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Review

Beneficial Microbes and Molecules for Mitigation of Soil Salinity in Brassica Species: A Review

by
Ines Petrić
1,
Dunja Šamec
2,*,
Erna Karalija
3 and
Branka Salopek-Sondi
4
1
Division for Marine and Environmental Research, Ruđer Bošković Institute, Bijenička 54, 10002 Zagreb, Croatia
2
Department of Food Technology, University Center Koprivnica, University North, Trg dr. Žarka Dolinara 1, 48000 Koprivnica, Croatia
3
Department for Biology, Faculty of Science, University of Sarajevo, Zmaja od Bosne 33-35, 71000 Sarajevo, Bosnia and Herzegovina
4
Department for Molecular Biology, Ruđer Bošković Institute, Bijenička 54, 10002 Zagreb, Croatia
*
Author to whom correspondence should be addressed.
Soil Syst. 2022, 6(1), 18; https://doi.org/10.3390/soilsystems6010018
Received: 16 December 2021 / Revised: 28 January 2022 / Accepted: 29 January 2022 / Published: 3 February 2022
(This article belongs to the Special Issue Advances in the Prediction and Remediation of Soil Salinization)
Versions Notes

Abstract

:
Salt stress results from excessive salt accumulation in the soil can lead to a reduction in plant growth and yield. Due to climate change, in the future climatic pressures, changed precipitation cycles and increased temperature will increase the pressures on agriculture, including increasing severity of salt stress. Brassica species contains oilseed and vegetable crops with great economic importance. Advances in understanding the mechanisms of salt stress in Brassica plants have enabled the development of approaches to better induce plant defense mechanisms at the time of their occurrence through the use of beneficial microorganisms or molecules. Both endophytic and rhizospheric microbes contribute to the mitigation of abiotic stresses in Brassica plants by promoting the growth of their host under stress conditions. In this review we summarized so far reported microorganisms with beneficial effects on Brassica plants and their mode of action. Another approach in mitigating the harmful effect of soil salinity may involve the application of different molecules that are involved in the stress response of Brassica plants. We reviewed and summarized their potential mode of action, methods of application and pointed out further research directions.

1. Introduction

Salt stress is one of the abiotic stressors that can significantly affect soil fertility, stability, and biodiversity and consequently affect crop food production by reducing plant growth and yield [1]. Soils in coastal and arid and semi-arid areas may naturally have increased salinity. However, the bigger problem are soils that are not naturally saline but where unsustainable management practices cause increased salinity [2]. Unsustainable practices include [2] the use of irrigation water that may be of low-quality (for example containing sediment content from agriculture-induced erosion and chemical pollution from agriculture and industry), inappropriate irrigation methods, poor drainage, removal of deep-rooted vegetation leading to increased groundwater levels, mismanagement of agricultural soil amendments and fertilizers, and pumping of water that can cause salt problems not only in coastal plains but also in semi-arid and arid lands. The FAO (Food and Agriculture Organization of the United Nations) has recognized salinization as one of the most important problems at the global level for agricultural production, food security and sustainability in arid and semi-arid regions [2]. It has always been known that soil salinization affects crop production (reviewed in [3]), but this effect has become even more pronounced in recent years due to climate change. According to FAO [2], climate change is exacerbating the accumulation of salts in soils due to the expansion of drylands, water scarcity, and sea-level rise, causing saltwater intrusion into coastal areas. Salts gradually accumulate in the soil, which starts as a small, hidden problem and develops into a serious degradation if not adequately addressed [2]. To cope with reduced crop production in affected areas, it is necessary to develop tools for sustainable management of salt-affected crop production by inducing salt tolerance in crops that can mitigate the harmful effects of soil salinization. In agriculture, sustainable practices mean good management of natural systems and resources, which includes building and maintaining healthy soils, judicious water use, minimizing pollution and promoting biodiversity. Therefore, increasing the salt stress tolerance of crops using sustainable practices is a challenging task.
Brassica, or cruciferous vegetables, is a genus of plants in the cabbage and mustard family (Brassicaceae). It contains oilseed and vegetable crops with a long history of agricultural use throughout the world. The most commonly grown and used Brassica plants include B. oleracea and B. rapa, which are used as vegetables. The seeds of B. nigra, B. carinata and B. juncea are also used as spices, and B. napus, B. rapa, B. juncea and B. carinata are mainly grown for the production of edible oils [4]. All developmental stages of Brassica species (from seed germination to adult plants), may be jeopardized by salinity stress, depending on salt stress intensity and duration, and the natural salt tolerance of the species [1]. It has been reported that the salt tolerance of Brassicaceae depends on the ploidy of their genome. Accordingly, amphitetraploid Brassica species, such as B. juncea, B. carinata, and B. napus, are relatively more tolerant to increased salinity compared to their diploid parents B. campestris, B. nigra, and B. oleracea [5]. However, there are some variations in salt tolerance within species and even within cultivars of the same species [6,7]. Salinity tolerance within Brassica genera exhibits significant inter- and intraspecific differences as evidenced by differential effects of salinity on total growth, electrolyte loss, proline accumulation, K+/Na+ ratio, and accumulation of hormones and specialized metabolites [8,9,10]. Conventional breeding approaches, considered energy-efficient and economical, are leading to several new promising salt-tolerant amphidiploid species (reviewed by [8]). Possible approaches include genetic engineering, but legislation in some parts of the world limits the use of such plants.
On the other hand, the use of sustainable tools to increase salt tolerance in Brassica crops and mitigate the negative effects of soil salinity is globally recognized and played an important role in the “green revolution” that brought great benefits to agriculture and mankind [11]. Recent advances in understanding the mechanisms of salt stress in Brassica plants (reviewed by [1]) have enabled the development of approaches to better induce plant defense mechanisms at the time of their occurrence through the use of beneficial molecules or microorganisms. We are focused on plant biomolecules as well as naturally occurring microorganisms that enable development of eco-friendly strategies in mitigating the harmful effects of soil stress in agriculture. In this review, we have summarized literature data about beneficial microorganisms and molecules and their mechanisms of action, and various methods of their application (seed priming, foliar application, and root application), in Brassica plants.

