Progress of Euhalophyte Adaptation to Arid Areas to Remediate Salinized Soil

Abstract

With the increasing shortage of water resources, the current management of saline–alkali lands in semi-arid and arid areas has gradually transformed from “flooding irrigation with drainage” in the past to the combination of controlling regional water and salt balance, phytoremediation, and comprehensive utilization of halophyte resources. However, soil salinization caused by natural and anthropogenic factors has still been a major global environmental problem, which changes the chemical and physical properties of soil, deteriorates the quality of underground water, and decreases biodiversity, contributing to the loss of soil productivity and the succession of the halotolerant species. Euhalophytes, as the materials for phytoremediation, have been confirmed to be effective species in improving saline–alkali soils. They can redistribute salts in soil profile through the interaction of their desalinization potential and irrigation water leaching, thereby preventing secondary salinization and improving soil productivity for long-term reclamation of saline soil. In this review, the adaptation mechanisms of euhalophytes to saline soils are generalized from the views of morphological, physiological, and molecular aspects and evaluated for their potential to remediate saline soil through salt removal and promoting leaching. Euhalophytes can not only sequestrate salts inside the central vacuole of cells to tolerate higher salt stress by means of organ succulence, ion compartmentalization, and osmotic adjustment but facilitate water infiltration and salts leaching through root–soil interaction. The root system’s mechanical penetration increases soil porosity, decreases soil density, as well as stabilizes soil aggregates. Moreover, the suitability of phytoremediation in arid situations with low precipitation and non-irrigation and some agricultural practices need to be taken into account to avoid salts returning to the soil as forms of litter and deep tillage altering salt distribution. Hence, euhalophytes planting in semi-arid and arid areas should be evaluated from their adaptation, desalinization, and prospective commercial values, such as foods, biofuels, and medical development to alleviate soil secondary salinization crisis and enhance the productivity of arable agricultural land.

1. Introduction

Soil salinization has become one of the major environmental and socioeconomic issues globally, and it is expected to be exacerbated further with projected climatic change [1]. Saline soils, which contain excess soluble salts, are mainly found in arid and semi-arid regions where rainfall is insufficient to meet crop water requirements and to leach salt from the root zone. Salt accumulation on the topsoil has an adverse influence on the growth and yield of most crops [2]. Statistically, the global salinized soil area has reached 8.33 × 10⁸ ha [3], which has seriously threatened global food security. Especially in semi-arid and arid areas, agriculture is particularly vulnerable to excessive accumulation of soluble salts in soil due to extreme climatic conditions, over-exploitation of groundwater, unreasonable irrigation practices, and overuse of fertilizers [1]. Historically, the remediation of salinized soil in arid or semi-arid regions has successively experienced four stages: flooding irrigation without drainage; flooding irrigation with drainage; drip irrigation without drainage; and comprehensive control, which mainly include four kinds of measures, such as water conservancy project, chemical amendments, agronomic practices and phytoremediation [4]. Therein, as a conventional strategy, water conservancy measures mainly leach salts out from saline soils through flooding irrigation in the ditches, which is easy to cause groundwater level uplift, water quality deterioration, and secondary soil salinization aggravation [5]. Chemical measures, which use amendments, such as gypsum, to improve soil quality, may cause secondary soil pollution if not applied in the right dosage [6]. Agronomic measures mainly control salt accumulation in the root zone by adding ground cover [7] and managing fertilization, but the costs of labor and materials are comparatively higher.

To address the shortage of water resources inland areas, drip irrigation has been widely adopted as an effective water-saving irrigation technology to enhance crop productivity and expand agricultural areas in arid regions. However, long-term drip irrigation without proper drainage has resulted in changes to soil water and salt movement patterns. The limited point source water infiltration from drip irrigation cannot effectively remove salts from the soil matrix, leading to a dynamic balance between leaching and accumulation under the interaction of water infiltration and evaporation. Consequently, salinity levels in the soil matrix have varied vertically, making it difficult to remove salts from affected lands. Statistical data shows that the average annual rate of salt accumulation in film-mulching drip-irrigated cotton fields is 5–10%, and 60–80% of drip-irrigated cotton fields have come forth new issues of secondary salinization [8]. As a result, crop roots tend to concentrate in the shallow soil salinity leaching zone, causing yield losses and posing a significant threat to the productivity of agricultural lands (Figure 1). Therefore, the development of salt-tolerant agriculture is promised as one of the effective ways to increase arable land area and grain yield [9]. Drip irrigation combined with halophytes as a new soil remediation technology has been recommended to decrease water consumption and improve soil quality for the remediation and utilization of salinized lands recently.

