Salinity is a severe environmental factor having adverse effects on the growth and productivity of many crops (Kamran et al., 2020; Semida et al., 2021a; Shaaban et al., 2022). Globally, salt-affected soil was recorded as approximately 1,125 million hectares (Shahid et al., 2018; Hossain, 2019). This salinity stress controls several physiological, biochemical, and molecular processes in plants (Munns and Tester, 2008; Gupta and Huang, 2014). High accumulation of soluble salts in the soil generates osmotic stress as a rapid response of the plant, consequently decreasing the absorption capacity of the root system. This stress response also induces alteration in some physiological responses, including membrane interruption and physiological drought, and decrease in stomatal aperture (Munns and Tester, 2008; Hanin et al., 2016). Subsequently, the accumulation of high potential toxic ions, especially Na⁺ and Cl^– in plant tissues, has several negative effects in cell metabolism and causes disruption of photosynthesis and respiration, and inhibits the antioxidant machinery (Semida et al., 2015; Abd El-Mageed et al., 2020).

Besides the increased Na⁺ accumulation, the reduction in K⁺ and Ca⁺² uptakes produced by cytosolic K⁺ and Ca²⁺ efflux impeded cell function, caused cell membrane instability, and hampered enzyme activities (Ahanger et al., 2017; Kamran et al., 2020). Additionally, salinity induces secondary stresses as oxidative stress that produces toxic reactive oxygen species (ROS; O², OH^–, and H₂O₂) (Sarker and Oba, 2020). These ROS damages cellular organelles (membrane, DNA, protein), disturbing several processes such as photosynthesis, transpiration, and stomatal conductance, as well as lowering photosynthetic pigment concentration (Acosta-Motos et al., 2017; Muhammad et al., 2021). Plants react and respond to salinity stress through various pathways such as ion homeostasis and compartmentalization, ions transport, osmotic adaptation, stimulation of antioxidant machinery, and osmolyte biosynthesis (Sarker and Oba, 2020; Semida et al., 2020). These reactions stimulates ROS detoxification, the stabilization of the membrane, mineral uptake, ion distribution, and the ultrastructure of organelles, which increases plant adaptability under saline conditions.

Sweet potato (Ipomoea batatas L.) (Lam.) is an herbaceous dicotyledonous plant belonging to the family Convolvulaceae (Byju and George, 2005) with the tuberous root as its most valuable part (Ekanayake and Collins, 2004). Sweet potato tubers are high in carbohydrates, particularly the orange-fleshed tubers being a good source of beta-carotene and vitamin A precursor (Dasgupta et al., 2008). It is ranked seventh among food crops globally; however, the productivity of sweet potato is adversely affected under soil salinity (Dasgupta et al., 2008; Meng et al., 2020).

Developing efficient, ecofriendly, and low-cost pathways for salinity stress management is a major challenge. The potential use of materials such as effective microorganisms (EMs) and nanofertilizer, including magnesium oxide (MgO) nanoparticles (MgO-NP), could minimize the harmful effects of salinity on plant growth and productivity.

EMs stock solution is an ecofriendly technology and one among the biofertilizers used in this concern (Abd El-Mageed et al., 2020). It contains various fermented mixed cultures of coexisting and mutually compatible microorganisms in an acidic medium, such as the beneficial and nonpathogenic microorganisms (aerobic and anaerobic), including photosynthetic bacteria, lactic acid bacteria, yeast, actinomycetes, and fermenting fungi (Higa and Parr, 1994; Talaat et al., 2015). The stimulating effect of EMs improves soil structure and fertility, organic matter, and nutrient cycling and reduces chemical fertilizers and pesticides dependency, resulting in increased profitability and sustainability (Talaat et al., 2015). Moreover, the combinations of EMs can synthesize bioactive substances such as amino acids, vitamins, sugars, lactic acids, enzymes, and hormones. These compounds promotes plant growth by stimulating root development, photosynthetic capacity, protein activity, germination, flowering, fruiting, and ripening of crops (Higa and Parr, 1994; Hu and Qi, 2013). Additionally, using EMs alleviated the effects of salinity and promoted salt resistance (Talaat, 2015; Abd El-Mageed et al., 2020; Porter et al., 2020). Furthermore, EMs application enhanced nutrient acquisition, accumulation of compatible solutes (soluble sugars, free amino acids, glycine betaine, and proline) (Talaat et al., 2015; Abd El-Mageed et al., 2020), and upregulated the ascorbate–glutathione cycle capacity; a key pathway that reduces oxidative damage (Talaat, 2014). Also, EMs-supplemented soil increased the photosynthetic efficiency of the Photosystem II (PSII), macronutrient contents, and seed yield of bean plants (Iriti et al., 2019).

