fig. 2, A–J). In S. persica, there was a significant increase in leaf DW (+32 %), stem DW (+42 %), shoot length (+34 %),

Arsenic and salinity cross tolerance of Salvadora persica by maintaining water status, ion homeostasis, osmotic balance, and restriction of As translocation to shoot

The halophytic plant species have adaptation mechanisms for salinity that allow them to survive under high salinity and other toxic ions including heavy metal(loid)s. This ability of halophytes makes them suitable applicants for phytoextraction and phytostabilization of heavy metal(loid)s polluted saline soil. In the present study, the facultative halophyte S. persica can cope up with high salinity and arsenic. It can survive and grow optimally under high salinity (up to 750 mM NaCl) and high

Conclusion

Taken together the results of this study, it can be concluded that the halophyte S. persica is able to survive under high As concentration and considered as an arsenic hyperaccumulator. It can efficiently survive and optimally grow under high salt, As, and combined treatment of salt and As. The external salinity reduces the uptake of As by the root tissue and improve the tolerance capacity of S. persica to resist the As toxicity which indicates that As and salinity cross tolerance in S. persica

Author contribution statement

MP performed most of the experiments, analyzed the data and prepared the manuscript. AKP designed and coordinated the experiments, interpreted the results, and improved the manuscript.

Novelty statement

In the present work, a comparative study on individual effects of salinity or the metalloid arsenic or combinations of both on growth, ion homeostasis, ROS level, modulations of phytochelatins and thiols, osmotic, and antioxidative components of S. persica have been carried out to decipher the salt and arsenic cross tolerance mechanisms in this halophyte. The results of the present study indicate that S. persica plant can be utilized for phytoremediation of soil contaminated with high salinity

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

The financial support from Department of Science and Technology (DST) by the grant of SERB (SERB/SB/SO/PS-14/2014), DST, Government of India, New Delhi to AKP is duly acknowledged. This work was funded by Department of Science & Technology, Government of India, New Delhi in the form of Inspire Fellowship to MP. The authors duly acknowledge the Analytical Discipline and Centralized Instrument Facility of CSIR-CSMCRI for providing analytical facilities. This manuscript has been assigned

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