Keywords

10.1 Introduction

To feed increasing population, there is urgent need to increase food production by more than 70% (World Bank 2008). However, with increase in the total area of salt-affected land (~831 million hectares), the productivity of agricultural land is dwindling. With this pace, it is estimated that by middle of twenty-first century, about 50% lands under cultivation will be lost (Gupta and Huang 2014). This global issue can be solved with the help of multidisciplinary approaches. It may include development of tolerant crops (which can tolerate different biotic and abiotic stresses, grow on nutrient deficient soil and give maximum yield), reclamation of degraded saline soil and/or domestication of wild plants with desired characters. In this context, domestication of halophytes is a viable option as these group of flowering plants are endowed with ability to survive under high salinity. Many conventional crops cannot survive under low (40 mM NaCl) salinity, while halophytes can grow and complete their life cycle under high (200 mM or more NaCl) salinity (Flowers and Colmer 2008). The strong pressure of selection also makes them to acquire adaptive features under high salinity. This includes some special anatomical features (salt hairs, salt glands, etc.), physiological and biochemical alterations and changes in metabolic profile. These implications make halophytes suitable candidate to study salt stress adaptation mechanism in plants. Some halophytes like Quinoa and Salicornia contains high nutrititive values. Quinoa contains 4.4g proteins, 21.3g carbohydrates, 0.9g sugar and 2.8g fibres per 100 g seeds, while Salicornia is used as vegetable which contains 5% Vitamnin A, 4% Vitamin C and 4% iron. Most of the halophytes contain polyphenols which can be utilized in food, pharmaceutical, cosmetics and medicinal industries (Hasanuzzaman et al. 2014). Along with such value addition, halophytes play a major role in environmental protection. Halophytes like Sesuvium, Medicago, Cackile, Salicornia and Atriplex were well studied for their application in phytodesalination, phytoremediation, sand dune fixation, phytostabilization (Table 10.1; Fig. 10.1), etc. In this article, we highlighted the prospective economic importance of halophytes and their diverse roles in sustainable agriculture and environmental protection.

Table 10.1 Diverse applications of halophytes
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Fig. 10.1
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Utilization of halophytes for economic benefits and environmental cleanup

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10.2 Economic Values of Halophytes

Enormous conventional and non conventional efforts are being taken to improve salt tolerance in crops, but these efforts have resulted in only few productive salt-tolerant varieties (Roy et al. 2014). Most of the work has been limited to the laboratory level with few studies at green house or field level. In this regard, domestication of naturally salt tolerant, halophytes can provide a better option to mitigate adequate food production. Halophytes can be irrigated with brackish/saline water or can be cultivated in salt-affected agricultural lands for food, fuel, fibres, fodder, medicines and other value added products (Glenn et al. 1999; Nikalje et al. 2017b). Halophytes can be utilized as alternative crops to conventional crops, and good quality water can be diverted to other highly productive cash crops like rice, sugarcane, wheat, etc. This will solve problem of water non-availability (Koyro et al. 2011). Therefore, different halophytes need to be studied for their economic potential for agricultural, industrial and/or ecological purpose. In the following subsections, economic benefits of halophytes are described.

