Keywords

8.1 Introduction

There are many halophyte definitions which deal with EC and NaCl concentrations that plants can tolerate. Practically halophytes are plants that tolerate salt concentrations that do not allow to live other species (Flowers and Colmer 2008). There are approximately 1450 halophytic plant species documented (eHALOPH Database), while we consider a total number of plant species which is approximately 350,000 (The Plant List Database); the percentage of halophytes in total plant species is only 0.4%. Saline habitats have great diversity from tidal marshes and coastal lagunas to inland salt lake shores and salt deserts. Even though great majority of halophytic plants concentrated on few plant families such as Amaranthaceae and Poaceae, the rest of them are dispersed to more than 50 plant families (eHALOPH Database). Since saline habitats and evolutionary history of halophytes are diverse, they have many different adaptation mechanisms. And most of them have more than one adaptation mechanism to be able to survive in saline places. There are many studies conducted to understand their adaptation mechanisms, but most of them concentrated on their morphology, anatomy, physiology, gene regulation, and ecology. Halophyte microbiome interactions as an adaptation mechanism are quite a new subject and got attention in the last decade. However, information about plant growth-promoting microorganisms colonizing in the halophytes and their role in adaptation to saline environments is limited. Still, many reports have been existing that plant growth-promoting microorganisms can assist plants in extreme conditions. The bacteria help the plants by nitrogen fixation, increasing nutrient availability, and production of certain metabolites which are promoting plant growth. The fungi help the plants with the modifications of root architecture, solubilization of certain minerals from decaying organic matter such as phosphorus, and the production of certain metabolites which plants needed to be fit in saline conditions.

Many places around the world are facing with increasing population to feed and decreasing freshwater resources. Saline and sodic soils impact nearly 20% of the all irrigated land surface and 2% of all dryland agricultural land surfaces in the world (FAO 2018). While we consider three-fourth of the earth surface covered with salty water, understanding of halophyte adaptations became more and more important. Halophytes can be used for human benefits directly as a crop or as a gene resource for biotechnology; plant-promoting microbiome that associated with halophytes is a promising resource which can be applied to glycophyte crops to increase salt resistance and yield.

8.2 The Halophytic Microbiome

The interaction among living organisms has a long history, where cases of synergism have gained importance among the beneficial relationships. The microbes being consistently on one side have been successfully fulfilling this synergism with macro-, meso-, and microflora and fauna. The anthropogenic factor led to manipulation of such natural relationships, and consequently, identification and application of such instances came into study and application. Plant-microbe interaction has developed certain shapes including antagonism and synergism, where the latter, besides providing space and food, also utilizes such relationships for coping biotic and abiotic stresses. Same is the case in the halophytes which in combination with epiphytic and endophytic microbes cope the stress more efficiently (Ruppel et al. 2013), serving as ecological stress tolerance along with genetic processes. The microbes in the discussion include fungi, bacteria, and archaea, which have different extent of salinity tolerance and ameliorating the stress. The fungi include epiphytic and endophytic species, along with the endomycorrhiza and ectomycorrhiza, the bacteria, and archaea also categorized as endophytic and epiphytic. Instances of such microbes from extreme environments, and their adaptation to the particular locale (Imhoff 2017; Siliakus et al. 2017), especially isolations from saline habitats indicate that the microbes have promising ability to counter such stress.

Such microbes depending on their ability to grow in the saline environments can be categorized as halotolerant and halophilic. The former can, occasionally, tolerate up to 25% sodium chloride (NaCl), and among the latter, microbes needing salts for their growth: the non-halophiles require less than 1% NaCl, slight halophiles grow in 1–3% NaCl, moderate halophiles grow in 3–15% NaCl, and the extreme halophiles can grow in an environment containing 15–25% NaCl concentrations (Margesin and Schinner 2001; Ventosa et al. 2008). The heterotrophic nature of the microbes contrasting to the autotrophs has enabled the formers with adaptation toward certain environments, as of saline, resulting in an abundance of microbes even in saturated environments. The tolerance and utilization mechanisms discussed later in the chapter bring forward the prospects of such microbes in saline and hypersaline soils.

