Major halophytic species and other saline vegetation spread across different ecological zones of India.
\r\n\t
\r\n\tOver the years, several models and theories have been developed, with the aim of explaining the recondite nature of crime: from unifactorial to multifactorial, passing through deterministic "cause-effect" theories, up to the present day, where neuroscientific approaches are becoming increasingly popular. In this perspective, knowledge in the domain of forensic psychopathology - in relation to the assessment of imputability and social danger - become fundamental and require taking into account the innovative perspective of clinical neuropsychology.
\r\n\t
\r\n\tThis book aims to provide the reader with a complete overview of the current state of the art in the criminological context (from a legal, sociocultural, psychological, and medical point of view), paying particular attention to the most important evidence-based developments in this area.
Oxidative stress can be defined as a disturbance in the balance between the production of reactive oxygen species and antioxidant defenses [1]. Reactive oxygen species (ROS) are free radicals, which are important for the cellular functions generated in different biological processes. A free radical is unstable and highly reactive and contains one or more unpaired electrons. These free radicals are involved in the regulation of various mechanisms and intercellular signaling and act as bactericidal agents [2]. ROS can also induce cellular senescence, apoptosis, and cell growth regulatory pathways [3]. ROS are generated as a by-product of the aerobic respiration where the superoxide anion (O2−) and H2O2 are formed when molecular oxygen chemically oxidizes electron carriers. Cellular sources of ROS are produced by the action of different oxidative enzymes, which include plasma membrane nicotinamide adenine dinucleotide phosphate (NADPH) oxidase, intracellular cytosolic xanthine oxidase, peroxisomal oxidases, endoplasmic reticular oxidases, and mitochondrial electron transport components [4]. Apart from this, auto-oxidation of catecholamines, ubihydroquinone, hemoproteins, and flavin enzymes also produces ROS [5]. In response to nutrient stress, cells enter autophagy that can lead to adaptation or death. Starvation-induced autophagy results in reactive oxygen species (ROS) production, DNA damage, and PARP-1 activation, leading to the inhibition of mTOR.
\nIn all these cases, the generation of free radicals is implied.
\nReactive oxygen species are naturally produced in all cells and organisms. Modifications of normal conditions alter reactive species generation and may result in oxidative stress. In this chapter, we have discussed the role of the most important causes of the ROS generation in the invertebrate systems.
\nInsects like mosquitoes which feed on human blood face severe oxidative stress due to the release of iron from hemoglobin which in turn can potentially induce oxidative damage and eventually death [6]. To face such odd situation, blood-feeding insects evolved with strong defense mechanisms against the stress. Mosquitoes protect themselves by secretion of the peritrophic matrix (PM) [7] in the midgut which is made up of chitin and a protein-containing layer. It also has a role in protecting the insect from invasive pathogens [8]. The direct contact of the gut epithelium with intermediates of hemoglobin digestion induces oxidative stress in sand fly and Aedes aegypti [9].
\nA source of ROS in the honeybee is the microsomal oxidation of xenobiotics. Microsomes contain enzymes of cytochrome P450 (CYP) system, which catalyzes polyvalent oxidation of xenobiotics with simultaneous generation of O2− and other ROS. The CYP hydroxylase system includes flavoproteins and a family of hemoproteins which are localized on the membranes of the endoplasmic reticulum. Different isoforms of CYP are involved in metabolism of various xenobiotics [10, 11]. CYP groups are distinguished based on the metabolism of endogenous and exogenous substances. Microsomal glutathione S-transferase (GST) is closely linked with the CYP system, which contributes to rapid inactivation of active metabolites produced during the metabolism of xenobiotics.
\nIn the insect nervous system, ROS-mediated decline of neuron survival can be observed. The dopamine-producing neurons show the highest sensitivity to oxidative stress as the dopamine production machinery is linked to an endogenous production of high amounts of ROS, thus making these cells prone to damages caused by ROS. These high levels of ROS lead to the development of Parkinson’s disease-like phenotypes [12]. It is a suitable mechanism to induce neurodegenerative processes using ROS as typically seen in Parkinson’s disease. One of the most reproducible ways to do this is through hyperoxia, which consequently is able to induce these phenotypes enabled Drosophila as a model for Parkinson’s disease [13]. In an Alzheimer’s disease model, based on tau activation in the nervous system, ROS has been shown to modulate the sensitivity, thus demonstrating that oxidative stress plays a major role in the development of Alzheimer’s disease.
\nThe intestinal microbiome is one of the densest populations on earth. Thus, attaining a homeostatic balance between fight against potential pathogens and maintenance of the microbial community within the intestinal tract is a major challenge for the gut immune system [14]. Fighting pathogens is achieved via enzymes producing ROS. Dual oxidase (DUOX) is a member of nicotinamide adenine dinucleotide phosphate oxidase (NADPH oxidase) family and the most important enzyme secreted from enterocytes in response to pathogen contact [11, 15]. It is independent of classical immune response pathways such as the Toll [16] or the IMD pathway [17]. The killing mechanism of DUOX comprises the production of H2O2, which is a typical feature of DUOX enzymes in general [18]. The fly phenol oxidases (POs) are another enzyme set that produces a melanin coat surrounding invaders of different nature. These enzymes are able to produce a locally high concentration of ROS, which may be one of the major effectors of the prophenoloxidase (PPO) system. This melatonin production is triggered by the recognition of bacterial patterns including peptidoglycans [19].
\nAirway infection is one of the well-studied areas in fruit fly [20]. In addition to classical aspects of an antibacterial response including antimicrobial peptide genes, some of these enzymatic antioxidants are strongly upregulated. The antioxidant system of the airway epithelium contains both producers of ROS and protectors against them.
\nMotile cells of the innate immune system use production of highly effective ROS which is a versatile method to fight pathogens. The oxidative burst produced by macrophages is the most impressive example highlighting this strategy. Reactive oxygen species (ROS) is generated by many phagocytic cells in response to membrane perturbations such as receptor-ligand interactions and phagocytosis [16, 21], which defend these cells against infectious diseases by virtue of their antimicrobial properties. Initially, superoxide anion (O2−) is produced which is spontaneously or enzymatically converted to hydrogen peroxide (H2O2), subsequently giving rise to even more toxic products, such as hydroxyl radical (•OH), hypochlorous acid (HOCI), and singlet oxygen (IO2). ROS are either directly toxic or exert increased antimicrobial activity in synergism with lysosomal hydrolases and/or reactive nitrogen species (RNS), plasma membrane-bound enzyme complexes, and the NADPH oxidase (NOX) system [22].
\n\nLeishmania parasite manages both to survive and proliferate within the mature phagolysosomal compartment of the macrophages [21]. Trypanosomatids do not express essential antioxidant enzymes like catalase and selenium-containing glutathione (GSH) peroxidases [23]. Defense system of the Leishmania parasite contains several mechanisms, which include trypanothione (N1, N8-bis(glutathionyl)spermidine adduct) [24, 25]. It is the primary thiol in these parasites and adopts the metabolic role of glutathione. Along with this, ovothiol A acts as a nonenzymatic scavenger of H2O2 though it is much less efficient than trypanothione [26]. Trypanothione reductase (TR) is a member of the disulfide reductase family, which is the enzyme responsible for maintaining trypanothione in its reduced form [27]. Tryparedoxin peroxidases or peroxiredoxins are a family of peroxidases that reduce H2O2 and alkyl hydroperoxides to water and alcohol, respectively, with the use of reducing equivalents provided by thiol-containing proteins [28]. The enzyme arginase is a part of the host as well as parasite defense. Phagocytosis of promastigotes leads toward the two opposing forms of classical and alternative activation of host macrophages which results in differential
Parasites can inhibit the activation of several inflammatory cytokines like interleukin-12 (involved in T-cell activation), interferon gamma, interleukin-1, and tumor necrosis factor-alpha that strengthens parasite survival. Few species induce heterologous population of host inflammatory cells, such as neutrophils and monocytes/macrophages, which are effective in controlling/clearing infections. The T helper cell type 1 (Th1) response as a result decreased expression of induced nitric oxide synthase and reduced activity of NK cells [32].
\nSelenocysteine is analogous to a cysteine residue but has sulfur substituted by selenium. Selenoprotein families, some with antioxidant properties, such as glutathione peroxidase (GPx) and thioredoxin glutathione reductase (TGR) appear to be essential in flatworms and in Plasmodium falciparum and other Plasmodium species [33, 34].
\nAscorbate peroxidase is another antioxidant, which is a heme peroxidase identified in the inner mitochondrial membrane of the Leishmania parasite. Overexpression of this enzyme confers tolerance to oxidative stress-mediated cardiolipin oxidation and thus protects the parasites from extensive protein damage. Leishmania promastigotes inhibit phagolysosome biogenesis via lipophosphoglycan (LPG), which causes periphagosomal accumulation of F-actin and impaired assembly of nicotinamide adenine dinucleotide phosphate (NADPH) oxidase complex and exclusion of vesicular proton ATPase from phagosomes [35].
\nThe major task of airway epithelial cells is enabling an effective oxygen transport and exchange. These cells react to different stimuli with appropriate responses including massive responses if pathogens are experienced. In principal, all oxygen transport systems are prone to damage caused by high oxidative stress because these cells have direct contact with the air and large volumes of air pass over their surface during the process of gas exchange.
