Adaptive Mechanisms of Halophytes and Their Potential in Improving Salinity Tolerance in Plants

doi:10.3390/ijms221910733

Review

. 2021 Oct 3;22(19):10733.

doi: 10.3390/ijms221910733.

Adaptive Mechanisms of Halophytes and Their Potential in Improving Salinity Tolerance in Plants

Md Mezanur Rahman¹, Mohammad Golam Mostofa^{1

2}, Sanjida Sultana Keya¹, Md Nurealam Siddiqui², Md Mesbah Uddin Ansary³, Ashim Kumar Das⁴, Md Abiar Rahman⁴, Lam Son-Phan Tran^{1

5}

Affiliations

¹ Department of Plant and Soil Science, Institute of Genomics for Crop Abiotic Stress Tolerance, Texas Tech University, Lubbock, TX 79409, USA.
² Department of Biochemistry and Molecular Biology, Bangabandhu Sheikh Mujibur Rahman Agricultural University, Gazipur 1706, Bangladesh.
³ Department of Biochemistry and Molecular Biology, Jahangirnagar University, Savar, Dhaka 1342, Bangladesh.
⁴ Department of Agroforestry and Environment, Bangabandhu Sheikh Mujibur Rahman Agricultural University, Gazipur 1706, Bangladesh.
⁵ Institute of Research and Development, Duy Tan University, Da Nang 550000, Vietnam.

PMID: 34639074
PMCID: PMC8509322
DOI: 10.3390/ijms221910733

Review

Adaptive Mechanisms of Halophytes and Their Potential in Improving Salinity Tolerance in Plants

Md Mezanur Rahman et al. Int J Mol Sci. 2021.

. 2021 Oct 3;22(19):10733.

doi: 10.3390/ijms221910733.

Authors

Md Mezanur Rahman¹, Mohammad Golam Mostofa^{1

2}, Sanjida Sultana Keya¹, Md Nurealam Siddiqui², Md Mesbah Uddin Ansary³, Ashim Kumar Das⁴, Md Abiar Rahman⁴, Lam Son-Phan Tran^{1

5}

Affiliations

¹ Department of Plant and Soil Science, Institute of Genomics for Crop Abiotic Stress Tolerance, Texas Tech University, Lubbock, TX 79409, USA.
² Department of Biochemistry and Molecular Biology, Bangabandhu Sheikh Mujibur Rahman Agricultural University, Gazipur 1706, Bangladesh.
³ Department of Biochemistry and Molecular Biology, Jahangirnagar University, Savar, Dhaka 1342, Bangladesh.
⁴ Department of Agroforestry and Environment, Bangabandhu Sheikh Mujibur Rahman Agricultural University, Gazipur 1706, Bangladesh.
⁵ Institute of Research and Development, Duy Tan University, Da Nang 550000, Vietnam.

PMID: 34639074
PMCID: PMC8509322
DOI: 10.3390/ijms221910733

Abstract

Soil salinization, which is aggravated by climate change and inappropriate anthropogenic activities, has emerged as a serious environmental problem, threatening sustainable agriculture and future food security. Although there has been considerable progress in developing crop varieties by introducing salt tolerance-associated traits, most crop cultivars grown in saline soils still exhibit a decline in yield, necessitating the search for alternatives. Halophytes, with their intrinsic salt tolerance characteristics, are known to have great potential in rehabilitating salt-contaminated soils to support plant growth in saline soils by employing various strategies, including phytoremediation. In addition, the recent identification and characterization of salt tolerance-related genes encoding signaling components from halophytes, which are naturally grown under high salinity, have paved the way for the development of transgenic crops with improved salt tolerance. In this review, we aim to provide a comprehensive update on salinity-induced negative effects on soils and plants, including alterations of physicochemical properties in soils, and changes in physiological and biochemical processes and ion disparities in plants. We also review the physiological and biochemical adaptation strategies that help halophytes grow and survive in salinity-affected areas. Furthermore, we illustrate the halophyte-mediated phytoremediation process in salinity-affected areas, as well as their potential impacts on soil properties. Importantly, based on the recent findings on salt tolerance mechanisms in halophytes, we also comprehensively discuss the potential of improving salt tolerance in crop plants by introducing candidate genes related to antiporters, ion transporters, antioxidants, and defense proteins from halophytes for conserving sustainable agriculture in salinity-prone areas.