Wide range of habitats has resulted in halophilic and/or halotolerant microbes, for instance, salt lakes (Hedi et al. 2009), seacoasts (Kumar et al. 2012), arctic terrains (Yukimura et al. 2009), salt mines (Enache et al. 2014), plants pickled in salt solution (Abou-Elela et al. 2010), soil (Orhan and Gulluce 2015), and endophytic environments (Zhao et al. 2013). Several examples of isolation from habitats mentioned above and application to other crops have shown salinity tolerance, along with enhancing the plant growth. Halophiles are also tolerant to temperature (Kunte et al. 2002), pressure, and dryness (Mesbah and Wiegel 2012), suggesting their biotechnological potential too. Halotolerance and halophilicity show different responses and adapt to such circumstances differently, offering the manipulation of such interactions for enhancing required and ever sought better plant growth.

8.2.1 Plant Growth-Promoting Bacterial Relationships in Saline Habitats

The bacterial interaction with the plants, halophytes particularly, offers the potential of ameliorating the salinity along with enhancing the growth of plants. Different species of bacteria, endophytic and epiphytic isolated from diverse kind of halophytic plants and applied for the amelioration of stress, are summarized in Table 8.1. The diversity of halotolerant bacteria has been reported from rhizosphere soil, and endophytic environment and genera like Arthrobacter, Azospirillum, Azotobacter, Bacillus, Burkholderia, Enterobacter, and Pseudomonas have been reported as enhancing salt stress tolerance in diverse kind of plants (Paul and Lade 2014). The isolations of endophytic bacteria from Medicago truncatula, followed by sequencing analysis, revealed similarities of the isolates with reported halotolerant and halophilic bacteria (Yaish et al. 2016). The study further documented the alteration of the bacterial community due to salinity and PGP mechanisms. Another instance showed the effect of salinity on the metabolism of rhizobacteria (Szymańska et al. 2016), suggesting the hinderance in physiology, thus leading the bacteria toward tolerance and utilization of salts. Such circumstances lead toward the biochemical and genetic adaptation of bacterial communities toward adverse environments (van der Meer 2003), such as salinity. Similarly, the plants that struggle growing in saline areas lead toward recruitment of bacteria, already adapted to such environments, helping the plants grow well.

Table 8.1 Halophyte-associated bacteria showing plant growth-promoting traits
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The bacteria help the plants thrive in extreme environments through plant growth promotion by nitrogen fixation, increasing nutrient availability, and production of certain metabolites, as well as coping the stress through ACC deaminase, activation of defense mechanisms like cell wall restructuring, and release of exopolysaccharides (Rampelotto 2010). Additionally, the problem of nutrient fixation within the soil, phosphate as an example when applied in the saline soils, is quickly immobilized, and bacteria capable of solubilization can help increase availability leading toward better plant growth (Goldstein 2009). The plant growth-promoting bacteria (PGPB) further categorized as endophytes (PGPE) and rhizobacteria (PGPR) show similar mechanisms for stress tolerance. The endophytic bacteria being facultative, and spending part of their life in the soil, also depict the potential of horizontal gene transfer, and other gene sharing strategies, thus enabling the widespread bacteria with stress tolerance.

Microbes when exposed to high salts environment show loss of turgidity and dehydration of cytoplasm due to water potential difference (Paul and Lade 2014). They cope such circumstances by maintaining the salt concentration inside the cells initially through uptake of (potassium ions) K+ (Whatmore et al. 1990). Rhizospheric bacteria have also been reported to make turgid biofilms by certain polymers (Xiang et al. 2008) protecting themselves from salinity (Wijman et al. 2007), release of polysaccharides which also help in sheath formation around the roots and in the soil (Chen et al. 2009), and osmolytes production, viz., amino acids, betaines, ectoines, polyols, and sugars including their derivatives for coping various kinds of stresses (Lamosa et al. 1998). The structural changes in the cell membrane through changes in proteins, glucans, and polysaccharides (Paul and Lade 2014), fatty acid composition, and acyl chains (Klein et al. 1999) have also been observed. The osmoregulation showed by bacteria includes the accumulation of compatible solutes, which protect against desiccation and other stress factors (Fernandez-Aunión et al. 2010). Chen et al. (2016a) postulated that bacteria could overcome the high salt stress through storage of sodium ions (Na+) within the vacuoles, removing Na+ from the roots, buildup of soluble sugars, improving the antioxidant level, and regulation of stress-related genes in maize. The physical biofilm formation by Bacillus amyloliquefaciens also limits effects of salinity on barley, thus proposing amelioration of stress with the help of bacteria (Kasim et al. 2016). Similarly, endophytic bacteria have also been reported producing trehalose-6-phosphate synthase as an example of osmoprotectants (Suárez et al. 2008), ammonium (Jha et al. 2012), volatile compounds, and exopolysaccharides (Vurukonda et al. 2016). The reports of efficient colonization by PGPR even under increased salinity propose the salinity amelioration by plant-associated bacteria.

