Abstract
Halophyte is a distinctive group of plants that can survive, even well flourish, at a concentration of Na+ and Cl− ions along with heavy metals that would be lethal to most of the agricultural crop species. These capabilities make certain halophytes good contenders for phytoremediation through phytoextraction or phytostabilization of the salt and heavy metals (HMs) in polluted soils. Thus, the present study elucidates the phytoextraction capacity of three halophytes (Suaeda monoica, Tamarix indica and Cressa critica) growing in saline soil (EC 112 ds m−1), with higher level of HMs rather than a cultivated soil. The accumulation of ions in above-ground tissue was determined in the all three studied plants, considering the fact that maintaining a stable cytosolic Na+/K+ ratio has become a crucial salinity tolerance mechanism. The higher salinity of soil resulted in high level of Na+ ions in leaves, increased synthesis of osmolyte components and robust antioxidant activities to combat the oxidative stress. As whole, changes in cellular metabolites were determined by using FT-IR spectroscopy, evident as differential FT-IR profiles in both leaves and stem specific to these metabolites. The considerable amounts of HMs accumulation including Zn, Fe, Mn, Cu, Cr, and Cd with highest being Fe in above-ground tissue of all three studied halophytes were obtained. These preliminary findings represent S. monoica, T. indica and C. cretica as potent phytoremediation plant using phytosequestration to accumulate HMs. The present study project a light on the use of these three plants in reclamation of degraded saline soils.
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Introduction
Soil or land degradation resulting from salinity associated with HMs is a major environmental constraint, particularly in arid and semiarid provinces of the world (Shahid et al. 2018; Khodaverdiloo et al. 2020). Argentina, China, Central Asia, Egypt, India, Iraq, Mexico, Portugal, Mongolia, Pakistan, Russia, Spain, Sudan and USA are the major provinces that turn out to be “Global Soil Salinization Hotspot” where most of the cultivated lands are either salt affected or facing the degradation glitches due to excessive salt or metal concentration (Qadir et al. 2014; Ivushkin et al. 2019). The growing concerns about soil degradation represent a threatening risk to agricultural productivity and sustainability of the economy and thus stimulated the efforts to propose new approaches on the remediation of polluted soil (Gomiero 2016). A number of physicochemical techniques were tested for treating polluted soils, but such processes are rather expensive and severely constrain soil fertility with adverse impacts on the environment (Khalid et al. 2017). Phytoremediation is a plant-based approach, which involves the use of plants to eradicate elemental pollutants from the soil or lower their bioavailability in soil (DalCorso et al. 2019). This approach is mainly based on the survival and accumulation efficacy of the particular plant in contaminated sites. It involves different strategies that can be lead to removal of salt as well as metals through phytoextraction (uptake, translocation and accumulation in aerial part of the plant) and phytostabilization (reduce bioavailability and immobilization in rhizosphere). It is hence interesting to study the capacity of different plant species to grow in polluted saline habitats and the way that they accumulate or distributes toxic ions and metals in both the above- as well as below-ground tissue. While a vast majority of the glycophyte plants are sensitive to saline habitats, halophytes inhabit substantially through evolving certain physiological, biochemical and molecular traits (Kumari et al. 2015; Flowers and Colmer 2015; Rajput et al. 2016). They evolved mechanism to controlled influx or outflux not only for Na+ and Cl− ions but also to metals like Fe, Mn, Zn, Cu and Cd. In that way, when these elements enter into the plants, they could be either be retained in their below-ground parts (i.e., root, root hairs and rhizome) or translocated to their aerial ones, i.e., leaves and stem (Van Oosten and Maggio 2015).
A salt hyperaccumulator is a plant capable of growing in soil or water with very high concentrations of salts, absorbing these salts through their roots and concentrating extremely high levels of salts in their tissues. In previous studies, various workers have advocated the use of halophyte for reclamation of salinity (reviewed in Hasanuzzaman et al. 2014; Nikalje et al. 2018) and HMs (Liang et al. 2017; Milić et al. 2012) as these hyperaccumulate salts or metals in their above-ground parts. Like C. cretica (Convolvulaceae), T. indica (Tamaricaceae) and S. monoica (Amaranthaceae) are the perennial halophytes, which can grow proficiently in soils with high concentration of salt and metals. There the C. cretica and the T. indica are the obligate halophytes and inhabit successfully in both the coastal and inland saline habitats (Joshi et al. 2018). S. monoica is a C4, true halophyte, native to coastal marshes and is invading successfully saline salt marsh of both the West and East coast of India (Arora et al. 2018; Joshi et al. 2019). Although these three species inhabit similar environmental condition of salt marshes of Gulf of Khambhat (Fig. 1), they have different growth form; it is hence interesting to relate their tolerance strategies and potential phytoremediation capacity. Even though some previous studies have shown phytoremediation ability of these species or their similar ones (Ghazaryan et al. 2019; Devi et al. 2016; Ayyappan et al. 2013; Agoramoorthy et al. 2008), there is a lack of information concerning appropriate mechanism in which all three species interact and exist in metal polluted saline soil, therefore providing a very comprehensive and intricate natural image. This could provide valuable information about the studied region of Gulf of Khambhat that could also be generalizable to other similar habitats of the world.
