
==== Front
iScience
iScience
iScience
2589-0042
Elsevier

S2589-0042(24)02029-7
10.1016/j.isci.2024.110804
110804
Review
Bridging gaps and seeding futures: A synthesis of soil salinization and the role of plant-soil interactions under climate change
Tang Hao 1
Du Lei 1
Xia Chengcheng cugxcc@163.com
2∗
Luo Jian jian.luo@imu.edu.cn
3∗∗
1 Key Laboratory of Land Resources Evaluation and Monitoring in Southwest, Ministry of Education, Sichuan Normal University, Chengdu 610068, China
2 School of Geography and Tourism, Chongqing Normal University, Chongqing 401331, China
3 Inner Mongolia Key Laboratory of River and Lake Ecology, School of Ecology and Environment, Inner Mongolia University, Hohhot 010021, China
∗ Corresponding author cugxcc@163.com
∗∗ Corresponding author jian.luo@imu.edu.cn
23 8 2024
20 9 2024
23 8 2024
27 9 110804© 2024 The Author(s)
2024
https://creativecommons.org/licenses/by/4.0/ This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
Summary

Soil salinization, exacerbated by climate change, poses significant threats to agricultural productivity, land restoration, and ecosystem resilience. This study reviews current knowledge on plant-soil interactions as a strategy to mitigate soil salinization induced by climate change, focusing on their role in soil salinity dynamics and tolerance mechanisms. The review examines how alterations in hydrological and temperature regimes impact soil salinity and how plant-soil mechanisms—such as salt exclusion, compartmentalization, and plant-microbe interactions—contribute to salinity mitigation. This, in turn, enhances soil quality, fertility, microbial diversity, and ecosystem services. The analysis identifies a growing body of research and highlights key themes and emerging trends, including drought, microbial communities, and salt tolerance strategies. This study underscores the critical role of plant-soil interactions in sustainable salinity management and identifies knowledge gaps and future research priorities, advocating for plant-soil interactions as a crucial pathway for improving ecosystem resilience to salinity stress amid climate change.

Graphical abstract

Soil science; Agricultural science; Agricultural soil science

Subject areas

Soil science
Agricultural science
Agricultural soil science
==== Body
pmcIntroduction

Soil salinization is a global problem that affects more than 800 million hectares of land, reducing agricultural productivity and threatening food security.1,2 It is caused by the accumulation of soluble salts in the soil, which can adversely affect soil physical, chemical, and biological properties, as well as plant growth and development.3,4 Soil salinization can be caused by natural or anthropogenic factors, such as arid and semi-arid climates, irrigation with saline water, poor drainage, fertilizer application, or land use changes.5,6 The interplay between evaporation, precipitation, irrigation practices, and the quality of irrigation water plays a pivotal role in the salinization process, making certain regions, especially arid and semi-arid areas, particularly vulnerable.

The impacts of climate change exacerbate the challenges posed by soil salinization. With the global climate system undergoing rapid changes, including rising temperatures, shifting precipitation patterns, and increasing frequency of extreme weather events, the dynamics of soil salinization are also being altered.5,7,8 These climatic shifts contribute to the acceleration of soil degradation processes, including salinization, thereby amplifying the stress on agricultural systems and natural ecosystems.2,9,10 The repercussions of soil salinization under climate change are far-reaching, impacting food security, livelihoods, and the health of terrestrial ecosystems.11

In this context, understanding the interactions between plants and soils emerges as a crucial aspect of mitigating the adverse effects of soil salinization.2 Plant-soil interaction is the dynamic interplay between plants and soil biota, mediated by various factors such as root exudates, soil organic matter, nutrients, and water.12 This interaction plays a crucial role in mitigating soil salinization and enhancing soil health by influencing salt dynamics, water relations, nutrient cycling, microbial activity, and ecosystem services.1,13 Strategies for plant-soil interaction include salt exclusion and tolerance mechanisms in plants, root system adaptations for salt dilution and excretion, and plant-microbe interactions for salinity management.14 These strategies have been applied or proposed for sustainable soil salinity management in various contexts such as agriculture, land restoration, or ecosystem conservation.2,8,10,15,16 They offer multiple benefits for soil salinization mitigation, such as reducing salt stress, improving plant performance and quality, restoring soil functions and services, and developing climate-resilient ecosystems (Figure 1).Figure 1 Soil Salinization Processes and Impacts

This figure outlines the processes leading to soil salinization, encompassing causes, the influence of global climate change, effects on soil composition, plant stress, root adaptations, and the role of soil microbes. It also highlights the interconnected feedback loops within this environmental challenge.

Given the growing body of literature on soil salinization and plant-soil interactions, there is a critical need to synthesize, analyze, and understand the current research landscape. The objectives of our review study are 2-fold: (1) to map the existing research landscape related to the soil salinization and plant-soil interactions, and (2) to highlight the significance of these interactions in mitigating the adverse effects of soil salinization under climate change. Through this analysis, we aim to seed future research directions that not only address the gaps identified but also contribute to the development of integrated and sustainable solutions for soil salinization challenges exacerbated by climate change.

Methodology

Description of the bibliometric analysis method using VOSviewer

A comprehensive bibliometric analysis of the scientific literature pertaining to soil salinization and plant-soil interactions was conducted utilizing VOSviewer (version 1.6.20), a robust instrument designed for the visualization and examination of trends and patterns within academic research.17 This tool aids in identifying principal nodes of research activity, uncovering emerging trends, and delineating potential avenues for future investigation through the generation of network maps of cited references, co-citation clusters, and keyword co-occurrence networks. The methodology adheres to the principles of scientometrics and capitalizes on the functionalities of VOSviewer to navigate the intricate terrain of interdisciplinary research encompassing soil science, plant biology, and climate change studies.

Criteria for selecting databases and search terms

Literature search was conducted in the Web of Science in April 2024 using the following search terms: (TS = “salinization” or TS = “soil salinity”) and ([TS = “plant” or TS = “vegetation”] and [TS = “bacteria” or TS = “mycorrhiza” or TS = “fungi” or TS = “soil microbe”]) and (TS = “climate change” or TS = “warming” or TS = “drought” or TS = “precipitation” or TS = “moisture”). The literature covers the period from 1986 to 2024, totally have 169 papers. However, since there were only 11 papers published before 2013 (5 in 2013, 1 in 2012, 2 in 2009, 1 in 2008, 1 in 1996, and 1 in 1986), we used 2013 as a cutoff point to present the annual publication data from 2013 onward.