\nEnvironment has a major role in the production of stress because of different pollutants like air, soil, and water. The compounds used in industry and agriculture include metals, metalloids, and numerous other organic compounds. Majority of these compounds have been shown to induce oxidative stress by generating ROS in nontarget species including invertebrates [36].
\nPlant phenolic compounds, such as flavonoids and tannins, which are involved in plant defense mechanism, can produce free radical in herbivorous insects [37]. The midgut of insect is a highly oxidizing environment. Hence in lepidopteran larvae, Helicoverpa zea and Spodoptera littoralis with phenolic acids were found to increase various indicators of oxidative stress in gut tissues [38, 39]. Additionally, furanocoumarins in some plants and herbicides like paraquat are well known to generate oxidative stress in insect species [36]. Insect growth regulator (IGR) is a substance (chemical) that inhibits the life cycle of an insect and has been used to control the insect pests. Hormonal IGRs typically work by mimicking or inhibiting the juvenile hormone (JH) or ecdysone. Studies on the IGRs like Applaud (buprofezin) as a chitin synthesis inhibitor and Admiral (pyriproxyfen) as juvenile hormone analog (JHA) in the larval body of the cotton leaf worm, S. littoralis, resulted in the occurrence of lipid peroxidation in the larval tissues which enhanced different antioxidant defensive systems to overcome its effect like malondialdehyde (MDA) and glutathione reduction [40].
\n\nDisruption of metal ion homeostasis may lead to oxidative stress, a state where increased formation of reactive oxygen species (ROS) overwhelms body antioxidant protection and subsequently induces symptoms for numerous diseases, involving cancer, cardiovascular disease, diabetes, atherosclerosis, neurological disorders (Alzheimer’s disease, Parkinson’s disease), chronic inflammation, and others [41].
\n\nMetals, such as iron (Fe), copper (Cu), chromium (Cr), and cobalt (Co), induce the formation of the superoxide and hydroxyl radicals (mainly through Fenton reaction) and other ROS, which ultimately leads to the production of malondialdehyde (MDA), 4-hydroxynonenal (HNE), and other exocyclic DNA adducts that are carcinogenic and mutagenic. On the other hand, the redox-inactive metals, such as cadmium (Cd), arsenic (As), and lead (Pb), induce toxicity through bonding to sulphydryl groups of proteins and depletion of glutathione. Zinc (Zn) is a redox-inert metal, which is an essential component of numerous proteins involved in the defense against oxidative stress. In addition, Zn possesses neuroprotective properties. Depletion of Zn may enhance DNA damage through impairments of DNA repair mechanisms. Cellular antioxidants (ascorbic acid (vitamin C), alpha-tocopherol (vitamin E), glutathione (GSH), carotenoids, flavonoids, and other antioxidants) and chelate metal ions reduce their catalytic activity to form ROS. A novel therapeutic approach to suppress oxidative stress is based on the development of dual function antioxidants which comprise of chelating and scavenging agents [39, 40].
\n\nOxidative stress is highly prevalent in marine invertebrates, particularly bivalve mollusks, due to the degradation of marine ecosystems, massive aquaculture productions, climate change, and pathogenic infections. Mollusk hemocytes produce ROS and RNS as part of their basal metabolism as well as in response to both endogenous and exogenous stimuli. However, sources, pathways, and mechanistic aspects of these reactive species production are currently poorly deciphered. Unique pathways seem to exist in marine bivalves [42].
\n\nHigh oxygen solubility in cold water is responsible for an elevated level of antioxidant protection in marine ectotherms from polar environments. However, tissue oxidative stress is a function of elevated or variable pO2, rather than of an elevated tissue oxygen level [43].
\nTo counteract or to regulate the free radical production, several antioxidant mechanisms were evolved (Figure 1) [44].
\nSchematic representation of the pathways activated by the oxidative stress on macromolecules like lipids and carbohydrates leads to the signal transduction through ROS-dependent and ROS-independent mechanisms. Glyoxal and methylglyoxal formed by the oxidation of the carbohydrates were detected by the AGE and activate cell surface molecule RAGE. It passes signal to NADPH oxidase through PKC, which activates the ROS. ROS activates several transcription factors such as AP-1; NF-kB: pro-inflammatory cytokines; Nrf2: detoxifying genes; HSF1: Hsp expression; and FOXO1: inhibition of B-cell proliferation. It also inhibits the PDX1 transcription factor which activates insulin gene expression and B-cell proliferation. In ROS-independent pathway, AGE can directly activate FOXO1 and inhibits PDX1. In lipid peroxidation, 4-hydroxynonenal (HNE) and acrolein-mediated signaling activate AP-1 through c-Jun and Nrf2. It blocks NF-kB–mediated transcription activation apart from the ROS-activated signaling.
Oxidative stress arises when there is a marked imbalance between the production and removal of reactive oxygen and nitrogen species. Free radical production is normally controlled by the antioxidant defense mechanisms [2]. Antioxidative defenses could essentially be divided broadly into two main mechanisms: one is enzymatic and the other is nonenzymatic.
\nInsects, like other animals, possess a suite of enzymes that are directed toward the removal of various radicals [45–48]. These include superoxide dismutase present in cytosol and mitochondria, catalase present in peroxisomes, ascorbate peroxidase [49], glutathione S-transferase peroxidase, thioredoxin/thioreductase system [50], and so on.
\nIn addition to the classical antioxidant enzyme systems, a number of small molecules also play a significant role in scavenging ROS, and some of these small molecules are plant derived, whereas others such as carotenoids, α-tocopherol, ascorbic acid, and glutathione (GSH) can be synthesized by insects [45, 50–52].
\nIn addition to the antioxidant mechanisms and systems described above, insects also possess several water-soluble molecules (uric acid, carbohydrates, and polyols) and iron-binding proteins (ferritin and transferrin) that serve crucial antioxidant functions [45]. Antioxidant properties of vitellogenin are specified by its Zn-binding capacity [53] and preferential oxidative carboxylation under oxidative stress in honeybees [54]. With respect to these properties, vitellogenin is compared to Cu/ZnSOD, a key metal-binding antioxidant enzyme that undergoes preferential carbonylation [55], and serum albumin, a metal-binding protein, that can function as free radical acceptors and reduce oxidative marker levels such as protein carbonylation [56].
\nResponses to oxidative stress induced by a blood meal were investigated in A. aegypti [7]. In female mosquitoes, higher levels of ferritin were observed after repeated blood meals. Ferritin is a sensitive defense mechanism against oxidative stress induced by blood meal [57]. An increase of secreted ferritin due to the induced synthesis of ferritin heavy chain homologue (HCH) was observed [58].
\nOxidative stress triggers a range of responses in insect cells which could be physiological, pathological, and adaptive. A large number of signaling pathways are involved in response to oxidative stress. Drosophila melanogaster is a well-studied organism in the field of oxidative stress. Among these signaling pathways, in fruit fly, PI3-kinase pathway is one of the important responses to oxidative stress by activating the transcription factor FOXO [13], and an alternative signaling is represented by the Nrf2/Keap1 pathway which is required for a proper and efficient expression of genes associated with an increase in oxidative stress resistance [41]. Other signaling systems include activator protein-1 (AP-1), nuclear factor-kB (NF-kB), protein kinase C (PKC), protein 53 (p53), and redox regulation by redox factor-1 and the nuclear factor erythroid 2–related factor 2 (Nrf2)-mediated antioxidant response. Nrf2 belongs to a group of specialized transcription factors termed xenobiotic-activated receptors (XARs). These recognize specific xenobiotics and coordinate the transcription of batteries of genes.
\nHoneybees possess only about half the genes of GST, CYP, and carboxyl/cholinesterases as in other insects [17–19]. This deficit can contribute to insufficient resistance to oxidative stress caused by incomplete microsomal oxidation of xenobiotics [59]. These insects have more genes of class sigma GST [60], which has a high affinity to the products of lipid peroxidation localized in the thorax muscle of flies to protect these tissues against oxidative stress by-products [61].
\nThe idea behind one of the first theories of aging was oxidative stress-induced damage [42]. Enzymes which regulate the oxidative stress are responsible for the longevity that was supported by shortened life span in flies lacking a functional thioredoxin-2 [60]. Peroxiredoxin of type 2, named Jafrac1 [61], and other peroxiredoxins, especially those present in mitochondria, are also relevant for life span, as their downregulation has a significant impact on this aspect of life [62] along with other enzymes like glutathione reductase [63], SODs, and catalase [64–66].
\nIntriguingly, genes belonging to the family of antimicrobial peptide genes are obviously relevant for this adaptation to extreme oxygen concentrations and therewith to higher levels of oxidative stress [67, 68]. In insects, compared to vertebrates, genes encoding glutathione reductase (GR) and glutathione peroxidase (GPX) are absent. Their functions are performed by homologous genes that encode thioredoxin reductase (TrxR) [52] and thioredoxin peroxidase (TPx) [67]. In addition, insects’ genes encode enzymes of antioxidant defense that act as peroxidases: phospholipid-hydroperoxide GPx homologues with TPx activity (GTPx) [69] and GST [70, 71]. Thus, the secondary antioxidant enzymes in insects that act on ROS indirectly include TrxR, which converts both Trx and GSH, and methionine sulfoxide reductases (MsrA and MsrB), which are involved in protein repair by catalyzing the Trx-dependent conversion of methionine sulfoxide to methionine [72, 73].