Magnesium (Mg^{2 +}) is a macronutrient involved in several physiological and biochemical processes required for plant growth and development (Jezek et al., 2015). For example, Mg^{2 +} plays an important role in manipulating a crucial biological polyphosphate compound such as ATP, DNA, and RNA (Shinde et al., 2020). Besides, it is the central atom of the chlorophyll molecule and thus essential for activating many enzymes, including ribulose-1,5-bisphosphate-carboxylase/oxygenase (RubisCO). Therefore, Mg^{2 +} plays a crucial role in plant metabolism processes such as sugar synthesis, nutrient uptake, protein biosynthesis, chloroplast formation, phloem loading, and the portioning of photo-assimilates from source to sink organs, and majorly in the light and dark reactions of photosynthesis (Shabala and Hariadi, 2005; Jezek et al., 2015; Feller et al., 2018).

Nanotechnology has recently received much attention as a promising approach in sustainable agricultural applications as an alternative to conventional fertilizers (El-Saadony et al., 2021). At their core, nanoparticles (NPs) have a novel small size (1–100 nm) feature that can alter and assemble atoms that possess and improve physical, chemical, and biological properties. This feature leads to improved performance of the NPs function due to the high surface-to-volume ratio and surface charges (Al-Mamun et al., 2021; El-Saadony et al., 2021). Therefore, nanoscale-basted materials are more reactive than their bulk-scale counterparts, with greater penetration ability into plant tissues and rapid translocation between plant parts (Zahedi et al., 2019; Semida et al., 2021b). Moreover, nanofertilizers ensure the slow and controlled release of the fertilizers and reduce nutrient losses during fertilization, improving the efficient use of nutrients (Rizwan et al., 2019; Al-Mamun et al., 2021). Additionally, available evidence reported that incorporating nanofertilizers of macro- and micronutrients in crop nutrition stimulates the growth and productivity of salt-stressed plants (Mohamed et al., 2017; Adjei et al., 2021; Etesami et al., 2021). Therefore, the development of nanoscale particles of Mg^{2 +} may help to trigger the metabolic pathways, including photosynthesis, leading to better growth and higher yield of plants (Rathore and Tarafdar, 2015).

The coapplication of EMs with nanomaterials such as Mg^{2 +} may be an interesting/novel application to improve sweet potato performance under salinity conditions. Therefore, this study was designed to investigate the coapplication of EMs and MgO-NP on the growth and yield of sweet potato plants cultivated in salt-affected soil. Additionally, this study examines the water status of the tissue, membrane stability, photosynthetic pigments content, nutrients content, accumulation of osmolytes, and antioxidant capacity of sweet potato plants.

In this study I. batatas plants were cultivated in salt-affected soil (7.56 dS m^–1; Table 1), causing several morphological and physio-biochemical function abnormalities. Sweet potato plants responded to the salt stress by reducing growth traits (Table 2), tuber yield (Table 3), tissue water status (RWC), index of membrane integrity (MSI), photosynthetic pigments (Table 4), and acquisition of nutrients (Table 5). This retardation of plant growth and productivity results from salinity, lowering the soil water potential, which reduces the water uptake by the roots (Sharma and Garg, 2021). Consequently, this impaired cell division, expansion, metabolism, ion imbalance, stomatal closure, gas exchange, and reduced tissue water content, including increased oxidative stress indicators over their scavenging antioxidants and deteriorated photosynthesis-linked pigments (Gupta and Huang, 2014; Arif et al., 2020; Rady et al., 2021b). Plants have developed various stress-responsive mechanisms to withstand salt stress, such as activating the antioxidative compounds, including enzymatic and non-enzymatic antioxidants functioning in tandem with osmolytes (Ahanger et al., 2017; Semida et al., 2020). However, the plant’s endogenous defense system is insufficient to relieve salinity stress under severe stress conditions, necessitating the addition of exogenous stimuli to help salt-stressed plants to adapt (Rady et al., 2021a).