Keywords: coastal areas; halophytes; phytoremediation; salt tolerance mechanisms; soil salinity; transgenic plants.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

**Figure 2**
Putative salt uptake and accumulation mechanisms in an ideal halophyte plant (modified from Zhao et al. [11], Arif et al. [34], and Arbelet-Bonnin et al. [72]. Na⁺ is transported from soils to/within plant root cells via two major pathways: symplastic and apoplastic. The major transporters/channels embedded in the root epidermis for up-taking Na⁺ are GLRs, CNGCs, LCT1, PIP2, HKT2, HAK5, and AKT1. In the presence of Na⁺, K⁺ is competitively uptaken via HKT2, HAK5, and AKT1. The entrance of Cl⁻ into the root cells is mediated by separate transporters, including NRT. NSCC and GORK channels, on the other hand, are involved in salinity-induced K⁺ exclusion from the root epidermis. Apoplastic barriers, consisting of Casparian bands and suberin lamellae in the epidermis and endodermis of the roots, can block and/or limit the bypass flow of Na⁺ and other solutes moving to the aboveground parts. Passive Na⁺ entry into the xylem is facilitated by NSCCs, while cotransporters like SOS1, CCC, and HKT2 are required for active loading of Na⁺ into the xylem. Na⁺ can return to xylem parenchyma using HKT1. The xylem-loaded Na⁺, K⁺ and Cl⁻ can be transported up through the transpiration stream, and subsequently enter into the aboveground organs via CCC and HKT1. Abbreviations: AKT1, *Arabidopsis* K⁺ transporter 1 (a shaker-type K⁺ channel); CCC, cation-chloride cotransporter; CNGC, cyclic nucleotide-gated channel; GORK, gated outwardly rectifying K⁺ channel; GLR, glutamate receptor-like channel; HKT, high-affinity potassium transporter; HAK, high-affinity potassium uptake transporter; LCT, low-affinity cation transporter; NRT, nitrate transporter; NSCC, non-selective cation channel; PIP2, plasma membrane intrinsic protein; SOS1, salt overly sensitive 1.