So, and for the first time, accumulation of ions (Na+, K+, Cl− and Ca2+), osmolytes (protein, proline, and soluble sugars), total phenolic content (TPC), antioxidant activity (SOD, DPPH and FRAP) and change in metabolite profile assessed through FT-IR profiles and potential to remediate heavy metal toxicity through accumulation of Zn, Fe, Mn, Cu, Cr, Cd were determined in above-ground tissues of three halophytes (S. monoica, T. indica and C. cretica). The present work demonstrates the spatial distribution of the parameters in leaves and stem in response to saline environment. In this context, all three halophytes are supposed to behave different and their tolerance strategy in terms of change in physiological and biochemical parameters can be assessed to establish phytoremediation potential of each.
Materials and methods
Description of sampling site
The sampling site is located near the Adhelai village (Latitude 22.3415035, Longitude 72.7435617), Bhavnagar district of Gujarat state of India (Fig. 2). It is a low-laying area, situated on the west margin of the Gulf of Khambhat. The zone gets inundated by tidal waters of the Gulf during the strong tidal currents. The magnitude and extent of inundation fluctuates in accordance with the tidal amplitude during the monsoon months. The sediments of the province are distinctly fine textured and are composed of stratified deposits of silt and clay, along with fine sand. The region receives an average annual rainfall about 650 to 700 mm and suffers from a hostile geoclimatic environment, highly saline shallow ground water and high concentration of salts and/or metals from both the ocean and inland zones. It is a vast salt-affected plain with sparsely distributed halophytic grasses and bushes. The dominant halophytic families are the Chenopodiaceae with Atriplex spp., Haloxylon spp., Sesuvium spp., Suaeda spp., Salsola spp., Poaceace with Aeluropus spp., Chloris spp., Sporobolus spp., Tamaricaceae with Tamarix spp. and Convolvulaceae with Cressa cretica.
Sampling and processing of the samples
In the March of 2019, both the soil (20 m × 15 m sampled area) and plant samples (100 g) were taken to determine the physicochemical physiognomies. The soil samples were taken from 0 to 15 cm depth, collected in triplicates, well-sealed in polyethylene bags and transferred to laboratory for analysis. The plant samples were stored at − 4 °C to avoid the degradation of the ingredients of the material till analysis. A detailed observation was made on the characteristics of the plants and specimens were separately submitted to the Botanical Survey of India, Jodhpur, for authentication.
Determination of physiochemical properties of soil
The pH, electric conductivity (EC) and organic carbon (OC) were estimated by the standard procedures detailed in USDA Handbook (1960). For the availability of Fe, Zn, Cd, Mn, Cu and Cr content, wet digestion of soil sample was done with the help of Di-acid mixture (3:1; concentrated HCl/HNO3 mixture [8 mL] and concentrated HClO4 [3 mL]) than analysis of suitable aliquot of digested material with the help of atomic absorption spectrometer (Perkin Elmer, Analyst 200 Germany) followed by Tüzen (2003).
Determination of ion content in plant tissues
Both the leaves and stem parts were washed before being dried out in an oven (60 °C for 72 h) and then crushed into a fine powder with a mortar and pestle. The Na+, K+, Ca2+, and Cl− content were determined in extracts prepared according to the method of Prakash and Prathapasenan (1988). In 5 mL of 0.1 N HNO3, 100 mg of the dried powder was suspended and the mixture was placed in a boiling water bath for 60 min, then analysis of suitable aliquot of digested material was carried out with the help of flame photometer (Eppendorf; Na+ and K+), atomic absorption spectrophotometer (Perkin Elmer, Analyst 200 Germany; Ca2+) and chloridometer (Buchler-Cotlove; Cl−).
Measurement of osmoprotective compounds
The amount of proline was estimated by the ninhydrin method (Bates et al. 1973). A modification of the method of phenol–sulfuric acid was used to determine soluble sugar content at 490 nm (Dubois et al. 1956). The total amount of soluble proteins was estimated according to the method of Bradford (1976) using bovine serum albumin as a standard.
Determination of antioxidant activity and TPC
Antioxidant activity was determined by extraction of samples, which was pooled and analyzed in triplicates. Dried powdered samples (250 mg) of selected species were extracted 12 h at room temperature by shaking on a test tube rotator with 5 mL of 70% methanol. The samples were centrifuged at 10,000 g for 10 min at 10 °C, and supernatant was used for antioxidant activities. The superoxide anions were generated using PMS/NADH system. The superoxide anions are subsequently made to reduce nitrobluetetrazolium (NBT) which yields a chromogenic product, which is measured at 560 nm (Jain et al. 2008). The inhibition percentage of superoxide anion generation was calculated as (%) = 100(A − B)/A, where A and B are the 517 nm absorption of the control and the corrected absorption of the sample reaction mixture. The DPPH radical scavenging activity was determined according to the method described by Hatano et al. (1988), and radical scavenging activity was calculated same as the SOD activity formula. The FRAP activity of plant extracts was determined using the method of Benzie and Strain (1996). Phenolic compounds were assayed using the Folin–Ciocalteu reagent, by following the method of Farkas and Kiraly (1962). TPC was expressed as mg gallic acid equivalents (GAE g−1 DW) through the calibration curve with gallic acid at 650 nm.