\nIn the nervous system, the dopamine metabolism produces high ROS concentration leading to the SOD overexpression. Increase in the glutathione S-transferase activity in the nervous system protects these dopaminergic neurons [74]. However, this ROS-based mechanism of neurodegenerative diseases is not applicable for Huntington’s disease. Neither overexpression of enzymatic antioxidants nor supplementation with nonenzymatic antioxidants decreased the lethality in this model [61].
\nThe intestinal microbiome regulation DUOX plays a crucial role with killing mechanism by production of H2O2 [31]. To protect the gut tissue from the action of ROS, an enzymatic antioxidant, immune-regulated catalase (IRC), is produced [29].
\nPrevious microarray studies in Drosophila suggested that IRC is the only catalase to be induced upon infection and may be regulated by the Toll pathway. The IMD pathway could be another candidate for regulation of antioxidants including IRC, since it is induced systemically by Gram-negative bacteria and in turn activates the JNK pathway.
\nMalpighian tubules also perform crucial roles in stress sensing and response [75]. At molecular level, multiple cell-specific signaling pathways including cAMP, cGMP, and calcium modulate the tissue and, hence, organism responds to various stress, such as detoxification and xenobiotic handling, and stress sensing of oxidative, osmotic (ionic/salt) and immune challenges [76–78].
\nIn the regulation of intestinal microbiome, apart from the ROS-induced OS regulation of pathogens, ROS production induces a JNK-triggered autophagy in the enterocytes in D. melanogaster [59].
\nMotile cells of the innate immune system use oxidative burst to control invading pathogens. Apart from that, ROS play an important role in the differentiation of hemocytes. In Drosophila, multipotent hematopoietic progenitors react to different ROS levels with a speeding up or arresting of their differentiation [79]. Both the JNK and the FOXO pathways are involved in the transduction of ROS levels into developmental signals [80].
\nThe insect endocrine system produces three main groups of hormones [81] including (a) ecdysteroids, (b) juvenile hormones (JHs), and (c) neurohormones. Out of these, a group of neurohormones belonging to the AKH/RPCH family (adipokinetic hormone/red pigment-concentrating hormone family) is associated with stress responses [82, 83]. Recently, it has been found that AKHs are also involved in the control of oxidative stress (OS) in insects [79]. The balance between the OS and its control by AKHs was attained by feedback regulation between an oxidative stressor and AKH actions. The effect is reported for paraquat [84, 85], Galanthus nivalis agglutinin and Bacillus thuringiensis toxin [84] and also for endosulfan and malathion [86] insecticides with an OS effect. Reports are available for the elevation of AKH in stress other than OS [53–56]. It was suggested that the activation of protective antioxidative mechanisms is derived from the effect of oxidative stressors on AKH level in the insect body.
\nNot only have AKHs been implicated to be involved in hormonal control of antioxidative protective reactions in insects, but other hormones such as glucagon, ecdysteroids, and JHs have also been suggested to be involved in antioxidative protective mechanisms. Analogous to vertebrates [87–89], it was suggested for insects that glucagon could play a role in defense against OS. Ecdysteroids were shown to be involved in the control of OS by inhibiting the oxidation of cholesterol and the peroxidation of polyunsaturated fatty acids in the lipoproteins, microsomes, and other components of biological systems [90].
\nIn D. melanogaster, ecdysone-induced methionine sulfoxide reductase A enhances resistance to hydrogen peroxide [91]. It also regulates the methionine sulfoxide reductase [92, 93] enzyme expression via the ecdysone receptor (EcR-UPS) complex [54]. Treatment with insect 20E protected mammals against cerebral ischemia injury by inhibiting production of ROS/RNS and modulating OS-induced signal transduction pathways. Treatment of B35 rat neuroblastoma cells with hydrogen peroxide led to OS-induced apoptosis, mitochondrial membrane potential dissipation, neuronal injury, generation of intracellular ROS/RNS, decrease of cellular antioxidant potential, and increase of lipid peroxidation, all of which were significantly eliminated by 20E [54, 94–97].
\nJHs are synthesized and secreted in/from the corpora allata in the insect brain. Recent studies have implicated that lack of JH may confer resistance to OS. The elimination of JH synthesis extended the survival of flies exposed to hydrogen peroxide. The survival times returned to those in control when the knockout flies were treated with JH analog methoprene. Moreover, another JH analog, pyriproxyfen, induced OS in the wax moth Galleria mellonella, as the antioxidative enzyme activities, CAT and SOD, increased after the pyriproxyfen application. Similarly, pyriproxyfen increased the activity of enzymes CAT and GST, as well as the accumulation of MDA and GSH, in larvae of S. littoralis. JHs are also involved in the control of antioxidative reactions albeit indirectly via the regulation of vitellogenin and transferrin synthesis [54, 94–97].
\nThis chapter summarizes current knowledge on pro- and antioxidant processes in invertebrates particularly insects. Reactive oxygen species (ROS) formation and their adaptations in different organisms were discussed in the context of the usage of invertebrates as a model organism in the field of OS to study the OS-mediated diseases in humans.
\nFood security and ecological security are the two pillars of all societies. The incessant growth of human population across the world is evident from the United Nations projection of 9.7 billion people by 2050 [1]. The global food demand is expected to rise by 70–100% and to meet this additional food demand, a predicted 50% increase in yields of the major food crops will be required [2]. Moreover, our global food security is significantly affected by drastic alterations in the climate [3]. This unpredictable change in climate has resulted in to several abiotic stresses such as salinity, drought, heat and low temperature, threatening the agricultural sustenance and productivity [4]. This has also brought about a significant spike in the occurrences of extreme climatic events like flood, cyclones, storms etc. [5]. Land degradation is one of the severe consequences of global climate change and it is happening at a viciously alarming pace because of other reasons too, like vegetation loss, soil erosion, inadequate water management, excessive use of fertilizers, soil and groundwater degradation, urbanization and poor agricultural practices [6]. One of the major causes of land degradation is buildup of soil salinity as a result of natural and anthropogenic factors [7, 8]. It is estimated that agricultural soils are decreasing about 1–2% every year especially in the arid and semiarid regions of the world due to soil salinity [9].
On an average, 831 million hectares (Mha) of global soil is affected by salt (397 and 434 Mha of saline and sodic soils, respectively) which is more than 6% of the world’s total land area [10]. Out of total irrigated land (230 Mha), almost 20% (45 Mha) area has already been damaged by excess soil salinity [11], whereas 14% (32 Mha) is affected by varying degrees of salt [12]. In India, the total land degraded due to soil salinity and sodicity is estimated to be 6.74 Mha [13] and it is likely to increase to 16.2 Mha by 2050 [14]. Soil salinization is grouped in to two typesviz. Primary salinization and secondary salinization. Primary salinization occurs due to the existence of subsoil salts and by other natural processes like weathering of parent material, deposition of sea salt carried by wind and rain, inundation of coastal land by tidal water, etc. Secondary salinization is a consequence of anthropogenic or human induced activities like excessive irrigation, irrigation with salt containing water, poor drainage due to loss of natural water passages, unscientific application of inorganic fertilizers and other soil amendments [14, 15].
The arid and semiarid regions of India along with our coastal zones are economically fragile regions and need much closer attention. Low rainfall and high temperature are two specific features of the arid and semiarid regions of India which are highly conducive to excessive soil salinity [16]. India has a coastline of 7516.6 km viz. 5422.6 km of mainland coastline and 1197 km of Indian islands spread across 9 Indian states and two Union Territories [17]. Soil salinity is estimated to have affected 1.25 Mha soils in these coastal tracts of the nation [13]. The predicted rise in sea level of 1 m due to global warming may aggravate this problem to take on serious dimensions in future [14]. Moreover, there is a predicted increase in water demand by 45% in coastal areas by 2050, which will inevitably result in increased ground water depletion and induce more and more soil salinity [14]. Altogether, in both these ecological zones of the nation, soil salinity has become an important factor limiting the growth of major crops and even some halophytes [18].
Moreover, factors like global climate change, diversion of more and more productive agricultural land towards other nonagricultural purposes as a part of rapid urbanization and the alarming rate of decline in soil organic carbon will lead to further increase in soil salinity [19, 20, 21, 22, 23, 24]. So we are running out of options, and the only option left is to bring these saline, sodic and other barren land in to cultivation to meet the growing food demand and more importantly to address the growing climatic and ecological concerns. Major agricultural crops and tress cannot be grown in such soils as they exhibit a low tolerance to salt [25]. So future agricultural production in these saline soils should be based on salt tolerant crops which are edible and/or of economic and ecological significance [26, 27].
