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Article

Effects of Bacillus cereus on Photosynthesis and Antioxidant Metabolism of Cucumber Seedlings under Salt Stress

by
Yaguang Zhou
1,†,
Ting Sang
2,†,
Mimi Tian
1,
Mohammad Shah Jahan
1,3,
Jian Wang
1,3,
Xiangyu Li
4,
Shirong Guo
1,3,
Hongyun Liu
1,
Yu Wang
1 and
Sheng Shu
1,3,*
1
College of Horticulture, Nanjing Agricultural University, Nanjing 210095, China
2
Institute of Horticultural Research, NingXia Academy of Agricultural and Forestry Science, Yinchuan 750002, China
3
Facility Horticulture Institute, Nanjing Agricultural University, Suqian 223800, China
4
Jiangsu Pufa Ecological Agriculture Co., Ltd., Suqian 223800, China
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Horticulturae 2022, 8(5), 463; https://0-doi-org.brum.beds.ac.uk/10.3390/horticulturae8050463
Submission received: 23 April 2022 / Revised: 11 May 2022 / Accepted: 19 May 2022 / Published: 20 May 2022
(This article belongs to the Section Biotic and Abiotic Stress)
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Abstract

:
Soil salinization is the leading environmental factor that restricts crop growth. This study studied the effects of Bacillus cereus (B. cereus) on growth, photosynthesis, and antioxidant metabolism in salt stressed-cucumber seedlings. The results showed that B. cereus could maintain high activity in the high salt environment (4% NaCl). B. cereus significantly increased plant height, stem diameter, fresh weight, and dry weight of cucumber seedlings under salt stress, and increased root vitality, net photosynthetic rate (Pn), stomatal conductance (Gs), intercellular CO2 concentration (Ci), and transpiration rate (Tr) of cucumber seedlings under salt stress. B. cereus significantly increased the maximum photochemical quantum yield of photosystem II (Fv/Fm), the actual photochemical quantum yield (ΦPSII), and the quantum yield of regulatory energy dissipation Y (NPQ) under salt stress, which were 9.31%, 20.44%, and 5.22% higher than those under salt stress, respectively. The quantum yield of non-regulatory energy dissipation Y (NO) was reduced by 19.81%. Superoxidase (SOD), peroxidase (POD), and catalase (CAT) activities in leaves and roots of cucumber seedlings were significantly increased by B. cereus under salt stress. Compared with salt stress, SOD activities in leaves were significantly increased by 1.70% and 6.32% on the first and third days after treatment. At 1 d, 3 d, and 5 d after treatment, SOD activity in roots increased by 3.06%, 11.24%, and 3.00%, POD activity in leaves increased by 113.38%, 38.81%, and 52.89%, respectively. The POD activity in roots increased by 56.79% and 10.92% on the third and fifth days after treatment, the CAT activity in leaves increased by 8.50% and 25.55%, and the CAT activity in roots increased by 30.59% and 84.45%. Under salt stress, the H2O2 and MDA contents of seedlings treated with B. cereus decreased significantly. Compared with salt stress, the proline content in leaves decreased by 12.69%, 3.90%, and 13.12% at 1 d, 3 d, and 5 d, respectively, while the proline content in roots decreased by 44.94% and 60.08% at 3 d and 5 d, respectively. These results indicated that B. cereus could alleviate salt-induced inhibition of growth and photosynthesis by regulating antioxidant metabolism of cucumber seedlings and thus enhancing salt tolerance of cucumber seedlings.