IR spectroscopy
For FT-IR analysis, pellets of the plant tissues were prepared in agate mortars, by mixing of tissue powder (2 mg) with KBr (1:100 p/p). All the samples were scanned from mid-infrared region (4000–400 cm−1) on Bruker (Model OPUS 7.5.18) FT-IR Spectrometer where 3000–2000 cm−1, 1800–1500 cm−1 and 1500–1200 cm−1 wave number was assigned for lipids, proteins and carbohydrates, respectively. The 1000–600 cm−1 wave number is assigned for cell wall components and other molecules including chlorophyll. Three samples were collected for each treatment, and three spectra were obtained from each sample of such species. KnowItAll software was used to find the functional groups for preliminarily analyzing IR spectra collected.
Determination of HMs and bioaccumulation factor (BAF) in plants
The above-ground tissues (leaves and stem) were separated, washed thoroughly with distilled water, and oven-dried at 65 °C. The dried plant parts (0.5 g) were washed in a muffle furnace at 550 °C for 12 h then subsequent extract was prepared followed by Tüzen (2003), and HMs in plant sample extracts was determined using an atomic absorption spectrophotometer (Perkin Elmer, Analyst 200 Germany). The BAF is defined as the ratio of metal concentration in plant above-ground structure (i.e., leaves and stem) to that in the soil of the growing site. It is a measure of the plants’ ability to take up, transport and accumulate metal in aerial parts (Wang et al. 2009; Petelka et al. 2019).
Experimental design and statistical analysis
The experiments were set up in complete randomized block design (RBD) and repeated twice. All the experiments were conducted with minimum three replicates for the both soil and plant samples. In case of plant samples, one replicate means a set of 3 individual plants that sampled from same sites. The significance of differences among the means of species was carried out using the Duncan’s multiple range tests (Duncan 1955) at P < 0.05. The results expressed are mean ± SD of three independent experiments and subjected to one-way analysis of variance (ANOVA) using SPSS v.17 (SPSS, Chicago, USA).
Results and discussion
Soil characteristics
Physicochemical characteristics of the soil of the studied location in Gulf of Khambhat cost are shown in Table 1. Results of soil analysis showed that soil of the studied site was alkaline in nature (pH 8.93) with a high EC of 112 ds/m−1 and lower OC content (0.16%), probably because of the higher salt inputs through soil–water movement or wind erosion in course of the year. It is well known that the pH and OC affect not only the physicochemical possessions of the soil but also the binding as well as retention capacity of HMs (Liu et al. 2014). In this saline habitat, high value of pH can be regarded as an indicator for a potential risk of HM pollution because under high pH conditions, HM (like Zn, Fe) become less mobile and more efficiently retained in the soil (Zeng et al. 2011; Minkina et al. 2017). Iron content indicated its greater concentration than that of Mn and other HMs in this habitat. The concentration of both the Fe (7620 mg/kg) and Mn (850 mg/kg) was in range of permissible limits, but Mn concentration exceeds the limit of Indian natural soil background (Gowd et al. 2010). Usually, Fe and Mn are not hazardous elements but their higher concentration possesses threatening risk to soil fertility. Furthermore, the Zn content was almost 1.2 fold greater than that of the Cu. Concentration of both Zn (127 mg/kg) and Cu (110 mg/kg) was higher than the threshold value for uncontaminated soil (Zn; 21 mg/kg, Cu; 56 mg/kg), but did not exceed the guideline value of 300–600 mg/kg for Zn and 135–270 mg/kg for Cu in the country (Kumar et al. 2019). In soil, Zn and Cu are among the most problematic metals and their availability depends greatly on their forms and soil properties, especially soil pH (Ghazaryan et al. 2018). The Cd (13 mg/kg) concentration exceeds the threshold value of Indian standards (3–6 mg/kg) and world soil (0.5 mg/kg) (Kumar et al. 2019; Kabata-Pendias and Mukherjee 2007). Cr concentration (11.5 mg/kg) was found in range of Indian natural soil background (Kumar et al. 2019).
Ion contents in plant tissues
The ion contents in all of the three halophytes varied significantly with respect to plant part (Table 2). The Na+ (12.29 to 21.09 mg/g), K+ (3.36 to 5.82 mg/g), Cl− (2.21 to 9.23 mg/g) and Ca2+ (2.28 to 3.98 mg/g) was higher in leaves rather than stem tissue. In the present study, significantly greater concentrations of Na+ in leaves of plants grown under high soil salinity were accompanied by equally elevated concentrations of K+, Cl−, and Ca2+. This indicates that the transmission of these ions to leaves may be adaptive mechanism to prevent the adverse impact of higher Na+. This aspect could be correlated with the fact that the K+ and Ca2+ plays crucial role in various turgor-driven movements(Munns and Tester 2008; Podar et al. 2019), even K+ has strong inhibitory effects on Na+ due to similarity in their ionic radius and ion hydration energy (Volkov and Flowers 2019). A steady Na+/K+ ratio was recorded in both the stem and leaves tissue with the highest being in C. cretica. This indicates that these plants show preference to maintain a favorable cytosolic Na/K ratio in both the leaves and stem, and it could be a part of adaptive strategy to tolerate higher salinity. The presence of higher amount of ions in above-ground tissue indicates that these plants could be able to decrease the soil electrical conductivity by absorbing soluble salts mainly the Na+ and Cl− (Bueno et al. 2020). The ion accumulation potential of studied halophytes is comparable to or even higher than several halophytic species that have been tried in the past for their possible use in reclamation of salt-affected soils (Ravindran et al. 2007; Rabhi et al. 2008; Devi et al. 2016; Nikalje et al. 2018).