Halophytes, salt mangroves, and other salt tolerant plants and trees are the options which can grow and survive in extreme environments. Many halophytes have potential agricultural value and can be grown in these highly saline areas. They not only survive in these conditions, but also produce considerable biomass coupled with various other potential/economic uses in industry, feed, medicine etc. [28]. Indian mangrove vegetation covers about 6749 km2 along the 7516.6 km long coast line, including island territories. 82 species of mangroves distributed in 52 genera and 36 families have been identified that are spread across 12 habitats of India [29]. They along with many other associate species thrive well in coastal saline soils. Moreover, these saline soils can further be brought in to cultivation through agroforestry, silvipasture, nonconventional crops including medicinal and aromatic plants and other high value crops. These will not only utilize the saline barren land for economic growth but will also help significantly in conserving our biodiversity and improvement of ecological and social environment.
A systematic attempt has been made in bringing together critical aspects of saline agriculture, including major halophytes and other saline vegetation of India, its salt tolerance mechanisms coupled with ecological and economic potential of these plants. This is highly imperative for effective utilization of these saline soils leading to improved livelihood and sustenance of resource poor farmers along with improved ecological balance.
Halophytes are plants capable of completing their life cycle under highly saline conditions [30]. To be more scientifically concrete, halophytes are those plant species which can successfully survive, grow and reproduce in soils of salt concentration more than 200 mM of NaCl (Electrical conductivity of soil saturation extract (ECe) of 20 dS m−1) [31]. Some halophytes can even grow well at higher salt concentrations than that of sea water (>500 mM Nacl) [32]).As they prosper well in severely saline soils, they are also considered to be extremophiles [33]. They constitute around 1% of the global flora [15]. The question of how they survive and complete their life cycle under such extreme conditions has led to detailed studies on the various morphological, anatomical, physiological and molecular mechanisms of high salt tolerance. The tolerance of halophytes to salts varies with species and developmental stage. In general, dicot halophytes are reported to be more tolerant (optimal growth in 100–200 mM NaCl) as compared to monocot species (optimal growth in 50–100 mM NaCl) [31].
During 1980s, James Aronson compiled a comprehensive database [34] of 1554 halophyte species, and named it as HALOPH. This database has been converted into an interactive eHALOPH repository [35] that provides online details and bibliography pertaining to halophytes. Till now 2000 to 3000 halophytic plant species are identified [32] in the world mainly belonging to angiosperms. In India, their distribution is mainly confined to arid, semiarid inlands and highly saline wetlands along the tropical and sub-tropical coasts [36]. The major halophytes/saline vegetation found across the various ecological hotspots spread across the country are summarized in Table 1.
Scientific name | Common name | Family | Area of occurrence | Plant type |
---|---|---|---|---|
Aeluropus lagopoides | Mangrove grass, usargas, kharoga | Poaceae | Kachchh, Thar Desert | Tufted grass |
Atriplex hortensis | French Spinach, Pahari Paleng | Amaranthaceae | Coastal marshes Ladakh, Kashmir | Herb |
Atriplex stocksii | Khati palakh, kharo tanko | Amaranthaceae | Kachchh (Gujarat) | Bush |
Avicennia marina | Whitemangrove, tavarian, tivar | Acanthaceae | Kachchh, Kerala Maharashtra, Tamilnadu, | Mangrove |
Cenchrus biflorus | Indian sandbur, bhurut | Poaceae | Kachchh, Thar Desert | Grass |
Chenopodium album | Lamb’s quarters, bathua | Amaranthaceae | Northarn India, Kachchh | Herb |
Cressa cretica | Rudravanti, machul | Convolvulaceae | Kachchh, Thar Desert | Sub-shrub |
Cyperus conglomeratus | — | Cyperaceae | Kachchh, Thar Desert, Kerala | Herb |
Cynodon dactylon | Bermuda grass, doob | Poaceae | Throughout India | Grass |
Dactyloctenium sindicum | Tantia, ganthio | Poaceae | Kachchh | Grass |
Dichanthium annulatum | Marvel grass, karad, bansi | Poaceae | Kachchh, Thar Desert | Grass |
Halopyrum mucronatum | Dariyai kans | Poaceae | Kachchh | Grass |
Haloxylon salicornicum | Rimth saltbush, khar, lana | Amaranthaceae | Kachchh, Thar Desert | Shrub |
Heliotropium bacciferum | — | Boarginaceae | Kachchh, Southern India | Herb |
Ipomoea pes-caprae | Atampa, dopatti lata | Convolvulaceae | Kachchh | Herb |
Limonium stocksii | Kharia | Plumbaginaceae | Kachchh, North west India | Herb |
Portulaca oleracea | Common purslane, lunia, badi-noni | Portulacaceae | Maharastra, Thar desert | Herb |
Prosopis juliflora | Mesquite, vilaiti keekar | Fabaceae | Throughout India | Shrub |
Salicornia brachiata | Glasswort, umari keerai | Amaranthaceae | Kachchh, Thar desert | Herb |
Salsola baryosma | Loonuk, lani | Amaranthaceae | Kachchh, Thar desert | Shrub |
Salvadora oleoides | Bada peelu, meethi jaal | Salvadoraceae | Kachchh, Thar desert | Shrub |
Salvadora persica | Meswak, piludi, khari jaal | Kachchh, Thar desert | Shrub/Tree | |
Sesuvium portulacastrum | Sea purslane, lunio, dhapa | Aizoaceae | Kachchh, Rajasthan, | Herb |
Sporobolus marginatus | poolongi, khevai | Poaceae | Kachchh | Grass |
Suaeda fruticosa | lunaki, moras | Amaranthaceae | Kachchh, Thar desert | Shrub |
Suaeda maritima | Annual sea blite, alur | Maharastra | ||
Suaeda nudiflora | Muchole | Kachchh | ||
Tamarix dioica | Red tamarisk, lai, arseli | Tamaricaceae | Kachchh | Shrub |
Urochondra setulosus | Kkariyu | Poaceae | Kachchh | Grass |
Ziziphus nummularia | Jhar beri, chanibor | Kachchh, Thar desert | Shrub | |
Zygophyllum simplex | Bean-Caper, pat lani | Zygophyllaceae | Kachchh, Thar desert | Herb |
Major halophytic species and other saline vegetation spread across different ecological zones of India.
A summary of classification of halophytes by researchers across the globe based on different aspects is compiled and presented below.
Mio-halophytes: Plants which grows in the habitats of low salinity levels (below 0.5% NaCl) [37].
Eu-halophytes: Plants which grow in highly saline habitats. They have been further sub-divided into the following groups:
Mesohalophytes: Plants that can tolerate salinity range of 0.5 to 1%.
Mesoeuhalophytes: Plants that can tolerate salinity range of 5% and higher.
Eneuhalophytes: Plants that can tolerate salinity range of 1% and above.
Salt excluding: The root architecture of this category of plants is embraced by an ultrafiltration mechanism which leads to establishment of such species in saline conditions. Mangrove vegetation shows such type of tolerance. e.G. Rhizophora mucronata, Bruguiera gymnorrhiza [38].
Salt excreting: This category of plants release excess salts in their internal tissues to outside via. Specialized structures called as salt glands. e.g. Avicennia officinalis, Avicennia alba, Avicennia marina.
Salt accumulating: These plants are able to maintain very high levels of salt in their tissues either by virtue of succulence or by compartmentation of excess salts in to comparatively safer cellular locations like vacuole. e.g. Salvadora persica, Sesuvium portulacastrum, Suaeda nudiflora.
Obligate halophytes: They grow only in salty habitats and show satisfactory growth and development under high saline condition. Many plant species belonging to chenopodiceae family comes under this category. e.g. Salicornia bigelovii [39].
Facultative halophytes: Plants of this group are able to establish themselves on salty soils, but their optimum growth is observed in a salt free or low salt condition. Most poaceae, cyperaceae, and brassicaceae species as well as a large number of dicotyledons like Aster tripolium, Glaux maritima, Plantagomaritima belong to this group.
Habitat-indifferent halophytes: They normally grow on salt free soils but can thrive better than sensitive species under saline conditions. Plants like Chenopodium glaucum, Myosurus minimus, and Potentillaanserina are categorized as habitat insensitive plants.
Hydro-halophytes: These are halophytic plants which grow in aquatic conditions. Most of the mangroves and salt marsh species along costal lines belong to this group [40].
Xero-halophytes: They grow in environment, where the soil is saline and the soil moisture content is very low due to high evaporation. Most plant varieties in desert areas and succulents belong to this group.
There is an enormous diversity among halophytes with regard to its ecological hotspots like coastal saline soils, arid and semiarid saline and sodic soils, soils of mangrove forests, wet lands, marshy lands and even agricultural fields [15]. A picturesque view of the major halophytes and mangroves found in India is given in Figure 1.
Major halophytes and mangroves found in India. (a) Sporobolus marginatus, (b) Salicornia brachiate, (c) Chenopodium album, (d) Portulaca oleracea, (e) Heliotropium curassavicum, (f) Haloxylon salicornicum, (g) Cresa cretica, (h) Aeluropus lagopoides, (i) Prosopis juliflora, (j) Salvadora oleoides, (k) Salvodera persica, (l) Sesuvium portulacastrum, (m) Suaeda fruticosa, (n) Halopyrum mucronatum, (o) Tamarix spp, (p) Urochondra setulosa, (q) Rhizophora mucronata, (r) Heritera fomes, (s) Avicennia marina, (t) Bruguiera cylindrical, (u) Bruguiera gymnorrhiza.