1. Introduction

Cucumber (Cucumis sativus L.) is one of the widely cultivated vegetable crops in global agricultural facilities, which has the characteristics of high yield and good benefit. Cucumber is a fibrous root plant, which is shallowly distributed in soil and sensitive to saline environment. Once subjected to salt stress, its yield and quality are significantly decreased. Most of the agricultural facilities are semi-enclosed, such as solar greenhouses, glass greenhouses, and so on. The internal environment of the facilities lacks rainwater leaching and the temperature is high, resulting in the salt in the soil rising to the surface with the evaporation of the water. In addition, unreasonable fertilization and irrigation methods further lead to the accumulation of salt in the soil and the continuous deterioration of plant growth environment. When the salt content in the soil is too high, plants will accumulate a large number of salt ions, which will cause osmotic stress on plants, resulting in a decline in plant water-absorption capacity, thereby reducing the net photosynthetic rate, transpiration rate, CO2 absorption capacity and leaf index of plants, and seriously inhibiting the growth of plants [1,2,3]. Plant growth promoting rhizobacteria (PGPR) as a biological control method can effectively alleviate multiple stresses and promote plant tolerance [4,5]. Bacillus subtilis can also combine with nano-molecules to effectively improve the disease resistance of plants by affecting plant histochemistry and their physio-biochemistry [6]. It was shown that phosphate-solubilizing bacteria N3 could significantly increase the levels of nitrogen, phosphorus, and potassium in roots of tomato seedlings under Cd stress, and induce the expression of stress resistance genes, effectively alleviating the damage caused by Cd stress on tomato seedlings [7]. Yasin et al. [8] isolated Paenibacillus SSB21 from pepper rhizosphere and found that SSB21 could significantly improve chlorophyll content, stem length, root length, biomass, and water use efficiency of pepper under salt stress. Otherwise, PGPR affects the growth environment of plants or directly regulates plant-related metabolic pathways by secreting pro-biomass to alleviate stress. Li et al. [9] isolated Kocuria rhizophila with IAA-producing traits from the rhizosphere of maize, significantly increased the growth indexes, photosynthesis, and antioxidant metabolism levels of maize under salt stress, and decreased Na+ and electrolyte permeability. Meanwhile, Kocuria rhizophila significantly increased the transcription levels of antioxidant genes (ZmGR1 and ZmAPX1) and salt tolerance genes (ZmNHXs, ZmWRKY5,8, and ZmDREB2A). Haroon et al. [10] showed that Bacillus megaterium, Bacillus tequilensis, and Pseudomonas putida with extracellular polysaccharide (EPS) and 1-aminocyclopropane-1-carboxylic acid deaminase (ACCD) characteristics could significantly enhance photosynthesis of wheat under salt stress, reduce ROS and electrolyte permeability of wheat, and induce salt tolerance of wheat by increasing the expression of Salt Overly Sensitive (SOS1 and SOS4) genes. Salt stress increases the ability of aerobic metabolism of plants, resulting in superoxide anion (O2·−), hydroxyl radical (OH·), hydrogen peroxide (H2O2), singlet oxygen (1O2), and other harmful reactive oxygen species (ROS). ROS causes protein denaturation, carbohydrate oxidation, membrane lipid peroxidation, enzyme inactivation, and programmed cell death (PCD) [11,12]. To reduce the harm of ROS and maintain their expected growth, the activity of antioxidant enzymes in plants is increased, so the activity level of antioxidant enzymes can be used to reflect the salt tolerance of plants. Many studies have shown that the antioxidant system of plants grown under stress is significantly enhanced after PGPR inoculation to resist stress. Ankati et al. [13] found that the antioxidant enzymes and biomass levels of chickpea seedlings treated with Streptomyces albus, Streptomyces africa, and Streptomyces coelicolor increased significantly, effectively reducing the damage caused by Fusarium wilt. Ali et al. [14] found that inoculation with Bacillus subtilis significantly reduced the contents of H2O2 and malonaldehyde (MDA) and alleviated the damage of metal stress on eggplant. Zhao et al. [15] analyzed Bacillus cereus WP-6 from three aspects of physiology, proteomics, and metabolomics, and verified that the inoculation of WP-6 reduced the MDA content of wheat under salt stress, increased the levels of proline, superoxidase (SOD), peroxidase (POD), and catalase (CAT), and promoted the growth of wheat seedlings under salt stress. Shi et al. [16] reported that Pseudomonas simiae enhanced stress tolerance of Atriplex canescens by regulating photosynthesis, antioxidant defense enzymes, and osmotic substances.
B. cereus not only plays a beneficial role in biodegradation, environmental regulation, aquaculture, and food processing, but also promotes plant growth [17,18,19,20,21]. However, the mechanism of B. cereus improving stress resistance of vegetable crops under salt stress is still unclear. Therefore, cucumber was used as the experimental material in this experiment, and B. cereus was used as the promoter for salt stress tolerance. We explored the physiological mechanism of B. cereus improving salt tolerance of cucumber, which provided a theoretical and practical basis for the efficient cultivation of cucumber in the greenhouse.

2. Materials and Methods

2.1. Material Cultivation and Treatment

B. cereus was isolated and purified by our laboratory and stored in a −80 °C refrigerator. The bacteria were activated by beef extract peptone (NB) solid medium when used. A single colony was selected to 10 mL new NB liquid medium, 200 rpm, 28 °C for 12 h, and the mother liquid of B. cereus was obtained. According to 1%, the mother liquor was inoculated into the new NB liquid medium for propagation. The product was centrifuged at 4000 rpm for 10 min, and the supernatant was discarded. Bacterial precipitation was re-suspended with sterile distilled water, and the concentration was adjusted to 108 CFU to obtain B. cereus suspension for subsequent experiments.
Cucumber seeds (Cucumis sativus L., Jinyou No. 4) were washed with 70% alcohol for 1 min, then shaken in 10% NaClO for 5 min, and then washed with sterile distilled water 5 times. When the seed radicle broke through the seed coat, it was seeded into the 32-hole plug. The solid substrate (EC: 0.62 mS·cm−1) was sterilized under high temperature and high pressure to avoid the influence of microorganisms in the substrate. When the seedlings grew out of two true leaves and one terminal bud, the seedlings were transplanted into the flowerpot (diameter × height × bottom diameter: 9 cm × 8.5 cm × 6.7 cm). The experiment was divided into four groups:
  • Cont: Seedlings were grown in the solid substrate and treated with sterile distilled water;
  • BS: Seedlings were grown in the solid substrate and treated with B. cereus suspension;
  • NaCl: The seedlings grew in the solid substrate and were irrigated with 150 mM NaCl solution (EC: 9.17 mS·cm−1);
  • NaCl+BS: Seedlings were grown in solid substrate containing NaCl (EC: 9.17 mS·cm−1) and treated with B. cereus suspension.
Each treatment was 20 pots, and each treatment group was treated by root irrigation on the 1st and 3rd day after transplanting, with 80 mL treatment solution per pot. During the experiment, the temperature was set to 28/18 ± 2 °C, the relative humidity was 65–70%, the light intensity was 300 μmol m−2·s−1, and the photoperiod was 14 h/10 h.

2.2. Salt Tolerance of B. cereus

Solid LB medium and liquid LB medium containing 0.5%, 1%, 1.5%, 2%, 2.5%, 3%, 3.5%, 4%, 4.5%, 5%, 5.5%, and 6% NaCl were prepared, respectively. Firstly, B. cereus was inoculated in solid LB medium for activation. Then, a single colony was selected, inoculated in liquid LB medium, and cultured at 28 °C and 200 rpm for 12 h. The greater the OD600 value of each liquid medium, the greater the number of B. cereus in the unit volume medium, and the stronger the survival and reproduction ability.