Accumulation of osmoprotective compounds
In the present study, protein contents in all species were minimal, and proline and soluble sugar content were relatively high (Fig. 3). Comparison of different species or different tissues of same species showed that proline content in S. monoica leaves (Fig. 3a) and soluble sugar content in the T. indica stem (Fig. 3b) were significantly higher than those in other species. For the protein content, the difference between different species was clear and reported highest in S. monoica (Fig. 3c). It is clearly observed that such species accumulated proline as a dominant organic osmolytes in leaves and soluble sugar in stem tissue, but accumulation of these two solutes considered may appear complementary. This suggests that these three species may simultaneously use diverse organic solute for osmoregulation and osmoprotection but that the relative importance of accumulation of each of them may be, at least partly, and associated with improved biosynthesis or reduced catabolism mechanism of individual species. These observations are reinforced by the fact that halophytes intensify and reallocating low molecular weight organic solutes in different subcellular compartments (Rajput et al. 2015; Parida et al. 2016; Mishra and Tanna 2017). A similar trend of osmotic adjustment has been observed in 19 alkali-tolerant halophyte species during adaptation to salt-alkalinized habitats (Yang et al. 2012). Such osmolytes might regulate overall metabolic pool via changes in the expression of signaling proteins and biosynthetic enzymes for salt stress responsive genes (Wang et al. 2020). However, the signals that provoke these changes in metabolic pool inside the plant cells have not been identified in present study.
Antioxidant activity and TPC
In this study, all halophytes showed differential response to scavenge the free superoxide, ferric and DPPH radicle ions (Fig. 4). The SOD activity was significantly higher in leaves than stem and reported highest in S. monoica (Fig. 4a). The FRAP activity was significantly higher in leaves of T. indica and C. cretica, although in S. monoica it was higher in stem (Fig. 4b). The DPPH scavenging in S. monoica was significantly higher than in other species (Fig. 4c). For the total phenolic contents, the difference between different species was clear and reported highest in T. indica leaves (Fig. 4d). In such halophytes, significantly greater free radicles scavenging efficacy in leaves followed by stem was accompanied by equally elevated concentrations of phenolic content. This indicates that these plant robust the phenolic antioxidant defense mechanism in leaves to prevent the damage caused by reactive oxygen species. It could be attributed to protect the photosynthetic contraption since light harvesting complex is a primary place for reactive oxygen species production in plants grown under salt stress condition (Bose et al. 2014). Our results taken together with previous studies indicating polyphenols are the first line of defense to minimize oxidative damage, and their robust synthesis could be an adaptive trait to enhance salt tolerance in halophytes (Thatoi et al. 2014; Stanković et al. 2015; Faustino et al. 2019). That might indicate that the polyphenolic compounds with much greater antioxidant activity would be an interesting premise to increase cultural and economic value of halophytes through saline cultivation.
FT-IR analysis
FT-IR is an imperative technique to explore molecular chemistry inside the cell with respects to any biotic or abiotic stress. It has ability to recognize the functional groups and provide information about the composition as well as structural characterization of the cellular metabolites (Westworth et al. 2019; Nikalje et al. 2019). In this study, FT-IR profiling was done so as to confirm the metabolic chemistry of S. monoica, T. indica and C. cretica during high salt exposure in their natural habitat. The FT-IR spectra peaks and their probable functional groups are shown in leaves and stem (Table 3). In the FT-IR profile, these halophytes showed differential response of leaves and stem (Fig. 5) to higher salinity. In the lipid region, the peak at 2981 cm−1 of both the leaves and stem was splitted into two peaks and this peak is characteristic of S, O–H stretch (carboxylic acids), C–H stretch (alkanes), (CO)–H (aldehydes). Earlier, Afifi et al. (2013) identified a peak at 2935 cm−1 belongs to –OCH2− group that represent peroxides and indicates peroxidation of lipids in Jojoba plant under salt exposure. Similarly, FT-IR profiling of Sesuvium portulacastrum under salt stress revealed involvement of glycolipids in salt adaptation (Nikalje et al. 2019). In the protein regions, the peak at 1732 cm−1 was splitted into two major peaks and the area of peak at 1630 cm−1 was increased in both the leaves and stem of T. indica (Fig. 5a, b) and C. cretica (Fig. 5c, d), respectively. However, a small peak at 1520 cm−1 disappeared in S. monoica (Fig. 5e, f). These peaks are characteristic of C=O (esters, carboxylic acids, ketones, aldehydes), C=C (benzenes), C–N (amino group) functional groups and indicates that high soil salt content influence the degree of protein accumulation. In our previous work, in S. monoica callus culture, it was 1.2-fold and 1.7-fold higher in low and high salt, respectively, as compared to control (Joshi et al. 2019). Earlier, using the FT-IR spectra of isolated protein and relative content of irregular confirmations in amide I region, Akyuz et al. (2018) identified salt-tolerant mutants of Soybean. In the carbohydrates region, the area of peak at 1322 cm−1 wave number was increased in both plant parts of such halophytes. This peak indicates presence of S (=O) 2 stretch (sulfones), N=O stretch (nitro compounds) and O–H bend (carboxylic acids, alcohols). In T. indica, area of peak at 1240 cm−1 wave number was disappeared that indicates the presence of C–N stretch (amines), C–O stretch (esters), C–O stretch (ethers, alcohols), O–H band (carboxylic acids). Similarly, in Jojoba plant, the band area of peaks in carbohydrate region was decreased by 19% and conformation of carbohydrate was altered under salt exposure (Afifi et al. 2013). In these halophytes, the peak at 780 cm−1 wave number [Characteristic of C–N stretch (amines), =C–H bend (benzene, alkenes), C–C (chlorides)] indicates cell wall components play substantial role in adaptation to salt stress.