Halophytes, which make up less than 2% of all terrestrial flora, have adapted to survive in saline conditions [10]. They can normally grow and develop under high salt situations and complete their life cycle, which is divided into three categories: euhalophytes; recretohalophytes; and salt-exclusion halophytes. Euhalophytes can sequestrate salts inside the central vacuole of cells. Recretohalophyte may excrete salts via specialized glands or vesicles at the leaf surface. While salt-exclusion halophytes can refuse or rarely absorb salts from outside due to the lower permeability or impermeability of the plasma membrane of root cells or directly store salts in the roots while not transported to the shoots [11]. Among them, euhalophytes can not only tolerate higher salt stress and store soluble salts through being equipped with mechanisms to tolerate osmotic, ion, and oxidative stresses, such as osmotic regulation [12], organ succulence [13], ion compartmentalization [14,15], as well as reactive oxygen species (ROS) homeostasis for decreasing soil salt concentration. The large-scale cultivation of euhalophytes can increase vegetation coverage to weaken salt accumulation on the soil surface [16]. As a result, halophyte planting in semi-arid or arid areas, as a promising approach for the remediation of salinized soil, has attracted extensive attention in recent years. This pattern will redistribute soil salts in the soil profile under the interaction of plant adsorption and irrigation water leaching, thereby improving salinized soil and preventing soil secondary salinization for long-term reclamation of the salinized soil.

This review explores and describes the response of euhalophyte to salinized soil in detail to provide context for a discussion regarding adaptive remediation mechanisms employed by halophytes in salinized soils. Halophyte-driven phytoremediation with low-cost salt removal can be utilized to integrate remediation strategies to minimize soil degradation through absorbing salts, improving soil properties, regulating water and salt movement, and creating habitats for crops and native species. Moreover, the harvested halophytes might be made into useable by-products, including biochar, fodder, compost, and biological salt, which is of great significance for the implementation of farmland salt balance and ease of secondary soil salinization in semi-arid and arid areas.

2. Hazards of Soil Salinization

Currently, the semi-arid and arid regions have the widest distribution range of salinized soil and the heaviest soil salt accumulation. Furthermore, the degree of secondary salinization has the tendency to increase year by year because of climate changes and anthropogenic intervention in agricultural management, including the rise of groundwater table caused by flooding irrigation, the buildup of agricultural soil salts caused by drip irrigation [17] and the increase in soil salt content led by excessive chemical fertilizer application [18]. Secondary salinization of soil is one of the main causes of crop failure, threatening global food security by affecting the quality and quantity of arable land in agricultural ecosystems. Soil soluble salts in the saline–alkali lands contain mainly some inorganic ions, such as sodium, calcium, and the following associated anions: chloride, sulfate; and carbonate [19]. Their excessive accumulation has severally affected the normal growth and development of crops except for salt-tolerant plants. Traditionally, soils with ECe ≥ 4 dS m⁻¹ (25 °C, Salinity Laboratory, United States Department of Agriculture) are considered saline soils, which vary actually according to plant species, climatic conditions, water–salt balance, and salt tolerance of sensitive plants or crops [20]. Salt stress can not only destroy transpiration in leaves of plants, reduce water uptake by roots and lead to osmotic stress [21,22], but excessive salts contribute easily to plant nutrient imbalance. Salt content with >4 dS m⁻¹ can decrease the yield of sensitive crops. Above 8 dS m⁻¹, most plants or crops will struggle to grow [23]. Additionally, soil salinity can weaken the biological functions of soil microorganisms [24], thereby interfering with soil respiration, nitrogen cycling, and organic matter input [25]. Conversely, vegetation loss may abate soil stability, making soil susceptible to geomantic erosion [26], and the dispersal of salt dust from salinized soil, abandoned farmland, and desertification land will further threaten environmental health and restrict the development of local society and economy [27].

Consequently, comprehensive exploration and utilization of saline–alkali lands have a profound influence on ensuring national food security and satisfying everyone’s food needs. In semi-arid and arid regions, management of these lands has evolved from the outdated practice of “leaching salts with flood irrigation” to creating a soil environment conducive to crop growth through a combination of controlling regional water and salt balances and implementing phytoremediation. These efforts are aimed at tackling the core problems of the unsuitability of salt-alkaline land for crop growth.

3. Response of Growth and Development of Euhalophytes to the Salinized Soils

Compared with recretohalophytes and salt-exclusion halophytes, euhalophytes, known as dilute salt halophytes, are kinds of real desalinizing plants that dilute the salts entering cells through organ succulence, ion compartmentalization into the vacuole, osmotic adjustment to avoid salt damage and bring out of salt from the soil matrix. Some strong evidence indicates that euhalophytes can survive and propagate in salinized habitats with a concentration of about 200 mmol L⁻¹ NaCl or higher [12] because they have undergone a series of adaptive changes in their morphological, physiological, and molecular processes to withstand high salt stress (

Table 1. Salt tolerance mechanism of some euhalophytes [30].