2. Beneficial Microorganisms to Mitigate Effect of Salt Stress Tolerance on Brassica Plants

2.1. Plant–Microorganism Interactions in Salinity Stressed Environments

Complex interactions between plants and microorganisms, which have evolved evolutionarily between plants and their associated microbiomes, are increasingly recognized as critical determinants of plant health and growth [12,13]. Plant biomass production is directly influenced by microbial biodiversity and established symbiotic relationship, which contributes to plant nutrient uptake and other physiological processes. In extreme environments, these relationships are often exclusionary and based on even more complex mechanisms [14,15,16]. The system integrating soil exposed to salt stress, plants, and microorganisms represents a unique extreme environment that provides a venue for mutualistic relationships in which plant–microbe interactions play a crucial role in activating or stimulating different adaptive mechanisms for survival under salt stress [14,17]. This phenomenon is also known as habitat-adapted symbiosis [18]. In this stressed environment, microbes enhance soil–water–plant relationships, manipulate phytohormonal signaling, and trigger other mechanisms that increase plant salt tolerance in an integrated manner, thereby maintaining plant fitness and health [19]. Unfortunately, salt stress strongly modulates physicochemical properties and reduces microbial activity, biomass and structure in and around plant roots [20,21,22]. This is believed to be due to their large area to volume ratio, high cell membrane permeability and rapid turnover rate, mainly due to osmotic pressure that shrinks the cells, resulting in water leakage from the microbial cells, thus slowing their growth [23].
In the study conducted by Andronov et al. [24] it was found that taxonomic composition of both bacterial and fungal microbial communities shifts with salinity gradients. Consequently, the vast majority of microbes fail to exert positive effects on plant growth under stressful conditions, giving an advantage to the population of salt stress-tolerant microbes [21,25,26]. These adapted microorganisms that inhabit the province of plants are selected from an enormous reservoir of microorganisms in the soil, including bacteria, archaea, and fungi, which eventually colonize plant roots (root microbiome), as well as shoots, leaves, flowers, and seeds (phytomicrobiome: endophytic (inside plant parts), epiphytic (on aboveground plant parts) and rhizospheric). When it comes to microbiomes that support plant growth under salt stress conditions, researchers often give preference to endophytic (living in root cells and tissues, abundance of 104–108 bacterial cells/g of root tissues) or rhizospheric microbes (living in close proximity to plant roots, an abundance of 106–1010 bacterial cells/g soil) [19,27]. Endophytes are considered to have advantages over rhizospheric microbes as being protected from changes in the environmental parameters [19] and could therefore become a potentially better tool for the improvement of plant growth under stress conditions. In addition, fungi have been shown to be more susceptible to salt stress compared to bacteria, so the ratio of bacteria to fungi may be elevated in saline soils [22].
Salinity-tolerant microorganisms can be divided into two groups: halophiles (including halotolerant bacteria, weak halophiles and intense halophiles), which live in high salinity environments and require salt for growth, and halotolerant organisms, that can adapt to saline environments [22]. Halophiles harbor (halo)zymes, such as cellulases, xylanases, proteases, amylases, lipase and gelatinase, having polyextremophilic features, i.e., salt tolerance or salt-dependent catalytic properties [22]. These specific enzymes also represent important biological molecules, such as phytohormones and exopolysaccharides, being crucial in plant–microbiome interaction, in keeping the stability of the soil structures and water-holding capacity and are also useful for bioremediation in saline environments [22]. On the other hand, halotolerant microorganisms can also overcome the effect of salt by the accumulation of compatible solutes for osmoregulation, production of extracellular proteases and activation of Na+/H+ antiporters [28]. Most bacteria survive under stress conditions by producing extracellular polymeric substances (EPS) that increase water retention and regulate diffusion of organic carbon sources [21]. The formation of biofilm is also one of the common features that enable microbes to adapt to salinity stress as they are supported by the formation of EPS.
Both endophytic and rhizospheric microbes contribute to mitigate abiotic stresses in plants with their potentially intrinsic metabolic and genetic capabilities [19,21,29]. The mechanism by which microbes promote the growth of their host under stress conditions can be in two ways: direct and indirect mechanisms [26]. In direct mechanisms, microbes can directly improve the reduced efficiency of plant nutrient uptake under salt-stressed conditions by providing to the plant already available soluble nutrients, such as phosphorus and potassium as well as mineral elements, by providing nitrogen via the N-fixation process or by increasing available iron in saline soils via the production of siderophores, while reducing sodium accumulation under saline conditions [19,21,26,29,30]. Microbes can also modulate hormonal imbalance in plant tissues by producing plant hormones such as auxins (IBA and IAA), cytokinins (CKs), abscisic acid (ABA), and gibberellins (GAs). These plant-associated microbes are also capable of producing 1-aminocyclopropane-1-carboxylase (ACC) deaminase, which can reduce the level of deleterious ethylene known to accumulate in plants under stress conditions. Production of secondary metabolites such as extracellular polymeric substances (EPS) and various volatile organic compounds (VOC) by salt-tolerant microorganisms was found to directly modulate plant cellular responses through regulation of the SOS1 gene, expression of stress-regulating genes, expression of high-affinity K+ transporter (HKT1) genes, antioxidant protein genes, and ethylene biosynthesis [31]. EPS helps in establishing plant–microbe interactions by providing a microenvironment in which microbes can survive under stress conditions [21]. In indirect mechanisms, microbes act as biocontrol agents by containing populations of surrounding fungal and bacterial pathogens through the production of antibiotics and hydrolytic enzymes [32,33]. Importantly, microbes can also reduce the effects of salt stress in plants by accumulating organic osmolytes, proline, glycine betaine, or total phenolics, or by increasing gene expression of various antioxidant enzymes such as superoxide dismutase (SOD), catalase (CAT), or glutathione reductase (GR) [19,26]. These compounds are extremely important plant allies in osmotic regulation, stabilization of cellular components, and scavengers of reactive oxygen species (ROS). Unfortunately, osmolyte production costs a considerable amount of energy and requires a massive C-skeleton, resulting in reduced activity and growth [22]. Abiotic stress is the primary cause for the generation of ROS in plants, the toxicity of which affects the structure and function of plant biomolecules [34]. Application of bacterial inoculum in plants subjected to salt stress has also been shown to increase the activity of defence-related enzymes such as polyphenol oxidase (PPO) and phenylalanine ammonia lyase (PAL) [26] or induce the expression of salt stress-responsive genes such as DREB2b, RD29A, RD29B and RAB18 [21].
Various studies have shown that all these different mechanisms aimed at altering plant physiology to better tolerate stress conditions are regulated by different microorganisms, including members of the genera Rhizobium, Trichoderma, Pseudomonas, Acinetobacter, Arthrobacter, Azotobacter, Bacillus, Dietzia, Klebsiella, Streptomyces, Seratia, Sphingomonas, Enterobacter and Burkholderia etc. [19,21,29]. Although different microbes have been associated with different mechanisms in supporting plant growth under saline conditions, it is now increasingly clear that the growth-promoting abilities are likely the result of an additive contribution of many taxa within the soil microbiome and not just from one particular species. Researchers are increasingly focusing on the use of growth-promoting bacteria (PGPB) and/or the microbiome as a biological tool to mitigate salt stress in plants for sustainable agriculture. However, there is a need to better explore the hidden diversity of these microbes to understand their physiological and functional properties and to exploit their potential.