Certain bacteria, for instance, Pseudomonas fluorescens, produced alanine, aspartic acid, glutamate, glycine, and threonine within the cell (Paul and Nair 2008). The same genus has also been observed releasing exopolysaccharides which by retaining water and controlling the carbon sources flux enhance the survival of the microbes under stress conditions (Sandhya et al. 2009). Similarly, the release of oleic acid and cyclopropane fatty acids in the lipid membrane by Lactococcus lactis has been reported in osmotic stress (Guillot et al. 2000). Similar to physiological adaptation, genetic adaptations, varied proteomics, and gene regulation have also been reported in bacteria induced by salt stress (Diby et al. 2005; Paul et al. 2006).

8.2.2 Plant Growth-Promoting Fungal Relationships in Saline Habitats

The plant growth-promoting fungi (PGPF) have long been known for beneficial effects on plant growth (Hyakumachi 1994) including several genera where Aspergillus, Fusarium, Penicillium, Phoma, Piriformospora, Rhizoctonia, and Trichoderma have been reported widely (Hossain et al. 2017). Similar to PGPR, PGPF also enhances the plant growth and helps confer different biotic and abiotic stresses. The mechanisms for plant growth include the modifications of root architecture, solubilization of certain minerals from decaying organic matter, and the production of certain metabolites (Hyakumachi 1994; Meera et al. 1994), whereas the mechanisms of stress suppression include production of antibiotics, enzymes, mycoparasitism, competitions, and the induced systemic resistance (ISR) (Benítez et al. 2004; Khan et al. 2008, 2012). The fungal cells can also melanize their cell walls against abiotic stresses, thus reducing the loss of compatible solutes (Plemenitaš et al. 2008). Similarly, the cell membrane adaptability under the stress circumstances, through regulation of sterol in response to fatty acid modifying enzymes, is another mechanism of salinity tolerance in fungi (Gostinčar et al. 2009; Turk et al. 2004).

The PGPF can also be categorized as halotolerant and halophilic, as they have the ability to adapt to external osmolarity (Ruppel et al. 2013). The report of obligate sodium requirement by fungus Thraustochytrium aureum has been published, which cannot be replaced by potassium (Garrill et al. 1992). The fungal associations with plants as affected by environmental and host factors have been studied, where the fungal community was found correlated with the level of salinity (Maciá-Vicente et al. 2012). Fungi have been isolated from vast saline environments like seawater, saline soils, and salt marshes. The isolation of fungus from salterns (Gunde-Cimerman et al. 2000) indicates the potential of fungal survival even in saturated environments.