Euhalophyte Species	Morphological Adaptation	Response to Salt Stress	Specific Mechanism
Suaeda Salsa	Succulence	Salt accumulation	Vacuolar sequestration of Na+; high NHX expression in leaves; SOS in roots
Salicornia europaea	Succulence	Salt accumulation	Na+ sequestration in succulent stems
Zygophyllum xanthoxylum	Succulence	Salt accumulation	Up regulation of ZxAKT1
Puccinnellia nuttalliana	Succulence	Salt accumulation	Vacuolar sequestration of Na+
Salicornia herbacea	Succulence	Salt accumulation	Induction of shikimic acid, vitamin K1, and indole-3 carboxylic acid
Cochlearia pyrenaica	Succulence	Salt accumulation	Na+ sequestration in leaves; high NHX expression in leaves; HKT in roots
Arthrocnemum macrostachyum	Succulence	Salt accumulation	Endophytic bacteria
Suaeda maritima	Succulence	Salt accumulation	Accumulation of proline and glycine betaine
Salvadora persica	Epidermal thickening	Salt accumulation	Increase in amino acids, reducing sugars, and proline
Beta vulgaris ssp. maritima	Succulence	Salt accumulation	High osmotic adjustment and succulence index; up-regulation of genes related to photosynthetic carbon fixation, ribosome biogenesis, cell wall-building and cell wall expansion
Sesuvium portulacastrum	Succulence	Salt accumulation	Vacuolar sequestration of sodium, increase in osmolytes, overexpression of proteins involved in ion binding, proton transport, photosynthesis, and ATP synthesis; activation of V-ATPase

), and they even can grow continually under the salinity of 200–400 mmol L⁻¹. However, below or above the optimal salinity, the biomass would decrease [28,29] and show a “curvilinear” response to salt, which may be related to the change in cell size induced by salt. Generally, salt content in the euhalophytes can reach more than 20% of the dry weight, such as Suaeda Salsa (S. salsa) and Salicornia europaea (S. europaea); their salt content may reach up to 30–40%, and they are called “highly enriched NaCl” plants [15]. Most of them belong to Chenopodiaceae and are mostly distributed in temperate desert areas, where the climate is extremely arid with annual precipitation of less than 250 mm.

3.1. Euhalophytes Morphological Adaptation to the Salinized Soil

In arid salinized soil, the deleterious effects of salt stress are commonly thought to result from low water potential, ion toxicity, and oxidative stresses. The morphological response of euhalophyte to salt stress is mainly manifested in organ plasticity, such as a leaf or stem specialization and root adjustment. On the aboveground, organ succulence, as one of the important markers, reflects the ability of plants adaptation to drought or salt stress. The succulent leaves and their surface attachments, such as cuticle and wax, could minimize the transpiration area and stoma numbers to retain the intracellular water for the plant’s survival. Previous studies showed that smaller leaves, fewer stomata per unit leaf area, thicker leaf cuticle, increased leaves or stem succulence [31], and wax deposition are the most basic morphological adaptation characteristics of euhalophytes [32], which are conducive to water interception for plant growth and utilization. Therein, succulence is also one of the most important evolutionary strategies for euhalophytes to grow in salinized habitats. Studies have shown that NaCl is an effective factor for inducing succulence formation in euhalophytes [33,34,35]. NaCl treatment can increase the number of aquaporins in plasma and vacuolar membranes and cell wall thickness [36]. Additionally, Na⁺ can promote ATP synthesis and participate in cell wall extension, thus increasing the degree of plant succulence [33]. In turn, succulence enhances the water content per unit weight [37] or per unit volume [38] of cells by increasing the number of parenchyma cells, increasing their size, and storing large amounts of water, so as to maintain the steady salt concentration in the plant. Meanwhile, succulent leaves may reduce the transpiration area of plants and improve the water use efficiency in arid salinized habitats. In the euhalophytes with succulent leaves, such as Suaeda, Salsola, Kalidium, and Anabasis, water-storing parenchyma cells in the palisade tissue of leaves account for more than 60% of the leaf radius [39]. In the euhalophytes with succulent shoots, such as S. europaea and Haloxylon ammodendron, their leaves mostly degenerate into the basal leaves, and succulent green branches have become the assimilative organs, which can involve in photosynthesis.

Take S. salsa as an example of a model plant for salt tolerance research is a typical annual euhalophyte, which widely distributes in the intertidal zone and inland saline areas. Besides the above morphological adaptation (leaf succulence), S. salsa can produce brown and black heteromorphic seeds after long-term ecological adaptation. In order to adapt to a diverse salt stress environment, these two types of seeds have obvious differences in morphology, dormancy, and germination [40]. The size of brown and black seeds in the intertidal zone is 4.2 and 5.5 times that of brown and black seeds in inland salinized habitats, respectively [41,42]. At the germination stage, brown seeds have a higher water absorption rate and salt tolerance than black seeds due to their soft seed coat and high contents of ions, phenols, flavonoids, and carrots [43]. Compared with seedling germinated from black seeds, seedlings produced from brown seeds grew well under 300 mmol L⁻¹ NaCl and had higher salt tolerance [44]. In the vegetative growth stage of S. salsa, low salt can obviously promote its seed germination and seedling formation [42]. Plant height, branching, and biomass have a significant increase in lower salt stress [45]. During the reproductive growth stage of S. salsa, the total number of flowers, pollen viability, and seed yield [46,47] were comparatively higher in low salt stress. While the salinity exceeded its optimum level, the growth and development of S. salsa showed a significant downward trend [48], and high salt stress could significantly reduce the biomass, including root biomass and root–shoot ratio [49], and delay flowering or even not flowering.