2.2. Microorganism with the Ability to Enhance Salinity Tolerance in Brassica Plants

The literature review on the possible beneficial effects of different microbes on the growth of Brassica species under salt-stressed conditions confirmed the positive relationships between microorganisms and Brassica plants (Table 1.), resulting from different mutualistic mechanisms, as mentioned earlier. Out of different Brassica species majority of the retrieved studies were found to be focused on B. napus with only a few dealing with B. juncea, B. campestris and B. rapa species. In general, studies followed the beneficial effects of the inoculation of Brassica plants or seeds with different bacterial or fungal species, designated as plant-growth promoting (PGP) microorganisms or adapted halotolerant microorganisms.
In the study by Li et al. [35], it was found that canola (B. napus) plants inoculated with the halotolerant bacterium Enterobacter cloacae HSNJ4 became more salt-tolerant, and the authors linked this new trait to the increase in endogenous indole-3-acetic acid (IAA) concentration. Cheng et al. [36], in their work on the same Brassica species, compared the differences in proteome profiles of plant shoots and roots in control plants and those inoculated with a different plant growth-promoting bacterium (PGPB) Pseudomonas putida UW4 under salt stress. The effects of the bacteria included higher expression of a number of different processes in the plant, including photosynthesis, antioxidant processes, transport across membrane carriers, and proteins associated with pathogenesis. Salinity tolerance of B. napus was also recently studied by Latef et al. [37]. They tested the possible role of the two PGPB Azotobacter chroococcum NBRC and Alcaligenes faecalis NBRC 13111 on the growth attributes, photosynthetic pigments, osmolytes, oxidative stress and antioxidant enzyme activities of the tested plants. The positive correlations obtained indicate that co-inoculation with selected beneficial bacteria can be considered an excellent tool to combat saline soil problems. To improve plant tolerance to (salt) stress, beneficial microbes can also be inoculated onto plant seeds [45]. This method, called biopriming, was tested on B. napus in the work of Stassionos et al. [38]. The authors tested the potential beneficial effects of the halotolerant strain Arthrobacter globiformis CD on the salt stress response of the oilseed rape plant by inoculating the selected bacteria into the seeds of cultivars with different salt tolerance. The results showed a better stress response of the inoculated plants to high salt concentrations, especially in the sensitive cultivar, with a significant increase in the content of phenolic compounds and increased enzymatic activity of phenylalanine ammonia lyase (PAL) and superoxide dismutase (SOD). The concentration of the osmolyte proline was also significantly increased in the inoculated plants compared with the noninoculated plants. With the aim of also better understanding the role of PGPB in promoting growth of oilseed rape cultivars with different salt sensitivity (salt-sensitive Sarigol and salt-tolerant Hyola308 cultivars) under salt-stressed conditions, Banaei-Asl et al. [39] inoculated plants with PGPB Pseudomonas fluorescens FY32. Positive effects were observed on plant morphology by increasing dry weight and length of the canola roots as well as on protein profiles of roots. The results suggest that tolerance to salt stress is increased by an increase in proteins related to energy metabolism and cell division (proteins related to amino acid metabolism and the tricarboxylic acid cycle).
For B. juncea, it has also been shown that treatment with beneficial fungi or bacteria results in favorable growth. Inoculation with the fungus Trichoderma harzianum T22, known as plant growth promoter fungi (PGPF) and biocontrol agent, improved plant oil content, plant uptake of essential nutrients, enhanced aggregation of osmolytes and antioxidants and reduced NaCl uptake [40]. In another study [41], co-inoculation of B. juncea grown under salt stress with halotolerant bacteria Pseudomonas argentinensis HMM57 and Pseudomonas azotoformans JMM15 resulted in significant increase in the root, shoot and dry weight of the plants. Due to the importance of biofilm formation under stress conditions, Hong et al. [42] investigated the effect of salinity fluctuations on exocellular polysaccharide (EPS) production, biofilm formation and flocculation in their work. This study was conducted on the species B. campestris by inoculating the plants with four different halotolerant bacteria: Brevibacterium iodinum RS16, Micrococcus yunnanensis RS222, Bacillus aryabhattai RS341, B. licheniformis RS656. The contingency analysis showed that the tested parameters were strain-dependent. It was clear that the correlation with salinity was positive, at least for the first two parameters (EPS production, biofilm formation). All halotolerant strains promoted the growth of B. campestris, as evidenced by the increased vigor index and fresh weight regardless of salinity. Finally, there are several studies on cabbage species. It was shown that the addition of Bacillus subtilis. (strain GOT9) during the growth of cabbage B. campestris L. ssp. pekinen under salt-stressed conditions improved to some extent both the drought and salt tolerance of the host plant [43]. Although no significant change was observed between controls and GOT9-treated plants, growth of aboveground parts was slightly improved in the presence of GOT9.
In research on Chinese cabbage (B. rapa L. ssp. pekinensis) [44], the addition of the strain Herbaspirillum sp. GW103, isolated from the rhizosphere of Phragmites australis, was shown to alleviate salt stress in the host plant. This occurred through the release of plant-promoting factors such as auxin, siderophores and 1-aminocylopropane-1-carboxylic acid deaminase. In addition, the authors observed an increase in the K+/Na+ ratio in the samples treated with the selected strain, resulting in an increase in plant biomass. All these research studies mentioned above suggest that various Brassica species are capable of establishing mutualistic relationships with their microbiome, which could eventually help them cope with the stress caused by increased salinity. However, much more interdisciplinary research is needed to fully characterize this positive relationship, with the ultimate goal of utilizing beneficial and/or salt-tolerant microbes as a biotic resource that could minimize the damage caused to Brassica plants by induced salt stress.

3. Beneficial Molecules to Mitigate Effect of Salt Stress Tolerance on Brassica Plants

3.1. Molecular Response of Plants to Salt Stress

Increased soil salinity triggers complex abiotic stress in plants, including osmotic stress caused by decreased water uptake, toxicity stress caused by excessive concentration of Na+ and Cl− ions, and oxidative stress caused mainly by increased accumulation of reactive oxygen species (ROS) [46]. Salinity stress causes disturbances in physiological, biochemical and metabolic processes important for plant growth and development. It can cause changes in gene transcription, primary and secondary metabolism, undesirable accumulation of ROS, impairment of ion homeostasis, alteration of membrane permeability, reduction in photosynthetic efficiency, inhibition of growth and reduction in biomass production and consequently lead to a significant reduction in crop yield [47]. Salt tolerance is achieved through regulation of Na+ and K+ transport, accumulation of various osmoprotectants, reduction of ROS toxicity through production and accumulation of antioxidants, and maintenance of hormone homeostasis that allow proper growth and development under adverse environmental conditions [48].