Accumulation of HMs in plants
Heavy metal concentrations in different plant organs of three halophytes from same locality are illustrated in Fig. 6. In all three sampled species, the leaves had significantly higher concentrations of metals compared to stems. Zn was the only metal the concentration of which was significantly higher in the stem than in the leaves. Although a number of metals are considered essential micronutrients for plants, their excess amount may be phytotoxic and cause several functional anomalies (Zhu et al. 2018; Ashraf et al. 2019). Total Zn concentration in plants shoot part ranged from 13.59 to 20.61 mg kg−1. The least concentration was detected in C. cretica and the highest concentration measured in S. monoica (Fig. 6a). The total Fe and Mn concentrations ranged from 137.97 to 171.23 mg kg−1 and 25.84 to 43.75 mg kg−1, respectively (Fig. 6b, c), with highest measured in S. monoica. Moreover, Cu concentrations in plants varied from 8.31 mg kg−1 in T. indica to 11.66 mg kg−1 in S. monoica (Fig. 6d). Adequate levels of Mn, Fe and Cu in plant tissue are 50, 60–600 and 5–25 mg kg−1, respectively. However, proposed criteria for Mn, Fe and Cu hyperaccumulators may be limited to 2000 to 10,000 mg kg−1 for Mn, up to 2500 mg kg−1 for Fe and up to 10,000 mg kg−1 for Cu (Reeves et al. 2000; Van der Ent et al. 2013; Ashraf et al. 2019). The concentration of Cd and Cr was also considerable in all three plants with a range of 1.92 to 4.6 mg kg−1 and 0.98 to 2.28 mg kg−1, respectively (Fig. 6e, f). The Cr serves as imperative cofactor for certain essential enzymes, yet it may be phytotoxic if the concentration exceeds their standard permissible limits 5 mg kg−1(Lewicki et al. 2014; Ashraf et al. 2019). In this study, S. monoica consistently shows higher concentration potential for all six elements rather than T. indica and C. cretica. However, accumulation capacity is significantly different in diverse tissue of plants but accumulation potential is not much reliant on taxonomic status. The plant-specific translocation mechanism probably leads to significant accretion of all six elements. This assumption is in line with the fact that when plant accumulates one element, it can be expected that it will accumulate other metals as well (Milić et al. 2012; Mujeeb et al. 2020). The bioaccumulation of metals from soil to above-ground parts (i.e., leaves and stem) of plant, which was expressed by the bioaccumulation factor (BAF), varied from 0.018 to 0.022 (Fe), 0.030 to 0.051 (Mn), 0.075 to 0.106 (Cu), 0.107 to 0.162 (Zn), 0.085 to 0.198 (Cr) and 0.147 to 0.350 (Cd) (Table 4). The investigated plant species most efficiently took up Cd, Cr and Cu followed by the Zn, Mn and Fe, but none of them reached BAF values higher than 1. However, the criterion of BAF > 1 does not necessarily have to be achieved by plants to succeed as hyperaccumulators (Wang et al. 2009). In this study, the criterion BAF > 1 not be considered as a significant parameter to identify hyperaccumulators because at field condition heavy metal concentrations in contaminated soil far exceed the toxic levels for plants and the criterion BAF > 1 would be impossible to achieve (Robinson et al. 1998; Zhao et al. 2003). Here, BAF is acknowledged to be an index of plant accumulation abilities and it would provide better understanding about the potential of hyperaccumulation when no data prior to the vegetation was given. A comparison of our results with previous investigations on phytoremediation prospective of the halophytes (Kouhi and Moudi 2020; Li et al. 2019; Lutts et al. 2016; Milić et al. 2012) has shown that the investigated species considered as moderately accumulator and could be used to remediate heavy metal polluted saline soil.
Conclusion for future biology
The present study proved S. monoica, T. indica and C. cretica, are potent halophyte contenders for saline agricultural lands and phytoremediation. With the large amount of Na+ and Cl− ions accumulation capacity in above-ground parts, such species could lead to the extension of cultivated land by exploiting the soil desalination abilities of these halophytes in regions that are the part of “Global Soil Salinization Hotspots.” The considerable amount of heavy metals accumulation including Zn, Fe, Mn, Cu, Cr and Cd suggested that all three halophytes can be used for phytoremediation of heavy metals from the polluted soils. These preliminary finding represents S. monoica, T. indica and C. cretica as potent phytosequestration plants that can easily thrive on degraded saline soils.