On the belowground, the root is the direct part of plant contact with soil, and its morphological characteristics, distribution depth in the soil profile, and physiological functions can directly affect the use efficiency of soil nutrients and water, the size of plant subsurface nutrient space, and the growth and yield of the shoots. Moreover, root system mechanical penetration, such as the physical extension of the root system, can directly participate in the flow and adsorption of soil water and nutrients and also loosen soil structure and enhance soil fertility. In salinized habitats, the response of root morphological changes to salt signals reflects the adaptability of halophytes to saline habitats. Studies have shown that the root system can not only determine the ability of halophytes to survive, adapt and modify their habitats but determine shoot biomass and phenology and affect soil water and salt transport [50]. At the early growth stage, photosynthates were mainly allocated underground for the rapid formation of the root system to ensure the adaptation of halophyte roots to soil salinity [51,52]. At the later growth stage, the shoots/roots ratio of halophytes was significantly higher than that of non-halophytes [53].

From the perspective of morphology, lengthening, and thinning of roots is an important response and adaptation strategy of euhalophyte responding to nutrient and salt stress [54,55]. Under drip irrigation in arid areas, crop roots were mainly distributed in the shallow salt-leaching area below the drip head [56], and brackish water irrigation easily reduced the distribution density of roots in the shallow layer, which was not conducive to root penetration [57]. Whereas, compared with glycophytes, root biomass, root length, and surface area of euhalophytes have corresponding increases to accelerate the nutrient uptake under low or moderate salinity stress, while high salt stress resulted in increased root density to improve salt tolerance [58,59]. Moreover, the root length and root surface area of halophytes had a non-monotonic relationship with the increasing salinity, while glycophytes showed a monotonic decreasing trend [60]. From the perspective of root architecture, the roots of euhalophytes showed the characteristics of “salinity tropism”. The roots with high salt tolerance were more distributed in the high-salt area; for example, the roots of S.europaea were more distributed in the shallow high-salt area. Conversely, the root system of glycophytes (e.g., Lepidium apetalum) concentrated more in the deep soil layer with less salt to avoid high salt stress [35]. Therefore, euhalophytes can also reduce or limit the uptake of ions by altering the root morphology and architecture, thus minimizing the transport of ions to shoots.

3.2. Euhalophytes Physiological Adaptation to the Salinized Soil

In the salinized habitat, ion toxicity, nutrient adsorption and transport, and water deficit caused by Ca²⁺ and K⁺ imbalance are the three main limiting factors affecting plant growth. Euhalophytes that grow in the salinized soil rely on osmotic adjustment to transmembrane transport of Na⁺, Cl^-, K^+, and other inorganic ions into vacuoles through Na⁺/H⁺ antiporters on tonoplast under proton driving force provided by V-H⁺-ATPase and V-H⁺-PPase. This maintains the stability of osmotic potential and turgor pressure and promotes water adsorption from habitats. Through this, they would overcome the difficulty of water uptake caused by the decline of soil water potential to avoid the disorder of physiological, biochemical, and other metabolic processes caused by excessive accumulation of ions in the cytoplasm. Meanwhile, euhalophytes also can synthesize compatible organic molecules, such as proline, betaine, and sorbitol, which are accumulated in the cytoplasm to balance the decrease in osmotic potential caused by Na⁺ and Cl^- in vacuoles, thus stabilizing protein structure and function and protecting endomembrane system. The mechanism of euhalophyte to tolerate osmotic and ion stresses is called ion compartmentalization, which is one of the important physiological measures for euhalophytes to adapt to salinized habitats [12,15].

Under salinized circumstances, euhalophyte is able to maintain adequate homeostasis between the formation and removal of ROS through particular enzymatic pathways or antioxidants. Studies showed that PSⅡ activity and net photosynthetic rate of euhalophyte growing in mildly salinized habitats were both higher [61]. However, the photosynthetic system was significantly inhibited in the heavily salinized habitats, such as photosynthetic pigments (chlorophyll), net photosynthetic rate and actual photochemical efficiency, maximum photochemical efficiency, photosynthetic oxygen release rate, and stomatal conductance all decreased significantly [52,61,62,63]. Similarly, the dynamic balance of ROS accumulation and removal in plants is easily destroyed. O₂•⁻, HO•, and H₂O₂ can cause oxidative stress, which damages membrane lipids, proteins, and nucleic acids, thereby interfering with normal metabolism. Euhalophyte has an effective antioxidant reaction system to avoid oxidative injury. For example, the activities of some antioxidant enzymes, such as superoxide dismutase (SOD), anticyclonic acid peroxidase (APX), peroxidase (POD) in chloroplasts, catalase (CAT), and glutathione reductase (GR) in peroxisome have increased with the increase in salinity [64,65,66,67]. This antioxidase could scavenge O₂•⁻, HO•, and H₂O₂ to protect cells from oxidative damage and improve the antioxidant capacity of plants. Moreover, NO, as a small bioactive molecule, also activates antioxidant systems to keep enhalophyte’s homeostasis of the redox process under different constraints, such as drought and salt stress [68]. Therefore, the ROS removal system is another important strategy for adapting to salinized habitats.