3.1.1. Proline

Proline has been described as a reliable stress marker under salt stress, suggesting a positive correlation between proline accumulation and plant stress [49]. It can act as an osmoprotectant, but is also known as a metal chelator, antioxidant defense molecule, and signaling molecule. A positive correlation between proline content and stress intensity was found in several Brassica species [7,50]. However, the correlation between proline accumulation and salinity tolerance is controversial. Comparative studies between B. oleracea varieties under salt stress indicate that higher proline content is associated with more sensitive species/varieties [7]. A positive correlation between proline accumulation and salt tolerance was found in a comparative study of different B. juncea cultivars [50] and in rapeseed (B. napus) subjected to salt stress [51]. Thus, proline accumulation and its correlation with salt stress tolerance appear to be species- or even cultivar-specific in Brassicaceae.

3.1.2. K/Na Ratio

Tolerance to salt stress is mainly related to the ability of plants to maintain K+ uptake despite competition from Na+. The prevention of ion toxicity under salt stress is driven by the compartmentalization of sodium (Na+) ions in vacuoles and the ability to maintain high K+/Na+ ratios [52]. Salt-tolerant brassicas (kale and white cabbage) have been shown to have higher K+/Na+ ratios in their leaves than salt-sensitive Chinese cabbage cultivars [7]. The observations of higher K+/Na+ ratios in leaves and lower ratios in roots of white cabbage and kale suggest that the control of Na+ transport from roots to leaves is more efficient in these cultivars. Studies show that plasma membrane (PM) H+-ATPases and tonoplast (TP) H+-ATPases/H+-PPases, K+ transporters, Na+/H+ exchangers (NHX), and the antiporter, Salt Overly Sensitive 1 (SOS1), are important components in the process of transporting K+ and Na+ and maintaining a favorable K+/Na+ ratio [53].

3.1.3. Plant Hormones

Plant hormones are small bioactive molecules that act as powerful signals. They play a key role in the ability of plants to adapt to different environmental conditions by regulating development, growth and nutrient partitioning. They are involved in signal transduction by interacting with ROS and orchestrating the plant response to abiotic stresses by causing changes in transcriptomic, metabolic and proteomic networks that lead to plant acclimation and survival [54]. Salt stress-induced growth reduction has been shown to be associated with an imbalance in plant hormones [55]. Plant response to salt stress is highly regulated by several interactions, including hormone/ROS signaling, the excessive salt-sensitive signaling pathway, or MAPK signaling cascades leading to the expression of stress-related genes [56]. In addition to growth-promoting hormones such as auxin, cytokinins (CKs), gibberellin (GA), brassinosteroids (BRs), and strigolactones (SLs), plant stress hormones such as ABA, SA, JA, and ethylene are highly involved in plant stress response and tolerance to salinity (reviewed by [57]).
The plant root is the first organ to be confronted with increased salinity in the soil. The plant hormone auxin, which controls root development and architecture, plays an important role in root response to salt stress. Root growth inhibited by salt has been shown to be associated with a significant reduction in IAA during short-term stress [58]. The auxin metabolome was consistent with gene expressions, with the most striking changes observed in the transcripts of YUC (YUCCA flavin monooxygenases), GH3 (auxin amidosynthetases), and UGT (uridine diphosphate glycosyltransferase) genes, suggesting a disruption of auxin biosynthesis, but particularly in the processes of amide and ester conjugation. In addition to metabolism, polar auxin transport has also been shown to be involved in reduced auxin accumulation in the root during salt stress [58,59,60]. Under salt stress, IAA showed a tendency to increase in B. rapa seedlings [61]. Moreover, bacteria secreting IAA, such as the root colonizing halotolerant bacterium B. licheniformis HSW-16 and selected rhizospheric Bacillus spp. have been reported to be able to mitigate the damage caused by elevated salinity [62]. Cytokinins (CKs) are plant hormones that are highly involved in the regulation of plant growth and development, but also in stress responses. Published data suggest that the role of CKs in salt stress can be contradictory and depends on plant species, applied salt concentration, and plant growth stage [63]. Reduced growth under salt stress is also associated with reduced gibberellic acid GA levels in plants [64]. Brassinosteroids (BRs) and strigolactones (SLs) are relatively new groups of phytohormones that play a central role in regulating plant growth and development and stress response [65,66]. Comparative studies on three brassicas with different salt tolerance showed a negative correlation between the content of endogenous active BRs and salt tolerance [7]. The high accumulation of brassinolide (BL) in the salt-sensitive cultivar correlated with its stronger inhibition of root growth observed in the root growth bioassay.
While endogenous growth-promoting phytohormones generally decrease under salinity conditions, the opposite is reported for most stress hormones. The ethylene precursor 1-aminocyclopropane-1-carboxylic acid accumulated and abscisic acid (ABA) increase under salinity [55]. ABA is the major player in response to salt stress by mediating a decrease in stomatal conductance, reducing the influx of toxic ions into aboveground plant parts, enhancing photosynthesis and osmolyte content, and reducing ROS -mediated toxicity. It is known to regulate salinity-responsive genes [64]. Significant increases in ABA were observed in a salt-tolerant Brassica cultivars [7] under elevated salinity conditions. JAs have also been reported to be involved in the response to salt stress and its level could decrease in some plant species (see reviews [67,68] including B. rapa seedlings [61], suggesting that the accumulation of jasmonic acid (JA)s in some species might be protective against salt stress. As there are controversial reports on JAs content and responses to salt stress, it is not possible to establish a general correlation between endogenous JAs content and salt tolerance [67]. In addition to its involvement in biotic stresses, salicylic acid (SA) also plays an important role in plant salt tolerance. Depending on the concentration of applied SA, the plant species and the developmental stage of the plants, contradictory effects of exogenously applied SA on plants exposed to salt stress have been reported. In general, low concentrations of SA can enhance abiotic stress tolerance, while high concentrations induce oxidative stress, resulting in increased sensitivity to abiotic stress [69,70]. The protective role of SA under salt stress on stomatal conductance, net photosynthetic rate, and transpiration, as well as activation of antioxidant systems, was found [71,72,73]. The relationships between endogenous SA level and salinity tolerance are also controversial. The level of endogenous SA was found to decrease in B.rapa seedlings [61], while the level of SA increased in adult plants [73] under salt stress compared to controls. Ethylene, the gaseous plant hormone, modulates responses to salt stress by maintaining homeostasis of Na+/K+, nutrients, and ROS by inducing antioxidant defense, stomatal conductance, water use efficiency, and osmotic adjustment [74]. More or less, no stress hormone acts alone on the response to salt stress. There are complicated interactions and signaling networks among different plant hormones involved in salt stress response and tolerance [54].