The resilience of higher fungi to extreme environments is due to their capability of producing osmotic substances, and it was observed that the Penicillium spp. and Aspergillus spp. could tolerate NaCl concentration as high as 20% or more (Tresner and Hayes 1971). The buildup of certain compatible solutes, for instance, betaine, glycerol, and proline, in their intracellular spaces induces resistance to high salt concentration (Ruppel et al. 2013; Blomberg and Adler 1992). Fungi including soil fungi as well as endophytic fungi can interact with many plant species and can promote plant growth, besides conferring abiotic and biotic stress. Trichoderma spp. well known as biological control agent have been isolated as PGPF (Table 8.2). Four types of mechanisms such as ACC deaminase, auxin, and gibberellin production, phosphate solubilization, and ISR for biocontrol in Trichoderma spp. have been reported (Viterbo et al. 2010; Contreras-Cornejo et al. 2009; Altomare et al. 1999). At the same time, some Trichoderma spp. significantly contributes to the adaptation of plant to salinity stress. Similarly, plant growth promotion and plant resistance were induced against nematodes in wheat by Trichoderma longibrachiatum T6 along with countering the salinity stress on seedling growth (Zhang et al. 2016). The same group discussed that the enhancement of antioxidant defense system and gene expression might have led to salinity tolerance by the plants. In another example, Trichoderma harzianum T83 was isolated and observed promoting the growth of Suaeda salsa L., a halophytic species. The fertilizer containing T. harzianum T83 effectively promoted the growth of S. salsa in soil affected by salinity, besides enhancing the quality of saline coastal soil (Chen et al. 2016b). They also investigated and found that the quantity of amino acids, Ca2+, K+, organic acids, proline, and soluble sugars was higher in S. salsa when inoculated with T. harzianum T83, and the strain also promoted root vigor and enzyme activities such as peroxidase and superoxide dismutase and reduced the malondialdehyde concentration (Chen et al. 2016b). Similarly, there are some reports of the Penicillium spp. and Aspergillus spp. having PGP ability under salt conditions. Their mechanisms are similar to those of Trichoderma spp.; however, some reports showed that they were not living in rhizosphere but inside the plant as an endophytic fungus. Khan et al. (2011) showed that endophytic Penicillium funiculosum LHL06 helped in countering the salinity stress in soybean along with reprogramming of the plants for improved growth and biosynthesis of isoflavone. The gibberellin production in Penicillium strains and the influence of salt stress on the gibberellin production have been reviewed (Leitão and Enguita 2015). Endophytes are attractive potential for the resource that confers plant resistance against abiotic and biotic stress through plant growth-promoting effect. In addition to endophytic Penicillium spp., Aspergillus spp., Fusarium spp., and Piriformospora indica stimulated plant growth, and some of them confer enhanced tolerance to salinity and resistance against biotic stresses (Khan et al. 2011; Bilal et al. 2018; Waller et al. 2005). There are still few reports of PGPF under salinity condition, and the future research should be conducted to clear the mechanisms responsible for the growth-promoting effect and investigate the isolates having an ability of plant growth promotion under salinity conditions.

Table 8.2 Halophyte-associated fungi showing plant growth-promoting traits
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8.2.3 Arbuscular Mycorrhizal Relationships in Saline Terrestrial Habitats

The fungi are chemoorganotrophic; most are aerobic or fermentative organisms referred to molds, mildews, rusts, smuts, yeasts, and mushrooms. They constitute a major portion of soil biota and dominant agents in organic matter decomposition and form important symbiotic relationships with algae, insects, and higher plants as well. Mycorrhizal fungi are the most abundant nonpathogenic and mutualistic symbioses on earth. It is a well-known phenomenon that almost 90% of terrestrial plants are associated with root-colonizing fungi, establishing an intimate and permanent mutualistic symbiosis, called “mycorrhiza.” In 1885, Bernhard Frank recognized these special structures in the roots for the first time and also noticed its physiological role in the soil (Frank 1888). This symbiotic life form has been referred to as “vesicular-arbuscular mycorrhiza” for many years and then replaced by “arbuscular mycorrhiza,” since not all endomycorrhizas of this type develop vesicles, but all form arbuscules (Strack et al. 2003).

The major mycorrhizal associations are “ericoid mycorrhizas” (EM), “ectomycorrhizas” (ECM), and “arbuscular mycorrhizas” (AM). Ericaceous plants are characteristic of acidic or peaty soils and harbor numerous symbiotic fungi, including EM characterized by the fine intracellular coils occupying rhizodermal and/or cortex cells of ericaceous hair roots (Vohnik and Albrechtová 2011). EM extend only a few millimeters from the roots but have been indicated to possess active chitinase and phosphatase to degrade resistant organic components such as lignin, chitin, and cellulose, in these acidic soil environments (Paul and Clark 1996).

ECM contains septate fungal cells infecting the roots of trees and shrubs of temperate regions. The plants such as pine, fir, spruce, hemlock, oak, and birch are almost exclusively ECM. Additionally, the eucalypts, casuarinas, and acacias in the tropics are also ECM. The mycelia of ECM have been proved to participate in water and nutrient absorption. Similar to EM, ECM is closely associated with the decomposition processes in the forest litter and synthesizes a range of enzymes, i.e., phosphatase cellulose and protease, but does not appear to degrade lignin (Paul and Clark 1996).