10.2.1 Food

Halophytes acquire their niche in saline soils, which are rich in different salts and micro- and macronutrients. It makes nutritional profiles of halophytes adequate for human consumption (Barreira et al. 2017). In addition, they contain polyunsaturated fatty acids, phenolic compounds, different vitamins and essential nutrients like manganese (Barreira et al. 2017). Halophytes such as Aster tripolium, Crithmum maritimum, Salicornia sp. and Portulaca oleracea are consumed as vegetable in culinary purposes (Tardio et al. 2006). In addition, they synthesize important metabolites like amino acids, sugars, antioxidants, quaternary ammonium compounds and polyols (Muchate et al. 2016). These compounds have primary role in reactive oxygen species scavenging, as osmolytes for ion homeostasis and protection from oxidation (Nikalje et al. 2017a). The osmolytes have nutritive value and health-promoting benefits and protective role against diseases (Buhmann and Papenbrock 2013). The ability of halophytes to grow in saline and brackish water has been utilized to conserve water resources for human consumption. Promotion of halophytes for sustainable biosaline agriculture is an emerging need due to their increasing market demand and high nutritional value, for e.g. Quinoa (Panta et al. 2016; Nikalje et al. 2017b). In European markets, halophyte products have high demand. The vegetables and salad crops (Salicornia and Aster) are being sold in markets at relatively high price (Boer 2006). Salicornia is a non-seasonal plant and can be cultivated throughout the year for vegetables (Boer 2006). Along with them Beta maritima, Crambe maritima and Salsola soda are new potential vegetables. In South America, Quinoa has long history of cultivation. It has more than 2500 accessions and tolerant to salinity, drought, frost and wind. It is rich in essential amino acids, fatty acids, minerals and vitamins, which gained interest to consider this plant in global food security programme (Adolf et al. 2013). Bolivia is the major producer of Quinoa; it produces 0.5 t ha−1 grain yield, but under optimized conditions of cultivation, it is expected that it may increase up to 3–5 t ha−1 (Adolf et al. 2013).

10.2.2 Fodder/Forage

The fodder crop must have high biomass, digestibility and palatability for animals. They contain high proteins, low oxalate, fibre and ash content (El Shaer 2004). Khan et al. (2009) systematically screened different halophytes and reported two halophytes, namely, Desmostachya bipinnata and Panicum turgidum as potential candidates for fodder production. They also developed mass scale fodder production on salinized land by saltwater irrigation and patented. This system has produced 50–60,000 kg/ha/year fodder (equivalent to maize) on saline soil (Khan et al. 2009). Halophytes irrigated with salt water, if provided with leaching conditions and optimum salinity, can give higher yield as compared to conventional crops and water use efficiency. The conventional forage crops like maize can be replaced with halophytic plants, but due to relatively high salt content and anti-nutritional properties, there are some restrictions in using them. The high palatability and good nutritional value (high protein and low fibre content) shows potential of halophytes as fodder (El Shaer 2004). The salt content of halophytes can be nullified by using mixture of forage plants for feeding. For example, A. nummularia was mixed with other herbaceous species, and annual grasses (with low salt content) can be a good fodder for animals (Barrett-Lennard and Setter 2010). According to Aronson (1985), there are about 95 halophytes with potential of forage or fodder. Among them some species of Atriplex contain 1.26–2.09 kg m−2 dry matter and 15.5–39.5% fibre and 10.2–19.5% crude protein. Trees like Aegiceras corniculata, Rhizophora mucronata, Avicennia marina and Ceriops tagal are used for camel and cattle feed. In arid and semiarid regions, Salvadora, Acacia, Prosopis and Ziziphus are incorporated in traditional fodder. Salicornia, Chenopodium, Atriplex, Suaeda, Salsola and Kochia are shrubs, while Chloris virgata, C. gayana, Echinochloa turnerana, E. colonum, Aeluropus lagopoides, Sporobolus marginatus, Dactyloctenium sindicum, Puccinellia distans and S. marginatus are grass species popularly used as animal feeds and fodder.