3.1.4. Polyphenolic Compounds

Phenolic compounds are usually potent antioxidants involved in combating ROS and protecting plants from abiotic stresses [75]. A positive correlation between salt tolerance and phenolic compound content has been observed in many halophytes (salt-tolerant species) [76]. Salt tolerance has been reported to correlate with the content of specific metabolites, including phenolic compounds, in different plant species and cultivars [75]. Comparative studies on three Brassica plants (kale, white cabbage, and Chinese cabbage) showed a positive correlation between phenolic acids and salt tolerance. The more tolerant kale and white cabbage accumulated significantly higher levels of phenolic acids, especially hydroxycinnamic acids (mainly sinapic acid (SiA), ferulic acid (FA), caffeic acid (CaA), 4-coumaric acid (pCoA)) and suffered less metabolic disturbance under salt stress than the more sensitive Chinese cabbage [9].

3.2. Molecules Used to Enhance Salt Tolerance in Brassica Plants

Knowledge of the molecular mechanisms that plants use to protect themselves from stress has enabled the development of application techniques that promote rapid plant response to stress, thereby mitigating the effects of stress. Beneficial molecules can be applied during different stages of growth, depending on the molecules used and the desired effect. The application methods can be seed priming, foliar application and root application.

3.2.1. Seed Priming

A commonly used method is the application of different molecules at the seed level, called seed priming. The principle of seed priming is based on controlled hydration of the seeds to absorb water and trigger pre-germinative metabolism, but without the formation of radicles (which is ensured by desiccation of the seeds before radicle emergence). Pre-germinative metabolism involves the activation of enzymes [77], the build-up of metabolites [78] and other processes that contribute to the reduction of lag time during germination [79] and other beneficial effects on seed performance. Through this process, seeds are in a “primed state” that stores this short pulse and provides for more robust and resilient plants [80,81,82]. Controlled hydration during the reversible stages of germination leads to metabolic changes and, in some cases, changes in gene expression patterns [82], resulting in improved vigor, germination rate, growth and stress tolerance [78,80,82]. Priming of seeds includes different types depending on the method/compounds used: hydropriming (water), halopriming (inorganic salt), osmopriming (osmotic solution), hormonal priming (phytohormones), biopriming (microorganisms), priming with nanoparticles, etc. In general, halopriming (i.e., NaCl, KNO3, CaCl2 and CaSO4) and osmopriming (sugars, polyethylene glycol, glycerol, sorbitol, mannitol, proline) have been most commonly used to improve salt stress tolerance in various plants [83], but other species are also under investigation.
Seed priming methods for improving salt stress tolerance of Brassica plants are shown in Table 2. As can be seen, halopriming with NaCl and KCl is a common method for Brassica plants and increases salt stress tolerance and production of specific metabolites, which may have a positive effect on the nutritional value of the shoots [84,85,86]. Research has shown that osmoprimation with PEG, ZnSO4 and CuSO4 or KNO3 solution with osmotic potential can be beneficial for Brassica plants as it improves germination and seedling growth under salt stress [87,88,89]. Priming seeds with gibberellic acid, a plant hormone, helps to mitigate the deleterious effects of salt on white cabbage (B. oleracea var. capitata) by reducing cellular damage under both control and NaCl stress conditions [90]. However, the positive effect of gibberellic acid under salt stress on B. napus was found only for the salt-tolerant cultivar, while it showed no effect in the salt-sensitive cultivar [91]. In addition to gibberellic acid, NO and triacontanol, with growth-regulating activity, showed promising effects in mitigating the adverse effects of salt stress on Brassica plants [92,93]. Hydropriming with distilled water increases germination and early seedling growth under salt stress in B. rapa subsp. pekinensis [94]. In a direct comparison of seed hydropriming with selenium nanoparticles (SeNPs) priming for protection against salt stress in B. napus, nanoparticles showed better mitigating effect [95]. Nanoparticles enhanced seed germination and improved antioxidant activities by modulating the expression levels of ABA and GA genes [95]. As per the literature, seed priming can be effectively used to improve Brassica seed performance, seedling vigor and resistance, tolerance to salt stress, and nutritional value of plants. However, the efficiency of seed priming may depend on the Brassica cultivar and the conditions to which the primed seed is exposed, as well as the type of seed priming used. This technique needs further research as it is a relatively simple method of improving seed performance that can be used in crop production and easily applied by farmers. Field trials and trials on fully matured plants are most needed because, as shown in Table 2, most experiments are conducted in laboratories and on seedlings or young plants.