Exhibiting no discernible root or outside structural change, the endotrophic AM is the most common mycorrhizal symbiosis occurring in the world ecosystems. There is a vast amount of literature emphasizing the fact that 80% of all world plants are colonized by AM fungi. Major plant families such as Brassicaceae, Caryophyllaceae, Chenopodiaceae, and, among the monocots, all families other than Poaceae (grasses) are generally accepted as non-AM due to poor colonization with only a few roots carrying intraradical hyphae (Bothe 2012). However, many crop plants are strongly AM positive, and AM has been reported to be found in many different ecosystems such as deserts (Corkidi and Rincön 1997; Dalpé et al. 2000; Titus et al. 2002), tropical rainforests (Brundrett et al. 1999; Guadarrama and Álvarez-Sánchez 1999; Siqueira and Saggin-Júnior 2001; Zhao et al. 2001; Gaur and Adholeya 2002), aquatic environments (Khan 1993), and strong saline (Carvalho et al. 2001; Sengupta and Chaudhuri 2002) and alkaline soils (Landwehr et al. 2002) as well as from ecosystems with salty marshes (Hildebrandt et al. 2001; Kim and Weber 1985; Hoefnagels et al. 1993; Sengupta and Chaudhuri 1990; Carvalho et al. 2001; Aliasgharzadeh et al. 2001) and halophytes (Ho 1987; Mason 1928; Kahn 1974; Hoefnagels et al. 1993; Brown and Bledsoe 1996; Bothe 2012).

Such diversity in the literature can also explain the reasons for a tremendous number of research efforts aiming at understanding the functional roles of this ancient and widespread symbiotic empire living in the plant root zone. As the most important microbial symbioses for the majority of plants, the benefits serviced to the plant-soil interface by AM fungi can be lined up as (i) regulatory effects on plant water potential under drought (Augé 2001; Füzy et al. 2008; Barzana et al. 2012) and salinity stress (Evelin et al. 2009; Porras-Soriano et al. 2010; Porcel et al. 2012); (ii) supplying plants with phosphate and other nutrients (Smith and Read 1997; Strack et al. 2003; Jeffries et al. 2003); (iii) improvement of water-stable soil aggregation (Andrade et al. 1998; Miller and Jastrow 2000) especially through binding of soil particles by means of a stable hydrophobic glycoprotein, glomalin produced by AM fungi (Wright and Upadhyaya 1998, 1999); (iv) acting as bioprotectants against pathogens (Bødker et al. 1998; Slezack et al. 2000); (v) facilitating the survival of their host plants growing on metal-contaminated land by enhancing their nutrient acquisition and, protecting them from the metal toxicity, absorbing metals (Jeffries et al. 2003; Leung et al. 2013); and (vi) the degradation of organic pollutants (Joner and Leyval 2003).

Despite all these efforts, there are still many challenges to be addressed for AM fungi, especially regarding their contribution to the sustainable maintenance of plant health over challenging climate and soil environments. In this sense, the symbiotic interactions between salt-tolerant plants, i.e., halophytes and AM fungi, have received an increasing attention because the mechanisms of salt and drought stress alleviation by AM fungi exist (Hildebrandt et al. 2001; Ruiz-Lozano and Azcón 2000; Scheloske et al. 2004; Füzy et al. 2008; Aroca et al. 2009; Ruiz-Lozano et al. 2012). Stocker (1928) defined halophytes as plants resistant to higher salinity levels at least during a period of their life that the majority of plants will not survive. Salt marshes worldwide are the common habitats with remarkably similar halophytic diversity and zonal distribution depending on the salt level in soils (Chapman 1960; Walter 1968).

The aim of this section of the chapter, therefore, is to compile the evidence and knowledge concerning AM fungi-halophytic plant symbiosis which existed mainly in salt marsh environments. The main driving factor attracting researchers to explore such connections can be referred to enhancing the potential for implementation of mycorrhizal biotechnology in agricultural plant production under stress conditions, i.e., drought, salinity, and alkalinity, through understanding physiological and molecular mechanisms within mycorrhizal and non-mycorrhizal halophytes.