Any review on halophytes/extremophiles is incomplete, without touching on the mechanisms by which these extremophiles survive under saline conditions. Indian Council of Agricultural Research- Central Soil Salinity Research Institute (ICAR-CSSRI) initiated such basic studies long back to critically understand the mechanism of salt tolerance in the local, native dry land saline vegetation [41]. This precise knowledge is highly imperative in developing other crops by a combination of improved salt tolerance and high yield. Another mandate was to document such species and, to the maximum extend, popularize them among the resource poor dry land farmers for better livelihood and sustenance.
Any plant species initially suffers from osmotic stress as a result of increased soluble salts in the soil solution and later gets subjected to ionic stress due to specific accumulation of toxic ions. The osmotic phase of salt stress is characterized by disruption of water potential gradient and there by leads to reduced water uptake and inhibition of cell expansion [42]. Most plant species tries to adapt to this osmotic stress by accumulation of compatible solutes and thereby lowering water potential of cells, but this process consumes lot of energy and hence growth is heavily compromised.
Another major deleterious effect of salt stress is nutrient imbalance where in which high Na+ ions in the soil solution reduces the availability of other cations like K+ Ca++ and Mg++ [43]. This second phase of salt induced injury (specific ion toxicity) results from very high levels of Na+ and Cl− in the plant cells. In normal soils, plants maintain around 100–200 mM of K+ and 1–10 mM of Na+ in cellular cytosol for optimum cellular functions. Any salt concentration above this threshold level disrupts enzyme activity, protein synthesis, photosynthesis and other metabolic activities [44]. The light reactions of photosynthesis are comparatively less affected by salt stress as compared to the carboxylation reactions. A summary of salinity mediated effects and responses of plant cells are presented in Table 2.
Causes | Effect | Response/adaptation |
---|---|---|
Osmotic stress | Reduced water uptake, inhibition of cell elongation and expansion and leaf bud development | Compatible solute accumulation (ions/organic compounds) |
Ion specific stress (high levels of Na and Cl in plant cell) | Inhibition of enzyme activity, protein synthesis, photosynthesis and leaf senescence and necrosis | Ion homeostasis through ion accumulation or ion exclusion |
Imbalanced ion uptake | Nutritional deficiencies, reduced availability of other cations like K, Ca and Mg | Ion reabsorption |
The cell membrane permeability, composition and integrity gets affected as excess Na+ replaces Ca2+ from its surface [46]. A lot of salt tolerant crop varieties have been developed by various research institutes which can survive up to moderate levels of salt stress. Under these circumstances, it is highly imperative to identify and propagate halophytic species in the arid and semiarid, high salt affected regions of the country, so that the vast tract of unproductive land can be put to cultivation for realization of sustainable income to resource poor farmers.
Halophytes and glycophytes have similar components in the stress tolerance network, but certain additional characteristics help these halophytes tolerate very high levels of salinity. Similar to glycophytes, halophytes also use osmoprotective and ion-detoxification strategies consisting of Na+ removal from cytosol, Na+ transport from root cells to xylem, and ion compartmentation in the vacuoles, involving salt overly sensitive (SOS1), high affinity potassium transporter (HKT1) and Na+ H+ antiporter (NHX) ion transporters, respectively. Under salt stress, most halophytes accumulate more Na+ in their shoots than in their roots while retaining higher levels of K+ and, thus, a more optimal K+/Na+ ratio [47, 48].
Salt stress induced accumulation of specific osmolytes like proline, glycine betaine and sugar alcohols have also been reported in both halophytes and glycophytes [47]. Nevertheless, halophytes exhibit a greater capacity to accumulate very high levels of such osmolytes, even under normal conditions which explains its preparedness to stress [49]. In line with this, over accumulation of proteins involved in carbohydrate metabolism have been reported in the leaves of many halophytes [50]. Specific transporter mediated intracellular compartmentalization of excess ions in to vacuole is another key mechanism used by halophytes to maintain a moderate cytosolic K+/Na+ ratio in the cytosol. Thus, membrane ATPases and ion transporters play vital roles in salt tolerance of halophytes [51].
Salvadorapersica, a very common inhabitant of dry saline tracts was grown at different in situ salinities, and the partitioning of sodium and chloride ions in to different plant parts were studied by [52] (Figure 2). The results showed very high content of these ions in the bark and senescing leaf tissue and a comparatively low content in photosynthetically active leaves [53]. The capacity of these sink tissues (bark and senescing leaves) to accumulate more and more salts increased with increasing salinity as well as with age of plant, which indicates a well established salt compartmentation mechanism in this halophyte species [41].
Sodium (Na+) and chloride (Cl−) ion partitioning in Salvadora persica grown at different in situ salinities. Data represents mean of 2nd, 3rd and 4th years [43]. DW = dry weight, Im. Leaf = immature leaf, M. leaf = mature leaf & S. leaf = senescing leaf.
However, recent physiological and molecular observations across the globe indicate that halophytes may employ different mechanisms in ion transportation and homeostasis under salt stress. Latest studies showed that over expression of SOS 1 and HKT 1 in the halophytes Eutrema salsugineum and Schrenkiella parvula conferred much stronger salinity tolerance than that of their glycophytic counterpart [54]. Many halophytic species have now been understood to be constitutively higher expressers of the component genes of salt overly sensitive (SOS) pathway [55]. Genome studies of Schrenkiella parvula via. next generation sequencing (NGS) platform revealed the presence of three tandem duplicates of nhx8 and two copies of hkt1 which clearly explains the higher transcript abundance of these genes as compared to their glycophytic counterpart [56]. Thus genomic variation may be another important factor leading to enhanced salt tolerance in these halophytes which needs further confirmation. Moreover, the presence of specific Na+/Ca2+ converse transportation mechanism also facilitates better adaptation to salt stress in halophytes [57].
Epidermal bladder cells (EBCs) is another important feature of certain halophytes by which they secrete excess salt. 50% of the existing halophytes have been reported to contain these EBCs [31]. Removal of these EBCs resulted in enhanced salt sensitivity in a facultative halophyte called quinoa (Chenopodium quinoa) [58]. These EBCs are 1000-fold bigger than the general epidermic cells in volume, indicating its enhanced sodium excretion ability [59]. EBCs are similar to the trichome cells of Arabidopsis and transcriptomic analysis of quinoa EBCs showed enhanced expression of salt stress responsive genes, genes belonging to transporter family, sugar transporters, while photosynthesis-related genes showed reduced expression [60]. Nevertheless, the genetic determinants of EBCs coupled with the molecular mechanism of sodium pumping in to the EBCs is far from clear except a few studies in Arabidopsis [61]. This EBCs mediated strategy to tolerate high salt stress is not present in all halophytes. So certain other mechanisms are adopted by those halophytes which do not rely on EBCs. One category of halophytes called as succulent halophytes, further classified in to stem succulent and leaf succulent, accumulate large quantities of salt in its cells and tissues instead of secretion or compartmentation [40].
Succulence aids them in resisting the salt induced toxicity which can even reach up to 60% of leaf dry weight [62]. Suaeda is a classic example of this category of halophytes which can tolerate very high levels of salt without external secretion [31, 63]. Several other succulent halophytes have been reported belonging to amaranthaceae family [26, 64]. Sesuvium portulacastrum is another typical example of succulent halophyte often called as euhalophyte which accumulates lot of salt in its succulent leaf tissue [65].
Photosynthesis is the most vital physiological process in plants, which if affected by any kind of stress, leads to significant yield reduction. Under salt stress, stomatal conductance gets reduced in order to save water, so internal CO2 also gets reduced leading to reduced photosynthesis [66]. This reduced CO2 limits the dark reactions of photosynthesis and leads to accumulation of reducing powers in grana thylakoid, thereby damaging the photosystem [67]. The differential effect of salt stress on photosystem II activity of halophytes has been studied in Spartina versicolor as compared to the glycophyte Cyperus longus. Cyperus displayed a significant reduction in the activity of photosystem II (PSII) under salt stress, but on the contrary, Spartina did not show distinct reduction [68]. Moreover, a deeper mechanism oriented study showed that halophytes were able to absorb light even under high salt stress, indicating a much stronger PSII complex [69]. Proteomic study showed that the halophytic relative of wheat was able to accumulate more chlorophyll a-b binding protein (CP24) protein under high salt stress, which in turn stabilized the PSII complex [70]. The ability of halophytes to change their carbon assimilation pathways from C3 to C4 and even crassulacean acid metabolism (CAM) according to stress levels is highly unique and vital trait for tolerance to high salt stress [57]. Altogether, the ability to protect PSII from oxidative damage coupled with situation specific shift of carbon assimilation pathways is the photosynthetic adaptive mechanism in halophytes under salt stress.