Analytical techniques to identify trends, gaps, and clusters

The analytical approach entailed a multi-step process to meticulously examine the collected literature. The initial phase comprised a temporal analysis aimed at delineating the evolution of research volume over time. This was followed by a keyword co-occurrence analysis to identify the most prevalently discussed concepts, thereby unveiling dominant themes and discerning emerging trends within the field.18 Moreover, cluster analysis was employed to delineate distinct research areas and elucidate their interconnections.19 This comprehensive suite of analytical tools facilitated the mapping of the intellectual landscape, revealing research trends, gaps, and clusters within the global discourse on soil salinization and plant-soil interactions amid the changing climate.

Part I: Bibliometric analysis

Publication numbers and distribution

Based on topic word searches, research on soil salinization and related plant-soil mechanisms shows a year-over-year upward trend. Exponential correlation modeling reveals a correlation coefficient (R2) of 0.98, indicating a strong relationship (Figure 2A). The results indicate that, prior to 2013, only 11 relevant papers were published, appearing in 1986, 1996, 2008, 2009, 2012, and 2013. From 2014 to 2024, there have been publications each year, totaling just 169 papers. This suggests that while research on plant-soil interactions in the context of soil salinization has garnered attention, it remains relatively limited. To further validate our findings, we conducted searches using individual topic keywords. We found 6,053 papers related to plant and soil salinization ([TS = “salinization” or TS = “soil salinity”] and [TS = “plant” or TS = “vegetation”]), 1,055 papers on microbes and soil salinization ([TS = “salinization” or TS = “soil salinity”] and [TS = “bacteria” or TS = “mycorrhiza” or TS = “fungi” or TS = “soil microbe”]), and 4,314 papers on climate change and soil salinization ([TS = “salinization” or TS = “soil salinity”] and [TS = “climate change” or TS = “warming” or TS = “drought” or TS = “precipitation” or TS = “moisture”]). These results further support our conclusion that research on the mechanisms of plant-soil interactions in soil salinization remains relatively underexplored.Figure 2 Global trends in publications (A) and distribution by country (B) on the mechanism of soil salinization

The different color represents the major class from the cluster analysis.

Analysis of publication volumes by country reveals that China, India, and the United States lead in the number of published articles, accounting for one-third of the global total. This high publication output reflects the significant impact of soil salinization on agricultural productivity and food security in these countries, driving them to actively conduct research to address this issue. Additionally, countries such as Pakistan, Iran, South Africa, Bangladesh, and Saudi Arabia also contribute 2–6% of the total publications (Figure 2B). This indicates that, while major economies dominate soil salinization research, other countries facing the threat of salinization are also actively investing in related research. This further highlights the widespread impact of soil salinization on a global scale, particularly in countries heavily reliant on agriculture. Therefore, it is crucial to further promote global knowledge sharing and technological exchange to address this common environmental challenge.

Co-occurrence and cluster analysis

The keyword co-occurrence analysis in soil salinization-related research highlights a primary focus on soil drought, salt stress, soil microbial community, and salt tolerance among other related areas of study. Furthermore, through cluster analysis, the keywords can be categorized into four major classes: plant growth mechanisms, soil microbiology, plant salt stress tolerance mechanisms (Figure 3). This categorization highlights the interdisciplinary nature of soil salinization research, encompassing both biological processes and practical approaches to mitigating salinity’s adverse effects. Interestingly, the analysis shows that studies focusing on soil-microbe interactions are relatively less frequent compared to other areas. This gap suggests that while the role of plants and their physiological responses to salinity stress has been extensively studied, the equally crucial role of soil microbial communities in mediating these interactions has not received as much attention. Soil microbes play a vital role in nutrient cycling, soil structure, and overall soil health, all of which are critical in saline environments.Figure 3 Network visualization of co-occurrence and cluster analysis regarding the mechanisms of soil salinization

The emergence of the keyword “Inoculation” in the context of plant-soil interactions is particularly noteworthy (Figure 3). Inoculation refers to the introduction of beneficial microbes, such as bacteria or fungi, into the plant rhizosphere to enhance plant tolerance to salinity stress. This strategy has gained increasing attention as a sustainable approach to mitigating soil salinization. Beneficial microbes, including plant growth-promoting rhizobacteria (PGPR) and mycorrhizal fungi, have been shown to significantly improve plant water uptake, nutrient assimilation, and stress resilience. By enhancing these processes, inoculation can alleviate the negative impacts of soil salinization on plant growth, leading to more resilient agricultural systems. This finding underscores the potential of harnessing microbial allies in the fight against soil salinization. However, it also points to the need for further research in this area, particularly to understand the specific mechanisms by which these microbes confer stress tolerance and how they interact with different plant species under varying environmental conditions. Expanding research on soil-microbe interactions could lead to more targeted and effective inoculation strategies, thereby enhancing the overall resilience of agricultural systems in saline-prone areas.

Part II: A conceptual framework for climate change-induced soil salinization and plant-soil tolerance mechanisms

Climate change-induced soil salinization

Climate change significantly impacts soil salinity dynamics through alterations in hydrological and temperature regimes.2,8 Key hydrological changes, such as variations in precipitation patterns including rainfall amount, frequency, intensity, and distribution, directly affect soil moisture, and salinity levels.2 These changes influence the processes of leaching—the removal of salts from the soil via water percolation or drainage—and evaporation, the loss of water from the soil through vaporization or transpiration.20 While higher leaching rates can decrease soil salinity by removing salts, increased evaporation rates tend to concentrate salts in the soil, thereby elevating soil salinity.