10.2.3 Edible Oil

The demand for edible or vegetable oil is increasing with time which is responsible for rapid growth of oil extraction industries (Weber et al. 2007). Cotton, mustard, rape and canola are the major domestic sources of edible oil. However, all of them are sensitive to high salinity, and their yield significantly reduces biomass production and oil content under influence of salt stress. Weber et al. (2007) analyzed six halophytes (Alhagi maurorum, Arthrocnemum indicum, Cressa cretica, Haloxylon stocksii, Suaeda fruticosa and Halopyrum mucronatum) for their edible oil-producing ability. The results revealed that except A. maurorum, all the halophytes possess about 65–74% unsaturated fatty acids, and all of them have 22–25% edible oil. A report on halophytes of Great Basin desert of North America revealed 85–90% unsaturated fractions of individual fatty acids and total lipids (Weber et al. 2001). The edible seed oil of halophytic origin is said to have comparable oil quality with that of conventional edible oils like olive, canola, etc. (Declercq and Daun 1998). The interesting point to consider is that under the influence of salt, halophytes like D. sophia contain high amount of linolenic acid as compared to non-saline conditions (Yajun et al. 2003). Similarly, there are several examples of halophytes which can grow in highly saline areas and produce high amount of edible oil, for example, Zygophyllum album, Kosteletzkya virginica, Chenopodium glaucum, Crithmum maritimum and Salicornia bigelovii (He et al. 2003; Yajun et al. 2003). Weber et al. (2007) reported that the unsaturated fatty acids (USFA) from S. fruticosa, S. stocksii, C. cretica, A. maurorum and A. macrostachyum appeared to be best from health prospective. Moreover, seeds of Salvadora persica and S. oleoides possess 40–50% fats and lauric acid which can be used in preparation of soap and candles. This oil of halophytes has potential to replace/substitute coconut oil (Weber et al. 2007).

10.2.4 Biofuel

The sources of petroleum are exhausting rapidly, and by middle of this century, 50% of it will be depleted (Debez et al. 2017). In addition, reduction in arable land due to increase in soil salinization and depletion of fresh water resources are posing threat to crop production (Sharma et al. 2016). Production of biofuels can be mitigated by plant feedstock if we succeed to identify alternate species other than conventional crops, which can grow in salinized and poor soils. It is convenient to use food crops like maize, soybean or sugarcane and non-food crops like Panicum virgatum for bioethanol production, but these crops are of good quality soil and fresh water irrigation. This created competition for resource allocation between bioenergy production and food production, which is under criticism. In this sense, halophytes can be a potential candidate because there are multiple examples of halophyte, which contain high amount of seed oils (Debez et al.). Halophytes like Desmostachya bipinnata, Halopyrum mucronatum, Panicum turgidum, Phragmites karka and Typha domingensis have potential as bioethanol-producing crops (Abideen et al. 2011). They have high growth rate and can produce high-quality lignocellulosic biomass containing 26–37% cellulose, 24–38% hemicellulose and <10% lignin required for ethanol production. Halophytes like Euphorbia tirucalli and Tamarix sp. can produce high biomass even under extreme desert conditions (Eshel et al. 2011). The T. jordanis contains high cellulose and low hemicelluloses and phenol content which is a desirable condition for ethanol production (Santi et al. 2014).

10.2.5 Medicines

During stress adaptation (both biotic and abiotic), halophytes synthesize several antioxidants and secondary metabolites. Arthrocnemum macrostachyum produces alkaloids, flavonoids, phenols and tannins for stress management. However, these compounds have strong antioxidant activities and can be utilized in medicines (Custodio et al. 2012). Some halophytes like Sesuvium produce 20-hydroxyecdysone (20E), an insect-moulting hormone which protects the plant from different biotic factors. This 20E is also used in sericulture industry to enhance moulting process of silkworms (Nikalje et al. 2017b). There are several examples, to show that halophytes are rich source of secondary metabolites and novel bioactive compounds that are essential to uplift of pharmaceutical industries and improve socioeconomic status of local peoples. Ethnobotanical studies on coastal halophytes revealed 50 halophytes with several medicinal properties (Qasim et al. 2010). Cressa cretica is used in traditional medicine of the skin, stomach, leprosy, asthma and urine-related problems (Shahani and Memon 1988). Halophytes are reported as effective against several diseases. For example, Achillea millefolium, Portulaca quadrifida and Solanum surattense for cold, flu and cough; Salsola imbricate and Zygophyllum propinquum for vermifuge; Juncus rigidus and Zaleya pentandra for stomach ailments; and Solanum surattense and Artemisia scoparia for pain relieving, etc. The saponins isolated from Acanthus ilicifolius and alkaloid from Atriplex vesicaria possess antileukemic and bactericidal activity (Kokpol et al. 1984). Ipomoea pes-caprae exhibits anti-inflammatory activity, and in Thailand it is used as a traditional medicinal plant for the treatment of various types of inflammation including jellyfish sting and dermatitis. For skin disorder, the fruits of the large glabrous shrub Lumnitzera racemosa are curative according to the folk medicines. Characterized from the leaves of the plant, there are 3 of the 11 hydrolysable tannins, and chemicals characterized from the Chinese tallow Sapium sebiferum possess hypertensive activity.