The unique molecular signatures of halophytes place them very high on the salt tolerance hierarchy as compared to glycophytes [71]. A concentrated effort is made to bring together diverse research attempts on the various signaling aspects under salt stress conditions in halophytes, starting from sensing, activation of downstream signaling elements and all other potential candidates in the salt stress signaling network. A much stringent regulation of gene expression has been reported in halophytes as compared to its glycophytic relatives. Research attempts to exploit the rich source of salt responsive genes and promoter regions of diverse halophytes have also yielded significant achievements in the recent past [72]. Moreover, halophytic gene sequences are more complex with the presence of transposons and intergenic sequences [73]. The copy number of genes related to salt tolerance is also high in halophytes as depicted by the presence of three copies of calcineurin B-like 10 (CBL 10) in Thellungiella parvula as compared to one copy in Arabidopsis [74]. SOS1,NHX1 and many other salt stress related genes have constitutive expression in halophytesas compared to salt induced expression in Arabidopsis [75]. Further, the transcript abundance of H+ ATPase gene was low in the halophyte Chenopodium quinoa as compared to Arabidopsis, but the activity of the transporter protein was much higher, indicating some kind of post translational modification in halophytes [76].
Harnessing the huge economic potential of the diverse halophytic plants and other saline vegetation is highly imperative to reduce the damage caused by soil and water salinization with special reference to the poor rural agrarian sector. This section of the chapter deals with the wide range of utilization of halophytes in various ecological zones of India as food, fodder, bio fuel, medicine and industrial raw materials for mass production of various compounds. The commercially untapped economic potential of certain abundantly found halophytes are also discussed as a possible livelihood source to the resource poor farmers of these saline dry lands. The oldest known attempt to use halophytic plants was the utilization of Alhaji maurorum as a soil ameliorant. However, Israel has to be credited for the prolific rediscovery and utilization of halophytes in saline tracts [77]. The first half of this section deals with the prime potential of halophytes that has to be harnessed from a national point of view, relating to replanting and ecological recovery of barren saline dry tracts, cheap biomass for renewable energy, climate change mitigation, CO2 sequestration and biological reclamation. The second part consists of the economic potential of halophytes related to use as food, fodder, medicine, chemicals, sea weed, mangrove based aquacultures etc. which can be a possible livelihood source to the resource poor farmers of these saline lands.
The climate foot print of present agricultural practices is univocally accepted to be similar to that of fossil fuel burning. The sustainability of current agricultural practices is questioned as they squander rich resources and acts as priming agents to global climate change [78]. So there has to be an inevitable change in the ethos of research and policy making to focus more on crops that grow well on limiting resources. Next generation agriculture should also be based on alternative crops like halophytes and mangroves which are water and nutrient use efficient and have sustainable yields across varying environmental conditions. The climate change mitigation potential of halophytes can be explained by just one example ie. Suaeda fruticosa thatcan survive and complete its life cycle under soil salinity of 65 dS m−1, pH of 10.5 and under little or no water [79]. Such halophytes and other saline vegetation has tremendous potential in saving water, preventing soil erosion and replanting barren saline and sodic soils which is highly imperative in the current scenario of global change. Moreover, halophytes are suited to our brackish or saline water resources there by helping in fresh water conservation and replenishment. Scientific management of halophytic fields has tremendous potential to prevent further salinization of aquifers and groundwater of adjacent landscape. Due to climate change, global flood has become quite common and it is accompanied by post flood rise in water table and waterlogging. Under such situation, halophytes possess the ability to reduce saline water table and reclaim the affected land [53].
Mangroves species play a pivotal role in protection of our coastal ecosystem. The abundant aerial roots of these species are home to hundreds of creatures which are mostly endangered. Many species are true to sandy beaches and hence prevent soil erosion. More importantly, the role of mangroves as a livelihood to resource poor farmers cannot be underestimated [28, 80, 81]. As per National cyclone risk mitigation project (NCRMP), 308 cyclones of varying intensity impacted the eastern coast of India between 1981 and 2000. Extreme wave conditions are very common after effect of such cyclones originating in the Bay of Bengal [82]. As a result thousands of fertile agricultural land gets transformed in to wastelands. To cope with this, ICAR-CSSRI, regional research station (RRS), canning town, West Bengal developed a land shaping technology [83]. In this technique, land was converted in to medium ridge and shallow furrows where suitable halophytic tress along with paddy cum fish cultivation was practiced in kharif and in rabi season, furrows were used for rice cultivation [83]. Deep furrow and high ridge shaping technique was also practiced on coastal land of Sundarbans to overcome post cyclone stress [84]. Altogether, this technology plays a major role in rain water harvest, improved drainage and there by reduction in soil salinity and reduces environmental foot print by increased carbon sequestration.
Carbon sequestration is defined as the process of increasing organic carbon reserves by appropriate scientific land management interventions [85]. A much up scaled effort has to be put forth to harness more and more atmospheric CO2 and store it in our soil. This has been reported to have enormous potential to reduce greenhouse gas (GHG) emissions [86, 87]. Halophytes helps in restoration of barren saline and sodic soils and sequester more and more carbon to enrich the organic carbon status of our infertile soils. ICAR-CSSRI has worked on the carbon sequestration potential of various agroforestry components in saline sodic soils. Results showed that these trees acts as carbon sink by virtue of their high growth rate, attractive wood and bio drainage properties. Eucalyptus tereticornis plantation was able to sequester 9.5 to 22.5 Mg ha−1 carbon in different spacing and 90.6 Mg ha−1 in block plantations along the canal after 6 years of planting in waterlogged saline soils of northwestern India [88, 89, 90]. Six years old Eucalyptus tereticornis plantation in sodic land showed a cumulative carbon stock (above ground biomass C+ below ground biomass C + soil carbon) of 122.6 Mg ha−1 with CO2 mitigation capability of 369.2 Mg ha−1. Moreover, carbon storage in soil was found to be 44.4% higher in agri-silviculture as compared to rice wheat cropping system in partially saline and sodic soils [91]. Several other studies by ICAR-CSSRI research groups showed very high carbon sequestration potential of tree species like Eucalyptus tereticornis, Syzygium cumini, Pongamia pinnata and Populus deltoides [92, 93].
The dream of producing bioenergy can only be conceptualized if we can identify alternate species that can grow and survive in barren saline and sodic soils and therefore, would not compete with our conventional agricultural components. Halophytes are potential candidates as bioenergy crops as they can be watered even with sea water without any significant reduction in biomass or seed yield. Second generation biofuels are the topic of discussion, where nonfood biomass is used as raw material for biofuel production. Four prominent raw materials used for second generation biofuel production in India are the lignocellulosic biomass of four halophytes namely Pongamia, Jatropha, Panicum virgatum and Miscanthus [94]. Two significant attributes of such fuels are reduced environmental foot print and improvement in soil quality [95]. The salt excluder category of halophytes is better suited to biofuel production as fouling is a common problem in fuel developed from salt accumulating halophytes as salt is noncombustible. The latest review on major halophytes used for second generation biofuel production in China is the benchmark reference [96]. Salicornia (glasswort), Suaeda (sea-blite), Atriplex (saltbush), Distichlis (arid salt grass) and Batis spp. are another set of promising halophytes rich in lignocelluloses content [26, 97]. Abundantly found halophytic species like Salicornia, sea grass along with two mangrove species, Avicenia berminans (black mangrove) and Rhizospora mangle (red mangrove) has found a place in the green lab of National Aeronautics and Space Administration (NASA), USA as a viable alternative energy resource [98]. Another innovative and attractive concept that has emerged is to develop an integrated seawater energy and agriculture system (ISEAS) where there will be a coupling of biofuel feed stock, aquaculture and mangrove silviculture for the ultimate aim of producing sustainable aviation fuel [99].
Recently, large tracts of agricultural lands in arid and semiarid regions have been subjected to heavy salinization and heavy metal pollution, arousing serious health and environmental concerns. Phytoremediation is defined as the use of plants to remove pollutants from soil and (or) render them harmless [15, 100, 101]. Deep rooted, high biomass producing accumulator category halophytes are potential candidates for phytoremediation of saline heavy metal contaminated soils [102]. It is cost effective and provides additional output in terms of forage [103]. The added advantage of halophytes in phytoremediation is its high tolerance to heavy metals and increased uptake of these heavy metals [104, 105]. Recent research attempts on halophytes mediated phytoremediation of heavy metal contaminated saline soils across the world are more in number indicating its environmental significance [106, 107]. Functional biology or potential of halophytes based studies also took place but are few in number [105, 108, 109]. Halophytes such as Atriplex halimus [110], Spartina alterniflora [111], Sesuviumportulacastrum [112] and Tamarix africana [113] are well proven examples in phytoremediation of heavy metal contaminated saline soils.
It is next to impossible to grow conventional crops in the barren salt affected soils spread across the country which develop the gap of demand and supply of quality food in such areas. It ultimately creates barrier to food and nutritional security of the resource poor farmers living in such harsh areas. So halophytes have a huge potential as an edible source of nutrition there by securing livelihood of farmers. Such concept is gaining popularity very quickly and has spread across the world [101]. Among other salt tolerant crops, beetroot (Beta vulgaris), date palm (Phoenix dactylifera), amla (Emblica officinalis), karonda (Carissa carandas), guava (Psidium guajava), jamun (Syzygium cumini), pomegranate (Punica granatum), ber (Ziziphus mauritiana), bael (Aegle marmelos) and clusterbean (Cyamopsis tetragonoloba) are well known for their food value, and these are successfully grown in such saline soils using saline water irrigation. Also in India there is an extensive traditional use of non-conventional halophyte crops and naturally occurring halophytic vegetation as a nutrition source and further value addition (Table 3).