Erratic or reduced precipitation can exacerbate soil salinization by promoting evaporation and salt accumulation, especially when water inputs from rainfall do not suffice to counterbalance water losses through evaporation or transpiration, resulting in a net increase in soil salinity.21 Conversely, increased or intense precipitation may either dilute or mobilize salts depending on whether rainfall inputs exceed evaporation losses, potentially reducing soil salinity through dilution and leaching, or conversely, increasing it by mobilizing salts from deeper layers or external sources into the root zone.21,22

Temperature changes, induced by climate change, further complicate soil salinity dynamics by influencing evaporation rates and microbial activities in the soil.23 Rising temperatures can elevate evaporation rates, leading to increased soil salinity due to higher water loss relative to inputs.5,24 This process can result in the formation of salt crusts on the soil surface, negatively impacting soil physical properties and plant growth.25 Additionally, increased temperatures boost microbial metabolic rates and enzyme activities, potentially enhancing the decomposition of organic matter, nutrient cycling, and carbon sequestration.26 While these microbial processes can mitigate soil salinization by transforming salts into less soluble forms, they may also intensify salinization under conditions of elevated soil salinity and water stress, thereby inhibiting microbial activity and exacerbating salt accumulation.27

Plant-soil tolerance mechanisms

Salt exclusion and tolerance mechanisms in plants

Plants use to cope with salt stress at the cellular and tissue levels is salt exclusion, which prevents or reduces the entry of salt into the plant from the soil solution (Figure 4). Salt exclusion is mainly based on the selective permeability of the plasma membrane or the cell wall to different ions, such as Na+, K+, Cl−, or Ca2+.28,29 Various proteins that act as transporters, channels, pumps, or enzymes regulate the movement of ions across these barriers under saline conditions.30 For example, the high-affinity potassium transporter (HKT) is responsible for Na+ uptake and transport in roots. Depending on its subfamily and isoform, HKT can function as a Na+/K+ symporter or a Na+ uniporter. HKT can mediate salt exclusion by removing Na+ from the xylem sap and returning it to the soil solution or sequestering it into the vacuole.31,32 In contrast, the sodium/hydrogen exchanger (NHX) is responsible for Na+/H+ exchange across membranes.33 Depending on its subfamily and isoform, NHX can function as a Na+/H+ antiporter or a K+/H+ antiporter. NHX can mediate salt exclusion by extruding Na+ from the cytosol to the apoplast or sequestering it into the vacuole.34,35 Both HKT and NHX are regulated by various signaling pathways and transcription factors that modulate their expression and activity in response to salt stress (Figure 4). Different plant species express different isoforms of these proteins that confer different levels of salt tolerance.36 For instance, a salt-tolerant rice cultivar (Nona Bokra) expresses a HKT1; 5 isoform that reduces Na+ accumulation in the shoot, while a salt-sensitive rice cultivar (Koshihikari) expresses a different HKT1; 5 isoform that increases Na+ accumulation in the shoot.31,37.Figure 4 Plant-soil interaction mechanisms for salinity mitigation

This figure highlights the diverse mechanisms plants employ to manage salt stress through intricate interactions with the soil. These mechanisms operate at multiple levels: cellular and tissue, organ and whole-plant, and community and ecosystem. At the cellular level, salt exclusion strategies regulate the movement of ions, with key roles played by proteins like HKT and NHX. On the organ and whole-plant scale, root system adaptations, guided by proteins such as ARF and SOS1, influence salt tolerance by modifying root traits. In the broader community and ecosystem context, plants engage in symbiotic relationships with soil microorganisms, such as rhizobia-legume, mycorrhizal, and endophytic symbioses, which enhance nutrition, water uptake, and growth.

Root system adaptations for salt dilution and excretion

Root system adaptation aims to increase the water uptake or decrease the salt uptake by roots from the soil solution by developing deeper or more extensive root systems that can access fresh water sources or avoid saline zones in soils, or modifying root anatomy or morphology to facilitate salt excretion through specialized structures such as salt glands or bladders.38,39 These adaptations are regulated by various genes, hormones, or signals that modulate root development, growth, or differentiation under salt stress.40 For instance, the auxin response factor (ARF) is a transcription factor that regulates auxin-responsive gene expression and root morphology.41,42 Depending on its domain structure and interaction partners, ARF can function as an activator or a repressor of auxin-responsive genes. ARF can mediate root system adaptation by modulating root length, depth, density, diameter, branching, or architecture under salt stress.43 In contrast, the sodium transporter (SOS1) is a plasma membrane-localized cation transporter that regulates Na+ efflux from roots.44,45 Depending on its subfamily and isoform, SOS1 can function as a Na+/H+ antiporter or a Na+/K+ symporter. SOS1 can mediate root system adaptation by facilitating salt excretion through specialized structures such as salt glands or bladders under salt stress.46 Both ARF and SOS1 are influenced by various signaling pathways and transcription factors that modulate their expression and activity in response to salt stress.47 Different plant species express different isoforms of these proteins that confer different levels of salt tolerance. For example, a salt-tolerant tomato cultivar (LA2714) expresses a ARF7 isoform that increases root length and density under salt stress, while a salt-sensitive tomato cultivar (Moneymaker) expresses a different ARF7 isoform that decreases root length and density under salt stress.34,35,48,49.

The role of plant-microbe interactions in salinity management

Plants cope with salt stress at the community and ecosystem levels is by forming symbiotic relationships with soil microorganisms that benefit both parties in exchange for resources or signals50 (Figure 4). These relationships include rhizobia-legume, mycorrhizal, endophytic, or cyanobacterial symbioses, which can improve plant performance under salt stress by enhancing plant nutrition, water uptake, growth, or quality.51,52 For example, rhizobia-legume symbiosis is the association between nitrogen-fixing bacteria (rhizobia) and leguminous plants (such as beans, peas, or clovers) that form root nodules where nitrogen fixation occurs.53 This association can provide nitrogen to plants under nitrogen-deficient conditions, which is a vital nutrient for plant growth and development but often scarce or unavailable in saline soils.54,55 In contrast, mycorrhizal symbiosis is the association between soil fungi (mycorrhizae) and most land plants (such as cereals, vegetables, or fruits) that form hyphal networks that connect plant roots with soil particles.56 This symbiosis can improve water uptake efficiency under water-deficient conditions, which is a crucial resource for plant growth and development but often scarce or unavailable in saline soils.23,57 Furthermore, endophytic symbiosis is the association between soil bacteria (endophytes) and most land plants (such as grasses, cereals, or trees) that colonize the internal tissues of roots, stems, leaves, or seeds without causing any apparent harm to the host.58 This association can produce plant growth regulators, antioxidants, osmolytes, or enzymes that modulate plant physiology or metabolism under salt stress.59

Discussion on research gaps: How plant-soil interactions mitigate the climate change-induced soil salinization

Comprehensive analysis of plant-soil synergies under climate-induced salinization

The nexus between plant and soil systems, particularly under the exacerbating influence of climate-induced soil salinization, emerges as a critical yet underexplored domain within environmental research.5 Although initial inquiries have illuminated the capacity of plant-soil interactions to counter salinization, the intricacies of the regulatory mechanisms operating under the duress of climate change necessitate further elucidation.21,23 To illustrate this, we can consider specific studies where plant-soil interactions have been shown to modulate salinity tolerance. For instance, research on Arabidopsis thaliana has demonstrated how certain soil microbes can induce the expression of stress-responsive genes that enhance the plant’s ability to cope with saline conditions.60 These findings suggest that understanding the genetic and molecular mechanisms at play is essential for developing comprehensive strategies to combat soil salinization. This gap underscores an imperative need for an integrated exploration into the nuanced modulation of plant responses to salinity by these interactions and their contribution to enhancing soil resilience against salinization.61 The complexity inherent in these mechanisms encompasses a broad spectrum of biological, chemical, and physical processes, thereby presenting an expansive challenge for current scientific investigations.

