4.1.3. Potassium

Plants develop a wide range of adaptive and resistive strategies that sustain productivity and survival under stressful conditions. Plant tissues may adjust osmotic potential through the absorption of various compatible osmolytes such as inorganic ions, carbohydrates, organic acids and free amino acids [123,124]. Plants adjust osmotic potential by regulating stomatal conductance, photosynthesis, leaf turgidity and plant growth rate under drought, salt and high-temperature stresses through potassium (K) osmolytes [125]. Potassium is one of the major inorganic osmolytes that enable osmotic regulation and adjustment during stress conditions. Potassium ion absorption protects plants from harmful impacts of different stresses including drought, salinity, metal toxicity and high or cold temperatures by osmotic adjustment and maintenance of stomatal conductance, protecting cell integrity and increasing photosynthesis as well as via the detoxification of reactive oxygen species [123].

In addition, K is a crucial element for the distribution of photo-assimilates in root systems [126] that protects plants against most abiotic stresses including metal toxicity such as Cd-induced oxidative damage [127], Zn toxicity [128], NaCl toxicity [129], drought stress [130] and high radiance incidence [131]. Potassium supplementation increases the adjustment of stomata, which regulates carbohydrate formation and the growth of *Nicotiana rustica* during stress conditions [125]. Samar-Raza et al. [132] reported that application of K fertilizer under drought stress enhanced the tolerance of wheat (*Triticum aestivum* L.) by reducing toxic elements' absorption and enhancing physiological efficiency and yield [133].

#### 4.1.4. Calcium

Calcium (Ca) plays a vital role in the physiological functions of plants and acts as a second messenger element of external signals for the higher performance of plants. It has an essential role in the structure and stabilization of the cell wall and membrane, regulating metabolic, enzymatic and hormonal processes [134]. The alteration in free cytosolic Ca2+ ion contents is validated during naturally occurring abiotic stimulants (low and high temperature/light, tensions, high osmotic and oxidative tensions, also during biotic stimulants (nodulation aspects and fungal drivers)) [135]. It also has an explicit function in the performance and maintenance of plant development and detoxification

of heavy metals [136]. The main function of Ca+ ions under heavy metal stress is to maintain the activities of antioxidant enzymes, reducing the peroxidation of lipids in the cell membrane and improving the physio-biochemical processes of plants [127,137].

#### 4.1.5. Magnesium

Magnesium (Mg2+) is an essential nutrient for plant growth [138], regulating cell membrane stability, carbon fixation, chlorophyll synthesis, carbohydrate transport, enzymatic activities and reproductive process [139–141]; thus, it helps plants to adapt defensive mechanisms against abiotic stresses [142]. Plants under Mg nutrition improve root growth and root surface area that increase water and nutrient uptake from the rhizosphere and enhance transportation of photo-assimilates and carbohydrate synthesis, which can mitigate drought-stress-induced deleterious changes [143]. Magnesium transports carbohydrates from roots to shoots and helps in the fixation of photosynthetic CO2 during the reproductive growth stage under salt stress. The efficiency of Mg foliar fertilization is right-away associated with the distribution of nutrients within plants [144]. Nutrient solution with Mg fertilization improved the shoot growth of *B. rapa* L. var. pervirdis under cadmium (Cd) toxicity [145].

Deficiency of Mg is one of the common nutritional syndromes in plants, which may have drastic impacts on agricultural productivity and quality [146] and lead to morphological and physiological abnormalities of plants [147]. Plants produce antioxidants and antioxidative defensive enzyme activities, especially ascorbic acid during the stress of Mg deficiency [148]. The glutathione-producing ascorbate-determined H2O2 scavengers are responsible for ascorbic acid that can enable the plants to detoxify ROS production to protect plants from climate extremes [149]. Glutathione homeostasis can be regulated through the over-production of glyoxalase genes that can help the plants to sustain Mg content during stressful conditions and increase tolerance to metalliferous soil [150,151].

Magnesium transporters are also involved in metal transport. Under the low Mg content, nickel (Ni+) is well-cited for the suppression of electron flow and impairing photosynthesis functions by replacing Mg2+ in chlorophyll fragments. Adequate fertilizer of Mg alleviates the Ni+ effect in the root rhizosphere that may reduce the negative probability of Ni at the outer surface of the plasma membrane by replacing the targeted ionic binding site [152]. The Mg transporter (AtMHX) from Arabidopsis acts as an H<sup>+</sup> exchanger with Zn and Mg and is confined to the vacuole membrane [153]. The AtMGT1 protein derived from AtMGT (transporter gene of Arabidopsis) family in the plasma membrane exhibited greater attraction to Mg2+ ion, which helped in the re-distribution of Ni+, Ca2+, Fe3+, Mn2+ and Cu2+, when they are present in high concentrations [154].