3.2.2. Foliar Application

In addition to seed priming, plants at an advanced stage of development can be treated with beneficial molecules. Any application of molecules/chemicals prior to stress exposure can be referred to as chemical priming, where different molecules are applied to contribute to the plant’s stress response. Foliar application (by spraying) has been shown to avoid the problem of leaching in the soil and elicit a rapid response in the plant. It is the method of choice for applying growth regulators or other mediators of the stress response.
Foliar application allows the treatment of plants at advanced stages of growth and monitoring of the effect on adult plants. Table 3 summarizes the molecules used for foliar application on Brassica plants. The effect of foliar application of proline, a known osmopro-tectant involved in salt stress response, on B. juncea showed a limited protective effect in a study by Wani et al. [96]. In another study by the same group on the same species, the simultaneous application of epibrassinolide, a plant hormone belonging to the brassinosteroid class, and proline completely neutralized the negative effects of salt at 78 mM or 117 mM, while the treatment partially neutralized the effects of the highest salt concentration of 156 mM, through the upregulation of the antioxidant system [97]. Foliar application of epibrassinolide, alone or in combination with silicone, also mitigated salt stress-induced damage in B. juncea [98].
So far, the most studied molecules applied through the leaves to mitigate the effects of salt stress in Brassica plants are salicylic acid (SA). It showed a promising effect on B. napus [99,100] and B. juncea [101]. The combination of SA and 28-homobrassinolide can completely offset the negative effects of salt stress on B. juncea [102]. However, the effect of SA on B. juncea may depend on the cultivar. Syeed et al. [101] reported that the effect of SA was more pronounced in salt-tolerant cultivars. In contrast, the beneficial effect of SA foliar application was not dependent on cultivar as found by Husen et al. [103] in B. carinata, an amphidiploid plant between B. oleracea and B. nigra. Vegetables from the brassica group, such as choysum (B. parachinensis) [104] and Chinese cabbage (B. rapa L. ssp. pekinensis) [73] also suffer less damage from salt stress after application of SA. In a research report by Linić et al. [73], ferullic acid resulted in better improvement of salt tolerance in Chinese cabbage compared to SA, suggesting that other phenolic acids may also have a beneficial effect on Brassica plants under salt stress. Methyl jasmonate, a volatile compound involved in various physiological processes in plants, counteracted the inhibitory effects of NaCl by increasing relative water content, soluble sugar content, and photosynthetic rate in an experiment by Ahmadi et al. [105] on B. napus. Similarly, inhibition of the negative effects of salinity showed 5-aminolevulinic acid (ALA), an important biosynthetic precursor of tetrapyrroles essential for plant growth and adaptation to stress environments [106]. Foliar application has great potential as a method of applying growth regulators that can help with salt stress tolerance. However, additional experiments are needed in Brassica plants, taking into account different developmental stages during spraying and Brassica varieties.
Table
Table 3. List of foliar treatments with molecules and their beneficial effect on Brassica plants under salt stress.
Table 3. List of foliar treatments with molecules and their beneficial effect on Brassica plants under salt stress.
AgetPlantExperimental DesignResults
proline [96]B. junceaAt 29 days after sowing, plants were sprayed with either 20 mM proline or water in the presence or absence of NaCl stress.Exogenous application of proline counteracted the effects of
salt stress in Varuna only, by increasing the antioxidative capacity of the plants. Moreover, proline was not effective in
alleviating the detrimental effects of higher salt concentrations
on the studied parameters.
Epibrassinolide and proline [97]B. juncea cv.
Varuna and cv. RH-30		The leaves of were sprayed thrice at an interval of 10 min with 20 mM proline at 28 DAS and/or 10−8 M EBL at 29 DAS. Plants were sampled at 60 DAS for stress parameters and at mature stage (120 DAS) for yield characteristics.Exogenous application of EBL with proline completely neutralised the adverse effects of salt at 78 mM or 117 mM, whereas the treatment partially neutralised the impact of highest salt concentration of 156 mM, through the upregulation of the antioxidant system.
Silicon (Si) 24-Epibrassinolide (EBL) [98]B. junceaSeeds of B. juncea were sown in pots and supplemented with NaCl at 15-day stage. Si and EBL treatments were given at 20- and 25-day stages, respectively.The spray of Si and EBL alone or in combination significantly increased the growth and photosynthetic traits in the presence/absence of NaCl stress. A combined effect of Si and EBL counters the damaged caused by the salt stress.
Salicylic acid [99]B. napus10 days seedlings groen for 48 h in Hyponex solution with 100 and 200 mM NaCl and with and without spraying 100 µM salycilic acidSA is an effective protectant in improving the activities of both antioxidant defense and glyoxalase enzymes in coffering salt stress tolerance in B. napus.
Salicylic acid [100]B. napusOne-month-old plants, where four fully expended leaves had appeared, were sprayed with salicylic acid (0, 0.5, 1 mM) on to the leaves. After the salicylic acid treatment, plants were grown under salt concentrations of (0, 4, 8 and 12) dsm−1 for ten days.SA application increased photosynthetic pigments (Chl a, b and carotenoids), protein and soluble sugars, free amino acids, including proline and MAD content compared to plants under salinity stress
Salicylic acid [101]B. junceaPlants were grown with 50 mM NaCl and were sprayed with 0.1, 0.5, and 1.0 mM salicylic acid (SA). Plants were harvested at 30 DAS (15 days after SA application)The application of 0.5 mM SA alleviated the negative effects of 50 mM NaCl maximally, but 1.0 mM SA proved inhibitory. The effect of SA was more conspicuous in a salt-tolerant cultivar.
Salicilyc acid [104]B. parachinensisTwenty-day-old choysum plants were subjected to different salt stress levels (0, 100, 150 and 200 mM NaCl) by applaying NaCl solutions were to the pots’ soil. A week after the first salt stress was commenced; salicylic acid (1 mM) was foliar applied once a week until harvesting at 45 DAS.SA application induced tolerance to salinity stress in choysum plants due to the synchronized increase in activities of enzymatic and non-enzymatic antioxidants, enhanced efficiency of AsA-GSH cycle and the MG detoxification systems.
Salicylic acid [103]B. carinataFour-week-old cultivars were treated with NaCl (50, 100 and 150 mM) and SA were applied by spraying to the aerial plant parts four times (at one-week interval) starting from the fifth week after germination up to the eighth week. Sampling was done when plants were 9 weeks old.SA significantly reduced the salinity-caused effects on the overall performance of plants and their antioxidant systems in both the cultivars.
28 homobrassinolide (HBL)
salicylic acid [102]		B. junceaThe leaves of 29-day-old plants grown in presence or absence of saline conditions (4.2 dsm−1) were sprayed with distilled water, HBL and/or SA and plant responses were studied at 30 days after sowing (24 h after spray) and 45 days after sowing.HBL excelled in its effects at both sampling stages. Toxic effects generated by salinity stress were completely overcome by the combination of the two hormones (HBL and SA) at 45 DAS
methyl jasmonate [105]B. napusThe salinization and MeJA application were simultaneously carried out when plants were 16 days old. Ethanol (0.04%, v/v) was added to the solution prepared for the foliar applications as solvent.Exogenously applied MeJA counteracted the inhibitory effects of NaCl by increasing relative water content, soluble sugar content and photosynthesis rate.
Ferulic acid (FA)
Salicylic acid (SA) [73]		B. rapa L. ssp. pekinensisAt 4 weeks of cultivation, hydroponically cultivated plants
were sprayed with phenolic acids: salicylic (SA) and trans-ferulic acid (FA) (10, 50, and 100 µM) and the NaCl concentration in the hydroponic solution was gradually increased up to 150 mM NaCl. The photosynthetic parameters were measured 72 h after salt application and plants were harvested for analysis.		SA and FA treatments, with a concentration of 10 µM, had attenuated effects on salt-stressed plants, causing a decrease in proline and SA level, and indicating that the plants suffered less metabolic disturbance. FA resulted in a better ameliorative effect on salt stress compared to SA.
5-aminolevulinic acid (ALA) [106]B. napus L.The leaves of plants grown in a pots under 200 mM NaCl were sprayed with 5 mL of ALA solution at a concentration of 0 or 30 mg·L−1 at 35 and 40 DAS. Plants were harvested 10 days after initially being treated with ALA.ALA improved salt tolerance by promoting the accumulation of chlorophyll and heme resulting from the increase of intermediate levels in the tetrapyrrole biosynthetic pathway, along with enhancing the proline accumulation in B. napus.