A pivotal aspect of advancing comprehension within this field lies in recognizing the interconnected impacts of climate change on soil salinization, which are intricately linked with dynamic responses from plant-soil systems.62 These responses are orchestrated through a series of mechanisms, including the selective permeability of plant cellular membranes to specific ions, the pivotal role of soil microbiota in augmenting plant salinity tolerance, and the evolutionary adaptations of root systems designed to minimize salt assimilation.63 For example, studies have shown that soil microbes like Pseudomonas species can enhance ion transport in plants under saline conditions, thereby improving salt tolerance.64 Such examples underscore the need for a more detailed exploration of how these microbial interactions can be leveraged to develop new agricultural practices. Investigating the modulation of these processes in the face of escalated soil salinity due to climate change demands a meticulous and detailed approach.

Moreover, the scarcity of longitudinal studies examining the persistent impacts of plant-soil interactions in mitigating soil salinization accentuates a significant research trajectory.65 Future endeavors must transcend the immediate physiological responses of plants to salinity stress to investigate the enduring implications of these interactions. This encompasses evaluating the adaptability of plant-soil systems to fluctuating climatic conditions and discerning the utility of these adaptations in formulating sustainable soil management strategies.

Addressing these multifaceted complexities mandates the adoption of an interdisciplinary methodology that integrates knowledge from soil science, plant physiology, microbiology, and climate science. Such a comprehensive approach is quintessential for devising predictive models capable of assessing the repercussions of plant-soil interactions across diverse climatic scenarios. It is through these rigorous, cohesive research efforts that the potential of plant-soil synergies can be fully realized, offering sustainable resolutions to the burgeoning challenges of soil salinization in the climate change epoch.

Deep-dive into mechanistic insights through advanced techniques

Advancements in genomic and transcriptomic technologies have revolutionized the scientific community’s ability to decode the molecular intricacies of how plants and their rhizosphere microbiota respond to salinity stress.66,67 These technologies allow for an unprecedented exploration of the genetic and molecular fabric of salinity tolerance, revealing the orchestration of gene expression, protein function, and metabolic pathways in response to saline environments.68 For example, transcriptomic studies on rice (Oryza sativa) have identified specific genes responsible for the synthesis of osmoprotectants, which play a crucial role in osmotic stress management.69 Similarly, genomic studies on barley (Hordeum vulgare) have pinpointed genetic variants associated with ion transporters that are critical for salinity tolerance.70 Furthermore, transcriptomic profiling can pinpoint specific stress-responsive genes that are upregulated in plants to manage osmotic stress, such as those encoding for osmoprotectants or ion transporters.71,72 Genomic analyses extend these findings by mapping the genetic variants that contribute to phenotypic traits associated with salinity tolerance, offering potential markers for breeding programs.

The “inoculation” of plants with salt-tolerant microbes is emerging as a transformative approach to bolster plant resilience against salinity. This technique leverages the symbiotic relationships between plants and beneficial microbes, which can enhance nutrient uptake, improve water efficiency, and induce systemic resistance to stress.73 Research is increasingly focusing on the identification of microbial strains that possess specific mechanisms for supporting plant health in saline conditions, such as the production of phytohormones or the solubilization of phosphorus, which can significantly alleviate the physiological burden of salt stress on plants.74,75 To further support this discussion, we have included a summary table that outlines key studies on “inoculation” techniques, listing the plant species involved, the specific microbes used, and the observed beneficial effects (Table 1).Table 1 Summary of key studies on “inoculation” techniques in soil salinization

Plant species	Microbe used	Technique employed	Observed beneficial effect	Reference	
Rice (Oryza sativa)	Pseudomonas fluorescens	Bacterial Inoculation	Enhanced salt tolerance through improved ion transport, increased root growth	Gupta et al., (2023)69;	
Wheat (Triticum aestivum)	Bacillus subtilis	Rhizobacteria Inoculation	Increased phosphorus solubilization, higher grain yield, enhanced drought resistance	Zahra et al., (2023)76	
Barley (Hordeum vulgare)	Azospirillum brasilense	Inoculation with PGPR	Improved osmotic balance, increased proline accumulation, enhanced stress resilience	Chieb & Gachomo (2023)70	
Tomato (Solanum lycopersicum)	Glomus intraradices (Mycorrhiza)	Fungal Inoculation	Enhanced nutrient uptake, increased water use efficiency, improved plant growth under drought	Zhang et al., (2024)77	
Maize (Zea mays)	Rhizobium spp.	Bacterial-Fungal Co-Inoculation	Synergistic effects on plant growth, reduced Na+ accumulation, improved chlorophyll content	Brambilla et al., (2022)78	
Sunflower (Helianthus annuus)	Bacillus licheniformis	Bacterial Inoculation	Increased plant biomass, improved root architecture, enhanced nutrient uptake	Khoso et al., (2024)79	
Soybean (Glycine max)	Bradyrhizobium japonicum	Rhizobacteria Inoculation	Improved nitrogen fixation, higher seed protein content, enhanced salinity tolerance	Riviezzi et al., (2020)80	
Note: PGPR-plant growth-promoting rhizobacteria.

In the context of plant-soil-microbial systems, the application of advanced research techniques is shedding light on the complex, bidirectional interactions that govern the resilience of these systems to salinity. For instance, understanding how plants can selectively enhance the recruitment of beneficial microbes under saline conditions, or how microbes can modulate plant gene expression to enhance salt tolerance, are areas ripe for exploration.81,82,83 Such insights are critical for designing integrated management strategies that harness the full potential of plant and microbial adaptations to combat soil salinization.