3.3. Euhalophytes Molecular Adaptation to the Salinized Soil

Euhalophytes have evolved some dominant genes to adapt to diverse saline habitats after long-term evolution. Previous studies showed that several salt stress-related genes expressed at a higher salt level had been explored, and these genes could predominantly compartmentalize inorganic ions (e.g., Na⁺) in the vacuoles to regulate the osmotic balance in the vacuole [69]. For example, the NHX1 and its encoded proteins (Na⁺/H⁺ antiporters) are thought to contribute to the vacuolar compartmentalization of Na⁺ in the euhalophyte [70], and the transcript amounts of NHX1 increase significantly with NaCl addition. SsNHX1 expression in succulent leaves of S. salsa and SeNHX1 in succulent shoots of S. europaea were up-regulated by the increasing NaCl stress [71,72]. Furthermore, salt also significantly induced the relative expression of Na⁺/H⁺ antiporter gene SsSOS1 in the plasma membrane of S. salsa [73,74]. In salinized habitats, SsSOS1 is preferentially expressed in the roots of S. salsa, promoting Na⁺ effluence. While expression level of SsNHX1 is comparatively higher in different organs of S. salsa, which in leaves is higher than that in roots. It mainly promotes Na⁺ sequestration into vacuoles. Therefore, in S. salsa, SsSOS1, and SsNHX1 genes can cooperatively control the Na⁺ transport system to regulate Na⁺ homeostasis and improve their tolerance to the salinized habitats, implying an efficient transcriptional regulatory network for salt stress response existence in halophytes [30].

Additionally, the changes in the activity and protein expression of H⁺-ATPase and H⁺-PPase on tonoplast are consistent with the accumulation of Na⁺, indicating that the tonoplast proton pump plays an important role in Na⁺ compartmentalization [73]. VHA-A/B and VP1 genes (responsible for V-H⁺-ATPase and V-H⁺-PPase, respectively) in the euhalophyte were up-regulated under salt stress for increasing their activity to provide the proton driving force for sequestering Na⁺ in leaf or shoot vacuoles [75]. Based on this, the leaf and stem are the main salt accumulation organs of euhalophyte. At low salt concentrations, Na⁺ in leaves and stems of S. salsa is about 6.4 and 7.5 times that of roots, accounting for approximately 93% of the Na⁺ content in the entire plant [76]. When these salt-responsive genes screened from euhalophyte, they were transplanted to crops through transgenic technology, which can improve their salt tolerance or resistance. Studies indicated that the tomato transformed with SsNHX1 cultured in 300 mmol L⁻¹ NaCl concentration could accumulate less Na⁺ in the leaves and maintained a higher K⁺/Na⁺ ratio than the wild-type; and the dry weight, the net photosynthetic productivity of the leaves were also much higher in transgenic plants [77]. A similar result was reported in the rice transformed with SsNHX1 with a higher K⁺/Na⁺ ratio in leaves than the wild-type under saline conditions [78]. Transgenic NHXI-expressing tobacco seedlings exhibited significant growth advantage under salinity, and NHXI overexpression can accumulate Na⁺ in the stem, thereby protecting the leaf from salt-induced injury [79]. These research findings could stimulate the genetic potential of euhalophyte with the aim of constructing tolerant crops. Consequently, these manipulations of salt-tolerant genes being screened are transplanted to common crops, and then the salt-tolerant crops are selected by directive breeding, which can shift the ideas of saline lands remediation for aid to crop growth to the tolerance and adaptation of crops to saline lands, thereby stimulating the potential utilization of the saline–alkali lands.

4. Effects of Euhalophytes on Improvement of the Salinized Soil

Soil salinization has gradually deepened in arid and semi-arid regions. In these areas, the competition for freshwater resources among agriculture, households, and industry has gradually increased [80,81]. In order to alleviate the contradiction between salinization aggravation, water shortage, and economic and social rapid development, it is imperative to reasonably domesticate and utilize halophytes to improve the salinized lands. Understanding the response patterns of euhalophyte to soil salinity will provide us with a holistic view of how plants adapt to abiotic and biotic stress and enable us to develop advanced strategies to enhance the tolerance of different crops to stress conditions. Therefore, as a low-cost and environmentally friendly biological measure, phytoremediation by halophytes that restrict disturbance to the soil and associated ecosystems has been gradually applied to the improvement of the salinized soil.

4.1. The Ability of Euhalophytes to Remove Salt

Currently, the increasing soil salinization makes people focus closer on the effect of phytodesalinization on soil restoration. As a result, the research on halophytes in saline agriculture gradually shifted from laboratory and small-field trials into large-scale commercial production. Euhalophytes, for their potential desalinization, have been extensively involved in rehabilitating saline–sodic or salt-affected lands. Generally, the desalination capacity of euhalophytes is determined by both salt content and biomass of plant at harvest; therefore, biomass and ash concentration were considered as two dominant reference factors for calculating plant salt output in saline–alkali land [82]. Although Barrett-Lennard [83] predicted that it would take 20 years of continuous rotation to remove the initial 50% of soil salinity if halophyte containing 25% salinity content was harvested with biomass of 10 × 10³ kg/ha per year under non-irrigated conditions, these research findings were insufficient to explain the phenomena that crop can grow under less than limited desalination of 6% in 0–30 cm soil tillage layers, implying that other mechanisms probably existed in the root–soil process underground to decrease the soil salinity.