3.2.3. Root Application

The third way of applying beneficial molecules is to the root system, by introducing molecules into the soil or media in which plants grow. Here it is important to note that such application can affect not only the plants but also the rhizosphere microbiome, whose role in responding to salt stress we discussed above. Most research focuses only on the plant response and more research is needed that comparatively examines the microbiota and the plants.
Information on molecules used on Brassica plants is summarised in Table 4. This type of application is appropriate for hydroponically grown plants, and most research on Brassica plants is conducted using B. napus as a model plant. Molecules that have a positive effect on salt stress tolerance in B. napus are strigolactone GR24, poly(γ-glutamic acid), silicone, melatonin, and serotonin [107,108,109,110,111,112]. Most of these molecules alleviate the oxidative stress caused by salinity and help to mitigate the negative effects. Thiourea, an ROS scavenger, also has a similar effect on B. juncea [113].
Although molecules have shown promise, there are no data from field trials that provide more realistic information, and such studies are certainly needed in the future.

4. Conclusions

Soil salinization is a global problem that can lead to significant losses in agricultural production. In this review, we summarized and reviewed recent data on several microorganisms and molecules whose application may be beneficial for mitigating salt stress in Brassica plants.
Several Brassica species are able to establish mutualistic relationships with their microbiome that could help them cope with stress caused by increasing salinity. However, further interdisciplinary research is needed to characterize this positive relationship and the potential to utilize beneficial and/or salt-tolerant microbes as a biotic resource that could minimize the damage to Brassica plants caused by induced salt stress.
The knowledge of the mechanisms involved in the stress response of Brassica plants provided the impetus for the research, which focused on the development of different application methods that induce a better and faster response to salt stress and consequently help to mitigate the negative effects of salt stress. The application of the beneficial molecules can be done through the seed, known as seed priming, or at advanced stages of development through foliar spraying or root application. Several molecules show promising activity, but all of these experiments were conducted in the laboratory/under controlled conditions and additional experiments under field are needed to determine optimal conditions of application. According to the data we summarized, the experiments are also limited to some Brassica plant species and research should extend to a wider range of different species/cultivars. Moreover, many of the available data show the beneficial effects of certain biomolecules and microorganisms on seedlings or young plants under stress conditions. Further research should evaluate their potential beneficial effects on plants at commercial or horticultural maturity.

Author Contributions

Conceptualization, I.P. and D.Š.; writing—original draft preparation, I.P., D.Š., E.K., B.S.-S.; writing—review and editing, D.Š.; I.P., E.K., B.S.-S.; supervision, D.Š.; project administration, D.Š., I.P., B.S.-S.; funding acquisition, I.P., B.S.-S., D.Š. All authors have read and agreed to the published version of the manuscript.

Funding

This article is the result of activities on the project “Exploring adaptation potential of rhizosphere microbiome to climate change: towards sustainable agriculture in the future- PERSPIRE” (KK.05.1.1.02.0001) funded by the European Regional Development Fund (ERDF). D.Š. research is supported by Grant for Scientific Research and Artistic Work from the University North under the no. UNIN-BIOTEH-21-1-1.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