By pushing the boundaries of the mechanistic understanding through the integration of genomic, transcriptomic, and microbiological research, current studies are laying the foundation for innovative solutions to soil salinization. These solutions, grounded in a deep understanding of the underlying biological processes, have the potential to transform agricultural practices and ecosystem management strategies, making them more resilient to the challenges posed by an increasingly saline world. This concerted effort toward unraveling and leveraging the natural resilience mechanisms within plant-soil-microbial systems represents a critical step toward sustainable salinity management and the preservation of agricultural and natural ecosystems in the face of escalating environmental stressors.

Implications

This review highlights the growing challenge of soil salinization, which is increasingly driven by climate change. It emphasizes the crucial role of plant-soil interactions in developing resilience and strategies for mitigating salinity stress. Advances in genomic and transcriptomic research have provided valuable insights into the molecular mechanisms by which plants and microbes respond to salinity. These findings offer promising directions for breeding salt-tolerant crops and developing microbial inoculants. By understanding the physiological and biochemical strategies that plants and their associated microbiomes employ, there is significant potential to improve soil salinity management practices. However, there are still important research gaps, particularly regarding the long-term effects of plant-soil interactions on soil salinity under different climate scenarios. The challenge also lies in translating these molecular insights into practical agricultural applications. Addressing these issues requires a multidisciplinary approach that brings together expertise in soil science, plant physiology, microbiology, and climate change research. Future work should focus on developing predictive models that simulate plant-soil interactions under salinity stress, which will be essential for planning effective mitigation and adaptation strategies in the face of climate change.

Conclusion

Our review calls for a coordinated global research effort to better understand and utilize plant, soil, and microbial adaptations in addressing soil salinization. By focusing on sustainable and innovative solutions, such efforts can contribute to enhancing food security, strengthening ecosystem resilience, and mitigating the effects of climate change. Additionally, there is a pressing need for research that bridges the gap between molecular discoveries and practical applications, ensuring that agricultural systems remain sustainable and that ecosystem functions are preserved in saline environments.

Acknowledgments

This study was funded by the Major Science and Technology Innovation Pilot Project for Water Resources Protection and Integrated-Saving Utilization in the Yellow River Basin of Inner Mongolia Autonomous Region (2023JBGS0007 ), Natural Science Foundation of Inner Mongolia A. R. of China (2023QN04001 ), Start-up Funding from 10.13039/501100003850 Inner Mongolia University (21800-5223728 ), the Science and Technology Research Program of 10.13039/501100007957 Chongqing Municipal Education Commission (KJQN202300541 ), Start-up funding from 10.13039/100010338 Chongqing Normal University (202305000221 ), and Start-up funding from 10.13039/501100016349 Sichuan Normal University (XJ20210431 ).

Author contributions

H.T.: conceptualization, methodology, resources, visualization, writing—original draft, writing—review and editing; L.D.: conceptualization, resources, and visualization; C.X.: visualization, funding acquisition, writing—review and editing, supervision; J.L.: conceptualization, methodology, writing—original draft, writing—review and editing, supervision, funding acquisition.