2.3. Growth Parameters

On the 5th day after treatment, the plant height of cucumber seedlings (the distance from root neck to top growth point) was measured. A vernier caliper measured the stem diameter of seedlings; the root substrate of the seedlings was washed with clear water and cut off from the root neck after drying. The fresh weight of the above-ground and below-ground parts were measured, respectively. Then, the above-ground and the below-ground parts were put into envelopes and dried in an oven to determine the dry weight of the above-ground and the below-ground parts.
Root activity was determined by the TTC method. 0.5 g root was weighed and mixed with 0.4% TTC solution and 0.1 mol·L−1 phosphate-buffered solution (PBS, pH 7.0) 5 mL in turn. The root was wholly immersed in the reaction solution and kept at 37 °C for 1 h. Then, 2 mL 1 M H2SO4 solution was added to the reaction solution to terminate the reaction. The root was taken out, and the surface was dried with filter paper and put into a mortar. Then, 3 mL ethyl acetate and a small amount of quartz sand were added for grinding. The obtained extract was transferred into the test tube and fixed with ethyl acetate to 10 mL. The absorbance of the extract was measured at 485 nm, and the root activity was calculated according to the standard curve.

2.4. Chlorophyll Content

Then, 0.2 g fresh leaves were cut and put into 20 mL reaction solution (acetone: ethanol: H2O = 4.5:4.5:1). After dark storage for 24 h, the OD645 and OD663 values were measured after the leaves were completely whitened. The contents of chlorophyll a (Chl a), chlorophyll b (Chl b), and total chlorophyll were calculated according to the method of Roca et al. [22].

2.5. Photosynthesis

On the 1st, 3rd, and 5th day after seedling treatment, the second fully expanded functional leaf from the growth point downward was taken. The net photosynthetic rate (Pn), stomatal conductance (Gs), intercellular CO2 concentration (Ci), and transpiration rate (Tr) of cucumber seedlings were measured by the portable photosynthetic system (Li-6400 XT, Li-COR, Lincoln, NE, USA). The temperature was set at 25 °C, light intensity was 1000 μmol·m−2·s−1, CO2 concentration was 400 ± 10 μmol·mol−1, and relative humidity was 70%.
After 1 d and 5 d of treatment, cucumber seedlings were exposed to dark for 30 min. The second fully expanded functional leaf was selected and placed upward in fluorescence imaging system (IMAGINE-PAM, Heinz Walz, Effeltrich, Germany) to determine chlorophyll fluorescence parameters. Maximum photochemical quantum yield (Fv/Fm), actual photochemical quantum yield (ΦPSII), the quantum yield of non-regulated energy dissipation Y (NO), and quantum yield of regulated energy dissipation Y (NPQ) were measured and calculated by reference to Wu’s method [23].

2.6. H2O2 and MDA Contents

H2O2: 0.2 g fresh sample was ground in the ice bath with 1.6 mL 0.1% TCA, and then centrifuged at 12,000× g for 20 min. 0.2 mL supernatant was added with 1 mL 1 M KI solution and 0.25 mL 0.1 M potassium phosphate buffer (pH 7.8). After dark reaction for 1 h, the absorbance of the reaction solution at 390 nm was measured.
MDA: 0.2 g fresh samples were grinded in the ice bath with 2 mL phosphate buffer (PBS) (pH 7.8), centrifuged at 12,000× g at 4 °C for 20 min, and the supernatant was collected. Take 1 mL supernatant, add 2 mL 0.6% TBA, sealed boiling water bath for 15 min, quickly cooled and centrifuged, take the supernatant, and determine the reaction solution’s absorbance at 600, 532, 450 nm.
The contents of H2O2 and MDA were calculated according to Zhu et al. [24].

2.7. Antioxidant Enzyme Activity

Then, 0.2 g fresh sample was ground in an ice bath with 2 mL PBS (pH 7.8) and centrifuged at 12,000× g at 4 °C for 20 min. The supernatant was collected for subsequent antioxidant enzyme detection. The contents of SOD, POD, and CAT were calculated according to Wu et al. [25].
Taking 50 μL supernatant, adding 3 mL NBT reaction solution (198 mL PBS, 0.0387 g methionine, 0.0123 g NBT, 0.0149 g EDTA-Na2, and 2 mL 200 μM riboflavin), 800 μmol·m−2·s−1 illumination for 30 min. Four test tubes were taken, one of which was added with the supernatant and the reaction solution in the dark, and the other three were mixed with PBS instead of the supernatant and the reaction solution as the control. The absorbance of the mixed solution at 560 nm was measured to calculate SOD content.
Then, 50 mL 0.1 M PBS (pH 6.0) and 28 μL guaiacol were heated and dissolved. After cooling, 19 μL 30% H2O2 was added to form the reaction solution. The supernatant was 20 μL, and added 3 mL guaiacol reaction solution. The absorbance of the mixed solution at 470 nm was measured to calculate the content of POD.
Then, 0.1 M H2O2 solution and 0.1 M PBS (pH 7.0) were mixed at a ratio of 1:4 to obtain the reaction solution. 0.1 mL supernatant was added with 2.5 mL reaction solution, and the absorbance of the mixed solution at 240 nm was measured to calculate the content of CAT.