The application of EMs or/and MgO-NP in the current study showed effective mechanisms for reducing salinity stress’s harmful effects. Also, due to their properties, the coapplication of EMs and MgO-NP may boost the physio-biochemical pathways against salt stress. In salt-stressed sweet potato plants, exogenously-applied EMs or/and MgO-NP (50 or 100 μg ml^–1) improved the morpho-physiological, biochemical, and productivity responses compared to the control plants. EMs or/and MgO-NP application also alleviated the adverse effects of salinity stress on the growth parameters of sweet potato plants, thereby promoting tuber yield and WUE compared to stressed control plants. The coapplication of EMs and MgO-NP assigned the highest positive effects, achieving the best results. These restorations in plant growth and productivity of sweet potato by application of EMs or/and MgO-NP are probably due to the improvements in growth-linked molecules of osmolytes and antioxidants that help plants recover from salt stress (Talaat, 2015). Furthermore, EMs could promote plant performance by synthesizing bioactive substances, including vitamins, amino acids, sugars, lactic acid, hormones, and enzymes (Higa and Parr, 1994; Hu and Qi, 2013).

The MSI detects cell membrane stability whereas RWC estimates the plant water status in terms of the physiologically available water in plant tissues (Slabbert and Krüger, 2014; Abd El-Mageed et al., 2019; Abdelkhalik et al., 2019); however, both were reduced under salt stress in the current study (Table 4). Thus, maintaining higher RWC in stress tissues maintains cell physiological functions (i.e., photosynthesis, stomatal aperture, gas exchange, and cell expansion and development), which proceed via osmoregulation as an effective stress tolerance mechanism (Abid et al., 2018; Desoky et al., 2021). Coapplication of EMs and MgO-NP improved the recovery of tissues in salt-stressed sweet potato by increasing the tissue water content (RWC; Table 4). This response may be due to the effect of EMs and MgO-NP in elevating the accumulation of osmolytes (e.g., soluble sugars, FP, amino acids, and K⁺ ion; Figure 1 and Table 5) and the antioxidative compounds (Figure 1). These modulated the osmotic pressure and mitigated the oxidative damage, preserving cellular turgor pressure and membrane integrity against stress damage (Talaat, 2014; Talaat et al., 2015; Cai et al., 2018).

Exogenous applied EMs and/or MgO-NP enhanced salt tolerance in stressed sweet potato plants, since enhanced the membrane integrity (Table 4). Higher enzymatic antioxidant activities, as well as GSH and AsA levels, as a result of EM and/or MgO-NP treatments (Figure 1), are linked to reduced ROS-induced oxidative damage and minimize lipid peroxidation, which help in cell membrane stabilization and function maintenance (Gomathi and Rakkiyapan, 2011). Under salinity stress, the buildup of Ca²⁺ in plant tissues by applying EMs and MgO-NP (Table 5) inhibits Na⁺ uptake and transport, as well as binding to the cell wall and increased cell membrane stability (Rahman et al., 2016).

Salinity stress decreased the cellular physiological functions, including photosynthetic pigment levels, due to the restriction in chlorophyll biosynthesis that elevates chlorophyll degradation (by chlorophyllase enzyme) or/and insufficient nutrient uptake (Sarker and Oba, 2020; Muhammad et al., 2021). Salinity stress could also be linked to oxidative damage to the chlorophyll pigments caused by ROS in the chloroplast and interferes with Na⁺ and Cl^– ions with the protein pigment complexes (Sarker and Oba, 2020). Photosynthesis is an important physio-chemical process in plants, with its efficiency mainly related to the changes in the number of photosynthetic pigments under salinity conditions (Arif et al., 2020). Therefore, increasing the chlorophylls and carotenoids content is employed as a biochemical signal of salt stress tolerance (Stefanov et al., 2016). Our results illustrated that the combined supplementation of EMs and MgO-NP significantly enhanced the chlorophylls (a and b) and carotenoid levels in salt-stressed sweet potato plants (Table 4). Magnesium is at the core of all chlorophylls involved in the activation/activity of Rubisco and, therefore, an essential component of photosynthesis (Moynier and Fujii, 2017; Hauer-Jákli and Tränkner, 2019). Its presence may be the sole cause of the stimulated response in the MgO-NP-treated plants. EMs were observed to relieve salinity-induced damages to the photosynthetic efficiency of Vicia faba and Phaseolus vulgaris plants by modifying several physiological processes such as maintaining cell turgor, membrane integrity, nutrient acquisition, levels of osmolytes, and antioxidant capacity (Talaat et al., 2015; Iriti et al., 2019). Besides acting as auxiliary light-harvesting pigments, carotenoids act as an antioxidant that protects the photosynthesis system by aiding the heat dissipation of excess excitation energy in the photosynthetic machinery, thus preventing superoxide generation (Hashimoto et al., 2016; Abid et al., 2018). Therefore, increasing the chlorophylls (a and b) and carotenoids in treated plants indicates the stimulatory role of EMs and MgO-NP under salinity stress.