In phytodesalinization, recent results showed that euhalophytes, as salt accumulators, have been used successfully for the reclamation of saline and sodic soils [84]. Such species as S. europaea, S. salsa, and Atriplex centralasiatica can reduce soil salinity and can improve the soil by increasing soil organic matter, the available nutrients of N, P, K, and the number of bacterial and fungal populations [85]. Aboveground parts of euhalophytes can remove certain amounts of salts from the soil and effectively reduce the salt content of the salinized soil wherever they grew in the fields or pots [86,87] (

Table 2. Salt removal capacity of some euhalophytes.

Halophyte Species	Planting Condition	Planting Style	Planting Duration	Reported Na+ Removal (t hmࢤ2 per Year)		Reference
				Total Salt	Na+
Suaeda salsa	Bare field	Continuous cropping	3 years	3.81	/	[89]
Suaeda salsa	Bare field	Intercropped with cotton	3 years	0.43–0.47	/	[93]
Suaeda salsa	Pots	Monoculture	1 year	/	3.09–3.86	[38]
Suaeda salsa	Bare field	Monoculture	120 days	/	1.25–1.92	[38]
Suaeda salsa	Bare field	Monoculture	1 year	5.19	/	[94]
Suaeda salsa	Field with drip irrigation	Monoculture	1 year	3.06	/	[92]
Salicornia europaea	Non-grazing land	Wild conditions	1 year	0.43–0.48	/	[91]
Salicornia europaea	Grazing land	Wild conditions	1 year	0.18–0.24	/	[91]
Salicornia europaea	Bare field	Monoculture	1 year	4.71	/	[94]
Salicornia europaea	Field with drip irrigation	Monoculture	1 year	2.08	/	[92]
Suaeda fruticosa	Field	Monoculture	180 days	/	0.22	[95]
Suaeda fruticosa	Pots	Monoculture	170 days	/	0.80	[96]
Suaeda maritima	Field	Monoculture	120 days	/	0.20	[97]
Suaeda altissima	Field with drip irrigation	Monoculture	1 year	3.50	/	[92]
Salsola soda	Pots	Monoculture	1 year	/	0.71	[98]
Arthrocnemum indicum	Field	Monoculture	1 year	/	1.65	[96]
Arthrocnemum indicum	Pots	Monoculture	170 days	/	0.71	[96]
Sesuvium portulacastrum	Pots	Monoculture	170 days	/	2.50	[96]
Sesuvium portulacastrum	Field	Monoculture	120 days	/	0.18	[96]
Atriplex aucheri	Field with drip irrigation	Monoculture	1 year	2.18	/	[92]
Portulaca oleracea	Pots	Monoculture	1 year	/	0.28	[98]
Atriplex nummularia	Field	Monoculture	1 year	/	2.48	[99]
Atriplex lentiformis	Field	Monoculture	1 year	/	0.49	[100]
Tecticornia indica	Field	Monoculture	180 days		0.75	[95]

). Studies also showed that the ash accumulation of euhalophytes belonging to Chenopodiaceae is about 187.4–447.9 g kg⁻¹, and soluble salts absorbed from the soil are up to 300–400 g kg⁻¹, accounting for about 30–40% of the dry weight of plants [88]. S. salsa could absorb 3228.8 kg/ha Na⁺ from the salinized soil under 225 kg/ha nitrogen application [34]. Besides absorption of Na⁺, S. salsa also has a strong ability to absorb Cl⁻ and SO₄²⁻, which is an important material for biological desalination in undrained irrigation areas [69]. In the arid region, the annual salts removed from the soil were as high as 3749–3911 kg/ha after three years of S. salsa’s consecutive cropping. After calculation, salts contained in the quota drip irrigation water can be completely taken away; salts in the soil matrix were partly removed, and most of them would leach downward to below 60 cm [89]. S. europaea also played an important role in salt removal. The content of Na⁺ and Cl^- in S. europaea accounted for about 35.5% of the dry weight [90]. In the grazing land and non-grazing land, salts can accumulate 182–237 kg/ha and 426–475 kg/ha per year, respectively [91]. The average annual soil salts removal by S. salsa, S. europaea, Suaeda altissima, and Atriplex aucheri planting under film-mulching drip irrigation was about 3061, 2080, 3499, and 2180 kg/ha, respectively [92].

4.2. The Factors Affecting Euhalophytes to Remove Soil Salt

Large biomass and high ash concentration were considered the best biological measure for salinized soil improvement. By contrast with several euhalophytes above, S. salsa has a high economic value, large biomass, and high ash concentration and is regarded as the best biological material for desalinization in arid areas. Some evidence showed that large-scale S. salsa cultivation with a duration of 2–3 years in saline soil had obtained the remarkable effect that normal growth of common crops could be achieved and a high yield harvested [94]. Therefore, planting strategies for S. salsa in arid areas, where soil nutrient traits are characterized by high potassium and low nitrogen and phosphorus levels, should focus on maximizing aboveground biomass and belowground extension of the root system for nutrient and salt acquisition in order to achieve high yields and increase salt adsorption. This can be achieved by optimizing nitrogen fertilizer input as basal manure and top dressing in the rooting zone, regulating root system growth, and manipulating root–soil interactions.

