Improvement of morphophysiological and anatomical attributes of plants under abiotic stress conditions using plant growth-promoting bacteria and safety treatments

Intended audience

The abiotic stress factors are significant for the researchers and broader audience because of the harmful effects of these factors on agricultural production and sustainable development. Our review is essential for researchers in plant breeding for abiotic stress, plant physiology, and genetics.

Survey methodology

We have checked about 480 articles and book chapters in this field to achieve our aim and introduce the recent information and results to the researchers and audience. We used search engines like Web of Science and PubMed. The date range searched was between 1999 and 2023. We focused on the manuscripts and book chapters that summarize the pivotal role of various PGPB and eco-friendly treatments as a promising strategy to alleviate the negative impacts of drought and salinity and increase plant yield and production under stressful conditions.

Effect of drought stress on morphological characteristics of plants

The growth characteristics of plants can be significantly affected by drought stress (Abdelaal et al., 2022b). This is a serious threat to agricultural production (Abdelaal et al., 2021d) since can affect all stages of plant growth and development, including germination, seedling growth, and yield (Elkoca et al., 2007; Kaya et al., 2006). As mentioned, the reduction in leaf number, leaf area, and plant height was recorded in many plants under drought stress, including faba bean plants (Abdelaal, 2015a), barley (Abdelaal et al., 2018; Abdelaal et al., 2020b) and wheat (Kutlu et al., 2021). Similar effects of drought were recorded in sugar beet (Abdelaal, 2015b) and wheat (Abdelaal et al., 2021d). Additionally, the decrease in fresh and dry weight is a common negative effect under drought stress conditions (Abdelaal et al., 2018) observed in many plants (AlKahtani et al., 2021a; Galal et al., 2023). Previous studies showed that water deficit caused significant decreases in morphological characteristics of faba bean and maize plants (Abdelaal, 2015a; Abdelaal et al., 2017). Moreover, a significant decrease in leaf area, plant height, and number of leaves per plant in pea was observed during two seasons under drought conditions. Also, pod number and dry weight of 100 seeds decreased significantly in drought-stressed pea plants (Arafa et al., 2021). In recent years many studies have been implemented to overcome the negative effects of drought stress on the morphological characters in plants (Table 1).

Effect of PGPB and safety treatments on morphological characteristics of plants under drought conditions

The harmful effects of drought stress can be alleviated with the application of safety treatments and compounds such as PGPB, yeast extract, mannitol, melatonin, silicon, trehalose, chitosan, α-Tocopherols (vitamin E) or biochar (Table 1). In sugar beet plants, the application of silicon and proline improved leaf number, root fresh weight, and root yield under water deficit conditions (Abdelaal et al., 2017). Abdelaal et al. (2021a), Abdelaal et al. (2021b), Abdelaal et al. (2021c), Abdelaal et al. (2021d) and Abdelaal et al. (2021e) reported that yeast extract significantly increased garlic yield under drought conditions. Seed priming with Bacillus thuringiensis boosted adaptation in pea plants under drought conditions and increased the number of leaves, leaf area, and flowers per plant in both seasons (Arafa et al., 2021). Biochar treatments may play a significant role in the enhancement of morphological features under drought stress conditions since this treatment led to improved plant height and branch number of drought-stressed barley plants (Abdelaal et al., 2022b). In the experiments of AlKahtani et al. (2021a), significant decreases in morphological characteristics under water deficit stress conditions were shown. However, the application of salicylic acid led to the improvement of morphological characteristics and the overcoming of drought stress negative effects. Furthermore, the application of yeast extract caused a significant improvement in the morphological characteristics of maize plants under water deficit conditions (Abdelaal et al., 2017). In experiments with wheat, exogenously application of yeast extract and ascorbic acid led to the improve the plant height and leaves number under water deficit (Abdelaal et al., 2021d).

Effect of drought stress on physiological and biochemical characteristic of plants

Antioxidant enzymes are a very important sign of drought stress conditions. In this context, Abdelaal et al. (2021c) reported that drought stress affects antioxidant enzyme activity, photosynthetic parameters, and relative water content in stressed garlic plants. Additionally, electrolyte leakage, and concentration of H₂O₂, and O₂₋ were significantly higher in garlic plants under drought conditions (Abdelaal et al., 2021c). Furthermore, concentrations of chlorophyll a and chlorophyll b, and relative water content of pea plants significantly decreased under drought stress conditions (Arafa et al., 2021). On the other hand, O₂₋ and H₂O₂ levels significantly increased in pea plants under drought stress. The maize plants exposed to water deficit stress showed that water deficit led to significant decreases in chlorophyll content in the stressed plants compared to control, whereas electrolyte leakage and MDA content significantly increased. Furthermore, a significant decrease in antioxidant compounds and protein was recorded in maize plants under water-deficit conditions (Abdelaal et al., 2017), while drought-stressed barley plants showed significant decreases in photosynthesis, relative water content, and water uptake (Hafez et al., 2020a; Hafez et al., 2020b).