Salt marshes are usually characterized as the lands influenced by tidal flooding with seawater that leads to partial or total submergence of vegetation, high salinity, and anoxia in the soil. These conditions create an anaerobic and chemically reduced plant rhizosphere causing oxygen deficiency and phytotoxin accumulation (Armstrong et al. 1991). Eventually, plant life, species diversity, and distribution pattern are largely affected by salt and oxygen and concentrations depending on flooding conditions and hot seasons affecting salt movement in soil (Armstrong et al. 1985; Pennings and Callaway 1992). This is the reason for decreasing soil salinity, soil moisture, and anaerobiosis from the lower to the higher zone of a salt marsh, forming a zonated pattern in the vegetation, and may explain complex biochemical, morphological, and physiological adaptations of salt marsh plants to waterlogging and salinity (Naidoo et al. 1992). The rhizosphere microorganisms, especially AM fungi, are therefore believed to enhance the ecological adaptation of these plants, including pioneer plant colonizers, to salt marsh environments (Sengupta and Chaudhuri 1990; Khan and Belik 1995).

Briefly, AMF symbiosis under salt stress was often found to result in enhanced nutrient uptake and production of osmoregulators, higher K+/Na+ ratios, and Na compartmentalization within plant tissues and also improved photosynthesis or water use efficiency (Evelin et al. 2009; Porcel et al. 2012). On the other hand, the literature on associations between AM fungi and salt marsh halophytes is somewhat controversial. For example, AM fungi have been indicated to improve plant tolerance to salinity under stressful environments (Jindal et al. 1993; Ruiz-Lozano et al. 1996), whereas some other findings pointed out to suppression of mycorrhizal infection by high soil salinity (Pfeiffer and Bloss 1988; Juniper and Abbott 1993) and soil inundation (Harley and Smith 1983). In between these contrary views, Miller (1999) showed that waterlogging only partially inhibits AM colonization of wetland grasses. Looking at these findings, it can be assumed that the halophyte-AM fungi symbiosis depends on the level of salinity and water content and halophytes that are living in extremely saline and flooded conditions are not colonized by arbuscular mycorrhizal (AM) fungi (Peat and Fitter 1993).

However, distribution of AM fungi in salt marsh ecosystems has been found to be related not only to fluctuating water regimes and saline-soil chemistry but also to host plant species. It was a long time ago that colonization of halophytes by AM fungi had been proved by Mason (1928), subsequently followed by some other researchers (Kahn 1974; Hoefnagels et al. 1993; Brown and Bledsoe 1996). Boullard (1959) indicated that the degree of mycorrhizal colonization within the rhizosphere of the salt aster (Aster tripolium) was considerably high and relevant to the amount of carbohydrate supplied by the plant. Rozema et al. (1986) found that there was a substantial degree of variation in AM fungal infections among about 20 salt marsh halophytes. Their field observations indicated that some of the species (Aster tripolium, Limonium vulgare, Festuca rubra ssp. litoralis, Salicornia brachystachya, S. dolichostachya, Plantago maritima, Glaux maritima, Puccinellia maritima) had a high or intermediate degree of AM infection, whereas other species (Atriplex hastata, Juncus gerardii, J. maritimus, Spartina anglica, Cochlearia anglica, Spergularia maritima, and Triglochin maritima) exhibited a very low mycorrhization or even no mycorrhizal hyphae in their root segments. More recently, Carvalho et al. (2001) contended that distribution of AM fungi in the salt marsh is more dependent on host plant species than on environmental stresses and salt marsh halophytes were shown to have different mycorrhization levels. For instance, several halophytes are strongly AMF positive, whereas many halophyte families such as Caryophyllaceae, Plumbaginaceae, or Cyperaceae are known to be non-mycorrhizal (Bothe 2012). On the other hand, the dominant salt marsh grass, such as Puccinellia spp., has a variable structure of AM colonization with many specimens lacking a positive sign of AMF colonization (Hildebrandt et al. 2001; Landwehr et al. 2002). Bothe (2012) stated A. tripolium as the best mycorrhizal halophytes as all samples of this plant collected from many different field sites over the years were strongly AM fungi positive with almost all roots showing intraradical hyphae, arbuscules, and vesicles. This can be attributed to well-developed aerenchyma in this species (Rozem et al. 1986). In their greenhouse experiments, Scheloske et al. (2004) indicated that non-colonized A. tripolium plants had large aerenchyma, which is typical for plants of often flooded areas, while AMF-colonized A. tripolium had much smaller aerenchyma and distinctly more parenchyma cells. Due to its high degree of mycorrhizal colonization, A. tripolium was applied as a model plant in many cases for understanding the connections between AMF-plant symbiosis and salt tolerance mechanisms (Carvalho et al. 2001, 2003; Neto et al. 2006). However, mycorrhizal status of Spartina anglica, Juncus gerardii, and J. maritimus are difficult to explain since they have high root porosities but have no mycorrhizal infection (Rozem et al. 1986), which is in accordance with other observations on Juncaceae (Mason 1928; Fries 1944). Boullard (1964) mentioned that the lack of AM fungal infection in Triglochin maritima could possibly be due to the resistance of fungal infection, based on the presence of the toxic cyanogenic glucosides and sulfurous substances.