Declaration of interests

The authors declare no competing interests.
==== Refs
References

1 Rengasamy P. World salinization with emphasis on Australia J. Exp. Bot. 57 2006 1017 1023 10.1093/jxb/erj108 16510516
2 Tarolli P. Luo J. Park E. Barcaccia G. Masin R. Soil salinization in agriculture: Mitigation and adaptation strategies combining nature-based solutions and bioengineering iScience 27 2024 108830 10.1016/j.isci.2024.108830 38318366
3 Singh A. Soil salinization management for sustainable development: A review J. Environ. Manage. 277 2021 111383 10.1016/j.jenvman.2020.111383 33035935
4 Machado R. Serralheiro R. Soil salinity: Effect on vegetable crop growth. Management practices to prevent and mitigate soil salinization Horticulturae 3 2017 30 10.3390/horticulturae3020030
5 Hassani A. Azapagic A. Shokri N. Global predictions of primary soil salinization under changing climate in the 21st century Nat. Commun. 12 2021 6663 10.1038/s41467-021-26907-3 34795219
6 Zhou M. Butterbach-Bahl K. Vereecken H. Brüggemann N. A meta-analysis of soil salinization effects on nitrogen pools, cycles and fluxes in coastal ecosystems Glob. Chang. Biol. 23 2017 1338 1352 10.1111/gcb.13430 27416519
7 Okur B. Örçen N. Soil salinization and climate change Climate Change and Soil Interactions 2020 331 350 10.1016/b978-0-12-818032-7.00012-6
8 Tarolli P. Luo J. Straffelini E. Liou Y.-A. Nguyen K.-A. Laurenti R. Masin R. D’Agostino V. Saltwater intrusion and climate change impact on coastal agriculture PLOS Water 2 2023 e0000121 10.1371/journal.pwat.0000121
9 Lakhdar A. Rabhi M. Ghnaya T. Montemurro F. Jedidi N. Abdelly C. Effectiveness of compost use in salt-affected soil J. Hazard Mater. 171 2009 29 37 10.1016/j.jhazmat.2009.05.132 19576686
10 Luo J. Straffelini E. Bozzolan M. Zheng Z. Tarolli P. Saltwater intrusion in the Po River Delta (Italy) during drought conditions: Analyzing its Spatio-temporal evolution and potential impact on agriculture International Soil and Water Conservation Research 12 2024 714 725 10.1016/j.iswcr.2023.09.009
11 Kopittke P.M. Menzies N.W. Wang P. McKenna B.A. Lombi E. Soil and the intensification of agriculture for global food security Environ. Int. 132 2019 105078 10.1016/j.envint.2019.105078 31400601
12 MEKI K. LIU Q. WU S. YUAN Y. Plant- and microbe-assisted biochar amendment technology for petroleum hydrocarbon remediation in saline-sodic soils: A review Pedosphere 32 2022 211 221 10.1016/S1002-0160(21)60041-3
13 Otlewska A. Migliore M. Dybka-Stępień K. Manfredini A. Struszczyk-Świta K. Napoli R. Białkowska A. Canfora L. Pinzari F. When Salt Meddles Between Plant, Soil, and Microorganisms Front. Plant Sci. 11 2020 553087 10.3389/fpls.2020.553087 33042180
14 Vaishnav A. Shukla A.K. Sharma A. Kumar R. Choudhary D.K. Endophytic Bacteria in Plant Salt Stress Tolerance: Current and Future Prospects J. Plant Growth Regul. 38 2019 650 668 10.1007/s00344-018-9880-1
15 Vimal S.R. Singh J.S. Arora N.K. Singh S. Soil-Plant-Microbe Interactions in Stressed Agriculture Management: A Review Pedosphere 27 2017 177 192 10.1016/S1002-0160(17)60309-6
16 Grover M. Ali S.Z. Sandhya V. Rasul A. Venkateswarlu B. Role of microorganisms in adaptation of agriculture crops to abiotic stresses World J. Microbiol. Biotechnol. 27 2011 1231 1240 10.1007/s11274-010-0572-7
17 van Eck N.J. Waltman L. Software survey: VOSviewer, a computer program for bibliometric mapping Scientometrics 84 2010 523 538 10.1007/s11192-009-0146-3 20585380
18 Ding X. Yang Z. Knowledge mapping of platform research: a visual analysis using VOSviewer and CiteSpace Electron. Commer. Res. 22 2022 787 809 10.1007/s10660-020-09410-7
19 van Eck N.J. Waltman L. Citation-based clustering of publications using CitNetExplorer and VOSviewer Scientometrics 111 2017 1053 1070 10.1007/s11192-017-2300-7 28490825
20 Li X. Chang S.X. Salifu K.F. Soil texture and layering effects on water and salt dynamics in the presence of a water table: A review Environ. Rev. 22 2014 41 50 10.1139/er-2013-0035
21 Eswar D. Karuppusamy R. Chellamuthu S. Drivers of soil salinity and their correlation with climate change Curr. Opin. Environ. Sustain. 50 2021 310 318 10.1016/j.cosust.2020.10.015
22 Aragüés R. Medina E.T. Zribi W. Clavería I. Álvaro-Fuentes J. Faci J. Soil Salinization as a threat to the sustainability of deficit irrigation under present and expected climate change scenarios Irrig. Sci. 33 2015 67 79 10.1007/s00271-014-0449-x
23 Ullah A. Bano A. Khan N. Climate Change and Salinity Effects on Crops and Chemical Communication Between Plants and Plant Growth-Promoting Microorganisms Under Stress Front. Sustain. Food Syst. 5 2021 618092 10.3389/fsufs.2021.618092
24 Yu X. Xin P. Hong L. Effect of evaporation on soil salinization caused by ocean surge inundation J. Hydrol. (Amst.) 597 2021 126200 10.1016/j.jhydrol.2021.126200
25 Pearson K.E. Basics of Salinity and Sodicity Effects on Soil Physical Properties - MSU Extension Water Quality 2003 Montana State University. MSU Extension Water Quality Program 1 11
26 Gao X. Huang R. Li J. Wang C. Lan T. Li Q. Deng O. Tao Q. Zeng M. Temperature induces soil organic carbon mineralization in urban park green spaces, Chengdu, southwestern China: Effects of planting years and vegetation types Urban For. Urban Green. 54 2020 126761 10.1016/j.ufug.2020.126761
27 Shrivastava P. Kumar R. Soil salinity: A serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation Saudi J. Biol. Sci. 22 2015 123 131 10.1016/j.sjbs.2014.12.001 25737642
28 Munns R. Tester M. Mechanisms of salinity tolerance Annu. Rev. Plant Biol. 59 2008 651 681 10.1146/annurev.arplant.59.032607.092911 18444910
29 Assaha D.V.M. Ueda A. Saneoka H. Al-Yahyai R. Yaish M.W. The role of Na+ and K+ transporters in salt stress adaptation in glycophytes Front Physiol. 8 2017 509 10.3389/fphys.2017.00509 28769821
