**1. Introduction**

Brassica is one of the most important and economical vegetables of the Brassicaceae family [1] and includes several species (*Brassica oleracea*, *Brassica rapa*, *Nasturtium officinale*, *Raphanus sativus*, *Diplotaxis tenuifolia* and *Eruca vesicaria*), containing secondary metabolites and beneficial contents of putative health-promoting compounds [2]. Brassicaceae are a rich source of primary and secondary metabolites (amino acids, sugars, indoles, phenolics and glucosinolates) that help in the production of antioxidants [3,4] to promote tolerance to biotic and abiotic stresses [5]. Brassicaceae are emergently adapting as a research model crop in plant science due to their interaction with biotic and abiotic stresses as their high defensive mechanisms and a series of alterations in metabolites allow them to survive under climatic extremes [6]. Therefore, proper management practices are needed when encountering extreme environmental conditions (drought, salinity, temperature, heavy metals and nutrients deficiency) and to ensure optimal plant growth and productivity [7].

**Citation:** Jalal, A.; da Silva Oliveira, C.E.; Galindo, F.S.; Rosa, P.A.L.; Gato, I.M.B.; de Lima, B.H.; Teixeira Filho, M.C.M. Regulatory Mechanisms of Plant Growth-Promoting Rhizobacteria and Plant Nutrition against Abiotic Stresses in Brassicaceae Family. *Life* **2023**, *13*, 211. https://doi.org/10.3390/ life13010211

Academic Editors: Wajid Zaman and Hakim Manghwar

Received: 23 November 2022 Revised: 29 December 2022 Accepted: 5 January 2023 Published: 11 January 2023

**Copyright:** © 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/).

Abiotic stresses disturb plant physiology and metabolism, which leads to the reduction of plant growth and productivity [8]. The growth, yield and quality of Brassica grown in arid and semi-arid areas were extremely affected by drought conditions [9]. In addition, nutrient limitation is another vulnerable condition that alters plant growth, production and quality. Plants adapt different physiological and biochemical functions to adjust to extreme challenges and avoid injuries under abiotic stresses [10]. Macronutrients mobilize and assimilate along with organic compounds that could improve plant growth and development and mitigate plant abiotic stresses [11]. The absorption of chromium (Cr), zinc (Zn), iron (Fe) and manganese (Mn) was increased with chelating agents of low molecular weight, which led to the improvement of oil content in *Brassica juncea* up to 35% [12]. The imbalanced utilization of macro and micronutrients may cause metal toxicity in several crop plants [13]. However, Brassica species deal with the hyper-accumulation of these nutrients by improving biochemical processes and the mobilization of nutrients through the roots–shoot system [14]. In addition, the root rhizosphere is influenced by different biotic and abiotic factors including soil and root type and plant species and age. Hence, plant growth-promoting rhizobacteria (PGPR) are classified into several groups on the basis of their capacities and taxonomical status. These bacteria activate several mechanisms that alter soil organic matter to an instantly available form [15], as well as the regularization and transformation of soluble sugars, proline, amino acids and mineral nutrients in the soil above plant parts, thus improving nutrient accumulation in nutrient-deficient soils [16].

The plant and bacteria association promotes nutrient uptake and assimilation, which favors the plants' tolerance to biotic and abiotic stresses [17]. Plants and microbial communities are the components of similar limited resources with a different relationship. However, plants assist microbial communities with available nutrients from the soil rhizosphere [18] and improve nitrogen mineralization, which can enhance the uptake of other nutrients for a higher performance and yield of plants [19]. The positive association (symbiosis) and negative association (pathogenesis) of the plant rhizosphere microbial community can affect nutrient availability and resource partition, thus increasing or reducing crop production, respectively [18,20]. The positive association of the microbial community increases their activities in the rhizosphere of host plants, which can improve the soil organic matter (SOM) content and nutritional status of the plant [21]. Beneficial bacteria are the first soil-borne communities that alter and re-adjust in stressful environments for their survival; however, their activities and configurations are the first affected factors under stress [22]. The plant growth-promoting rhizobacteria community is vulnerable to stressful conditions of low water potential and nutrient availability that may be reflected in the form of physiological stress in the plants [23].

The eco-physiological and functional activities of nutrients and PGPRs need proper attention and extensive research to improve plant tolerance to abiotic stresses. Therefore, this review highlighted the interaction between plant growth-promoting rhizobacteria and mineral nutrition and their influence on the tolerance to abiotic stresses in the Brassicas plant species.

#### **2. Adverse Effects of Abiotic Stress in Plants**

Abiotic stresses are the foremost confining factors for agricultural productivity. Crop plants overcome the drastic external pressure of intrinsic mechanisms caused by environmental and edaphic conditions that affect the growth, development and productivity of plants [24,25]. The sustainable production of vegetables such as Brassicas around the world has been compromised due to several harsh environmental conditions and the unbalanced use of synthetic fertilizers and uncertified chemicals over the years that affect the environment and human health and led to inadequate climatic conditions. Abiotic stresses consist of drought, low/high temperature, salinity, light intensity, flooding, heavy metals toxicity and nutrient starvation. The extensive use of chemicals, macro and micronutrients, nonessential elements and radionuclides are the main sources of metal toxicity in soil [13,25]. Brassicaceae are capable plant species that deal with the hyper-accumulation of heavy met-

als through their biochemical expression, acquisition and re-mobilization in roots [13,14]. Waterlogging/flooding is an excess of soil water that can reduce oxygen availability in plant root systems and thus negatively affect crop growth and yield [26]. Flooding has negatively affected lipid biosynthesis and the yield of several rapeseed varieties [27].