2.8. Proline Content

Take the 0.2 g fresh sample, add 5 mL 3% sulfosalicylic acid solution, boiling water bath 10 min, cooling, 3000 g centrifugal 10 min. Take 1 mL supernatant, add 1 mL water, 1 mL acetic acid, and 2 mL acid ninhydrin solution, boiling water bath 60 min, the solution is red. After cooling add 4 mL toluene, vortex oscillation 30 s, standing for a minute. The red solution on the upper layer was absorbed in a colorimetric dish, and toluene was used as the blank to zero. The absorbance of the mixed solution at 520 nm was measured. The proline contents were calculated according to Han et al. [26].

2.9. Statistical Analysis

All data were statistically analyzed using SPSS v.26.0 (SPSS Inc., Chicago, IL, USA). All determinations were repeated in triplicate, and the data obtained are expressed as the mean ± standard error. Turkey test was used to analyze the data between different treatments at a p < 0.05 level of significance.

3. Results

3.1. Salt Tolerance of B. cereus

To ensure that B. cereus could survive under salt stress, the salt tolerance of B. cereus was determined. As shown in Figure 1, the OD600 value of B. cereus on the medium with a certain salt concentration (within 3%) has been maintained above 2.5, implying that all microorganisms can survive. With the increase in salt concentration, the activity of B. cereus sharply decreased, and when the salt concentration was 5.5%, B. cereus could not survive.

3.2. Effect of B. cereus on the Growth of Cucumber Seedlings under Salt Stress

Under salt stress, the growth of cucumber seedlings was inhibited, mainly manifested as dwarf plants and yellow leaves (Figure 2A). As shown in Figure 2B, inoculation of B. cereus had no significant effect on plant height, stem diameter, shoot fresh weight, shoot dry weight, root fresh weight, and root dry weight of cucumber seedlings. NaCl treatment significantly reduced plant height, shoot fresh weight, shoot dry weight, root fresh weight, and root dry weight of cucumber, compared with the control, which decreased by 51.20%, 64.13%, 64.90%, 53.11%, and 86.14%, respectively. Under salt stress, the growth inhibition of cucumber seedlings was alleviated, and the plant height, shoot fresh weight, shoot dry weight, root fresh weight, and root dry weight of cucumber seedlings were significantly increased by 53.70%, 60.16%, 56.18%, 91.81%, and 506.02%, respectively, compared with salt stress.

3.3. Effect of B. cereus on the Root Vitality of Cucumber Seedlings under Salt Stress

As shown in Figure 3, compared with the control, the root vitality of seedlings increased by 478.79%, 74.5%, and 56.26% at 1 d, 3 d, and 5 d after inoculation of B. cereus, respectively. On the first day after NaCl treatment, the root vitality of seedlings increased significantly by 149.41% compared with the control and then decreased sharply. On the first and fifth days after NaCl treatment, the root vitality decreased by 36.59% and 47.76% compared with the control. Compared with salt stress, the root vitality of seedlings increased by 58.40%, 74.50%, and 134.29% at 1 d 3 d, and 5 d after inoculation of B. cereus under salt stress.

3.4. Effect of B. cereus on the Chlorophyll Content of Cucumber Seedlings under Salt Stress

As shown in Table 1, on the first day after treatment, there was no significant difference in Chl a, Chl b, and total Chl content in each treatment group. Compared with the control, B. cereus treatment had no significant indigenous effect on Chl a, Chl b, and total Chl content of cucumber seedlings. Compared with the control, the Chl a content of cucumber seedlings on the third and fifth days after NaCl treatment significantly decreased by 31.54% and 54.72%, the Chl b content significantly decreased by 33.34% and 54.77%, and the total Chl content significantly decreased by 31.96% and 54.73%. Compared with salt stress, on the third and fifth days after inoculation with B. cereus under salt stress, the Chl a content of cucumber seedlings increased by 20.77% and 58.06%, the Chl b content increased by 20.63% and 50.23%, and the total Chl content increased by 20.74% and 56.24%.

3.5. Effect of B. cereus on Gas Exchange Parameters of Cucumber Seedlings under Salt Stress

As shown in Figure 4, compared with the control: Pn was significantly increased by 17.18%, and 16.63% at 3 d and 5 d after B. cereus treatment; Gs significantly increased by 15.72%, 23.71%, and 11.90% at 1 d, 3 d and 5 d after B. cereus treatment; Ci increased by 4.24% at 5 d after B. cereus treatment; Tr increased by 6.76% on the 1st day after B. cereus treatment. On the 1st, 3rd, and 5th days after salt stress treatment: the Pn of seedlings decreased by 59.52%, 81.58%, and 37.09%; Gs decreased by 91.31%, 91.37%, and 41.58%; Ci decreased by 60.35%, 13.77%, and 7.04%; and Tr decreased by 88.51%, 87.44%, and 26.37%, respectively, compared with the control. Under salt stress, the gas exchange parameters of seedlings were significantly increased at 1 d, 3 d, and 5 d after B. cereus treatment. Compared with salt stress: Pn was significantly increased by 144.08%, 342.27%, and 24.95%; Gs was significantly increased by 1017.14%, 784.83%, and 10.98%; Ci was significantly increased by 150.70%, 16.42%, and 4.69%; and Tr was significantly increased by 685.43%, 524.22%, and 10.04%.