Thanks to advances in methodology and technology achieved over the last two decades, the ecology and diversity of AM fungi have gained new insights into the species that are present within the rhizosphere of halophytes. The PCR-RFLP analysis performed on the AM fungi spores isolated from diverse alkaline soil environments (dominated by NaCl, Na2CO3, Na2SO4, or CaSO4) in Central Europe indicated that 80% of all spores from the different sites belonged to one single PCR-pattern which closely matched that of Glomus geosporum BEG11 (Landwehr et al. 2002). The preponderance of G. geosporum in salt marshes was also confirmed by some other authors in Portugal (Carvalho et al. 2001) and Poland (Grzybowska 2004) or Germany (Bothe 2012) as well. Based on these important findings, G. geosporum has been considered to have a specific role in conferring salt tolerance to halophytes, and many experiments over the years were conducted concerning the effects of G. geosporum on the growth of various plants in the greenhouse conditions (Bothe 2012). Although some of the results were encouraging, plants inoculated with G. geosporum did not gain a consistent resistance against to salt stress over the control trials (Füzy et al. 2008).

However, there are many works in the literature reporting positive results on the alleviation of salt stress of crops by AMF, i.e., Cantrell and Linderman (2001), Feng et al. (2002), Giri and Mukerji (2004), Sharifi et al. (2006), Zuccarini and Okurowska (2008), Porras-Soriano et al. (2010), Wu et al. (2010), and Evelin et al. (2012), which has been extensively reviewed by other authors Evelin et al. (2009), Ruiz-Lozano et al. (2012), and Porcel et al. (2012). Bothe (2012) attributes the high number of experimental results with positive outcomes in the literature to the low publication potential of investigations with failure. Another inconvenience can be changing salt tolerance of Glomus isolates differing from saline and nonpolluted soils (Ruiz-Lozano and Azcón 2000). Therefore, such experiments are not easy to perform and mimic natural field conditions.

Consequently, increasing scientific and public attention worldwide on sustainable land management have pointed out to sustainable use of saline-alkaline soil resources through the approaches such as breeding of salt-tolerant plants, engineering plants using different genes, and leaching of excessive salts or desalinizing seawater for irrigation purposes (Evelin et al. 2009). However, most of these approaches are laborious and costly for developing countries (Cantrell and Linderman 2001), and unfortunately, only a few genetic traits of salt tolerance have been explored so far (Schubert et al. 2009). Therefore, an increasing number of investigations have been recently carried to elucidate the role of AM fungi in the alleviation of salinity stress in halophytes (Evelin et al. 2009; Porcel et al. 2012). However, although AM fungi seem to alleviate the salt stress of plants, the results published so far do not appear to be convincing enough.

8.3 Mechanisms of Salinity Tolerance and Utilization

The halophytic microbiome confers salinity tolerance to plants through various mechanisms, indirectly by promoting the plant growth, modifications of root system, and enhancing the supply of certain essential nutrients (Hashem et al. 2016) and directly by influencing the defense system of the plants, through promoting the enzymatic and nonenzymatic defense systems (Ahmad et al. 2015; Wu et al. 2014) in case of AMF, 1-aminocyclopropane-1-carboxylate (ACC) deaminase (Cheng et al. 2007; Mayak et al. 2004), diverse proteins production, accumulation of osmolytes, regulation of genes, and ion transporters, and finally through production of exopolysaccharides (Etesami and Beattie 2018) and buildup of solutes, glycerol being the most common (Zajc et al. 2014), accumulation of Na+ within the cell (Prista et al. 2005), cell wall melanization (Gunde-Cimerman and Zalar 2014), and reducing the membrane fluidity (Gostinčar et al. 2011), in case of fungi.