Cold stress is associated with chilly weather (0–15 ◦C) and frosty weather (<0 ◦C) that leads to the disturbance of the photosynthetic process and reduces the primary production of *B. oleracea* [28]. Cold stress impairs metabolic and enzymatic activities that can disrupt the cell membrane and cause seed rotting in Brassica plants [29,30]. Light radiation (low or high) affects plant morphology and the root–shoot ratio [31]. Exposure of broccoli (*B. oleracea*) to ultraviolet (UV) light can increase ascorbic acid [32,33]. High light causes photoinhibition of the photosystem and protein degradation in *B. rapa* plants [34]. In short, abiotic stresses alter several internal functions of plants by disturbing homeostasis, physio-biochemical and molecular attributes, such as water and nutrient use efficiency and assimilation, osmotic adjustment, disruption of membrane integrity and enzymatic activities, as well as reduction in photosynthetic efficiency [29,31,34]. The abiotic stresses and their consequences are summarized in Figure 1.

**Figure 1.** Effects of abiotic stresses and their consequences on Brassicaceae.

#### **3. Use of Plant Growth-Promoting Rhizobacteria to Mitigate Adverse Effects of Abiotic Stress**

In recent years, the contribution of rhizosphere microorganisms to increasing plant growth and crop productivity as well as tolerance to biotic and abiotic stresses without causing pathogenicity have been discussed in the literature [35]. Several genera of plant growth-promoting rhizobacteria (PGPR) including *Azospirillum*, *Bacillus*, *Rhizobium*, *Pseudomonas* and *Bradyrhizobium* showed positive interactions with different vegetables species [36,37]. Several previous studies highlighted the capacity of different PGPRs in biological nitrogen fixation (N2) [38,39], increasing the availability of iron (Fe) [40], phosphorus (P) and zinc (Zn) solubilization and transportation [41,42]. The PGPRs also improved the

performance and growth of plants through the production of phytohormones such as gibberellins, ethylene, cytokinin, auxins and salicylic acid [43,44].

The use of PGPRs has contributed to combating climate-induced changes (abiotic factors) such as uneven rainfall (drought), soil and water salinization and heavy metal contamination that limit the general performance of plants [44,45]. These microorganisms improve soil fertility and structure, which contribute to a successful adaptation of the plant under stressful conditions [45]. Researchers have been focused on the use of these microorganisms with emphasis on bacteria of the genera *Azospirillum*, *Bacillus*, *Pseudomonas*, *Rhizobium*, *Bradyrhizobium*, *Herbaspirillum* and *Burkholderia* [36,38].

PGPRs exist in the rhizosphere and tissues of plants, which may adapt multiple mechanisms including the synthesis and exudation of phytohormones (indole-3-acetic acid (AIA)), cytokinin, ethylene and gibberellins [46]; synthesis of plant growth-regulators including nitric oxide [47]; abscisic acid [48]; polyamines such as spermidine and spermine [49]; increase solubilization and availability of nutrients [50,51]; increase nitrate reductase activity and nutrient use efficiency [38,52]; biocontrol of phytopathogens and diseases [53]; and protection of plants against water and saline stress and toxic chemical elements of the soil [54]. In addition to assisting in biological nitrogen fixation, PGPRs have the ability to enhance cell membrane stability of the leaf and reduce the rate of leaf abscission during drought stress conditions [55]. Several PGPRs improve the tolerance capability of plants by producing certain phytohormones [56] that can be used for heavy metal remediation, mobilization or immobilization from soil into plant tissues [57,58]. These microbes also utilized 1-aminocyclopropane-1-carboxylic acid (ACC) to prevent ethylene production [59] and mitigate stresses by endophytic biota, which were caused due to high radiation and light stress [60]. Plant growth-promoting rhizobacteria adapted several mechanisms to improve the growth and development of the plants of the Brassicaceae family under abiotic stresses (Figure 2).

**Figure 2.** Role of plant growth-promoting rhizobacteria in Brassica species against abiotic stresses.

Plant growth-promoting rhizobacteria (PGPR) promote plant tolerance to abiotic stresses through the adaptation of several mechanisms as well as down- or up-regulating stress genes [61]. The inoculation of rapeseed plants with *Pseudomonas* sp. and *Azospirillum* sp. mitigate salt stress [62] by increasing the solubilization and availability of macro- and micronutrients for better uptake in the above-ground part of the host plant [63,64]. PGPRs prominently improved root–shoot fresh and dry weights, leaf area, chlorophyll and several growth-promoting hormones, which ultimately improved the seedling growth of *B. oleracea*

and *B. napus* [65,66]. Flooding is another abiotic stress that harshly reduces antioxidant activities; however, inoculation with bio-fertilizers (*Azotobacter chroococcum*, *Azospirillum* spp. and *Pseudomonas* spp. and *Azospirillum* spp., *Pseudomonas fluorescens* and *Basillus subtilis*) via seeds and foliar efficiently alleviate flooding affects in canola by increasing growth and yield [67]. In this context, the supply of these rhizobacteria or PGPRs to plants of the Brassicaceae family brought benefits to their cultivation in abiotic conditions (Table 1).