3.6. Effects of B. cereus on Chlorophyll Fluorescence of Seedlings under Salt Stress

As shown in Figure 5, B. cereus had no significant effect on Fv/Fm and Y (NO) of cucumber seedlings under control conditions. Salt stress reduced Fv/Fm, which decreased by 5.79% and 13.63% on the first and fifth days after treatment, respectively, compared with the control. Under salt stress, B. cereus significantly increased Fv/Fm, which increased by 2.92% and 9.31% on day 1 and day 5, respectively, compared with salt stress. Compared with the control, the ΦPSII of the seedlings treated with B. cereus decreased by 10.49% on the first day and increased by 10.54% on the fifth day. On the first and fifth days after treatment, salt stress reduced the ΦPSII of seedlings by 10.35% and 12.46% compared with the control. Under salt stress, ΦPSII was significantly increased by 2.92% and 9.31% at 1 d and 5 d after B. cereus treatment. Compared with the control, B. cereus had no significant effect on the Y (NO) of seedlings. Y (NO) increased by 21.61% and 50.55% at 1 d and 5 d after NaCl treatment. Under salt stress, Y (NO) of seedlings was significantly decreased by 8.43% and 19.81% at 1 d and 5 d after B. cereus treatment. Under the control condition, the Y (NPQ) of seedlings increased by 4.17% on the first day and decreased by 4.20% on the fifth day after B. cereus treatment. On the first and fifth days after NaCl treatment, the seedling Y (NPQ) decreased significantly, by 3.74% and 14.05% compared with the control. Under salt stress, the Y (NPQ) of seedlings treated with B. cereus had no significant change on the first day, and the significant change increased by 5.22% on the fifth day.

3.7. Effects of B. cereus on the Contents of MDA and H2O2 in Cucumber Seedlings under Salt Stress

As shown in Figure 6, compared with the control, there was no significant change in MDA content in the leaves of seedlings 3 days before inoculation, but the MDA content decreased by 49.95% on the fifth day. Under the control condition, salt stress increased MDA content in seedling leaves by 123.20% and 108.58% on the third and fifth days after treatment. Compared with salt stress, the MDA content of seedling leaves decreased by 32.43%, 61.22%, and 26.17%, respectively, at 1 d, 3 d, and 5 d after treatment with B. cereus. On the first day after B. cereus treatment, MDA content in seedling roots increased by 75.88% compared with the control. At 1 d, 3 d, and 5 d after NaCl treatment, the MDA content in seedling roots increased by 169.83%, 51.93%, and 81.14%, respectively, compared with the control. Under salt stress, the content of MDA in seedling roots was significantly reduced by B. cereus. Compared with salt stress, the content of MDA in seedling roots decreased by 30.36%, 52.38%, and 20.16% at 1 d, 3 d, and 5 d after treatment, respectively.
Compared with the control, the H2O2 content in the leaves of seedlings decreased by 12.36% on the third day after inoculation with B. cereus, and increased by 26.02% on the fifth day. Salt stress significantly increased H2O2 content in seedling leaves at 3 d and 5 d after treatment, which increased by 33.47% and 108.19% compared with the control. Under salt stress, the H2O2 content of B. cereus significantly decreased on the third and fifth days after treatment, 13.34% and 14.59% lower than that under salt stress, respectively. Compared with the control, there was no significant change in H2O2 content in the root of seedlings in the first 3 days after B. cereus treatment, but it decreased by 29.69% on the fifth day. On the third and fifth days after NaCl treatment, the H2O2 content in the root of seedlings increased significantly by 18.11% and 100.55%, respectively, compared with that under salt stress. Under salt stress, the H2O2 content in the roots of seedlings treated with B. cereus decreased significantly on the third and fifth days, and decreased by 14.15% and 28.08% compared with salt stress, respectively.

3.8. Effect of B. cereus on the Antioxidant Enzyme Activities of Cucumber Seedlings under Salt Stress

As shown in Figure 7, the B. cereus treatment had no significant effect on SOD content in seedling leaves compared to the control. Salt stress significantly increased SOD content in seedling leaves at 1 d and 3 d after treatment, which increased by 3.53% and 4.11% compared with the control. Under salt stress, the SOD content in the leaves of seedlings on the first and third days after B. cereus treatment increased by 1.70% and 6.32%. Compared with that. Compared with the control, the SOD content in seedling roots increased by 12.27% on the third day after B. cereus treatment. On the fifth day after NaCl treatment, the SOD content in seedling roots increased significantly, by 6.62% compared with the control. Under salt stress, B. cereus significantly increased SOD content in seedling roots by 3.06%, 11.24%, and 3.00%, respectively.
Compared with the control, the POD content of seedling leaves decreased by 62.62% on the first day and increased by 160.74% on the third day after B. cereus treatment. POD content in leaves gradually increased on the third and fifth days after NaCl treatment, which increased by 197.78% and 45.16% compared with the control, respectively. Under salt stress, B. cereus treatment significantly increased POD content in seedling leaves by 113.38%, 38.81% and 52.89%, respectively, compared with salt stress. On the first three days of B. cereus treatment, there was no significant difference in POD content in seedling roots compared with the control group, but on the fifth day, it was significantly increased by 51.35% compared with the control group. Salt stress significantly increased POD content in roots on the fifth day after treatment, which increased by 17.29% compared with the control. Under salt stress, the POD content in seedling roots increased significantly at 3 d and 5 d after treatment with B. cereus, which increased by 39.71% and 43.12% compared with salt stress, respectively.
Compared with the control, the CAT content in seedling leaves decreased by 10.61% on the first day and increased by 18.6% on the third day after B. cereus treatment. At 3 d and 5 d after NaCl treatment, CAT content in seedling leaves increased by 36.47% and 23.81% compared with the control. Compared with salt stress, inoculation of B. cereus under salt stress increased CAT content in seedling leaves by 2.91%, 8.50%, and 25.55%, respectively. B. cereus increased the CAT content in seedling roots and reached the peak at 5 d after treatment, which was 125.10% higher than that of the control. Compared with the control, salt stress increased CAT content in seedling roots by 71.88%, 25.93%, and 51.01%, respectively. Under salt stress, the CAT content in seedling roots increased on the third and fifth days after treatment with B. cereus, which increased by 30.59% and 80.45%, respectively, compared with that under salt stress.