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Table
Table 1. Beneficial microorganisms in mitigating salt stress and its mechanism of action in Brassica species.
Table 1. Beneficial microorganisms in mitigating salt stress and its mechanism of action in Brassica species.
Identity of the Beneficial MicroorganismHost
Plant		Mechanism for the Salinity Mitigation
Enterobacter cloacae HSNJ4 [35]B. napusIncrease in indole-3-acetic acid
Pseudomonas putida UW4 [36]Higher expression of photosynthesis and anti-oxidative processes; transportation across membranes; pathogenesis-related proteins
Azotobacter chroococcum NBRC, Alcaligenes faecalis NBRC 13111 [37]Enhanced growth and photosynthesis, higher levels of soluble sugars and proteins as well as antioxidant enzymes, decline in proline, malondialdehyde (MDA), and hydrogen peroxide, increase in N, K, Ca and Mg uptake
Arthrobacter globiformis CD [38]Increase in phenolic compounds and proline; enhanced activities of phenylalanine ammonia-lyase (PAL) and superoxide dismutase (SOD)
Pseudomonas fluorescens FY32 [39]Increase in plant dry weight and length of roots; increase in proteins related to energy metabolism and cell division
Trichoderma harzianum T22 [40]B. junceaImproved uptake of nutrients; aggregation of osmolytes and antioxidants; reduced uptake of NaCl
Pseudomonas argentinensis HMM5, Pseudomonas azotoformans JMM15 [41]Increase in root, shoot and plant dry weight
Brevibacterium iodinum RS16, Micrococcus yunnanensis RS222, Bacillus aryabhattai RS341, Bacillus licheniformis RS656 [42]B. campestrisIncreased vigor index, fresh weight and growth hormones; production of stress alleviating enzymes
Bacillus subtilis GOT9 [43]Improvement of the growth of aerial parts
Herbaspirillum sp. GW103 [44]B. rapaProduction of auxin, siderophore, and 1- aminocylopropane-1-carboxylic acid deaminase; increase in K+/Na+ ratio in roots; increase of plant biomass
Table
Table 2. List of molecules, experimental design and results of a study on use of seed priming for salt stress tolerance improvement on Brassica plants.
Table 2. List of molecules, experimental design and results of a study on use of seed priming for salt stress tolerance improvement on Brassica plants.
MoleculesBrassica PlantExperimental DesignResults
NaCl [84]B. napusSeed primed with 14 dS m−1 NaCl solution for 24 h at 20 °C. Plants grown in the greenhouse and watered with five different NaCl solutions (0.4 (control), 4, 8, 12 and 16 dSm−1), for a period of 3 weeks.Increased salt tolerance
NaCl priming enhanced proline accumulation and prevented toxic and nutrient deficiency effects of salinity due to less Na+ but more K+ and Ca2+ accumulation.
KCL
NaCl [85]		B. oleracea var.
capitata		Seeds were soaked in KCl 50 mmol·L−1; NaCl 150 mmol·L−1 for 10 h in a controlled dark chamber at 25 °C Seedlings were sprayed with 150 mM NaCl.Increase of secondary metabolite production, KCl seed priming adding nutritional value to cabbage sprouts
NaCl
KNO3 [86]		B. napusSeed priming with 1% NaCl or 3% KNO 3 48 h at 25 °C in darkness. Seeds cultivated in Petri dishes containing filter paper soaked with water, NaCl or CaCl2 solutions 2:1 molar
ratio of NaCl and CaCl2.		Increase in germination percentage and index, seedling fresh and dry weight probably due to repair mechanisms during imbibition. KNO3 had stronger stimulation of germination percentage.
Polyethylene glycol (PEG) [88]B. napusSeed priming with PEG solution with osmotic potential 1.2 MPa for 7 days in the darkness at 25 °C. Seeds cultivated in Petri dishes containing filter paper soaked with NaCl solution (100 mM NaCl) or water (control).Improved germination and seedling vigour under salt conditions. Increase of gene expression for proline biosynthesis (P5CSA and P5CSA)—up to 279% higher expression of P5CSA under NaCl stress.
ZnSO4 and CuSO4 [87]B. rapaSeed priming with ZnSO4 and CuSO4. Seed germination under different levels of NaCl (60, 90 and 120 mM)Increase in germination and seedling growth in both salinity levels as well as in non-saline conditions.
KNO3 [89]B. napusSeed priming with KNO3 solution with osmotic potential −1.0 MPa one day at 30 °C. Pots placed in a greenhouse and irrigated with NaCl with different levels of salinity (0.2, 5, 10, 15 and 20 dS m−1)Improvement of seedling growth, development, and establishment of primed plants under salinity stress.
GA3 [91]B. napus
var. oleifera		Seed priming with GA3 (1 mM), solution for 12 h. Seeds cultivated in Petri dishes containing filter paper soaked with water, seedlings transferred to chromatography paper strips dipped in 100- and 250-mM NaClGA3 improved salt tolerance in salt-tolerant cultivar with no effect on salt-sensitive cultivar
gibberellic acid (GA3) [90]B. oleracea var.
capitata		Seeds were soaked for 10 h in 0, 100, 150 or 200 mg/l GA3. Plants were grown in a greenhouse. Salt treatments were started 15 DAS by adding 0, 50, 100 or 150 mM NaCl to the nutrient solutions, and plants were harvested 30 DAS.GA3 alleviated the harmful effect of salt stress on cabbage in terms of fresh and dry weights. Plants grown from GA3-primed seeds suffered lower cellular injury both under control conditions and under NaCl stress.
distilled water [94]B. rapa
ssp. pekinensis		Seed priming with distilled water 10 h at 20 °C in darkness Seeds cultivated in Petri dishes containing filter paper soaked with NaCl (50, 100, 150, 200 and 250 mM).Increase in germination traits and early seedling growth under salt stress
NO [92]B. oleraceaSeeds were soaked in 0.02 mM NO for 12 h. Broccoli seedlings were subjected to saline stress (NaCl) in Hoagland’s solution enriched with all essential nutrientsNO was effective in increasing plant growth, chlorophyll pigments, glycine betaine, proline and oxidative defense system
triacontanol [93]B. napus L.Seeds were soaked in different levels of TRIA (i.e., 0, 0.5, 1.0 mg L-1) for 12 h and salt stress (100 and 150 nM) was applieed on 56-days-old plants and data recorded three weeks after treatmentPre-sowing seed treatment with TRIA increased shoot fresh weight, number of seeds per plant, photosynthetic rate, transpiration rate, ratio of chlorophyll a/b, q, electron transport rate, shoot and root K contents, and free proline and glycine betaine contents of canola plants at various TRIA levels under no-saline or saline conditions.
Selenium nanoparticles (SeNPs) [95]B. napus
cultivars		Seed priming with 10 mM sodium selenite (Se (IV)) for 72 h,
ddH2O for hydropriming. Seeds cultivated in plastic boxes with filter paper soaked with 150 mM NaCl.		Nanoparticles elevated seed germination and improved antioxidant activities by modulating expression levels of ABA and GA genes
Table
Table 4. List of root treatments by beneficial molecules and their ameliorative effects on Brassica species under salinity stress.
Table 4. List of root treatments by beneficial molecules and their ameliorative effects on Brassica species under salinity stress.
AgetBrassicaExperimental DesignResults
GR24, strigolactone [107]B. napusFour-week-old plants grown in half-strength Hoagland nutrient solution were treated with salinities (0, 100, and 200 mM NaCl) and withh presence or absence of GE24.Strigolactones GR24 improve plant growth, photosynthesis, and alleviate oxidative stress.
Poly(γ-glutamic acid) (γ-PGA) [108]B. napusA salinity model was simulated by exposing the hydroponicly grown roots of rape seedlings to 100 mM NaCl solution for 48, 96 and 144 h with or without the presence of 20 mg/L γ-PGA.γ-PGA improved resistance to salt stress in by activating the proline synthesis pathway and promoting proline accumulation.
silicone [109]B. napus12 DASplants, growing semi-hydroponic, SiO2 (1 mM) and NaCl (100 and 200 mM) were added in the solution—alone or in combination. The first leaves were harvested and used for quantifying parameters after 48 h of treatment exposure.Si improved plant tolerance to salinity stress through enhancement of both antioxidant defense and glyoxalase systems that led to reduced oxidative damage and methylglyoxal toxicity.
melatonin [110]B. napusNine-day-old seedlings analysed after growing in solution with different NaCl and melatonin concentrations.Melatonin improves the H2O2 -scavenging capacity, alleviate osmotic stress by promoting the accumulation of osmoregulators, facilitate root development and improve the biomass
melatonin [111] (µM) (MT) and lipoic acid (LA)B. napusSeeds were sown in Petri dishes (HS) with 0 or 100 mM NaCl or melatonin (µM) (MT) or lipoic acid (LA) treatments (0.5 µM) below and above the seeds. Seedlings grown until the shoot attained 5 to 6 cm height and root attained 7 to 8 cm.The alteration of metabolic pathways, redox modulation, and ions homeostasis in plant tissues by the combined LA and MT application are helpful towards the adaptation in a saline environment.
Seratonin [112]B. napusHydroponically grown seedlings with two leaves were treted with seratonin (0, 50, 100,200, 300 µmol/L) under 0.75% NaCl.Serotonin improved the ability of ROS scavenging, osmotic pressure regulation and promoting growth, thus alleviating the salinity of seedlings
Thiourea (TU) [113]B. junceavar. TPM1Hydroponically grown plants were subject to salinity stress (150 mM NaCl) with and witout of the presence of 75 µM TU. Alalysis were performed 7-d post-treatment.Thiourea (TU, a ROS scavenger) has delineates salt stress ameliorating action. The ameliorative potential of TU towards NaCl stress was related with its ability to decrease ROS accumulation in roots and increase Na+ accumulation in shoots.
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Petrić, I.; Šamec, D.; Karalija, E.; Salopek-Sondi, B. Beneficial Microbes and Molecules for Mitigation of Soil Salinity in Brassica Species: A Review. Soil Syst. 2022, 6, 18. https://doi.org/10.3390/soilsystems6010018

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Petrić I, Šamec D, Karalija E, Salopek-Sondi B. Beneficial Microbes and Molecules for Mitigation of Soil Salinity in Brassica Species: A Review. Soil Systems. 2022; 6(1):18. https://doi.org/10.3390/soilsystems6010018

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Petrić, Ines, Dunja Šamec, Erna Karalija, and Branka Salopek-Sondi. 2022. "Beneficial Microbes and Molecules for Mitigation of Soil Salinity in Brassica Species: A Review" Soil Systems 6, no. 1: 18. https://doi.org/10.3390/soilsystems6010018

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