Abbreviations
- EC:
-
Electric conductivity
- OC:
-
Organic carbon
- SOD:
-
Superoxide dismutase
- DPPH:
-
1,1-Diphenyl-2-picrylhydrazyl
- FRAP:
-
Ferric reducing power
- PMS:
-
Phenazine methosulfate
- NADH:
-
Nicotinamide adenine dinucleotide phosphate
- TPC:
-
Total phenolic content
- FT-IR:
-
Fourier-transform infrared spectroscopy
References
Afifi AA, Youssef RA, Hussein MM (2013) Fourier transform infrared spectometry study on early stage of salt stress in jujube plant. Life Sci J 10:1973–1981
Agoramoorthy G, Chen FA, Hsu MJ (2008) Threat of heavy metal pollution in halophytic and mangrove plants of Tamil Nadu, India. Environ Pollut 155:320–326
Akyuz S, Akyuz T, Celik O, Atak C (2018) FTIR spectroscopy of protein isolates of salt-tolerant soybean mutants. J Appl Spectrosc 84:1019–1023
Arora J, Joshi A, Sharma V (2018) Suaeda A promising sustainable halophyte of future. Lap Lambert Academic Publishing, Mauritius
Ashraf S, Ali Q, Zahir ZA, Ashraf S, Asghar HN (2019) Phytoremediation: environmentally sustainable way for reclamation of heavy metal polluted soils. Ecotoxicol Environ Saf 174:714–727
Ayyappan D, Balakrishann V, Ravindran KC (2013) Potentiality of Suaeda monoica Forsk A salt marsh halophyte on restoration of saline agricultural soil. World Appl Sci J 28:2026–2032
Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207
Benzie IF, Strain JJ (1996) The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: the FRAP assay. Anal Biochem 239:70–76
Bose J, Rodrigo-Moreno A, Shabala S (2014) ROS homeostasis in halophytes in the context of salinity stress tolerance. J Exp Bot 65:1241–1257
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Bueno M, Lendínez ML, Calero J, del PilarCordovilla M (2020) Salinity responses of three halophytes from inland saltmarshes of Jaén (southern Spain). Flora 266:151589
DalCorso G, Fasani E, Manara A, Visioli G, Furini A (2019) Heavy metal pollutions:state of the art and innovation in phytoremediation. Int J Mol Sci 20:3412
der Ent Van, Baker AJM, Reeves RD, Pollard AJ, Schat H (2013) Hyperaccumulators of metal and metalloid trace elements: facts and fiction. Plant Soil 362:319–334
Devi S, Nandwal AS, Angrish R, Arya SS, Kumar N, Sharma SK (2016) Phytoremediation potential of some halophytic species for soil salinity. Int J Phytoremediat 18:693–696
Dubois M, Gilles KA, Hamilton JK, Rebers PT, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356
Duncan DB (1955) Multiple range and multiple F tests. Biometrics 11:1–42
Farkas GL, Kiraly Z (1962) Role of phenolic compound in the physiology of plant diseases and disease resistance. Phytopathol Z 44:105–150
Faustino MV, Faustino MA, Silva H, Cunha Â, Silva A, Pinto DC (2019) Puccinellia maritima, Spartina maritima, and Spartina patens halophytic grasses: characterization of polyphenolic and chlorophyll profiles and evaluation of their biological activities. Molecules 24:3796
Flowers TJ, Colmer TD (2015) Plant salt tolerance: adaptations in halophytes. Ann Bot 115:327–331
Ghazaryan KA, Movsesyan HS, Khachatryan HE, Ghazaryan NP, Minkina TM, Sushkova SN, Mandzhieva SS, Rajput VD (2018) Copper phytoextraction and phytostabilization potential of wild plant species growing in the mine polluted areas of Armenia. Geochem Explor Environ Anal 19:155–163
Ghazaryan KA, Movsesyan HS, Minkina TM, Sushkova SN, Rajput VD (2019) The identification of phytoextraction potential of Melilotus officinalis and Amaranthus retroflexus growing on copper-and molybdenum-polluted soils. Environ Geochem Health. https://doi.org/10.1007/s10653-019-00338-y
Gomiero T (2016) Soil degradation, land scarcity and food security: reviewing a complex challenge. Sustainability 8:281
Gowd SS, Reddy MR, Govil PK (2010) Assessment of heavy metal contamination in soils at Jajmau (Kanpur) and Unnao industrial areas of the Ganga Plain, Uttar Pradesh, India. J Hazard Mater 174:113–121
Hasanuzzaman M, Nahar K, Alam MM, Bhowmik PC, Hossain MA, Rahman MM, Prasad MNV, Ozturk M, Fujita M (2014) Potential use of halophytes to remediate saline soils. Biomed Res Int 2014:589341
Hatano T, Kagawa H, Yasuhara T, Okuda T (1988) Two new flavonoids and other constituents in licorice root: their relative astringency and radical scavenging effects. Chem Pharm Bull 36:2090–2097
Ivushkin K, Bartholomeus H, Bregt AK, Pulatov A, Kempen B, De Sousa L (2019) Global mapping of soil salinity change. Remote Sens Environ 231:111260
Jain PK, Ravichandran V, Agrawal RK (2008) Antioxidant and free radical scavenging properties of traditionally used three Indian medicinal plants. Curr Trends Biotechnol Pharm 2:538–547
