Plants face a multitude of stressors throughout their lifecycles, which can originate from both abiotic and biotic sources. Among these challenges, high salinity stands out as a prominent abiotic stressor that poses a significant environmental threat
(Jisha et al., 2013). Additional abiotic stresses impacting plants include heat, salt, irradiation and light stress, all of which have detrimental effects
(Reyes and Cisneros-Zevallos, 2007;
Singh et al., 2022). Abiotic stresses impose severe limitations on crop production worldwide, exacerbated by global warming, climate fluctuations and unpredictable weather patterns
(Deshmukh et al., 2017). Notably, soil salinity has emerged as a paramount global concern
(Attia et al., 2021: Hafeez et al., 2021; Mukhopa
dhyay et al., 2021; Hossen et al., 2022; El-Beltagi et al., 2023;
El-Hawary et al., 2023). Disturbingly, research indicates that over 33% of agricultural regions are currently grappling with salinity issues
(El-Beltagi et al., 2023). The rise in salinity within agricultural lands can be attributed to factors such as global warming and inappropriate farming practices
(Shrivastava and Kumar, 2015). This salinity stress disproportionately affects many plant species that are crucial for human nutrition, as they exhibit varying degrees of sensitivity or tolerance to salt stress. Consequently, ensuring food security, safe food access and sustainable agriculture for our growing global population becomes an increasingly daunting challenge.
Adverse effects of salt stress on plants
Germination and plant growth
Salinity exerts its influence on all plant processes
(Xiong and Zhu, 2002;
Johnson and Puthur, 2021;
Linic et al., 2021), resulting in disruptions across various developmental stages, including seed germination, plant growth, development, reproduction and yield
(Shrivastava and Kumar, 2015). The adverse effects of salinity on germination and the hampering of plant growth are closely linked to ion toxicity, thereby subjecting plants to stress
(Katambe et al., 1998). The impact of salt accumulation in soils on plant growth varies across different developmental stages
(Bernstein, 1975). While plants can experience salinity stress at all growth stages, germination and the early growth phase are notably more sensitive for the majority of plant species
(Ibrahim et al., 2018; Ali et al., 2020; Ali et al., 2021; Dhanyasree et al., 2022). Seed germination, a pivotal and delicate stage in plant development, plays a critical role in shaping plant growth, yield and quality
(Gupta and Huang, 2014) (Fig 1).
Stomatal Conductivity, photosynthesis and carotenoids
High salt concentrations in the soil or water not only hinder the uptake of water through plant roots but also lead to the inhibition of stomatal conductivity, photosynthesis and overall plant growth
(Shrivastava and Kumar, 2015;
Gürsoy, 2022a;
Oliviera et al., 2023). The impact of salt stress on photosynthesis involves a reduction in stomatal conductivity, a critical process that diminishes nutrient and water uptake, ultimately leading to a decrease in chlorophyll content
(Ahanger et al., 2020). Furthermore, disruptions in stomatal arrangement, attributed to ion imbalances, result in decreased photosynthesis capacity, reduced leaf surface area and a host of related morphological and biochemical disturbances, ultimately diminishing yield and its components
(Granaz et al., 2022; Hossen et al., 2022). Salt stress inflicts damage on plant membranes, alters the activity of plant growth regulators and further suppresses photosynthesis, impacting all physiological processes and potentially leading to plant death
(Ibrahim et al., 2016). Some studies have reported that carotenoid levels may increase under stress conditions
(Gürsoy, 2020;
2022b) (Fig 1).
@figure1
Plants responses to salt stress
When confronted with stress-induced changes, plants employ a variety of mechanisms for self-protection. One such method involves increasing the production of reactive oxygen species (ROS), which in turn triggers oxidative stress and leads to ion imbalance issues within the cells
(Nabi et al., 2019). Plants initiate the generation of ROS as an initial response to various abiotic stresses, such as salinity and drought, among others (Fig 1). This response is recognized for its potential to inflict significant damage to cell structures and disrupt normal cellular functions
(Deshmukh et al., 2017).