**Figure 3**
Putative salt tolerance mechanisms in an ideal halophyte plant (modified from Zhao et al. [11], Arif et al. [34], Arbelet-Bonnin et al. [72], Tran et al. [75], and Himabindu et al. [76]. The absorption of Na⁺ in plant cells is counterbalanced by active Na⁺ extrusion through SOS1 Na⁺/H⁺ exchanger (I). The RBOH-mediated ROS formation in the plasma membrane can activate ANN1-induced Ca²⁺-signaling pathway (I). The Na⁺ bound GIPCs can trigger Ca²⁺ influx through an unknown Ca²⁺ channel (I). Ca²⁺ influx mediated by either ANN1 or GIPCs is essential for activating the SOS-signaling pathway (I). The SOS3 relays salt-triggered Ca²⁺ signals to SOS2 kinase, forming the SOS3-SOS2 protein complex that phosphorylates SOS1 to induce Na⁺ efflux (I). To maintain ion homeostasis, halophytes can also sequestrate excess Na⁺ into the vacuoles and/or excrete Na⁺ via two unique structures, namely salt glands and salt bladders (II and **III**). It is also possible to avoid excessive Na⁺ accumulation in the cytosol by sequestrating it into the vacuoles (IV). Predominantly, Na⁺-sequestration in the vacuoles is conferred by tonoplast-based Na⁺/H⁺ exchangers of the NHX family (e.g., NHX1 or NHX2), fueled by either H⁺-PPase or H⁺-ATPase pumps (IV). Another equally important mechanism of vacuolar Na⁺-sequestration is the efficient control of tonoplast slow vacuolar (SV) and fast vacuolar (FV) activating ion channels, which may allow vacuolar Na⁺ to leak back into the cytosol (IV). Once, if both channels are downregulated or blocked by choline, Na⁺ leakage is inhibited, resulting in an increased level of salt tolerance (IV). On the other hand, Cl⁻ influx in the vacuoles is mediated by CLC (IV). To maintain cytosolic Ca²⁺ homeostasis under saline conditions, the influx of Ca²⁺ into the vacuole is mediated by CAX1 (IV). In response to salt stress, halophytes often accumulate various osmoprotectants, including proline, total free amino acids, sugars, polyols, glycine betaine, and GABA, which play vital roles in conferring an efficient osmotic adjustment (V). In addition, changes in the levels of different phytohormones may also help in stress adaptation; for instance, increased ABA level aids in controlling stomatal closure to maintain better water status at the tissue level (VI). It is worth mentioning that changes in the levels of phytohormones (e.g., JA, SA, and GA) in halophytes under salt stress varies dependently on the type of halophytes (VI). Furthermore, excessive salt accumulation can trigger oxidative stress via overproduction of ROS, such as O₂^•– and H₂O₂ (**VII**). To fight against ROS-mediated oxidative damage, halophytes induce a vibrant antioxidant defense system by activating both enzymatic (SOD, CAT, APX, MDHAR, DHAR, GR, GPX, and GST) and non-enzymatic (AsA and GSH) antioxidants (**VII**). Abbreviations: ABA, abscisic acid; ANN1, annexin1; APX, ascorbate peroxidase; AsA, ascorbic acid; CAT, catalase; CAX, Ca²⁺/H⁺ exchanger; CLC, chloride channel (H⁺/Cl^– antiporter); DHA, dehydroascorbate; DHAR, dehydroascorbate reductase; EBC, epidermal bladder cell; GA, gibberellic acid; GIPC, glycosyl inositol phosphoryl ceramide; GST, glutathione S-transferase; GPX, glutathione peroxidase; GSH, glutathione; GSSG, oxidized glutathione; GR, glutathione reductase; GABA, gamma amino butyric acid; H₂O₂, hydrogen peroxide; JA, jasmonic acid; MDHA, monodehydroascorbate; MDHAR, monodehydroascorbate reductase; NHX, Na⁺/H⁺ exchanger; O₂^•–, superoxide; RBOH, respiratory burst oxidase homolog; ROS, reactive oxygen species; SOS, salt overly sensitive system; SA, salicylic acid; SOD, superoxide dismutase; V-PPase, vacuolar pyrophosphatase; V-ATPase, vacuolar H⁺ ATPase.

**Figure 4**
Putative phytoremediation process by halophyte plants in salinity-affected areas, and their beneficial effects on soil properties (modified from Qadir et al. [140] and Jesus et al. [126]. Deep-rooted plants help reduce soil bulk density and increase soil porosity, enabling storage of excessive salt ions in deeper soil layers through leaching. On the other hand, the reclamation of saline soils needs a source of Ca²⁺ that replaces excessive Na⁺ from the cation exchange sites of soil colloid. Decay of plant parts enhances soil organic matter (SOM) content, leading to the improvement of soil fertility. The microbes-mediated SOM decomposition and root respiration increase the concentration of carbon dioxide (CO₂) in the soil atmosphere. Water (H₂O) from irrigation and soil moisture sources reacts with CO₂ to generate carbonic acid (H₂CO₃). In halophyte roots, H₂CO₃ dissociation and N₂-fixation release proton (H⁺) that enhances dissolution of calcium carbonate (CaCO₃) to release Ca²⁺, H₂O and CO₂. The released Ca²⁺ could help remove Na⁺ from cation exchange sites of soil colloid. Finally, the exchanged Na⁺ can be uptaken by roots, and compartmentalized in aboveground shoots or leached into the deeper layer of soils via irrigation. In non-calcareous soils, an increase in CO₂ induces the release of H⁺, which results in a decrease in the pH of the soil. The acidic nature of soil enhances the dissolution of CaCO₃, which helps reduce the amount of salt ions in soils via Ca²⁺ exchange with Na⁺.

**Figure 1**
Overview on soil salinization across the world. (A) Salinity-affected soil categories *. (B) Types and severity levels of salinity-affected soils. (C) Salinity-affected soils in different parts of the world *. * Due to rounding, the sum may not resemble the actual statistics of salinity-affected lands. Mha, million hectares.