Joshi A, Kanthaliya B, Arora J (2018) Halophytes of Thar Desert: potential source of nutrition and feedstuff. Int J Bioassays 8:5674–5683
Joshi A, Kanthaliya B, Arora J (2019) Evaluation of growth and antioxidant activity in Suaeda monoica and Suaeda nudiflora Callus cultures under sequential exposure to saline conditions. Curr Biotechnol 8:42–52
Kabata-Pendias A, Mukherjee AB (2007) Trace elements from soil to human. Springer, New York, p 550
Khalid S, Shahid M, Niazi NK, Murtaza B, Bibi I, Dumat C (2017) A comparison of technologies for remediation of heavy metal contaminated soils. J Geochem Explor 182:247–268
Khodaverdiloo H, Han FX, HamzenejadTaghlidabad R, Karimi A, Moradi N, Kazery JA (2020) Potentially toxic element contamination of arid and semi-arid soils and its phytoremediation. Arid Land Res Manag 7:1–31
Kouhi SMM, Moudi M (2020) Assessment of phytoremediation potential of native plant species naturally growing in a heavy metal-polluted saline–sodic soil. Environ Sci Pollut Res 27:10027–10038
Kumar V, Sharma A, Kaur P, Sidhu GPS, Bali AS, Bhardwaj R, Cerda A (2019) Pollution assessment of heavy metals in soils of India and ecological risk assessment: a state-of-the-art. Chemosphere 216:449–462
Kumari A, Das P, Parida AK, Agarwal PK (2015) Proteomics, metabolomics, and ionomics perspectives of salinity tolerance in halophytes. Front Plant Sci 6:537
Lewicki S, Zdanowski R, Krzyzowska M, Lewicka A, Debski B, Niemcewicz M (2014) The role of chromium III in the organism and its possible use in diabetes and obesity treatment. Ann Agric Environ Med 21:331–345
Li B, Wang J, Yao L, Meng Y, Ma X, Si E, Wang H (2019) Halophyte Halogeton glomeratus, a promising candidate for phytoremediation of heavy metal-contaminated saline soils. Plant Soil 442:323–331
Liang L, Liu W, Sun Y, Huo X, Li S, Zhou Q (2017) Phytoremediation of heavy metal contaminated saline soils using halophytes: current progress and future perspectives. Environ Rev 25:269–281
Liu G, Xue W, Tao L, Liu X, Hou J, Wilton M et al (2014) Vertical distribution and mobility of heavy metals in agricultural soils along Jishui River affected by mining in Jiangxi Province, China. Clean Soil Air Water 42:1450–1456
Lutts S, Qin P, Han RM (2016) Salinity influences biosorption of heavy metals by the roots of the halophyte plant species Kosteletzkya pentacarpos. Ecol Eng 95:682–689
Milić D, Luković J, Ninkov J, Zeremski-Škorić T, Zorić L, Vasin J, Milić S (2012) Heavy metal content in halophytic plants from inland and maritime saline areas. Cent Eur J Biol 7:307–317
Minkina TM, Fedorov YA, Nevidomskaya DG et al (2017) Heavy metals in soils and plants of the Don River Estuary and the Taganrog Bay coast. Eurasian Soil Sci 50:1033–1047
Mishra A, Tanna B (2017) Halophytes: potential resources for salt stress tolerance genes and promoters. Front Plant Sci 8:829
Mujeeb A, Aziz I, Ahmed MZ, Alvi SK, Shafiq S (2020) Comparative assessment of heavy metal accumulation and bio-indication in coastal dune halophytes. Ecotoxicol Environ Saf 195:110486
Munns R, Tester M (2008) Mechanisms of salinity tolerance. Ann Rev Plant Biol 59:651–681
Nikalje GC, Srivastava AK, Pandey GK, Suprasanna P (2018) Halophytes in biosaline agriculture: mechanism, utilization, and value addition. Land Degrad Dev 29:1081–1095
Nikalje GC, Kumar J, Nikam TD, Suprasanna P (2019) FT-IR profiling reveals differential response of roots and leaves to salt stress in a halophyte Sesuvium portulacastrum (L.) L. Biotechnol Rep 23:e00352
Parida AK, Veerabathini SK, Kumari A, Agarwal PK (2016) Physiological, anatomical and metabolic implications of salt tolerance in the halophyte Salvadora persica under hydroponic culture condition. Front Plant Sci 7:351
Petelka J, Abraham J, Bockreis A, Deikumah JP, Zerbe S (2019) Soil heavy metal (loid) pollution and phytoremediation potential of native plants on a former gold mine in Ghana. Water Air Soil Pollut 1:230–267
Podar D, Macalik K, Réti KO, Martonos I, Török E, Carpa R, Székely G (2019) Morphological, physiological and biochemical aspects of salt tolerance of halophyte Petrosimonia triandra grown in natural habitat. Physiol Mol Biol Plants 25:1–13. https://doi.org/10.1007/s12298-019-00697-x
Prakash L, Prathapasenan G (1988) Effect of NaCl salinity and putrescine on shoot growth, tissue ion concentration and yield of rice (Oryza sativa L. var. GR-3). J Agron Crop Sci 160:325–334
Qadir M, Quillerou E, Nangia V, Murtaza G, Singh M, Thomas RJ, Drechsel P, Noble AD (2014) Economics of salt-induced land degradation and restoration. Nat Res Forum 38:282–295