Effect of PGPB and safety compounds on physiological and biochemical characteristics of plants under drought conditions

Several studies were conducted to improve plants’ growth and physiological features under water deficit stress conditions (Table 2). Yeast extract significantly improved antioxidant enzyme activity and relative water content and decreased ROS in garlic plants under drought conditions. Additionally, garlic’s physiological and biochemical characteristics were improved with chitosan treatment under drought conditions, including relative water content and photosynthetic parameters (Abdelaal et al., 2021c). Furthermore, the number of seeds per pod, pod length, and dry weight of 100 seeds of pea plants were significantly increased with the application of carrot extract under drought stress conditions (Arafa et al., 2021). Also, Bacillus thuringiensis treatment improved the biochemical characteristics of pea plants such as chlorophyll a, chlorophyll b, relative water content, and decreased O₂₋ and H₂O₂ under drought conditions. The carrot extract can be very significant due to the presence of essential vitamins such as vitamins A and C, which significantly improve plant growth and development by increasing plant height, leaf area, and number of leaves in pea plants. The positive impacts of carrot extract were also recorded on the physiological features of faba bean plants under drought conditions (Kasim, Nessem & Gaber, 2019). The application of biochar led to an increase in chlorophyll a and b content, relative water content, and antioxidant compound activity in barley plants under drought-stress conditions (Hafez et al., 2020a; Hafez et al., 2020b). Under water deficit conditions, PGPB can be used to enhance the morphophysiological and biochemical characteristics via phosphorus solubilization, nitrogen uptake, and the availability of essential nutrients (Kasim, Nessem & Gaber, 2019; Ghosh, Gupta & Mohapatra, 2019). Treatment with PGPB such as Serratia spp. (Heinrichs et al., 2009), Azoarcus sp., Pseudomonas spp. (Egener, Hurek & Reinhold-Hurek, 1999; Igiehon & Babalola, 2021; Sandhya et al., 2010; Zahir et al., 2009), and Rhizobium spp. led to better morphophysiological features and yield of several plants (Table 2). Furthermore, the application of Azospirillum gave the best results regarding the drought tolerance of maize plants (García et al., 2017). The positive role of PGPB could be attributed to the improvement of water accessibility and antioxidant components as well as the production of osmoprotectants which improve plant growth under drought conditions. Meenakshi et al. (2019) stated that Bacillus thuringiensis, Bacillus subtilis, and Bacillus megaterium treatments significantly increased chlorophyll content in stressed plants. The useful effects of PGPB under stressful conditions might be due to the formation of osmolytes and the improvement of the antioxidant system.

Effect of salt stress on morphological characteristics

Under salinity conditions, plants display many variations and changes in all developmental stages. Salinity stress significantly decreases plant height, number of leaves, and leaf area in stressed plants such as calendula (El-Shawa, Rashwan & Abdelaal, 2022), sweet basil, and pea plants (Jakovljević et al., 2017; Sapre, Gontia-Mishra & Tiwari, 2021). Also, fresh weight and dry weight were significantly reduced under salinity conditions in barley (Elsawy et al., 2022), rice (Mohamed et al., 2022), basil (Jakovljević et al., 2017) and bean (Kutlu & Gulmezoglu, 2023). Khedr et al. (2023) reported that the salt-stressed wheat plants were negatively affected since most of the studied characteristics significantly decreased under salinity conditions. In the experiment with lettuce, both salinity concentrations (4 dS m^-1 and 8 dS m^-1) caused a significant decrease in leaf number and head weight in the stressed plants compared to the control in two seasons. This harmful effect of salt stress may be due to decreased water uptake from the soil, and the inhibition of cell elongation and cell division. Salinity stress is also followed by toxicities of Na+ and Cl−, which reduce the uptake of essential elements like nitrogen, phosphorus, and potassium (ALKahtani et al., 2021b) reducing the stressed plants’ morphological features.