The salinity besides affecting the growth and production of plants also limits the activity of microbes (Szymańska et al. 2014). Such problems also cause the biochemical and genetic adaptation toward saline habitats. Archaea adapt to saline environments through the accumulation of salts within the cytoplasm by the function of intracellular enzymes, whereas bacteria being superior in metabolism adapt to such kind of environments by organic solute accumulation (Margesin and Schinner 2001). Generally, the microbes adapt to such habitats through two major strategies, namely, “high salt in,” in which the stability and activation of proteins are aimed, and “low salt, organic solutes in” in which significant production and accumulation of organic solutes occur (Ma et al. 2010), like Halobacillus recognized as chlorine-dependent species that shows the adaptation toward different levels of salinity through releasing glutamate and glutamine in case of lower and medium salinities and proline and ectoine at higher saline environments (Saum and Müller 2008a, b). These osmoregulators also protect enzymatic structures, leading toward stress tolerance (Lamosa et al. 2000). The mechanisms include salt avoidance through cell membrane modifications, removing the salts out of the cells, and adjustments of the cellular environment by the accumulation of osmolytes, and certain proteins, including enzymes regulations (Ruppel et al. 2013). Finally, the induced systemic tolerance (IST) has also been put forward which is induced by physical and chemical changes with the help of plant growth-promoting microorganisms. The term IST introduced by Yang et al. (2009) encompasses various mechanisms of salinity tolerance showed by microbes. The Bacillus amyloliquefaciens induced salt tolerance in Arabidopsis has been reported, which also led toward an increase in plant biomass (Liu et al. 2017).

8.4 Prospects

The isolation from halophytes and application to the non-halophytic plants has potential benefits, and a growing interest has been shown toward utilization of halophyte-associated microbiome (He et al. 2018; Navarro-Torre et al. 2017; Yuan et al. 2016). The evolution of salinity tolerance by the halophyte-associated bacteria, either endophytic or epiphytic, can enhance the plant tolerance to the level of salinity, thus enhancing the plant growth even in saline environments eradicating the threat of poor growth (Dimkpa et al. 2009). Widespread saline land and the threat of salinization offer the use of halophilic microbes for remediation and reclamation of soils. Secondly, the new insights suggesting the heavy metal phytoremediation through halophytes assisted by associated microorganisms have shown promising results, as many soils are co-contaminated by salts and heavy metals (Lutts and Lefèvre 2015). The potential of plant growth promotion by halophytic microbes can be successfully manipulated, leading toward better plant growth even in heavy metal-polluted soils (Dodd and Pérez-Alfocea 2012). Furthermore, the biotechnological options using halophiles and halotolerant microbes can be explored for novel genes and pathways.

8.5 Application of Microbes

Application of such microorganisms to the plants has been practiced through various mechanisms including seed coating, covering, and inoculation, soil application, root dipping, foliar application, and biopriming, each showing potential merits and demerits (Mahmood et al. 2016). For saline environments, the bacterial survival being an issue, broth culture has been applied for inoculation (Ali et al. 2017). Considering the saline environments, the emergence and initial growth of the plants are limited by higher levels of salts, thus asking for either transplantation of hardened plant nursery or efficient osmoregulation assisted by applied halophytic microbiome, allowing plants to withstand salinity, with lesser or no effects on the plant growth.

8.6 Conclusion

The halophytic microbial associations with plants help the latter not only in salinity tolerance but also in amelioration of the stress besides the supplementary functions. The microorganisms, with variations among the functions, help the plants through enhancing the stress-related characteristics in direct mechanisms, improved nutrient availability, and production of certain metabolites in indirect mechanisms, consequently leading toward better plant growth and survival in saline habitats. This relationship can thus be modified and manipulated for the desired plant growth, where besides bioaugmentation, stimulation of local microbes can be carried out through nutrient management. The microbial aspect integrated with phytoremediation can be more sustainable and economical when compared with other saline soils reclamation strategies. The bio-phytoremediation also offers output from least utilized marginal lands, as feed, if not food.

So far, the literature has revealed that there are certain communications between halophytic plants and diverse endophytic and epiphytic bacteria and fungi in which stress suppression mechanisms are directly or indirectly designed to facilitate the survival of these mysterious plants through harsh environmental periods and conditions in nature. Understanding of these connections is crucial not only for pure-science purposes but also for putting this knowledge into the practice under degraded soil environments, where we might have to grow agricultural plants in the future.