Rabhi M, Talbi O, Atia A, Abdelly C, Smaoui A (2008) Selection of a halophyte that could be used in the bioreclamation of salt-affected soils in arid and semi-arid regions. In: Abdelly C et al (eds) Biosaline agriculture and high salinity tolerance. Birkhäuser, Basel, pp 241–246
Rajput VD, Chen Y, Ayup M (2015) Effects of high salinity on physiological and anatomical indices in the early stages of Populus euphratica growth. Russ J Plant Physiol 62:229–236
Rajput VD, Minkina T, Yaning C, Sushkova S, Chapligin VA, Mandzhieva S (2016) A review on salinity adaptation mechanism and characteristics of Populus euphratica, a boon for arid ecosystems. Acta Ecol Sin 36:497–503
Ravindran KC, Venkatesan K, Balakrishnan V, Chellappan KP, Balasubramanian T (2007) Restoration of saline land by halophytes for Indian soils. Soil Biol Biochem 39:2661–2664
Reeves RD, Baker AJM, Ilya R (2000) Metal accumulating plants. In: Raskin I, Ensley BD (eds) Phytoremediation of toxic metals: using plants to clean up the environment. Wiley, New York. ISBN 0-471-19254-6
Robinson BH, Leblanc M, Petit D, Brooks RR, Kirkman JH, Gregg PEH (1998) The potential of Thlaspi caerulescens for phytoremediation of contaminated soils. Plant Soil 203:47–56
Shahid SA, Zaman M, Heng L (2018) Soil salinity: historical perspectives and a world overview of the problem. In: Zaman M et al (eds) Guideline for salinity assessment, mitigation and adaptation using nuclear and related techniques. Springer, Cham, pp 43–53
Stanković MS, Petrović M, Godjevac D, Stevanović ZD (2015) Screening inland halophytes from the central Balkan for their antioxidant activity in relation to total phenolic compounds and flavonoids: are there any prospective medicinal plants? J Arid Environ 120:26–32
Thatoi HN, Patra JK, Das SK (2014) Free radical scavenging and antioxidant potential of mangrove plants: a review. Acta Physiol Plant 36:561–579
Tüzen M (2003) Determination of heavy metals in soil, mushroom and plant samples by atomic absorption spectrometry. Microchem J 74:289–297
USDA Handbook (1960) Diagnosis and improvement of saline and alkali soils. In: Richards LA (ed) Oxford & IBH Publ Co. Pvt. Ltd., New Delhi, p 60
Van Oosten MJ, Maggio A (2015) Functional biology of halophytes in the phytoremediation of heavy metal contaminated soils. Environ Exp Bot 111:135–146
Volkov V, Flowers TJ (2019) Mechanisms of ion transport in halophytes: from roots to leaves. In: Gul B et al (eds) Sabkha ecosystems, tasks for vegetation science VI. Springer, Cham, pp 125–150
Wang SL, Liao WB, Yu FQ, Liao B, Shu WS (2009) Hyperaccumulation of lead, zinc, and cadmium in plants growing on a lead/zinc outcrop in Yunnan Province, China. Environ Geol 58:471–476
Wang R, Wang X, Liu K, Zhang XJ, Zhang LY, Fan SJ (2020) Comparative transcriptome analysis of halophyte Zoysia macrostachya in response to salinity stress. Plants 9:458
Westworth S, Ashwath N, Cozzolino D (2019) Application of FTIR-ATR spectroscopy to detect salinity response in Beauty Leaf Tree (Calophyllum inophyllum L). Energy Procedia 160:761–768
Yang C, Zheng S, Huang H, Liu Z, Zheng W, Liu B, Shi D (2012) Comparison of osmotic adjustment and ion balance strategies in nineteen alkali-tolerant halophyte species during adaptation to salt-alkalinized habitats in northeast China. Aust J Crop Sci 6:141
Zeng F, Ali S, Zhang H, Ouyang Y, Qiu B, Wu F, Zhang G (2011) The influence of pH and organic matter content in paddy soil on heavy metal availability and their uptake by rice plants. Environ Pollut 159:84–91
Zhao FJ, Lombi E, McGrath SP (2003) Assessing the potential for zinc and cadmium phytoremediation with the hyperaccumulatorThlaspi caerulescens. Plant Soil 249:37–43
Zhu G, Xiao H, Guoc Q, Song B, Zheng G, Zhang Z, Zhao J, Okoli CP (2018) Heavy metal contents and enrichment characteristics of dominant plants in wasteland of the downstream of a lead–zinc mining area in Guangxi, Southwest China. Ecotoxicol Environ Saf 151:266–271
Acknowledgements
Abhishek Joshi acknowledge the support of UGC, New Delhi, for the award of BSR meritorious fellowship [25-1/2014-15(BSR) 7-125/2007(BSR)] and Ministry of Science and Higher Education of the Russian Federation (No. 0852-2020-0029).
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Joshi, A., Kanthaliya, B., Rajput, V. et al. Assessment of phytoremediation capacity of three halophytes: Suaeda monoica, Tamarix indica and Cressa critica. BIOLOGIA FUTURA 71, 301–312 (2020). https://doi.org/10.1007/s42977-020-00038-0
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DOI: https://doi.org/10.1007/s42977-020-00038-0