Enzyme activities
Plants employ a range of mechanisms to shield themselves from the detrimental effects of ROS. Among these protective strategies is the upregulation of antioxidant enzymes that serve to neutralize the impact of excessive ROS production
(Shaki et al., 2017) (Fig 1). Some prominent members of these enzymes include superoxide dismutase (SOD), peroxidase (POX) and catalase (CAT), all belonging to the group of enzymatic antioxidants. In addition to enzymatic defenses, plants produce non-enzymatic antioxidants, like phenolic compounds, as a shield against heightened ROS production
(Grassmann et al., 2002; Zamljen et al., 2022). Consequently, the augmentation of antioxidant enzymes and the presence of non-enzymatic phenolic compounds play a vital role in the plant’s response mechanism to stress. Furthermore, high salinity stress in plants not only triggers the formation of superoxide but also induces the generation of singlet oxygen, hydroxyl radicals and hydrogen peroxide
(Rajput et al., 2021).
Malondialdehyde (MDA) and proline
In addition, the excessive intake of sodium ions (Na+) leads to an ion imbalance within plant cells and results in membrane damage, primarily through the production of malondialdehyde (MDA) and proline
(Kishor and Sreenivasulu, 2014;
Fang et al., 2021; Gürsoy, 2022b). In response to the effects of salt stress, both MDA and proline production increase (Fig 1). MDA, or lipid peroxidation, is recognized as a byproduct of active oxygen species under various stress conditions
(Fu and Huang, 2001;
Yang et al., 2009; Gürsoy, 2022b) and it serves as a natural indicator of oxidative damage induced by salt stress. Meanwhile, proline assumes critical roles in scavenging free radicals during salinity stress
(Zhu et al., 2019). This versatile compound, proline, ranks among the most commonly encountered osmolytes
(Saxena et al., 2013).
Seed priming and its beneficial effects
Various techniques have been adapted to enhance plant tolerance to stresses
(Jisha et al., 2013). Among these methods, seed priming stands out as a low-risk, cost-effective and easily applicable technique that effectively boosts plant resistance to various stressors
(Jisha et al., 2013; Thakur et al., 2019; Garcia et al., 2022; Gürsoy, 2022c;
Paul et al., 2022). Moreover, the priming process is highly efficient in enhancing both seed germination and seedling growth by triggering numerous vital processes
(Johnson and Puthur, 2021). Seed priming contributes to stress reduction through various means, including early and uniform germination, accelerated root and shoot development and the promotion of overall plant growth
(Ghosh and Atta, 2022;
Patel et al., 2023). It not only ensures consistent and rapid germination but also fortifies resistance against a range of environmental stressors
(Afzal et al., 2016; Johnson and Puthur, 2021). Priming induces enhanced germination by introducing significant physiological variation in the seed
(Damalas et al., 2019). Essentially, seed priming involves the initiation of diverse processes in plants through the treatment with natural and synthetic compounds
(Jisha et al., 2013) and these applications enhance various characteristics along with cellular and plant development
(Savvides et al., 2016). Numerous studies have explored the effects of priming applications against one or more stress factors
(Savvides et al., 2016; Van Oosten et al., 2017).
Priming methods
Various priming techniques are available to reduce the effects of stress factors which includes hydropriming, halopriming, osmopriming, hormonal priming and biopriming
(Neto et al., 2020; Chakraborty and Dwivedi, 2021).