In general, sowing seeds of S. salsa could be carried out from April to May with a sowing capacity of 15–20 kg/ha as the mean of broadcast along drip irrigation belts in arid regions. Urea fertilizer is applied to the soil through the coupling of water and fertilizer four–five times, and the total amount is about 450–600 kg/ha. Nitrogen application can enhance the salt tolerance of S. salsa and adjust nutrient allocation into the root system so as to possibly absorb more salinity. Recent studies demonstrated that nitrogen application displayed significance in improving the growth of S. salsa with a “dose effect” in light and moderate salinized soil; to some extent, high nitrogen use efficiency could determine the root architecture and distribution through enhancing root formation, such as taproot development and lateral root elongation. Additionally, adequate nitrogen was beneficial for Na⁺ and Cl⁻ uptake, probably due to increasing the synthesis of osmotic substances (e.g., proline, betaine) to mitigate salt stress [101]. So as to acquire the large biomass and salt removal amount of S. salsa, nutrients, especially nitrogen input, are essential to improve the salinized soil.

4.3. The Effect of Euhalophytes to Remediate the Salinized Soil

The desalination amounts of euhalophytes acquired in the saline–alkali lands were possibly used to estimate gross residual amounts of the soil salts. We found that compared with less than 10% of the desalinization, more than 90% of salt in the salinized soil could be discharged downward out of the soil matrix under planted S. salsa [102]. Based on this phenomenon, we speculate that besides biological desalination, the root–soil processes led by euhalophytes after colonization, such as rhizosphere, soil, and microbial processes, change the soil ecological environment and speed up the vertical movement of water and salt.

4.3.1. Effects of Euhalophyte and Crop Intercropping on Soil Salinity

Euhalophytes can improve soil quality in other ways rather than simply removing salt. Under interaction with irrigation, soil water and salt dynamics show obvious synchronicity. With salt transport from the surface down, salt content on topsoil decreased significantly. Studies using S. salsa showed that whether they were planted in the field or abandoned lands, monoculture or intercropping with crops have promoted salt leaching, thereby reducing soil salinity. Compared with non-halophytes bare lands, salinity in the 0–30 cm soil layer in the S. salsa cultivated lands showed a greater decrease, and that of the 30–60 cm soil layer also presented a decreasing trend [94]. With the increase in planting years, the salt accumulation zone in the newly reclaimed bare land has gradually migrated downward in the soil, which was in the 20–40 cm soil layer after one year, and reached the 40–60 cm soil layer after two years, and kept below 60 cm after three years [89]. Moreover, compared with cotton intercropping with euhalophytes, soil salinity in the cotton monoculture field, which was affected by long-term drip irrigation, showed a steady dynamic of desalinization. The salt leaching zone remained at 0–20 cm, and salts varied drastically. The transition zone was in the middle, with a stable salt variation. Moreover, heavy salt accumulation zone occurred at 50–60 cm [103]. After cotton intercropping with euhalophytes, it was found that soil physical properties had significantly improved, soil bulk density planted with S. salsa and S. europaea decreased by 20.12% and 13.77%, respectively, and soil porosity increased by 35.54% and 23.27%, respectively, which significantly reduced soil salt content and increased cotton yield [93,104].

Based on the research above, we found that the intercropping system provided a potential pathway for saline soil management to improve crop adaptability and crop yield in arid areas. Cotton/S. salsa, maize/S. salsa, and cotton/S. salsa/alfalfa strip intercropping systems have gradually been established from the perspective of euhalophyte desalination and biofertilization in these regions. Euhalophyte can gather the salt surrounding the root zone besides decrease in soil salt content through aboveground physiological processes and their root system architecture to facilitate crop growth. However, interspecific belowground salt facilitation and nutrient competition caused by euhalophyte should be focused on in the rhizosphere and root–soil processes. Previous field and pot trials had manifested that maize/S.salsa intercropping could significantly reduce Na⁺ contents, whereas decreasing the maize biomass duo to nutrient competition, particularly nitrogen [101], within that nitrogen acquisition of cotton by intercropped alfalfa was an effective approach to compensate for nitrogen deficiency caused by S. salsa in the cotton/S. salsa intercropping system [93].