#### 4.1.6. Sulfur

Sulfur (S) is among the very active macronutrients in plant metabolism, which is why it is recognized alongside nitrogen (N) as a key nutrient for plant development [155]. Sulfur is used by plants to assimilate with a variety of organic compounds that are essential for the growth, development and mitigation of plant stress [11,156]. It is also responsible for making vegetables softer and adding greater commercial value [157]. Sulfur is predominantly found in the soil and is one of the main nutrients that is absorbed by plants in the form of sulfate anion (SO4 <sup>2</sup>−) from organic matter and a small proportion from the atmosphere in the form of sulfuric gas [158].

Kohlrabi (*B. oleracea* L.) is one of the crucially demanding S vegetables of the Brassicas family, which absorbs 1.5 kg S ton−<sup>1</sup> of yield. Sulfur deficiency can inhibit leaf formation and change young leaves' color from dark green to light green or yellowish. Proper S fertilization in kohlrabi (*B. oleracea* L.) improves tuber yield and reduces the undesirable nitrate content in consumable parts [159]. Canola (*B. napus* L. var. Oleifera) is also one of the most demanding S vegetables in reproductive phases as compared to other winter crops, as it exports a large amount of S to the grains [160]. Sulfur is one of the known nutrients that performs an imperative role in the tolerance to heavy metal toxicity [161].

Chromium is actively transported across the plasma membrane and appears to be mediated by transporters, which are primarily responsible for sulphate uptake [162,163]. This suggests the action of this molecule inhibit the absorption of heavy metals that are toxic to plants (Table 2).

**Table 2.** Summary of the positive effects of N, P, K, S, Mg, Ca and Si fertilization in mitigating abiotic stress conditions in Brassicas (2004–2020).



**Table 2.** *Cont.*


**Table 2.** *Cont.*

#### *4.2. Silicon*

Silicon (Si) is the second most abundant chemical element after oxygen in the earth's crust [199,200]; however, it is still not available directly to plants and is commonly adsorbed with oxides and silicates, affecting plant nutritional status [180,201–203]. In addition, the low dissolution of Si in the soil decreases its availability; thus, it occurs in a very low amount [204].

Plants uptake Si mainly from dissoluble mono-silicic acid (H2SiO4), a noncharged molecule which plays a significant role to increase plant resistance to abiotic and biotic conditions [205–207]. Silicon is distributed via xylem in the form of hydrated amorphous silica/silica bodies (SiO2.nH2O) and pledged to the epidermis of cell membrane. After deposition to the cell membrane, Si is no longer available for further distribution into the above-soil parts of the plants [208]. The transport of H4SiO4 occurs in a similar direction to transpiration (mass flow). Therefore, drought conditions increase the deposition of Si in the regions of leaf epidermis to protect water from high transpiration [209].

All soil-grown plants had Si constituents ranging from 0.1 to 10% of dry weight of plants [180,210]. However, Si is classified as a beneficial element, with it being an imperative element for several crops, specifically rice (*Oryza sativa* L.) and sugarcane (*Saccharum officinarum* L.). Moreover, its role has been well documented for the performance, growth and development of different Gramineae family crops [180,206,207,211–213]. This chemical element has been reported to be beneficial in mitigating abiotic stresses including heavy metal toxicity, salinity, high temperature, drought, radiation, aluminum toxicity, lodging, nutrient imbalance, wounding and freezing [214,215]. Rapeseed is one of the most studied plants of the Brassicaceae family regarding Si application to alleviate abiotic stress conditions [211], with the most common improvements reported in plant resistance to cold stress conditions, as well as the formation of larger seeds [216]. Table 2 summarizes the studies with Si fertilization in Brassicaceae plants under abiotic stress in the last decade (2004–2020).

#### *4.3. Micronutrients*

Micronutrients (zinc (Zn), iron (Fe), manganese (Mn), molybdenum (Mo), boron (B), copper (Cu) and chlorine (Cl)) improve plant health, water use efficiency, biomass production and provide systemic response against abiotic stresses [217–219]. Whereas plant growth-promoting rhizobacteria (PGPR) promote plant growth and tolerance to abiotic stresses by adapting and altering certain mechanisms, the production of ACC (1-aminocyclopropane-1-carboxylate) deaminase reduces ethylene synthesis, as well as alters phytohormones and antioxidative enzymes synthesis, and improves nutrient uptake [115,220].

Micronutrients may influence directly or indirectly the stress affecting plants due to their role in several enzymatic and metabolic activities [221]. Abiotic stress such as drought harshly impairs mineral nutrient translocation from soil to plant parts [222,223]. The Brassicaceae family is one of the most nutrient-demanding plant species, which is highly affected by inadequate nutrients application [224]. Therefore, deficiency of micronutrients

disrupts the net-assimilation rate and stomatal conductance, electron transportation in photosynthesis, chlorophyll content, root–shoot ratio and antioxidant activities of cabbages, turnip and canola under abiotic stresses [225–231]. Salinity is a critical challenge to high production, physiological and biochemical attributes and nutrient uptake in Brassicaceae species [232]. Brassicas adapted certain mechanisms and variations, especially physiological variations to cope with salinity [233]. Salinization in plant systems can be ameliorated with foliar nutrient spray and rhizosphere micronutrient availability and uptake [234]. The accumulation of sodium (Na+) and chlorine (Cl−) ions increases osmotic potential and decreases water availability and nutrient uptake through plant roots [235].