Hydropriming
One of the most widely employed priming techniques in recent times is hydropriming. Hydropriming is an environmentally friendly, cost-effective and easily applicable method for stress protection
(Forti et al., 2020; Garcia et al., 2022) (Fig 2). Essentially, hydropriming involves soaking seeds in pure water for a specified duration, subject to specific light and temperature conditions
(Zhao et al., 2018; Damalas et al., 2019; Tanwar et al., 2023). This approach has been shown to have positive effects on plant growth, both during the initial stages and later in development
(Rhaman et al., 2020). Hydropriming is particularly valuable for crops where germination and growth may be hampered by stressful conditions
(Castro-Colina et al., 2012). The application of hydropriming has a significant impact on the antioxidant system of plants under various stress conditions. For instance, in a study involving alfalfa seeds subjected to salt stress conditions,
Amooaghaie (2011) observed an increase in the activity of various enzymes following hydropriming. Concurrently, proline content, electrolyte leakage (EL) and malondialdehyde (MDA) levels decreased. Similarly, when hydropriming was applied to
Quercus rugosa seeds, rapid and synchronized germination and improved growth parameters were observed
(Castro-Colina et al., 2012). In the case of corn seeds exposed to salt stress, hydropriming positively affected germination and seedling growth parameters
(Jayesh and Meeta, 2015). Moreover, hydropriming has been found to enhance photosynthetic activity, stomatal conductivity and evapotranspiration in bread wheat seeds under both normal and stress conditions
(Tabassum et al., 2017). Researchers have also reported that hydropriming can increase the salt tolerance of sunflower plants, with no accumulation of proline in hydroprimed seedlings, indicating protective properties
(Matias et al., 2018). In rice seeds, hydropriming has had a positive impact on morphological and physiological properties
Mondal et al. (2018), while in faba bean seeds, it has improved germination parameters and seedling emergence
(Damalas et al., 2019). An increase in chlorophyll content has been observed after hydropriming
(Bourioug et al., 2020). Furthermore, in
Medicago truncatula seeds, hydropriming resulted in the best germination outcomes Forti
et al. (2020). In the context of enhancing resistance to
Aspergillus niger in wheat plants, various priming treatments were applied, with hydropriming proving to be particularly effective. Physiological and biochemical properties of wheat demonstrated that hydropriming was more effective in disease reduction and it led to higher expression levels of β-1,3-glucanase, Thaumatin-like protein (TLP) and chitinase, further contributing to increased disease resistance
Gul et al., (2022). Additionally, a 6-hour hydropriming treatment was found to be highly effective in increasing the germination of rice cultivars
(Ranmeechai et al., 2022).
Halopriming
Halopriming is another commonly employed technique, wherein seeds are primed in a solution containing organic salts. This method expedites germination and fosters uniform seedling growth even under the influence of stress factors
(Afzal et al., 2008; Hidayah et al., 2022). Halopriming has been demonstrated to offer numerous advantages, including improved crop establishment, enhanced uniformity, increased plant growth and higher productivity, particularly in the face of abiotic environmental stresses, which are essential to meet future food demand sustainably and reliably
(El-Sanatawy et al., 2021). When seeds undergo halopriming, it can bolster plant growth even in the presence of salt stress conditions
(Hidayah et al., 2022). It achieves this by regulating the activities of existing enzymes and producing essential germination metabolites
(Ahmad et al., 2017). For instance, research conducted with wheat seeds treated with different inorganic salts (CaCl
2, NaCl and CaSO
4) found that halopriming enhanced salt stress tolerance and improved germination, seedling growth parameters, seedling vigor, ion homeostasis and starch metabolism
(Afzal et al., 2008). Halopriming also helps prevent the accumulation of sodium ions (Na+) through tissue tolerance effects. Additionally, halopriming contributes to enhanced plant and seedling growth and increases salinity tolerance, especially during the seedling stage
(Hidayah et al., 2022). Halopriming plays a pivotal role in regulating enzyme activities, ensuring the production of necessary germination metabolites
(Ahmad et al., 2017). In the case of rice seeds, priming under salt stress conditions stimulated metabolism and increased seedling vigor
(Jisha and Puthur, 2014). Furthermore, when halopriming treatment was applied to
Gerbera jamesonii and
Zinnia elegans seeds with CaCl
2, KNO
3 and KCl, it resulted in uniform maturity and improved flower harvesting
(El-Sanatawy et al., 2021). In a study that examined the effects of halopriming in conjunction with different irrigation systems on corn seeds, researchers found that it enhanced germination uniformity, speed, rate and strength. Additionally, it increased water use efficiency in field conditions compared to the control, which was significant in mitigating the adverse effects of water scarcity
(El-Sanatawy et al., 2021). Halopriming has also been applied to
Hibiscus sabdariffa seeds under salt stress conditions, leading to an increased germination rate and emergence percentage
(Taghvaei et al., 2022).