This current study showed that soil salinity induced ionic imbalance in the cells of sweet potato plants. It reduced P, N, K⁺, Mg²⁺, and Ca²⁺ acquisition, but increased Na⁺ accumulation (Table 5) attributed to changes in ionic homeostasis, potential nutrients uptake, and specific toxic ion (Parida and Das, 2005; Talaat et al., 2015). Besides their importance in plant growth and productivity, K⁺ acts as an osmoregulator in plants under abiotic stress (Assaha et al., 2017). However, the increased Na⁺ concentration in plant tissues competitively affected the K⁺ uptake since both share similar transport channels (Farooq et al., 2018; Isayenkov and Maathuis, 2019), thus reducing the cytosolic K⁺/Na⁺ ratio (Table 5). This resultant effect also provokes the disruption of cellular homeostasis, oxidative stress, nutrient deficiency, interference among K⁺ and Ca²⁺ functions, and hampered growth (Assaha et al., 2017). Interestingly, coapplication of EMs and MgO-NP mediated recovery of ionic homeostasis and nutrient uptake, decreasing Na⁺ level, whereas increasing P, N, K⁺, and Ca²⁺ acquisition in salt-stressed sweet potato. A crucial salinity tolerance mechanism is maintaining a balanced cytosolic K⁺/Na⁺ ratio (Farooq et al., 2018) achieved by the integrative application of EMs and MgO-NP. Further, increased Ca²⁺ and Mg²⁺ levels in the supplemented plants with EMs and MgO-NP would assist stressed plants in preventing Na⁺ accumulation in the cell to a lethal level, as indicated by Talaat et al. (2015).

Ion analysis demonstrated the amelioration of the nutrient status in Mg-treated plants in terms of Mg^{2 +}, K⁺, and Mn in different Zea mays organs, minimizing the adverse effects of salt stress (Jezek et al., 2015). Our results conform to Kanjana (2020), who observed positive effects by exogenous application of Mg-NP in increasing the nutrient (N, P, K⁺, and Mg^{2 +}) concentration in cotton plants. However, the application of EMs exhibited a favorable effect on nutrient acquisition in salt-stressed sweet potato plants. The application of EMs probably provokes such a response due to their involvement in promoting tissue water content and cell membrane integrity (Table 4). Furthermore, EMs supplementation stimulated root growth of Phaseolus vulgaris plants under salinity stress that enhanced the potential nutrient uptake (Talaat et al., 2015). Finally, EMs promote the decomposition of organic materials and improve the mineralization of organic matter, releasing more nutrients into the soil for plant absorption (Hu and Qi, 2013).