10.2.6 Ornamentals and Landscaping

The floriculture and landscaping industries have high demand in market, and their success is dependent on new and attractive plants (Zaccai 2002). The conventional ornamental plants require high-quality water, nutrient supply and extensive care to maintain their proper growth and external appearance (Shillo et al. 2002). In some studies, attempts were made to irrigate ornamentals with low-quality brackish water, but the plants show reduced quality of flowers and adverse effect on growth (reviewed by Cassaniti et al. 2013). In this sense, utilization of salt-affected soil for ornamental and landscaping by halophytic plants is a viable solution. Some halophytes that accumulate high amount of salt may contain anti-nutritional compounds and hence not suitable for food/fodder purpose. However, these can possess unique morphology and beautiful flowers like Aster tripolium. About 13 families with 42 species with ornamental potential recorded from Mediterranean region (Cassaniti and Romano 2011). The subspecies of Aster tripolium, Pannonicus, is unsuitable for consumption because of its bitter test. It has distinct and attractive morphology, which makes it suitable for cultivation as flowering pots and cut flowers (Sagi and Erdei 2002). A facultative halophyte, Sesuvium portulacastrum, is a salt-, drought-, heavy metal-, toxic dyes-tolerant plant and recommended for biosaline agriculture (Nikalje et al. 2017b). It has conspicuous, attractive, tiny flowers; its colour varies from pink, purple and rarely white (Lokhande et al. 2013) dependant on locality. It blooms throughout the year and has the potential to utilize in landscaping as ornamental plant. The Crithmum maritimum possess 30-cm-long, umbrella-like inflorescence which can be utilized in rock gardens (Ben Hamed et al. 2005). Its flowers and succulent leaves both have aesthetic value. Like wise, Mesembryanthemum crystallinum (ornamental ground cover), Inula crithmoides (yellow flowers) and Salicornia (ornamental) are potential candidates for landscaping and floriculture (Jessop 1986; Zurayk and Baalbaki 1996).

10.3 Environmental Cleanup Potential of Halophytes

10.3.1 Phytoremediation

Halophytes are characterized by their ability to survive and complete their life cycle in highly saline soils. Such saline soils are rich in toxic sodium and chloride ions. The adaptation mechanism of halophytes may not be exclusive to these two ions only. The habitat of halophytes is often contaminated with other toxic metal ions. Therefore, halophytes must have developed strategies to combat with toxic metals like arsenic, cadmium, chromium, lead, zinc, copper, manganese, etc. Halophytes like Sesuvium, Atriplex and Salicornia have shown their ability to accumulate such heavy metals (Nikalje and Suprasanna 2018). These characteristics make some halophytes suitable candidates for phytoremediation of toxic compounds. Some of the metal hyper-accumulating halophytes include, Avicennia alba (250 mg ml−1 Pb), Rhizophora mucronata (500 mg ml−1 Zn) and Kandelia candel (400 mg kg−1 Cu and Zn) which show high metal tolerance (Chiu et al. 1995). All these halophytes have their own strategy to combat with toxic metal ions. Halophytes like Avicennia sp. tend to restrict metal ions in roots (Peters et al. 1997), while Sesuvium portulacastrum sequester metal ions in vacuoles or leaves (Nikalje and Suprasanna 2018). Therefore, depending on the adaptation mechanism, potential candidate for phytoremediation can be utilized.