Osmopriming
Osmopriming involves the immersion of seeds in various osmotic solutions, such as polyethylene glycol, mannitol, sorbitol and more
(Ghassemi-Golezani et al., 2008;
Garcia et al., 2022). This technique can enhance seed resistance to salt stress (Fig 2). When seeds are exposed to osmotic solutions, it promotes the expression of numerous stress-related genes and proteins, expediting stress and cross-tolerance mechanisms
(Benadjaoud et al., 2022). Osmopriming operates by facilitating the movement of components within seeds at low water content, enabling seeds to slowly take up water while reducing cell damage
(Garcia et al., 2022). This process activates stress tolerance mechanisms, including enhanced antioxidant capacity and the activation of signaling molecules, ultimately leading to higher productivity
(Kerchev et al., 2020; Stasio et al., 2020). Osmopriming induces molecular changes in seeds, consequently enhancing seed germination and emergence across a wide range of plant species
(Hassanpouraghdam et al., 2009). For instance, maize seeds subjected to osmopriming exhibited improved germination and vigor characteristics
(Ghiyasi et al., 2011). The effects of osmopriming on rapeseed varieties were examined, revealing higher germination percentages, increased radicle and seedling height, greater dry weight and higher sodium (Na) content in primed seeds compared to unprimed seeds. Notably, potassium (K) content in primed seeds was also relatively higher than in unprimed seeds
(Hassanpouraghdam et al., 2009). In another study involving soybean seeds treated with polyethylene glycol (PEG 6000), the application of osmopriming at -1.2 MPa for 12 hours yielded the most favorable results across the examined properties. Primed seeds generally exhibited better characteristics than the control group
(Sadeghi et al., 2011). Osmopriming has been found to enhance seed germination and seedling growth in barley
(Tabatabaei, 2013). Additionally, when osmopriming was applied to rapeseed seeds using polyethylene glycol, transcription factors, small interfering RNA, hormones and germination properties all showed positive effects
(Kubala et al., 2015). Furthermore, the application of osmopriming to
Lavandula stoechas L. plant seeds under salt and water stress conditions effectively mitigated the adverse effects of stress on germination
(Benadjaoud et al., 2022).