Salinity composes stress by damaging ionic and osmotic balances in plants. Our study shows that the plant’s defense machinery, including accumulation of osmolytes (Figure 1) and upregulating the activity of antioxidant molecules (Figure 2), was enhanced by the integrative effects of EMs and MgO-NP, which enabled the stressed plants to withstand the salinity stress. Similarly, osmotic adaptation is vital for maintaining cell turgor, essential for growth and productivity. Therefore, plants synthesize several osmolytes under salt stress, such as soluble sugars, total free amino acids, and FP. The coapplication of EMs and MgO-NP significantly increased the free amino acids, TSS, and FP levels of osmotically-stressed sweet potato plants compared to the control plants (Figure 1). These osmolytes may assist salt stress tolerance in sweet potato plants by promoting osmotic adjustment, therefore stimulating root water uptake by aiding its diffusion into the cells, thereby maintaining cellular turgor, and increasing RWC (Table 4), consequently allowing the plant to continue the physiological processes under salinity stress (Abid et al., 2018; Desoky et al., 2021). Moreover, the osmolytes effectively scavenge the ROS and stabilize the protein and membrane integrity (Arif et al., 2020), consequently increasing MSI (Table 5). Our results also showed that salt stress-induced physiological disorders in sweet potato plants reduced the phenolic and protein concentration. This result correlates with the reports of Talaat (2015) that salt stress reduced total protein levels by increasing protein hydrolysis and lowering protein synthesis enzymes activity. However, our results demonstrated that the application of EMs and MgO-NP ameliorated salt-induced inhibitory effect on protein and phenolic levels, given that protein and phenolic content increased in EMs and MgO-NP-treated plants compared to the control. This enhancement in protein level may be linked to increased nutrient acquisition and higher K⁺ accumulation by applying EMs and MgO-NP under salt stress, which helps to maintain a higher ratio of K⁺/Na⁺, thus preventing the inhibitory effect of salt stress in various enzymes, including protein biosynthesis (Talaat, 2015). Similarly, phenolic molecules have antioxidant properties for scavenging ROS, including a significant reported link between phenolic compounds and abiotic-stress tolerance as an effective predictor of the level of redox state maintenance in salinity-stressed cells (Kiani et al., 2021; Šamec et al., 2021). Therefore, it is worth noting that increasing protein and phenolic content can be effective ways for EMs and MgO-NP-treated plants to achieve salinity tolerance.

Under salinity stress, ROS overproduction induces oxidative damage, therefore activating the antioxidant machinery, including enzymatic and non-enzymatic, in the plants (Sarker and Oba, 2020). Our results revealed that coapplication of EMs and MgO-NP upregulated the activity of AsA, GSH, SOD, APX, GR, and CAT (Figure 2). These antioxidative compounds (enzymatic and non-enzymatic), soluble sugars, proline, phenolic compounds, and photosynthetic auxiliary pigments such as carotenoids, are the powerful ROS quenchers and scavengers, making them effective salinity mitigators (Zhang and Dai, 2019). Additionally, externally applied EMs mediated an increased activity of the enzymatic antioxidants and the AsA and GSH in bean plants, indicating an improved ascorbate–glutathione cycle (AsA-GSH) as a potent mechanism in the detoxification of oxidative stress indicators; H₂O₂ and MDA (Talaat, 2014). Furthermore, MgO-NP application boosted tobacco plant growth and increased the activity of SOD and peroxidase (POD) enzymes (Cai et al., 2018). Accordingly, our findings demonstrated the importance of applying EMs and/or MgO-NP to relieve the salinity stress on the sweet potato.

The results of present study clearly showed that the application of EMs and/or MgO-NP alleviates the inhibitory effects of salt stress on sweet potatoes. It also showed the coapplication of EMs and MgO-NP as a more effective method exceeding all individual approaches. Furthermore, the integrative application of EMs and MgO-NP enhanced the antioxidant activity (AsA, GSH, SOD, APX, GR, and CAT) and osmolytes accumulation (FP, total free amino acids, soluble sugars, K⁺) as well as increased the phenolic and protein contents. Additionally, the coapplication of EMs and MgO-NP induced improvements in RWC, MSI, photosynthetic pigments (chlorophylls a and b, and carotenoids), and nutrient acquisition, consequently promoting the growth and productivity of salt-stressed sweet potato. Moreover, the results suggested that biostimulants, i.e., EMs and MgO-NP, should be used in future applications to improve plant performance (growth and productivity) under salinity conditions.

The original contributions presented in the study are included in the article/Supplementary Material, further inquiries can be directed to the corresponding authors.

TAA, MG, KH, SAQ, KE-T, and AA conceived and designed the research. TAA, SAQ, and KE-T supervised the study. TAA, MG, KH, ME-S, SAE-M, and AA performed field experiments. TAA, MG, KH, ME-S, SAE-M, and AA developed the biochemical and physiological analyses. TAA, SAQ, and KE-T analyzed the data. TAA, MG, KH, SAE-M, HA, and AA assisted with experiments and/or data evaluation. All authors contributed to the article and approved the submitted version.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.