Plant scientific name/common name | Plant parts | Nutritional aspects and uses |
---|---|---|
Anthrocnemum indicum | Phylloclades | Highly nutritious, used in pickles |
Amaranthus spinosus (Kanta chaulai, kante bhaji) | Tender shoots, young leaves | High in Ca content, leaves cooked as vegetable, mature stems cooked with small fishes |
Aster tripolium (Salt bush) | Leaves | Fresh salads, cooked vegetable |
Atriplex hortensis (Pahari paleng) | Leaves | High nutritive value as a green leafy vegetable |
Balanites aegyptiaca (Hingor, hingod) | Fruits | Both fresh and dried fruits are edible |
Beta maritime (Palak) | Young shoots | Highly nutritious, consumed like spinach |
Borassus flabellifer (Palmirah palm) | Edible radicles, fruits | Consumed as toddy, jaggery and vinegar |
Capparis decidua (Kair) | Raw Fruits | Used as pickles and high medicinal values |
Carissa carandas (Karaunda) | Fruits | Rich in iron, vitamin C, A, Ca and P, immature fruits are pickled and eaten raw. |
Centella asiatica (Brahma manduki) | Leaves, young shoots | Widely used in Indian regional cuisines as a culinary vegetable. |
Chenopodium album (Bathua) | Leaves, young shoots | High in protein, vitamin A, Ca, P, and K, cooked as vegetable, curries, raita and paratha-stuffed breads in northern India |
Corchorus capsularis (Chanachedi, mora-pat) | Leaves, shoots, fruits | Rich in vitamins and minerals, used in salads, leafy vegetable |
Eleocharis dulcis (Neerchelli) | Tubers | Rich in vitamin B6, Mn, and K, tubers cooked |
Grewia tenax (Gondni, kanger, kaladi) | Fruit, leaves, seeds | Fe-rich fruit, consumed raw or use as refreshing drink or porridge, leaves eaten as a green vegetable |
Haloxylon salicornicum (Lana, khar) | Leaves, stem, seed | Fatty acids, vitamin C & A, used as salad and pickles, seeds mixed with bajra for roti making |
Hemidesmus indicus (Anantbel, nannari) | Roots | Roots used for pickle, “nannari sharbat” also made from roots |
Leptadenia pyrotechnica (Khimp, jivanti) | Pods | Pods are of medicinal value and used as vegetables in Rajasthan |
Morinda citrifolia (Noni) | Fruit | Starvation fruit during famine, consumed as raw, pickled and used for extracting juice |
Nypa fruticans (Nipa palm) | Young shoots, Fruits | Eaten as a green vegetable and the immature fruit is used in deserts |
Oxalis corniculata (Amrit sak) | Young shoots, Leaves | Rich in vitamin C, Ca, beta-carotene and P, consumed as vegetables |
Pisonia alba (Chandu, muruval) | Leaves | Leaves are eaten as a green vegetable |
Portulaca oleracea (Lunia, badi-Noni) | Above ground part | Vitamin-rich with high omega-3 fatty acids, consume as a salad or with yoghurt |
Prosopis cineraria (Khejri) | Pods | Pod called as Singhri or Sangri used in various types of bhaaji and kadhi in Thar desert of India |
Salicornia brachiata (Umari keerai) | Biomass | High protein edible oil similar to safflower, value-added by-products like vegetable salt |
Sesuvium portulacastrum (Lunio, dhapa) | Leaves, stems | Rich in Ca, Fe, and carotene, consumed as vegetables by local peoples in arid region |
Suaeda fruticosa (Khario luno) | Leaves, shoots | Protein rich, eaten by local people as vegetables |
Suaeda maritimum (Luno, lano) | Young leaves | Leafy vegetable, can be used in combination foods as seasoning |
Suaeda nudiflora (Morus) | Leaves | Pickles, salad, and as a vegetable |
Terminalia catappa (Deshi badam) | Fruits | Sweet fruit and edible kernel |
Ziziphus nummularia (Jhar beri, chanibor) | Fruits | Fruits eaten raw |
“Saji” or “barilla” is anindigenous value addition of locally available halophytes. It is the soda ash obtained from the air dried foliage materials of chenopod shrubs like Haloxylon, Salsola and Suadea. It is an essential ingredient of papad, and contributes to organoleptic qualities in terms of crispness and expansion of fried papad. The local Rajasthani Banwaria community has expertise in making Saji. The Saji produced from Khara lana (Haloxylon recurvum) is of the best quality, whereasSaji produced from Pichki lana or luni (Suaeda fruticosa) is of medium quality, and that produced from lani (Salsola baryosma) is of inferior quality [121]. Another aspect on which ICAR-CSSRI has extended its research is edible cactus (Opuntiaficus indica) and its growth and yield potential under saline soils. Certain specific moderately salt tolerant clones have been identified for raised bed planting in saline tracts [122].
Moreover, around 50 species of seed producing halophytes are potential sources of edible oil and proteins. The best part of their use for oilseed is that they generally do not accumulate salts in their seeds. Prominent halophytes such as Suaeda fruticosa, Arthrocnemummacrostachyum, Salicornia spp., Halogeton glomeratus and Haloxylon stocksii have been reported to produce high grade edible oil with an unsaturation content of 70–80% [123]. Seeds of Salvadora oleoides and S. persica contain 40–50% fat and are a good source of industrially important lauric acid and myristic acids. Its purified fat is used for soap and candle making. Terminalia catappa (seed oil 52%) is another tree species widely used for edible oil production at industrial level. Salicornia bigelovii is another halophytic species used for commercial oil production in the western states of India. The seed (31% protein) is pressed for its high quality edible oil (28%) which is an alternative source of omega-3 polyunsaturated fatty acids [124].
Quinoa (Chenopodium quinoa) is another annual facultative halophyte which has every potential to become a highly economic crop in saline areas of India. The exceptional tolerance of this crop to soil salinity has already been reported [125]. Protein content of quinoa ranges from 12 to 17% depending on variety, environment and crop management practices [126]. This is higher than our conventional cereal crops like rice (6–7%), wheat (10.5–14%) and barley (8–14%). More importantly, it is rich in lysine and methionine which are the two amino acids absent in cereals and pulses respectively [127]. ICAR-CSSRI has initiated a network project on morpho physiological characterization and standardization of agronomic practices of quinoa (Chenopodium quinoa) for salt affected agro-ecosystems. Nineteen germplasm lines were evaluated under four levels of irrigation water salinity ie. best available water, 8 dS m−1, 16 dS m−1 and 24 dS m−1. Germplasm EC 507740 gave maximum grain yield of 9.20 g per plant at highest levels of salinity (24 dS m−1) [128].
“Kharchia 65” is a wheat race native to Pali district of Rajasthan which is commonly called as red wheat. It is universally recognized as highest salt tolerant genotype. This genotype has been extensively used in the development of salt tolerant wheat varieties by ICAR-CSSRI, Karnal, namely KRL1-4, KRL 19 and KRL 39. It is a universal donor to salinity breeding in wheat coupled with high yield and has been registered in ICAR- National Bureau of Plant Genetic Resources (NBPGR), New Delhi (registration number: INGR99020). The main reason for growing this wheat variety in the arid and semiarid regions of the country is that it is highly salt tolerant and requires very less water as compared to other hybrids and can also be grown as rain fed crop purely on conserved soil moisture. Another useful trait of this genotype is that the plants are tall with high straw content which can be effectively used as a fodder to cattle as it is much preferred by animals as compared to other wheat straw [129].
Biodrainage is a term that is getting more and more popularized which signify the use of salt tolerant trees and grasses for reducing salinity and waterlogging [130]. Apart from reclamation of these saline lands, silvipastural system aids in improved carbon sequestration [131], increased soil rhizosperic activity [20], reduced greenhouse gas emissions [132] and long term adaptation to changing climates [133]. Mesquite (Prosopis juliflora) combined with Kallar grass (Leptochloa fusca) was reported to be a promising silvipastoral system in sodic soils [134]. Other successful silvipastural combinations are Acacia nilotica + Desmostachya bipinnata, Dalbergia sissoo + Desmostachya bipinnata and Prosopis juliflora + Desmostachya bipinnata [134]. Tamarix articulate is another very productive halophytic tree species with a biomass production of 93 Mg ha−1 in 7 years [135]. Aromatic grasses like lemon grass (Cymbopogon flexuosus) and palmarosa (Cymbopogon martinii) were studied by ICAR-CSSRI and found to be suitable to moderate alkali soils up to pH 9.2. Moreover, the most popular aromatic grass called vetiver (Vetiveria zizanioides) was found to be dual tolerant to high pH and waterlogged soils [136]. Licorice (Glycyrrhiza glabra) was reported by ICAR-CSSRI to be highly tolerant to sodicity level up to 9.8 [81]. Other promising grasses suitable to saline sodic soils are Aeluropus lagopoides, Dichanthium annulatum, Chlorisgayana, Bothriochloa pertusa, Eragrostis spp., Sporobolus spp. and Panicum spp. [130]. Other farmer preferred halophytes in saline sodic soils are Ziziphus, Atriplex, Kochia, Suaeda, Salsola, Haloxylon and Salvadora as they are preferably browsed by camel sheep and goat [137].