Effect of PGPB and safety treatments on morphological characteristics of plants under salinity conditions

Many studies were conducted to find suitable methods to overcome the negative effects of salinity stress. Bharti et al. (2016) reported that the application of PGPB Dietzia natronolimnaea caused improvement in the morphological features of wheat plants under salt-stress conditions. Bacillus thuringiensis treatment increased leaves number, head weight, and total yield in lettuce plants under salinity stress compared to untreated plants (AlKahtani et al., 2021a). In the study of El-Flaah et al. (2021), the treatment with Rhizobium improved the growth characteristics of salt-stressed faba bean plants such as branch number, plant height, and flower number. Additionally, Abdelaal, Mazrou & Hafez (2020) reported that stress tolerance-inducing compounds alleviate salinity stress effects on sweet pepper plants and improve growth characteristics. The application of chitosan caused a significant improvement in morphological characteristics of sweet pepper plants including plant height, leaf number, and fresh shoot weight under salt stress (Abdelaal et al., 2021c). Al-Shammari, Altamimi & Abdelaal (2023) found an improvement in the seed yield of pea plants under salinity conditions with melatonin treatment, the growth characteristics also were improved under these conditions. One of the crucial treatments in alleviating the negative effects of salinity stress is biochar, which may overcome the harmful effects and improve the growth characteristics of faba bean plants (El Nahhas et al., 2021).

Effect of salt stress on physiological and biochemical characteristics of plants

Salinity stress significantly affects the physiological and biochemical characteristics of plants, resulting in an imbalance of ions and a decrease in nutrient uptake, especially nitrogen, phosphorus, and potassium (Kumar et al., 2017; Putra, Santosa & Salsinha, 2023). The harmful effects on physiological and biochemical features may be due to the decrease in the synthesis of growth-promoting hormones. IAA is a hormone that stimulates cell division and elongation (Putra, Santosa & Salsinha, 2023). High salinity levels can decrease amino acid production (like tryptophan) which is involved in the IAA synthesis, resulting in decreased IAA concentration. Many physiological and biochemical changes were observed under salinity conditions, such as the synthesis of compatible solutes, antioxidant components, and stress proteins, as well as the excessive production of ROS, which negatively affects cellular structures, inhibits carbon fixation, decreases the photosynthetic rate, and causes hormonal balance disorder (Abdelaal, Mazrou & Hafez, 2020). Moreover, electrolyte leakage, MDA content, and superoxide and hydrogen peroxide production increase, while chlorophyll content and relative water content decrease. The synthesis of antioxidant compounds, including both enzymatic and non-enzymatic antioxidants, is one of the mechanisms to deal with salinity and it is based on the protection of cells against oxidative damage. Glutathione reductase, peroxidase, catalase, superoxide dismutase, and ascorbate peroxidase are the main enzymatic antioxidants (Usman et al., 2023; Jahanbani et al., 2023), while non-enzymatic antioxidants including ascorbic acid, proline, carotenoids and α-Tocopherols (vitamin E) (Rigi, Saberi & Ebrahimi, 2023; Hafez et al., 2020a; Hafez et al., 2020b). El Nahhas et al. (2021) reported that salinity stress significantly decreased relative water content and chlorophyll concentration, while lipid peroxidation, electrolyte leakage, and ROS significantly increased in salt-stressed faba bean plants. Additionally, salt concentration was positively correlated with the content of secondary metabolites such as phenolics (including flavonoids), and proline (Beheshti, Khorasaninejad & Hemmati, 2023). The decrease in the content of photosynthetic pigments under salinity conditions could be due to the chlorophyll photooxidation and chloroplasts oxidative damage under salinity conditions (Beheshti, Khorasaninejad & Hemmati, 2023; Singh et al., 2022).

Mitigation of salt stress effects on the physiological and biochemical characteristics of plants

It can be concluded that the adverse effects of salinity can be detected in all stages of plant growth and development, including both vegetative and reproductive stages in numerous plants (El-Flaah et al., 2021; Aziz et al., 2023). Application of PGPB was used to improve plant growth and increase productivity under salinity stress (Table 3). It is shown that plant growth-promoting rhizobacteria can improve physiological and biochemical characteristics such as water absorption, nutrient uptake, and photosynthesis, and promote plant growth and development. PGPB can produce essential compounds such as siderophores and ACC-deaminase which increase the availability of some nutrients in the soil. For example, the Enterobacter treatment led to increased ACC deaminase activity and alleviated salinity stress by reducing ethylene concentration (Singh et al., 2022; Agha et al., 2023). Under salt stress conditions, MDA production, electrolyte leakage, and concentration of H₂O₂ significantly decreased with the application of Bradyrhizobium japonicum + Enterobacter in the stressed soybean plants, while chlorophyll concentrations increased (Bisht et al., 2022). AlKahtani et al. (2021a) and Bisht et al. (2022) reported that the application of PGPB markedly improved photosynthetic rate, stomatal conductance, and chlorophyll and carotenoid content in lettuce and Trigonella under salinity stress. Moreover, Ali et al. (2022) found that inoculation with Enterobacter cloacae improved relative water content, flavonoid, and protein content in maize under salt stress (Mahmood et al., 2016). Also, Mukherjee, Mitra & Roy (2019) reported that the application of Halomonas sp. promotes the growth characteristics of rice plants and increases siderophore production under salinity stress. Likewise, Klebsiella variicola produced many compounds under salinity conditions such as siderophore, 1 aminocyclopropane-1-carboxylate deaminase, IAA, exopolysaccharides, and antioxidant enzymes (Sen & Chandrasekhar, 2014).