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References

1. Zhang J., Shi H. Physiological and molecular mechanisms of plant salt tolerance. Photosynth. Res. 2013;115:1–22. doi: 10.1007/s11120-013-9813-6. - DOI - PubMed
1. Qadir M., Quillérou E., Nangia V., Murtaza G., Singh M., Thomas R.J., Drechsel P., Noble A.D. Economics of salt-induced land degradation and restoration. Nat. Resour. Forum. 2014;38:282–295. doi: 10.1111/1477-8947.12054. - DOI
1. Calone R., Bregaglio S., Sanoubar R., Noli E., Lambertini C., Barbanti L. Physiological adaptation to water salinity in six wild halophytes suitable for Mediterranean agriculture. Plants. 2021;10:309. doi: 10.3390/plants10020309. - DOI - PMC - PubMed
1. Minhas P., Qadir M., Yadav R. Groundwater irrigation induced soil sodification and response options. Agric. Water Manag. 2019;215:74–85. doi: 10.1016/j.agwat.2018.12.030. - DOI
1. Wang Y., Xiao D., Li Y., Li X. Soil salinity evolution and its relationship with dynamics of groundwater in the oasis of inland river basins: Case study from the Fubei region of Xinjiang Province, China. Environ. Monit. Assess. 2007;140:291–302. doi: 10.1007/s10661-007-9867-z. - DOI - PubMed

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[1] Zhang J., Shi H. Physiological and molecular mechanisms of plant salt tolerance. Photosynth. Res. 2013;115:1–22. doi: 10.1007/s11120-013-9813-6. - DOI - PubMed

[2] Zhang J., Shi H. Physiological and molecular mechanisms of plant salt tolerance. Photosynth. Res. 2013;115:1–22. doi: 10.1007/s11120-013-9813-6. - DOI - PubMed

[3] Qadir M., Quillérou E., Nangia V., Murtaza G., Singh M., Thomas R.J., Drechsel P., Noble A.D. Economics of salt-induced land degradation and restoration. Nat. Resour. Forum. 2014;38:282–295. doi: 10.1111/1477-8947.12054. - DOI

[4] Qadir M., Quillérou E., Nangia V., Murtaza G., Singh M., Thomas R.J., Drechsel P., Noble A.D. Economics of salt-induced land degradation and restoration. Nat. Resour. Forum. 2014;38:282–295. doi: 10.1111/1477-8947.12054. - DOI

[5] Calone R., Bregaglio S., Sanoubar R., Noli E., Lambertini C., Barbanti L. Physiological adaptation to water salinity in six wild halophytes suitable for Mediterranean agriculture. Plants. 2021;10:309. doi: 10.3390/plants10020309. - DOI - PMC - PubMed

[6] Calone R., Bregaglio S., Sanoubar R., Noli E., Lambertini C., Barbanti L. Physiological adaptation to water salinity in six wild halophytes suitable for Mediterranean agriculture. Plants. 2021;10:309. doi: 10.3390/plants10020309. - DOI - PMC - PubMed

[7] Minhas P., Qadir M., Yadav R. Groundwater irrigation induced soil sodification and response options. Agric. Water Manag. 2019;215:74–85. doi: 10.1016/j.agwat.2018.12.030. - DOI

[8] Minhas P., Qadir M., Yadav R. Groundwater irrigation induced soil sodification and response options. Agric. Water Manag. 2019;215:74–85. doi: 10.1016/j.agwat.2018.12.030. - DOI

[9] Wang Y., Xiao D., Li Y., Li X. Soil salinity evolution and its relationship with dynamics of groundwater in the oasis of inland river basins: Case study from the Fubei region of Xinjiang Province, China. Environ. Monit. Assess. 2007;140:291–302. doi: 10.1007/s10661-007-9867-z. - DOI - PubMed

[10] Wang Y., Xiao D., Li Y., Li X. Soil salinity evolution and its relationship with dynamics of groundwater in the oasis of inland river basins: Case study from the Fubei region of Xinjiang Province, China. Environ. Monit. Assess. 2007;140:291–302. doi: 10.1007/s10661-007-9867-z. - DOI - PubMed

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Adaptive Mechanisms of Halophytes and Their Potential in Improving Salinity Tolerance in Plants

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Adaptive Mechanisms of Halophytes and Their Potential in Improving Salinity Tolerance in Plants

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