4.3.2. Effects of Euhalophytes on the Saline Soil Physical Properties

Root systems in rhizosphere soil could affect soil porosity and permeability through preferential water flow channels, alter soil structure, and promote soil water interception by releasing some rhizosphere exudates, such as organic acids, mucilages, and phosphatases. The growth and extension of plant roots might stimulate microbial activities and accumulate large amounts of organic matter to enhance the stability of soil aggregates [105], thus reducing soil macropores, increasing soil micropores, and improving the water-holding capacity of the soil [106]. Root exudates, in addition to stabilizing the rhizosphere soil, can also change the hydraulic properties of the soil by reducing the saturated hydraulic conductivity of the rhizosphere [107,108]. However, in non-rhizosphere soil, the improvement of soil physicochemical properties and structure by plant roots can improve soil permeability and promote salt leaching [67,109]. Some pieces of evidence pointed out that the planting of S. salsa in heavily salinized soils can reduce soil bulk density, improve porosity, increase the proportion of large pores, and enhance water infiltration, with significant differences in the 0–20 cm soil layer compared to bare ground. At the same time, the initial, stable, and cumulative infiltration rates of soil in the halophyte field were 2.5, 3.0, and 3.6 times higher than those in the bare field, respectively [102]. Therefore, S. salsa has a certain contribution to constructing a benign soil structure. So, it is inferred that the root–soil interaction of S. salsa performs an important role in improving soil structure and promoting the downward leaching of salt.

4.3.3. Effects of Euhalophytes on the Saline Soil Chemical Properties

Besides the physical processes induced by the root system in the rhizosphere and soil matrix, the chemical processes that occurred in euhalophyte planting lands also pose a vital role in remediating the salinized soil and discharging the salt. Euhalophytes could reduce soil pH by releasing CO₂ from the roots and solubilizing CaCO₃ [110]. Root activities and organic matter decomposition of euhalophytes could increase the CO₂ partial pressure in the root zone, thereby enhancing the solubility of CaCO₃ in the soil. Similarly, Ca²⁺ in the soil solution would transfer excess Na⁺ absorbed on soil colloids out of the soil matrix [111,112] (Figure 2). Euhalophytes, similar to all plants, also increase soil organic matter, sequester soil carbon and recruit salt-tolerant microorganisms. The root exudates of euhalophytes are mainly sugars, lipids, steroids, nucleic acids, polypeptides, organic acids, hormones, vitamins, etc. Such exudates not only reduce soil rhizosphere pH and increase and activate soil nutrients but also increase the variety and number of microorganisms [113]. Root-specific exudates enhance the salt tolerance of euhalophytes by changing the number and composition of microorganisms, thereby promoting the absorption of mineral nutrients and the synthesis of hormones [114,115].

4.3.4. Effects of Euhalophytes on the Saline Soil Microbial Diversity

The microbial diversity in the salinized bare soil is generally low, but there is a significant increase in bacterial diversity and biomass in the salinized soil with growing euhalophytes, and the number of microorganisms in the rhizosphere soils is significantly higher than in the non-rhizosphere soils [116,117]. After 10 years of continuous halophyte cropping in the salinized soil, the number of soil microorganisms increased by nearly 65%, and the community characteristics also changed significantly, especially halophilic bacteria, with the ratio of bacteria to fungi increasing by 1.65-fold, thus improving the soil fertility [113,118]. In addition, the salt-tolerant micro-organisms isolated from the euhalophyte soil inoculate into the soil where crops are grown, which can significantly improve crop growth and resistance to salt stress. For example, S. salsa root-associated bacteria Providencia vermicola BR68 and fungi Sarocladium kiliense FS18 could effectively promote the growth of maize seedlings and improve their physiological traits to alleviate salt damage under the high NaCl concentration via changing soil properties, maize physiologies, and certain microorganism abundance [119]. Thus, microorganism also provides viable materials for studying the mechanisms of how plants respond and acclimate to high salt concentrations.

5. Conclusions

Euhalophytes can not only effectively remove soil salt through the leaf or stem succulence but hinder soil salt accumulation by increasing vegetation cover and improving soil physical and chemical properties through the root–soil interaction to accelerate underground salt discharge. This process may play an important role in improving the saline–alkali lands because the growth of the root system can reduce soil bulk density, increase soil porosity, improve water infiltration, and then promote the salt leaching out of the soil matrix. However, the interaction mechanism of root–soil remains questionable in how it affects the movement of water and salt, and the response and adaptive improvement mechanisms of the root system to the saline habitats have not been clarified.

Presently, euhalophytes cultivation in situ heavy salinized soils has been widely applied to improve and remediate the saline–alkali soil. Especially, the intercropped combination of ecological, economical euhalophytes varieties (e.g., S. salsa), leguminous green manure varieties (e.g., alfalfa) with common crops (e.g., maize and cotton) has been established as a technology system in terms of water-saving and salt-suppression, biological desalinization, biological fertilization for improvement and utilization of the saline–alkali land. However, there are still some issues that need to be taken into account in the planting and management processes; (i) plant organs with high salt concentration could be returned to the soil as forms of litter; (ii) deep tillage would bring the salts accumulated on topsoil into the subsoil and alter the patterns of salt distribution; (iii) planting density may affect the desalinization process by determining up-ground biomass and down-ground roots function. Moreover, euhalophytes planting in the arid regions should be evaluated overall from their desalinization and prospective commercial values, such as foods, biofuels, medical development, etc., to alleviate soil secondary salinization crisis and enhance the productivity of arable agricultural lands (Figure 3).