30 Pizzagalli M.D. Bensimon A. Superti-Furga G. A guide to plasma membrane solute carrier proteins FEBS J. 288 2021 2784 2835 10.1111/febs.15531 32810346
31 Ren Z.H. Gao J.P. Li L.G. Cai X.L. Huang W. Chao D.Y. Zhu M.Z. Wang Z.Y. Luan S. Lin H.X. A rice quantitative trait locus for salt tolerance encodes a sodium transporter Nat. Genet. 37 2005 1141 1146 10.1038/ng1643 16155566
32 Rodríguez-Navarro A. Rubio F. High-affinity potassium and sodium transport systems in plants J. Exp. Bot. 57 2006 1149 1160 10.1093/jxb/erj068 16449373
33 Nikolovska K. Seidler U.E. Stock C. The Role of Plasma Membrane Sodium/Hydrogen Exchangers in Gastrointestinal Functions: Proliferation and Differentiation, Fluid/Electrolyte Transport and Barrier Integrity Front. Physiol. 13 2022 899286 10.3389/fphys.2022.899286 35665228
34 Bassil E. Tajima H. Liang Y.C. Ohto M.A. Ushijima K. Nakano R. Esumi T. Coku A. Belmonte M. Blumwald E. The arabidopsis Na+/H+ antiporters NHX1 and NHX2 control vacuolar ph and K+ homeostasis to regulate growth, flower development, and reproduction Plant Cell 23 2011 3482 3497 10.1105/tpc.111.089581 21954467
35 Turan S. Cornish K. Kumar S. Salinity tolerance in plants: Breeding and genetic engineering Aust. J. Crop. Sci. 6 2012 1337 1348
36 Athar H.U.R. Zulfiqar F. Moosa A. Ashraf M. Zafar Z.U. Zhang L. Ahmed N. Kalaji H.M. Nafees M. Hossain M.A. Salt stress proteins in plants: An overview Front. Plant Sci. 13 2022 999058 10.3389/fpls.2022.999058 36589054
37 Hao S. Wang Y. Yan Y. Liu Y. Wang J. Chen S. A review on plant responses to salt stress and their mechanisms of salt resistance Horticulturae 7 2021 132 10.3390/horticulturae7060132
38 Galvan-Ampudia C.S. Testerink C. Salt stress signals shape the plant root Curr. Opin. Plant Biol. 14 2011 296 302 10.1016/j.pbi.2011.03.019 21511515
39 Kawa D. Julkowska M.M. Sommerfeld H.M. Ter Horst A. Haring M.A. Testerink C. Phosphate-dependent root system architecture responses to salt stress Plant Physiol. 172 2016 690 706 10.1104/pp.16.00712 27208277
40 Ma L. Liu X. Lv W. Yang Y. Molecular Mechanisms of Plant Responses to Salt Stress Front. Plant Sci. 13 2022 934877 10.3389/fpls.2022.934877 35832230
41 Powers S.K. Strader L.C. Regulation of auxin transcriptional responses Dev. Dyn. 249 2020 483 495 10.1002/dvdy.139 31774605
42 Li S.B. Xie Z.Z. Hu C.G. Zhang J.Z. A review of auxin response factors (ARFs) in plants Front. Plant Sci. 7 2016 47 10.3389/fpls.2016.00047 26870066
43 Li P. Yang X. Wang H. Pan T. Wang Y. Xu Y. Xu C. Yang Z. Genetic control of root plasticity in response to salt stress in maize Theor. Appl. Genet. 134 2021 1475 1492 10.1007/s00122-021-03784-4 33661350
44 Shi H. Quintero F.J. Pardo J.M. Zhu J.K. The putative plasma membrane NA+/H+ antiporter SOS1 controls long-distance NA+ transport in plants Plant Cell 14 2002 465 477 10.1105/tpc.010371 11884687
45 Liu W. Li R.J. Han T.T. Cai W. Fu Z.W. Lu Y.T. Salt stress reduces root meristem size by nitric oxidemediated modulation of auxin accumulation and signaling in Arabidopsis Plant Physiol. 168 2015 343 356 10.1104/pp.15.00030 25818700
46 Xie Q. Zhou Y. Jiang X. Structure, Function, and Regulation of the Plasma Membrane Na+/H+ Antiporter Salt Overly Sensitive 1 in Plants Front. Plant Sci. 13 2022 866265 10.3389/fpls.2022.866265 35432437
47 Li Q. Qin Y. Hu X. Li G. Ding H. Xiong X. Wang W. Transcriptome analysis uncovers the gene expression profile of salt-stressed potato (Solanum tuberosum L.) Sci. Rep. 10 2020 5411 10.1038/s41598-020-62057-0 32214109
48 Zha S. Li Z. Chen C. Du Z. Tay J.C.K. Wang S. SPA-based methods for the quantitative estimation of the soil salt content in saline-alkali land from field spectroscopy data: A case study from the Yellow River Irrigation regions Remote Sens (Basel) 11 2019 967 982 10.3390/rs11080916
49 Gálvez F.J. Baghour M. Hao G. Cagnac O. Rodríguez-Rosales M.P. Venema K. Expression of LeNHX isoforms in response to salt stress in salt sensitive and salt tolerant tomato species Plant Physiol. Biochem. 51 2012 109 115 10.1016/j.plaphy.2011.10.012 22153246
50 Kumar A. Singh S. Gaurav A.K. Srivastava S. Verma J.P. Plant Growth-Promoting Bacteria: Biological Tools for the Mitigation of Salinity Stress in Plants Front. Microbiol. 11 2020 1216 10.3389/fmicb.2020.01216 32733391
51 Porcel R. Aroca R. Ruiz-Lozano J.M. Salinity stress alleviation using arbuscular mycorrhizal fungi. A review Agron. Sustain. Dev. 32 2012 181 200 10.1007/s13593-011-0029-x
52 Goyal R.K. Habtewold J.Z. Evaluation of Legume–Rhizobial Symbiotic Interactions Beyond Nitrogen Fixation That Help the Host Survival and Diversification in Hostile Environments Microorganisms 11 2023 1454 10.3390/microorganisms11061454 37374957
53 Wang Q. Liu J. Zhu H. Genetic and molecular mechanisms underlying symbiotic specificity in legume-rhizobium interactions Front. Plant Sci. 9 2018 313 10.3389/fpls.2018.00313 29593768
54 Chen Z. Cao X.L. Niu J.P. Effects of exogenous ascorbic acid on seed germination and seedling salt-tolerance of alfalfa PLoS One 16 2021 e0250926 10.1371/journal.pone.0250926 33914821
55 Ansari M. Shekari F. Mohammadi M.H. Juhos K. Végvári G. Biró B. Salt-tolerant plant growth-promoting bacteria enhanced salinity tolerance of salt-tolerant alfalfa (Medicago sativa L.) cultivars at high salinity Acta Physiol. Plant. 41 2019 195 10.1007/s11738-019-2988-5
56 Huey C.J. Gopinath S.C.B. Uda M.N.A. Zulhaimi H.I. Jaafar M.N. Kasim F.H. Yaakub A.R.W. Mycorrhiza: a natural resource assists plant growth under varied soil conditions 3 Biotech 10 2020 204 10.1007/s13205-020-02188-3
57 Porras-Soriano A. Soriano-Martín M.L. Porras-Piedra A. Azcón R. Arbuscular mycorrhizal fungi increased growth, nutrient uptake and tolerance to salinity in olive trees under nursery conditions J. Plant Physiol. 166 2009 1350 1359 10.1016/j.jplph.2009.02.010 19342122