Salvadora persica is an oil yielding salt bush that has been extensively studied by ICAR-CSSRI. A Salvadora persica based silvipastural system was developed and popularized with forage grasses like Leptochloa fusca, Eragrostis sp. and Dichanthium annulatum on the saline Vertisols of Gujarat, India [138]. This model was successful in saline soils of electrical conductivity ranging from 25 to 70 dS m−1.Moreover, high biomass producing halophytic trees like Acacia tortilis (hybrid), Ziziphus mauritiana, Pithecellobium dulce, Melia azedarach, Cassia fistula, C. javanica, Callistemon lanceolatus, and Acacia farnesiana were popularized among the resource poor farmers of the saline and sodic soil tracts of northern India. The waterlogged soils of semiarid regions of northern India were also subjected to reclamation via. Eucalyptus based agroforestry [81, 139]. Eucalyptus tereticornis was the preferred species. Elaeagnus angustifolia is another tree species recently found to be effective for bio drainage based on its water use efficiency, salt tolerance and growth rate [89].
Salicornia is an obligate halophyte belonging to chenopodeaceae family commonly found at the edges of wetlands, marshes, sea shores, and mudflats [140]. It is commonly called as pickleweed, glasswort, sea beans and sea asparagus across India. Some species of Salicornia can even tolerate and complete its life cycle under 3% Nacl [141]. In India, this halophyte has been used as an edible crop as well as for non-edible purposes. Use of this plant as a source of soda for glass manufacture is time immemorial. Salicornia brachiata, a leafless shrub, was indeed the first source of salt produced from plants in 2003 by Council of Scientific and Industrial Research (CSIR)- Central Salt and Marine Chemicals Research Institute (CSMCRI), Gujarat, India. This vegetable salt, unlike common salt contains salts of potassium, calcium, magnesium and iron. On farm trials have shown that it has the potential to produce 3–4 tons of vegetable salt/hectare which can fetch a market of Rs 10–12 per Kg to the resource poor farmers of these barren saline tracts [142]. Further, recurrent selection mediated germplasm improvement was also carried out for better yield. In order to minimize the cost of cultivation, this species (improved variety: SOS 10) were sown in monsoon along the western coast of India in a large scale. Public private partnership based salt product named “Saloni” was also developed on a commercial scale in Gujarat [142].
Low content of seed sodium makes it a very good source for human heart, apart from its other medicinal properties against diabetes, asthma, hepatitis, gastroenteritis and cancer [143]. Moreover, the edible oil from its seeds is rich in poly unsaturated fatty acids and similar to safflower in fatty acid composition. It is also used as a green salad in the western areas of India. Antibacterial, antitubercular and antioxidant activities of Salicornia brachiata has been previously reported [144]. It is very popular and commonly used by villagers of western and eastern coast as an animal fodder, herbal salt and as a source of oil, while the ash of the whole plant has been reported to be useful in itch treatment [145, 146]. Most recently, prolific study on its polysaccharides and other phytochemical profile for phenolic compounds, oils, proteins, flavanoids, sterols, saponins, alkaloids and tannins are under way and shows promising results [147]. The oligosaccharide profiling of Indian species Salicornia brachiata was performed and the results showed this plant to be rich source of dietary supplements [148]. The ecological benefits of large scale cultivation of this plant along the coasts of India may be summarized as utilization of barren saline lands, upscaling of green belt, coastal development and protection and biodiversity conservation [89]. Finally, the equity benefits are vast export income and private industrial and institutional collaboration. So, this plant is a plant of future which needs special mention.
One of the major physiological adaptations of halophytes to saline stress is the production of different biomolecules which possess highly useful biological activities like antioxidant, antimicrobial, anti-inflammatory and antitumoral [149]. So, if introduced in to our diet, it has the potential to prevent a lot of diseases like cancer and cardiac disorders [36]. These biomolecules also enhances the neutracutical value of halophytes as the concentration is very high as compared to their glycophytic counterparts [150]. Moreover, certain biomolecules are specific to halophytes and hence have great agri food, pharmaceutical and cosmetic value [151]. Presence of a wide array of compounds like alkanes, fatty acids, carbohydrates, aminoacids, alcohols, terpenoids, flavanoids etc. have been reported from major halophytes [152]. Halophytes have long been used as folklore medicine by villagers and very little documentation is done in this aspect. A few glimpses off current use of halophytes as medicine in India is discussed here. Salicornia sp. is widely used as a folk medicine for constipation, diabetes and cancer [153]. Suadea sp. and Atriplex sp. are widely known to possess hypoglycaemic and hypolipidaemic activities [154].
Catharanthus withstands EC of 12 dS m−1 and produces about 130 catharanthus alkaloids compounds, including vinblastine and vincristine, two drugs used to treat cancer. Mangroves are also good source of biomolecules. For instance, the mangrove Cynometra ramiflora oil has antibiotic properties and is used in skin diseases [155]. Among other notable use of halophytes as medicine, use of Pandanus odoratissimus in leprosy, scabies, heart diseases, Salvadora persica, in cough, rheumatism, toothache and piles, Salsola baryosma, S. kali as anthelmintic, emmenagogue, diuretic, Tamarix articulata in eczema, ulcers, piles, sore throat, diarrhea, liver disorders andCress cretica as tonic, aphordisiac, stomachic deserves special mention [28]. Among other products, biopetrol/diesel from Jatropha curcas and Euphorbia antisyphilitica, multiple bioactive compounds from Salsola baryosma, essential oil from Pandanus sp., Terminalis catappa, aromatic oil from Grindelia camporum, Larrea tridentate and Simmondsia chinensis, rubber from Chrysothamus nauseousus and Parthenium argentatum, multiple beverages from the mangrove palm Nypa fruiticans, pulp and fiber from Phragmitesaustralis, P. karka, Juncus rigidus and J. acutus deserves special mention [28].
Sea weeds are an integral component of coastal ecosystems that lend invaluable support to the diverse marine life. The economic value of these sea weeds is of significant importance to the resource poor farmers of saline coastal areas. It is used as a food, but more importantly the phycocolloids derived from it is of significant export value [156]. In India, apart from phycocolloid production, sea weeds are being used for the commercial production of crop growth stimulating agents. Moreover, the agar and alginate industry full depends on this valuable coastal resource. Off late, they are extensively being explored for biofuel, neutracuticals, medicines and food additives [157]. In Indian context, carrageenophytes (red sea weeds), Gracilaria spp. and Gelidiella spp. for agar production, Sargassum spp. and Turbinaria spp. for alginate production, Kappaphycus alvarezii, Hypnea musciformis and Sarconema filiforme for phycocolloid kappacarrageenan production is of major economic importance [156]. Another matter of pride for Indian Council of Agricultural Research (ICAR) is the endorsement of ICAR-CIFT (Central Institute of Fisheries Technology) by world health organization (WHO) to fight COVID-19 pandemic. The research group proposed that sulphated polysaccharide from seaweed can be a potent molecule to fight against the COVID-19 Pandemic, hence, is a candidate molecule to be studied against SARS-CoV-2 [158].
Tangible evidences of global climate change and land degradation due to salinization are quite evident and so it is highly imperative to bring more and more salt affected land into cultivation to satisfy the food and nutritional security of our burgeoning population. In this context, halophytes and other saline vegetation has paramount importance to ensure economic returns and maintain ecological balance. India has a very rich source of halophytic, mangrove and other saline vegetation which has huge potential in monetary as well as environmental terms. It can reduce the gap between demand and supply of food and fodder for livestock, besides being a source to numerous other products of economic significance. The role of halophytes in climate change mitigation, carbon foot print reduction, renewable energy source and greening of our barren saline lands has to be conceptualized on field basis. Moreover, deteriorating water resources and lower availability of good quality water for agriculture demands a paramount shift to edible halophytic crops like quinoa, already being termed as super food, highly tolerant to drought and salinity stress.
Identification and documentation of region specific halophytes, access to seeds, establishment of halophytic nurseries, optimizing package of practice and development of processing plants are immediate requirements to spread the concept of halophyte based biosaline agriculture. Long term experiments are the need of the hour to prove the sustainability of halophyte based cultivation and economic security. More importantly, breeding programs should be initiated to improve traits such as yield, taste, biomolecule quantity and quality for faster adoption of halophyte based production. Another major issue to be tackled is the low or nonexistent demand on the market and a lack of value chain. For this consumer awareness need to be created and a value chain which consists of different players need to be established. Let us all hope that the ultimate dream of greening our barren saline lands and replenishing soils with saline water table in to sites of bio saline agriculture gets fulfilled in coming years as a boon to mankind.
We acknowledge the funding and support from Indian Council of Agricultural Research (ICAR), Ministry of Agriculture and Farmers Welfare, Government of India. Vineeth TV acknowledges Dr. Ashwani Kumar, ICAR-CSSRI for providing photographs of major halophytes.
The authors declare no conflict of interest.
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