Several studies regarding the Brassicaceae family indicated that most of the species grown on contaminated soils with high accumulation of nutrients (Zn and Cu) and nonessential metals (Pd, Cd, Ni and Cr) [236–239]. Plants of *B. juncea* have the ability to accumulate high amounts of Cd, Cu, Ni, Cr, Zn, Fe, Co, Pb and Se from metal-contaminated sites [240–242]. Rapeseed subjected to early waterlogging stress resulted in higher accumulation of Mn, Fe, Zn and Cu in the leaves and caused toxicity [243]. Zinc is one of the efficient nutrients in the reduction of heat stroke by improving biochemical activities and superoxide dismutase (SOD) content in *B. rapa* [244,245]. Boron and Mn application in winter rapeseed (*B. napus*) positively influenced pod production, photosynthetic rate, N-metabolism, antioxidant activities and improved N and Ca contents in seeds [227,246]. High UV-B radiation may alter nutritional status, disturb plant cell metabolism, increase pathogens and disease tolerance [247], whereas light-emitting diodes (short duration blue light) enhanced phytochemical activities and micronutrient (Zn, Mn, Mo, B, Na, Fe and Cu) concentration in Broccoli (*B. oleacea* var. italica) [248,249] (Table 3).


**Table 3.** Summary of the positive effects of micronutrients fertilization in mitigating unfavorable abiotic stress conditions in Brassicas (2005–2020).


**Table 3.** *Cont.*

### **5. Conclusions**

Based on the updated literature, this review highlighted the importance of adequate and balanced nutrition against abiotic stresses in Brassicas species to ensure food and nutritious security. Proper management of macronutrients, micronutrients and silicon under certain conditions of abiotic stress could improve nutritional and physiological status, thus resulting in higher productivity and quality of Brassicas plants. Balanced application of macro- and micronutrients mitigates abiotic-stress-induced changes in Brassicas plant species by stimulating absorption and accumulation mechanisms for better survival.

The use of plant growth-promoting rhizobacteria (PGPR) has a critical role in combating climate-induced changes such as uneven rainfall (drought), soil and water salinization and heavy metal contamination, which limit the general performance of Brassicas plant species. Among the PGPRs, the genera *Azospirillum*, *Bacillus*, *Pseudomonas*, *Herbaspirillum* and *Burkholderia* are well studied for increasing plant nutrition, tolerance to pathogens and climate extreme conditions, and hence could improve plant performance and productivity in adverse growing conditions. Therefore, inoculation with PGPRs can increase productivity of Brassicas grown under abiotic stress conditions.

In the future, attention needs to be paid to the response of Mg and micronutrient application on crop resilience under different abiotic stresses. Dose-response management and multiple interactions of nutrients and heavy metals still need further investigation. Bio-fortification via foliar spray of micronutrients is a cost-effective strategy in alleviating global food and nutritious security which requires future advances and intensified research. The intervention of nano-fertilizers on the basis of integrated evidence is required to reduce the gap. The expansion of enhanced detection, tracking and monitoring strategies may be the best early detection technique for abiotic stresses which can also control yield losses and lethal impacts on the nutritional security of crops.

**Author Contributions:** Conceptualization, A.J. and M.C.M.T.F.; methodology, A.J. and C.E.d.S.O.; software, C.E.d.S.O. and F.S.G.; validation, A.J., F.S.G. and C.E.d.S.O.; formal analysis: A.J., I.M.B.G.; resources, M.C.M.T.F.; data curation, A.J., C.E.d.S.O., P.A.L.R. and B.H.d.L.; writing—original draft preparation, A.J. and F.S.G. writing—review and editing, M.C.M.T.F. and F.S.G.; visualization, B.H.d.L. and I.M.B.G.; supervision, M.C.M.T.F.; project administration, A.J. and M.C.M.T.F.; funding acquisition, A.J. and M.C.M.T.F. All authors have read and agreed to the published version of the manuscript.

**Funding:** This review received funding from The World Academy of Science (TWAS) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), for the first author's doctoral fellowship (CNPq/TWAS grant number: 166331/2018-0), and the productivity research grant (award number 311308/2020-1) of the corresponding author.

**Institutional Review Board Statement:** Not applicable.

**Informed Consent Statement:** Not applicable.

**Data Availability Statement:** No new data were created or analyzed in this study. Data availability is not applicable to this article.

**Acknowledgments:** The authors thank São Paulo State University (UNESP) for providing the technology and support as well as CNPq for the financial support.

**Conflicts of Interest:** The authors declare no conflict of interest.

#### **References**


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