58 Eid A.M. Fouda A. Abdel-rahman M.A. Salem S.S. Elsaied A. Oelmüller R. Hijri M. Bhowmik A. Elkelish A. El-Din Hassan S. Harnessing bacterial endophytes for promotion of plant growth and biotechnological applications: An overview Plants 10 2021 935 10.3390/plants10050935 34067154
59 Khan A.L. Al-Harrasi A. Al-Rawahi A. Al-Farsi Z. Al-Mamari A. Waqas M. Asaf S. Elyassi A. Mabood F. Shin J.H. Lee I.J. Endophytic fungi from frankincense tree improves host growth and produces extracellular enzymes and indole acetic acid PLoS One 11 2016 0158207 10.1371/journal.pone.0158207
60 Fan D. Subramanian S. Smith D.L. Plant endophytes promote growth and alleviate salt stress in Arabidopsis thaliana Sci. Rep. 10 2020 12740 10.1038/s41598-020-69713-5 32728116
61 Chele K.H. Tinte M.M. Piater L.A. Dubery I.A. Tugizimana F. Soil salinity, a serious environmental issue and plant responses: A metabolomics perspective Metabolites 11 2021 724 10.3390/metabo11110724 34822381
62 Bannari A. Al-Ali Z.M. Assessing climate change impact on soil salinity dynamics between 1987-2017 in arid landscape using Landsat TM, ETM+ and OLI data Remote Sens (Basel) 12 2020 2794 10.3390/RS12172794
63 Lephatsi M.M. Meyer V. Piater L.A. Dubery I.A. Tugizimana F. Plant responses to abiotic stresses and rhizobacterial biostimulants: Metabolomics and epigenetics perspectives Metabolites 11 2021 457 10.3390/metabo11070457 34357351
64 Liu Y. Xun W. Chen L. Xu Z. Zhang N. Feng H. Zhang Q. Zhang R. Rhizosphere microbes enhance plant salt tolerance: Toward crop production in saline soil Comput. Struct. Biotechnol. J. 20 2022 6543 6551 10.1016/j.csbj.2022.11.046 36467579
65 de Vries F. Lau J. Hawkes C. Semchenko M. Plant–soil feedback under drought: does history shape the future? Trends Ecol. Evol. 38 2023 708 718 10.1016/j.tree.2023.03.001 36973124
66 Nongpiur R.C. Singla-Pareek S.L. Pareek A. Genomics Approaches For Improving Salinity Stress Tolerance in Crop Plants Curr. Genomics 17 2016 343 357 10.2174/1389202917666160331202517 27499683
67 Wang X. Li N. Li W. Gao X. Cha M. Qin L. Liu L. Advances in Transcriptomics in the Response to Stress in Plants Glob. Med. Genet. 7 2020 30 34 10.1055/s-0040-1714414 32939512
68 Diwan D. Rashid M.M. Vaishnav A. Current understanding of plant-microbe interaction through the lenses of multi-omics approaches and their benefits in sustainable agriculture Microbiol. Res. 265 2022 127180 10.1016/j.micres.2022.127180 36126490
69 Gupta A. Tiwari R.K. Shukla R. Singh A.N. Sahu P.K. Salinity alleviator bacteria in rice (Oryza sativa L.), their colonization efficacy, and synergism with melatonin Front. Plant Sci. 13 2022 1060287 10.3389/fpls.2022.1060287 36714774
70 Chieb M. Gachomo E.W. The role of plant growth promoting rhizobacteria in plant drought stress responses BMC Plant Biol. 23 2023 407 10.1186/s12870-023-04403-8 37626328
71 Li C. Zhang W. Yuan M. Jiang L. Sun B. Zhang D. Shao Y. Liu A. Liu X. Ma J. Transcriptome analysis of osmotic-responsive genes in ABA-dependent and -independent pathways in wheat (Triticum aestivum L.) roots PeerJ 7 2019 6519 10.7717/peerj.6519
72 Joshi R. Wani S.H. Singh B. Bohra A. Dar Z.A. Lone A.A. Pareek A. Singla-Pareek S.L. Transcription factors and plants response to drought stress: Current understanding and future directions Front. Plant Sci. 7 2016 1029 10.3389/fpls.2016.01029 27471513
73 Kumawat K.C. Sharma B. Nagpal S. Kumar A. Tiwari S. Nair R.M. Plant growth-promoting rhizobacteria: Salt stress alleviators to improve crop productivity for sustainable agriculture development Front. Plant Sci. 13 2022 1101862 10.3389/fpls.2022.1101862 36714780
74 Ali Q. Ayaz M. Mu G. Hussain A. Yuanyuan Q. Yu C. Xu Y. Manghwar H. Gu Q. Wu H. Gao X. Revealing plant growth-promoting mechanisms of Bacillus strains in elevating rice growth and its interaction with salt stress Front. Plant Sci. 13 2022 994902 10.3389/fpls.2022.994902 36119605
75 Gupta A. Mishra R. Rai S. Bano A. Pathak N. Fujita M. Kumar M. Hasanuzzaman M. Mechanistic Insights of Plant Growth Promoting Bacteria Mediated Drought and Salt Stress Tolerance in Plants for Sustainable Agriculture Int. J. Mol. Sci. 23 2022 3741 10.3390/ijms23073741 35409104
76 Zahra S.T. Tariq M. Abdullah M. Azeem F. Ashraf M.A. Dominance of Bacillus species in the wheat (Triticum aestivum L.) rhizosphere and their plant growth promoting potential under salt stress conditions PeerJ 11 2023 14621 10.7717/peerj.14621
77 Zhang W. Xia K. Feng Z. Qin Y. Zhou Y. Feng G. Zhu H. Yao Q. Tomato plant growth promotion and drought tolerance conferred by three arbuscular mycorrhizal fungi is mediated by lipid metabolism Plant Physiol. Biochem. 208 2024 108478 10.1016/j.plaphy.2024.108478 38430785
78 Brambilla S. Stritzler M. Soto G. Ayub N. A synthesis of functional contributions of rhizobacteria to growth promotion in diverse crops Rhizosphere 24 2022 100611 10.1016/j.rhisph.2022.100611
79 Khoso M.A. Wagan S. Alam I. Hussain A. Ali Q. Saha S. Poudel T.R. Manghwar H. Liu F. Impact of plant growth-promoting rhizobacteria (PGPR) on plant nutrition and root characteristics: Current perspective Plant Stress 11 2024 100341 10.1016/j.stress.2023.100341
80 Riviezzi B. Cagide C. Pereira A. Herrmann C. Lombide R. Lage M. Sicardi I. Lage P. Castro-Sowinski S. Morel M.A. Improved nodulation and seed yield of soybean (Glycine max) with a new isoflavone-based inoculant of Bradyrhizobium elkanii Rhizosphere 15 2020 100219 10.1016/j.rhisph.2020.100219
81 Margarita S. Sviatoslav M. Yelena O. Makhpal Y. Can salt-adapted microorganisms alleviate salt stress in plants and enhance their non-specific resilience? Front. Agron. 5 2023 1287108 10.3389/fagro.2023.1287108
82 Peng M. Jiang Z. Zhou F. Wang Z. From salty to thriving: plant growth promoting bacteria as nature’s allies in overcoming salinity stress in plants Front. Microbiol. 14 2023 1169809 10.3389/fmicb.2023.1169809 37426022
83 Santoyo G. How plants recruit their microbiome? New insights into beneficial interactions J. Adv. Res. 40 2022 45 58 10.1016/j.jare.2021.11.020 36100333