3.9. Effect of B. cereus on the Content of Proline in Cucumber Seedlings under Salt Stress

As shown in Figure 8, compared with the control, the proline content in the leaves of seedlings decreased by 51.83% and 17.34% in the first three days after B. cereus treatment, and increased by 26.58% on the fifth day after treatment. Salt stress significantly increased proline content in seedling leaves and peaked at 5 d after treatment, which increased by 58.55% compared with the control. Under salt stress, the proline content in leaves of seedlings treated with B. cereus decreased on the fifth day after treatment, which was 13.12% lower than that under salt stress. After B. cereus treatment, the proline content in the roots of seedlings increased first and then decreased, reaching the peak on the third day, which was reduced by 32.84% compared with the control. Compared with the control, the proline content in seedling roots increased by 230.16%, 54.46%, and 324.28% on the first, third, and fifth days after NaCl treatment. Under salt stress, the proline content in roots increased first and then decreased. Compared with salt stress, the proline content decreased by 44.94% and 60.08% on the third and fifth days after treatment.

4. Discussion

As a global problem, soil salinization is one of the main abiotic stresses limiting crop growth, yield, and quality, hindering the sustainable development of modern agriculture. The results showed that B. cereus significantly improved plant height, stem diameter, dry weight, fresh weight, chlorophyll content, and photosynthetic capacity of rice, wheat, tomato, and other crops under stress, and ensured yield and quality while enhancing crop resistance [27,28]. PGPR plays an increasingly prominent role in promoting plant growth and development and improving plant stress resistance [3,29]. Ajilogba et al. [30] showed that the fresh and dry weight of tomato plants were significantly increased after inoculation with B. cereus, and the fruit quality improved. Ate et al. [28] isolated B. cereus from the rhizosphere of wheat increased the stem length and root length of wheat, alleviated salt stress by affecting Na+, K+, and Ca2+, and promoted the growth of wheat. Vishal et al. [31] showed that B. cereus improved the root environment of mung beans, promoted root growth, and significantly reduced the inhibition of salt stress on mung bean growth. In this experiment, although B. cereus had no significant indigenous effect on the growth indexes of cucumber seedlings under normal conditions, the plant height, stem diameter, dry weight, and fresh weight of cucumber seedlings under salt stress increased significantly after inoculation with B. cereus. In addition, the root vitality of seedlings under normal growth conditions was significantly increased on the first day after inoculation with B. cereus. Although it decreased in the next few days after treatment, it was always higher than in the treatment group. Root vitality of cucumber seedlings under salt stress was also significantly enhanced after inoculation with B. cereus. These results indicated that inoculation of B. cereus increased the growth index of cucumber seedlings under salt stress, and a good growth index was inseparable from stable photosynthesis. Therefore, B. cereus may improve the salt tolerance of cucumber seedlings by improving the photosynthesis of cucumber seedlings under salt stress.
Photosynthesis converts CO2 and H2O into organic matter, which is the basis for crop biomass and yield [32]. In this study, B. cereus significantly increased the dry weight and fresh weight of seedlings under salt stress, indicating that the inoculation of B. cereus may enhance the photosynthesis of seedlings under salt stress, thereby promoting the accumulation of biomass. The gas exchange parameters of cucumber seedlings were studied. It was found that salt stress significantly inhibited the photosynthetic performance of cucumber seedlings. In contrast, the net photosynthetic rate, intercellular CO2 concentration, stomatal conductance, and transpiration rate of cucumber seedlings inoculated with B. cereus under salt stress were significantly increased, and the photosynthetic ability was improved considerably, which verified the previous speculation. Cardoso et al. [33] showed that the CO2 assimilation, stomatal conductance, transpiration rate, and cis-carboxylation efficiency of coconut seedlings inoculated with B. cereus increased significantly, which was consistent with the results of this study. Chlorophyll is an essential pigment for light energy conversionand transmission in plants, which is closely related to photosynthesis. Therefore, the change of chlorophyll content directly affects the photosynthesis of plants. When cucumber seedlings were subjected to salt stress, chlorophyll a, chlorophyll b, and total chlorophyll contents decreased significantly. The decrease in chlorophyll content will also destroy the function of the photosystem I and photosystem II in the chloroplast, thus affecting the photochemical efficiency of plants. In this study, after cucumber seedlings were treated with 150 mM NaCl solution, Fv/Fm, ΦPSII, and light protection index Y (NPQ) decreased significantly, and light damage index Y (NO) increased significantly, indicating that salt stress caused severe damage to the photosystem of cucumber seedlings. Under salt stress, the chlorophyll content and chlorophyll fluorescence parameters of cucumber seedlings inoculated with B. cereus were significantly improved, which effectively promoted the photosynthesis of seedlings. Alkahtani et al. [34] showed that Bacillus thuringiensis significantly increased chlorophyll content and chlorophyll fluorescence parameter (Fv/Fm) of sweet pepper under salt stress; this is the same as our research results. Chen et al. [27] proved that the net photosynthetic rate, gas exchange parameters, and chlorophyll fluorescence parameters of rice inoculated with B. cereus under drought stress changed to beneficial to plant growth. The light conversion efficiency of leaves was significantly improved. The degradation and reduction in chlorophyll were significantly inhibited, which promoted rice photosynthesis and alleviated the damage of drought stress on rice. The above results showed that B. cereus played an important role in alleviating the damage of stress to crops by improving the photosynthesis of crops under different stresses. It is worth noting that chloroplasts are important organelles that produce ROS [35]. The production and removal of ROS maintain a dynamic balance under normal conditions, but when plants are stressed, this balance is disturbed, and a large number of ROS accumulation destroys the normal function of plants. Therefore, the effect of B. cereus on the chlorophyll of seedlings will further affect the change of ROS and improve the growth of seedlings under salt stress by regulating the change of ROS.
A large amount of H2O2 and MDA rapidly accumulated in plants under stress could be significantly reduced after PGPR treatment. Studies by He et al. [36] showed that the H2O2 and MDA contents of Haloxylon ammodendron decreased significantly after inoculation with B. cereus and Pseudomonas under drought stress. It is well known that plants remove harmful substances produced by stress through antioxidant substances, such as SOD, POD, and CAT, to maintain homeostasis in plants. In this study, salt stress significantly increased the contents of H2O2 and MDA in the leaves and roots of cucumber seedlings. With the increase in B. cereus treatment time, SOD, POD, and CAT activities in cucumber seedlings increased gradually under salt stress. The levels of H2O2 and MDA decreased, which effectively reduced the damage of reactive oxygen species to plant cells. Islam et al. [37] also obtained the same results with mung bean plants as experimental materials. Under salt stress, SOD, POD, and CAT activities in mung bean plants inoculated with B. cereus increased significantly. The contents of MDA and H2O2 decreased significantly, which enhanced the salt tolerance of mung beans. Not only that, Bacillus can improve the soil environment, enhance the plant antioxidant system and alleviate the damage of drought on plants [38]. These results showed that B. cereus could enhance the resistance of plants to stress by improving the antioxidant system of plants. As a very effective antioxidant, proline scavenges peroxides in vivo by synergistic action with the antioxidant enzyme system [39]. Under normal conditions, the production and degradation of proline are in a dynamic equilibrium, and H2O2 induced by salt stress inhibits the activity of proline dehydrogenase (ProDH), thereby inhibiting the degradation of proline and the proline content increased significantly [40]. In this study, the contents of H2O2 and proline in cucumber seedlings under salt stress were significantly decreased after inoculation with B. cereus, indicating that B. cereus broke the inhibition of H2O2 on proline degradation and maintained the proline content in a dynamic equilibrium state. Moreover, the proline content of cucumber seedlings grown under normal conditions also decreased at some time points after inoculation with B. cereus. On the other hand, it also showed that the inoculation of B. cereus improved the osmotic environment in plants and did not require excessive proline for regulation. El-Esawi et al. [41] showed that Bacillus firmus significantly reduced the content of proline, H2O2, and MDA in soybean under salt stress, effectively alleviated the damage of peroxide on the cell membrane, and improved considerably the growth and production performance of soybean under salt stress. Moreover, the inoculation of Lysinibacillus fusiform and Bacillus amyloliquefaciens reduced the electrolyte leakage, proline content, and H2O2 content of lentils under drought stress, significantly improved cell membrane stability, and significantly increased the yield of lentils under drought stress [42].