**Table 1.** Summary of the positive effects of PGPR in mitigating unfavorable abiotic stress conditions in Brassicas (2008–2020).


#### **4. Plant Nutrition to Mitigate Adverse Effects of Abiotic Stress on Brassicas**

Plants develop extensive adaptive and/or resistance mechanisms to sustain productivity and survival under stressful conditions. However, adequate nutrient application is an imperative tool to meet the Sustainable Development Goals to attain food and nutritious security and promote sustainable productivity under climate extremes [79]. Optimization of nutrient content (macro- and micronutrients, secondary nutrients and heavy metals) in

soil and plant systems have been reported to enhance crop adaptation to resilience conditions, as these are structural elements of several co-factors and enzymes. Nutrients assist structures' stability of protein and alleviate reactive oxygen species (ROS) production. The versatility of nutrient application under severe environmental conditions has significantly improved the yield and quality traits of various crops [80].

Fertilizers are considered the most important and crucial inputs to achieve greater crop growth and production in modern agriculture [81]. Plants require NPK and other essential micronutrients such as iron (Fe), copper (Cu), zinc (Zn), manganese (Mn), molybdenum (Mo), nickel (Ni), chlorine (Cl) and boron (B) in very small quantities for better performance and yield. These elements are collectively considered as essential for humans and animals and their deficiency can affect their metabolic, physical and mental development. Macroand micronutrients play a critical role in the effectiveness of several biological compounds and enzymes for the proper functioning of different metabolic processes. The relevance of macronutrients' essentiality for higher yield and nutritional status has been increasing over several decades [82]. Ensuring that plants are well-fed with essential nutrients is a cost-effective strategy with the capacity to mitigate abiotic stresses and enhance productivity [79,81]. The effect of macro- and micronutrients on different functions of Brassicaceae crops promotes plant growth and increases tolerance to abiotic stresses (Figure 3).

#### *4.1. Macronutrients*

Macronutrients are considered to be significant drivers for enhancing the yield and quality parameters of crop plants. Traditional fertilizer application in a field may not fulfill the demands of individual plants while over and/or under application causes soil quality degradation, groundwater pollution and reduction in productivity. Leaf nutrition of rapeseeds is an important factor to optimize fertilization and productivity, alongside contributing to commercial and environmental profits [83]. Better management of macronutrient fertilizers can improve plant growth and yield under stressful conditions. The nutrients and their functions in the crop plants are discussed below in detail.

#### 4.1.1. Nitrogen

Nitrogen (N) is the most needed nutrient for most cultivated plants, and it directly affects plant development and yield [84–89]. Nitrogen is the main constituent of the atmosphere, but its availability is still one of the main limiting factors for the productivity of terrestrial ecosystems including agro-ecosystems [90]. Nitrogen plays an important role in plant nutrition and development [87], such as the synthesis and production of phytohormones, co-enzymes, nucleic acids, secondary metabolites, chlorophyll and proteins content [91].

Several studies have reported that N fertilization promoted different species of Brassicaceae including oilseed producer crops such as rapeseed (*B. napus*) [92,93], brown mustard (*B. juncea*) [94,95] and turnip rape (*B. rapa*) [96] and horticultural crops such as radish (*Raphanus sativus*) [97], cauliflower (*B. oleracea* L. var. botrytis) [98,99], cabbage (*B. oleracea* L. var. Capitata) [100,101], broccoli (*B. oleracea* L. (var. italica) [102,103], kale (*B. oleracea* L. var. sabellica) [104,105] and arugula (*Eruca vesicaria* subsp. Sativa) [106].

Abiotic stress conditions alter the N metabolism of Brassicaceae plants [94], negatively affecting N uptake and assimilation, N use efficiency (NUE), photosynthetic capacity and plant growth [107], particularly under prolonged (24 h) stress exposure [108]. The interaction of N fertilization and abiotic conditions plays an important role in determining the potential of plant development and abiotic stress tolerance. Stress relief depends on the type of N fertilization; applying ammonium (NH4 +) to plants resulted in a stronger tolerance to heat stress as compared to the fertilization with nitrate (NO3 −) [109]. In addition, N fertilization can compensate for the negative effects of abiotic conditions by facilitating carbon partitioning, cell membrane stability, osmoregulation and antioxidative mechanisms that could improve plant growth and development as well reduce leaf senescence under extreme environmental conditions [110].

**Figure 3.** Effect of macronutrients (indicated in blue color), silicon (orange color) and micronutrients (green color) on different functions of Brassicaceae crops.