10.3.2 Phytodesalination

Halophytes are said to be wonders of saline soil because they live in such condition where other plants cannot survive. The toxic salt ions are inimical to plant growth and development, but halophytes cleverly utilize these ions (especially Na+) as cheap source of osmolytes and get benefited. Three strategies of salt adaptation have been proposed: the first is salt exclusion where halophytes like Rhizophora sp. exclude excessive salt ions from roots; second is salt excretions where halophytes readily absorb salt ions from root zone and excrete from leaves with the help of specialized salt glands, e.g. Avicennia; and the third one is salt accumulation, in this halophyte rapidly absorbs salt ions and sequesters them in to vacuole, e.g. Sesuvium portulacastrum. Based on severity of the salt-affected soil, for stabilization, salt excluders can be utilized, and salt accumulators will be helpful for reclamation. Apart from these properties, halophyte having high salt tolerance and high biomass production high nutritional properties and value-added products will be desirable (Nikalje et al. 2017b). Halophytes like Sesuvium portulacastrum (474 kg ha−1 NaCl; Ravindran et al. 2007), S. maritima (504 kg ha−1 NaCl; Ravindran et al. 2007) and Portulaca oleracea (3948 kg ha−1 Na, Hamidovet et al. 2007) are the representative examples of potential candidates for desalination. However, still utilization of halophytes for amelioration of saline soil is at primitive stage. There is need to screen more halophytes and their cultivation in saline and degraded soils for reclamation purpose.

10.3.3 Other Economic Benefits

Halophytes grows in tidal, coastal swamps and are referred as mangrove plants. They provide forest products like charcoal, firewood, timber, honey and fishery products. Halophytes like Avicennia are a good source of cheap and nutritive fodder for animals (Vannucci 2004). In addition, these plant extracts have medicinal value. Kathiresan (2000) has reported that extract of Bruguiera leaves is used to reduce blood pressure and Excoecaria agallocha to cure leprosy, epilepsy, etc. (Table 10.1). It also provides seeds for fishery industries. In West Bengal, Sundarban mangroves yield 540 millions of seeds of Penaeus monodon (Chaudhuri and Choudhury 1994). These plants have role in protection of coastal region from UV-B radiation, sea level rise, coastal erosion, fury of cyclones, wave action and greenhouse effect (Kathiresan 2012).

10.4 Conclusion and Future Prospects

Among various abiotic stresses, increasing soil salinity is the major threat to agricultural production. To overcome these issues, different biotechnological tools are applied to make tolerant and high-yielding crop varieties. The transgenic lines developed using biotechnology approaches are yet to occupy market place to mitigate the increasing food demand. For the past few decades, a novel concept of “Biosaline Agriculture” has been emerging. In this, different halophytes (salt-tolerant plants) are cultivated using saline/brackish water irrigation as substitute for conventional crop plants. In this way, three major issues can be solved: First, saline/brackish water will be used for biosaline agriculture, and good quality water could be diverted to human consumption and irrigation of high-yielding glycophytic crops. Second, the halophyte can be used as food (vegetable, edible oil), fodder/forage, biofuel, medicines, ornamentals and landscaping. Third, the nonedible halophytes can be utilized in environmental cleanup such as phytoremediation of toxic metals, textile dyes, etc.; phytodesalination of salt-affected soils; and ecological balance. Having natural tolerance to different biotic and abiotic stresses, halophytes can survive and flourish in adverse conditions without yield penalty. These multipurpose plants need to be screened for their products and potential use in environmental cleanup. Domestication of these plants with multiple uses may be prioritized to become an alternative to conventional crops. In the years to come, bio-saline agriculture will surely hold a great promise to supplement sustainable agriculture practices.