@figure2
Hormonal priming
Hormonal priming is a priming technique that involves the use of various plant growth regulators
(Bryksova et al., 2020) or phytohormones to stimulate seed metabolism, subsequently promoting plant growth and ultimately increasing yield
(Bryksova et al., 2020). Plant growth regulators and phytohormones like gibberellins, cytokinins, auxins and salicylic acid are commonly employed to enhance germination and plant growth, especially under stress conditions
(Gürsoy, 2019;
2022a). For example, applying kinetin to
Salvia officinalis seeds under salt stress conditions was found to be effective in mitigating the stress effects
(Tounekti et al., 2011). In a study examining salt tolerance in wheat seeds primed with gibberellic acid, positive effects were observed on seed yield, salt tolerance, ion uptake in roots and seedlings
Iqbal and Ashraf (2013). Gibberellic acid applied to oat varieties under salt stress conditions resulted in increased germination percentages, shoot and root length, total weight and water content parameters, effectively alleviating the negative effects of stress
(Chauhan et al., 2019). Hormopriming with gibberellic acid positively affected the germination properties of safflower varieties
(Gürsoy, 2019). When salicylic acid (SA) was applied from the leaf under saline conditions, it positively affected plant height, stem diameter and chlorophyll content
(Rehman et al., 2019). Additionally, in lentil seeds, both hydropriming and osmopriming applications were found to improve seed germination and seedling growth
(Ghassemi-Golezani et al., 2008). Wheat seeds primed with kinetin and gibberellic acid under salt stress conditions displayed interesting outcomes. Gibberellic acid increased K+ levels and decreased the accumulation of Na+ and Cl- in seedlings, whereas kinetin increased Cl- accumulation and decreased K+ accumulation
(Akhtar et al., 2021). Hormopriming with salicylic acid had positive effects on the morphological and biochemical properties of sunflower and linseed seeds under salt stress conditions
Gürsoy (2022a). Furthermore, the application of salicylic acid to the seeds of the
Ocimum basilicum plant under salt stress was effective in mitigating the adverse effects of stress on gas exchange and total chlorophyll parameters
(Silva et al., 2022).
Biopriming
Biopriming is a seed priming technique involving the inoculation of seeds with living bacteria, including plant growth-promoting rhizobacteria
(Mahmood et al., 2016). It typically entails soaking seeds in solutions containing beneficial bacteria for specific durations
(Abuamsha et al., 2011). This environmentally friendly method can be applied to all plants
(Deshmukh et al., 2020; Miljakovic et al., 2022) and serves to reduce the transmission of pathogens to both the seeds and the soil by coating the seeds with beneficial microorganisms
(Forti et al., 2020). Beneficial microorganisms used in biopriming include
Bacillus spp.,
Pseudomonas spp. and
Trichoderma spp.
(Paparella et al., 2015). Biopriming offers a means to protect seeds from bacterial damage and enhance their resistance to various biotic and abiotic stresses
(Rajendra Prasad et al., 2016; Miljakovic et al., 2022). For instance, biopriming of chickpea seeds demonstrated significant improvements in disease control and yield compared to untreated seeds
(Parmar et al., 2021). Soaking pigeonpea seeds in liquid cultures, such as pink-pigmented facultative methylotroph (PPFM) at a 1:100 dilution for 3 hours or
Rhizobium or phosphobacteria at a 1:50 dilution for 4 hours, increased germination and seed vigor
(Raja et al., 2019). While the populations of
Rhizobium and phosphobacteria in microbial-infused seeds showed only slight reductions during three months of storage, the population of PPFM decreased significantly. Nevertheless, PPFM exhibited better seed quality enhancement among the cultures. A consortium of
Rhizobium and PPFM at a 1:1 ratio for 3 hours increased seed vigor with improved microbial populations
(Raja et al., 2019). Biopriming with
Bacillus spp. applied to
Medicago truncatula seeds resulted in increased seedling growth and biomass
Forti et al., (2020). Seed germination and seedling development were also positively affected. In another study, biopriming with
Pseudomonas geniculata was applied to corn seeds in salty sodic soil, leading to the mitigation of salt-induced damage, enhanced plant growth and reduced crop losses. This application of
P.
geniculata reduced the uptake of sodium ions (Na+) while increasing potassium (K+) and calcium ions (Ca
2+) in maize roots, maintaining ionic balance and homeostasis under excessive salt conditions
(Singh et al., 2020). Additionally, biopriming with a commercial biostimulant and plant growth-promoting rhizobacteria (PGPR) in
Abelmoschus esculentus genotypes increased plant development, yield and biochemical parameters
(Makhaye et al., 2021). Furthermore, soybean seeds primed with
Bradyrhizobium japonicum and
Bacillus megaterium exhibited improvements in seedling height, seedling vigor, seedling and root weight and germination in both old and normal seeds under stress conditions
(Miljakovic et al., 2022).