5. Conclusions

Under salt stress, the application of B. cereus significantly improved photosynthetic capacity and enhanced the antioxidant metabolism of cucumber seedlings, thereby reducing the accumulation of reactive oxygen species in the plants. In addition, B. cereus can reduce the accumulation of proline in cucumber plants under salt stress, thereby promoting seedlings’ growth and improving cucumber’s salt tolerance. This study clarified the physiological metabolic pathway mechanism of B. cereus to enhance salt tolerance of cucumber seedlings. It provided a theoretical basis for applying of beneficial microorganisms in stress tolerance and growth promotion cultivation of protected vegetables.

Author Contributions

Conceptualization, Y.Z. and S.S.; methodology, Y.Z., M.T., Y.W., and S.S.; investigation, Y.Z. and S.S.; resources, H.L. and S.S.; data curation, Y.Z.; writing—original draft preparation, Y.Z.; writing—review and editing, M.S.J. and S.S; supervision, J.W., S.G., and S.S.; project administration, S.S.; funding acquisition, T.S., X.L., and S.S. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the National Natural Science Foundation of China (No.32072649), sponsored by the Independent Innovation Fund of Ningxia Hui Autonomous Region Agricultural Science and Technology (NGSB-2021-8-02), sponsored by Jiangsu Province North Jiangsu Science and Technology Project (SZ-SQ202062), and sponsored by Priority Academic Program Development of Jiangsu Higher Education Institutions (PDPA).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