The positive role of PGPR may be due to improved uptake of nitrogen, phosphorus, and potassium (Zahir et al., 2009; Choudhary et al., 2022). PGPR may trigger the antioxidant defense system to scavenge ROS which are produced as indicators of salt stress in many plants (Sapre, Gontia-Mishra & Tiwari, 2018; Ansari, Jabeen & Ahmad, 2021). Previous studies showed that the application of Pseudomonas sp. and Serratia sp. led to improved physiological characteristics in the salt-stressed wheat plants (Table 3) via enhanced ACC-deaminase production in plants (Tufail et al., 2021; Patel et al., 2021). Also, the secretion of phytohormones and nitrogen fixation is one of the various mechanisms to decrease the negative effect of salinity stress. Generally, PGPB can play an important role in improving the plant tolerance to drought and salinity stress conditions (Fig. 1).

Furthermore, the application of melatonin caused significant increases in chlorophyll concentrations and relative water content in the stressed pea plants. However, a significant decrease in the MDA production, EL%, and H₂O₂ and O₂₋ concentration was recorded in the stressed plants compared with the stressed pea plants without treatments (Kour et al., 2020). Serotonin is a vital bioregulator that is formed during the biosynthesis pathway of melatonin and has light-absorbing properties. Serotonin and melatonin are indolamines, they have a pivotal role for life in living organisms (Azmitia, 2011). Serotonin application led to decreased MDA content and EL% level of tomato plants, while relative water content was increased under salinity and drought stress conditions (Akcay & Okudan, 2023).

Exogenously applied melatonin mitigates the negative effect of salt stress by improving the IAA content, photosynthesis rate, and photosynthesis efficiency and reducing the accumulation of H₂O₂ in stressed wheat seedlings (Ke et al., 2018). Guo et al. (2023) reported that melatonin applied as foliar spray increased root length, leaf area, proline content, and soluble protein as well as the activity of antioxidant enzymes such as catalase and peroxidase in the salt-stressed alfalfa plants, while the levels of MDA were decreased. Melatonin can also mitigate the adverse effects of salinity and drought (Wang, Reiter & Chan, 2017). Furthermore, melatonin stimulates the essential enzymes, such as CAT, APX, SOD, POD, and GR, as well as some important metabolites such as flavonoids, glutathione, ascorbate, and anthocyanins which activate the antioxidant system and protect plants from oxidative damage under various stresses. Melatonin can also play a significant role in controlling H₂O₂ levels (Anwar et al., 2023). The positive effect of melatonin may be due to its role in maintaining root development and photosynthetic rate under salinity conditions (Arnao & Hernández-Ruiz, 2017). Application of yeast extract and proline led to increased concentration of elements such as N, P, K, and Ca in calendula plants under salinity stress, whereas concentration of Na, proline, O₂₋ and H₂O₂, and electrolyte leakage were decreased in the stressed plants (El-Shawa, Rashwan & Abdelaal, 2022).

The application of yeast extract and/or gibberellic acid (GA₃) gave the highest increase in plant growth characteristics such as plant height and fresh and dry weight of shoots, as well as photosynthetic efficiency, macronutrient content, total soluble sugars, and total phenolics in Solidago plants under alkaline soil conditions (Youssef et al., 2022). Additionally, the application of biochar and compost (alone or together) led to a significant improvement in plant growth compared to the control. Furthermore, the combined application of compost and biochar significantly reduced the sodium in the shoots and roots of tomato plants (Ud Din et al., 2023). It was also observed that the application of arbuscular mycorrhizal fungi (Rhizophagus intraradices) led to an increase in nutrient uptake, accumulation of compatible osmolytes, and decreased electrolyte leakage in Pisum sativum under salinity stress conditions (Parihar et al., 2020). Shahzad et al. (2017) found that the ability of rice plants to tolerate salinity stress was significantly increased by inoculation with arbuscular mycorrhizal fungi, which alter the endogenous phytohormone and essential amino acids such as glutamic acid, phenylalanine, cysteine, and proline. Additionally, arbuscular mycorrhizal fungi can improve the availability of nutritional elements via biological processes (Ma, Vosátka & Freitas, 2019) under various environmental factors. Navarro-Torre et al. (2023) reported that the application of halotolerant/halophilic bacteria can be one of the important strategies in improving plant tolerance to salinity stress in grapevines in the context of climate change. Furthermore, PGPB can improve plant tolerance to several abiotic stresses, especially salinity, by regulating the enzymatic and nonenzymatic antioxidants to prevent the accumulation of ROS, which results in improved plant growth (Abdou et al., 2023).