Thank my tutor for the strong support of my research content. Thank the professors and colleagues in the laboratory for their help in my research.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Survival of B. cereus in media with different NaCl concentrations.
Figure 1. Survival of B. cereus in media with different NaCl concentrations.
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Figure 2. Effects of B. cereus on the phenotype (A) and growth (B) of cucumber seedlings under salt stress. Bars represent standard errors. Different letters indicate a significant difference in the same parameter between treatments at p < 0.05.
Figure 2. Effects of B. cereus on the phenotype (A) and growth (B) of cucumber seedlings under salt stress. Bars represent standard errors. Different letters indicate a significant difference in the same parameter between treatments at p < 0.05.
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Figure 3. Effect of B. cereus on the root vitality of cucumber seedlings under salt stress. Bars represent standard errors. Different letters indicate a significant difference in the same parameter between treatments at p < 0.05.
Figure 3. Effect of B. cereus on the root vitality of cucumber seedlings under salt stress. Bars represent standard errors. Different letters indicate a significant difference in the same parameter between treatments at p < 0.05.
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Figure 4. Effect of B. cereus on photosynthetic performance of cucumber seedlings under salt stress. Bars represent standard errors. Different letters indicate a significant difference in the same parameter between treatments at p < 0.05.
Figure 4. Effect of B. cereus on photosynthetic performance of cucumber seedlings under salt stress. Bars represent standard errors. Different letters indicate a significant difference in the same parameter between treatments at p < 0.05.
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Figure 5. Effects of B. cereus on chlorophyll fluorescence imaging (A) and chlorophyll fluorescence parameters (B) of cucumber seedlings under salt stress. Bars represent standard errors. Different letters indicate a significant difference in the same parameter between treatments at p < 0.05.
Figure 5. Effects of B. cereus on chlorophyll fluorescence imaging (A) and chlorophyll fluorescence parameters (B) of cucumber seedlings under salt stress. Bars represent standard errors. Different letters indicate a significant difference in the same parameter between treatments at p < 0.05.
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Figure 6. Effects of B. cereus on contents of MDA and H2O2 in cucumber seedlings under salt stress. Bars represent standard errors. Different letters indicate a significant difference in the same parameter between treatments at p < 0.05.
Figure 6. Effects of B. cereus on contents of MDA and H2O2 in cucumber seedlings under salt stress. Bars represent standard errors. Different letters indicate a significant difference in the same parameter between treatments at p < 0.05.
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Figure 7. Effect of B. cereus on the antioxidant enzyme activities of cucumber seedlings under salt stress. Bars represent standard errors. Different letters indicate a significant difference in the same parameter between treatments at p < 0.05.
Figure 7. Effect of B. cereus on the antioxidant enzyme activities of cucumber seedlings under salt stress. Bars represent standard errors. Different letters indicate a significant difference in the same parameter between treatments at p < 0.05.
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Figure 8. Effect of B. cereus on the content of proline in cucumber seedlings under salt stress. Bars represent standard errors. Different letters indicate a significant difference in the same parameter between treatments at p < 0.05.
Figure 8. Effect of B. cereus on the content of proline in cucumber seedlings under salt stress. Bars represent standard errors. Different letters indicate a significant difference in the same parameter between treatments at p < 0.05.
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Table
Table 1. Effect of B. cereus on the chlorophyll content of cucumber seedlings under salt stress. Different letters indicate a significant difference in the same parameter between treatments at p < 0.05.
Table 1. Effect of B. cereus on the chlorophyll content of cucumber seedlings under salt stress. Different letters indicate a significant difference in the same parameter between treatments at p < 0.05.
TimeTreatmentsChl a
(mg·g−1)		Chl b
(mg·g−1)		Total Chl
(mg·g−1)
1 dCont23.95 ± 1.55 a7.37 ± 0.46 a31.32 ± 2.01 a
BS23.33 ± 1.44 a7.19 ± 0.48 a30.51 ± 1.92 a
NaCl22.94 ± 1.63 a7.12 ± 0.51 a30.05 ± 2.14 a
NaCl + BS21.13 ± 1.59 a6.48 ± 0.53 a27.62 ± 2.12 a
3 dCont23.69 ± 1.21 a7.12 ± 0.34 a30.81 ± 1.54 a
BS21.84 ± 0.98 ab6.60 ± 0.33 ab28.44 ± 1.30 ab
NaCl16.22 ± 1.88 c4.74 ± 0.68 c20.96 ± 2.56 c
NaCl + BS19.59 ± 2.03 b5.72 ± 0.57 b25.31 ± 2.59 b
5 dCont22.29 ± 1.63 a6.73 ± 0.53 a29.01 ± 2.16 a
BS21.02 ± 1.24 a6.73 ± 0.69 a27.75 ± 1.04 a
NaCl10.09 ± 0.75 c3.04 ± 0.23 c13.14 ± 0.97 c
NaCl + BS15.95 ± 0.21 b4.57 ± 0.08 b20.52 ± 0.29 b
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Zhou, Y.; Sang, T.; Tian, M.; Jahan, M.S.; Wang, J.; Li, X.; Guo, S.; Liu, H.; Wang, Y.; Shu, S. Effects of Bacillus cereus on Photosynthesis and Antioxidant Metabolism of Cucumber Seedlings under Salt Stress. Horticulturae 2022, 8, 463. https://0-doi-org.brum.beds.ac.uk/10.3390/horticulturae8050463

AMA Style

Zhou Y, Sang T, Tian M, Jahan MS, Wang J, Li X, Guo S, Liu H, Wang Y, Shu S. Effects of Bacillus cereus on Photosynthesis and Antioxidant Metabolism of Cucumber Seedlings under Salt Stress. Horticulturae. 2022; 8(5):463. https://0-doi-org.brum.beds.ac.uk/10.3390/horticulturae8050463

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Zhou, Yaguang, Ting Sang, Mimi Tian, Mohammad Shah Jahan, Jian Wang, Xiangyu Li, Shirong Guo, Hongyun Liu, Yu Wang, and Sheng Shu. 2022. "Effects of Bacillus cereus on Photosynthesis and Antioxidant Metabolism of Cucumber Seedlings under Salt Stress" Horticulturae 8, no. 5: 463. https://0-doi-org.brum.beds.ac.uk/10.3390/horticulturae8050463

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