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Article

The Coupling Effects of Plant Growth Promoting Rhizobacteria and Salicylic Acid on Physiological Modifications, Yield Traits, and Productivity of Wheat under Water Deficient Conditions

by
Emad Hafez
1,*,
Alaa El Dein Omara
2 and
Alshaymaa Ahmed
3
1
Department of Agronomy, Faculty of Agriculture, Kafrelsheikh University, Kafr-Elsheikh 33516, Egypt
2
Department of Agricultural Microbiology, Soil, Water and Environment Research Institute, Agricultural Research Center (ARC), Giza 12112, Egypt
3
Department of Agricultural Microbiology, Faculty of Agriculture, Beni-Suef University, Beni-Suef 18126, Egypt
*
Author to whom correspondence should be addressed.
Agronomy 2019, 9(9), 524; https://doi.org/10.3390/agronomy9090524
Submission received: 6 August 2019 / Revised: 2 September 2019 / Accepted: 3 September 2019 / Published: 9 September 2019
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Abstract

:
Water deficit and soil infertility negatively influence the growth, nutrient uptake, and productivity of wheat. Plant growth promoting rhizobacteria (PGPR) and salicylic acid (SA) were evaluated as possible solutions to mitigate the impacts of water deficit on growth, physiology, productivity, and nutrient uptake of wheat (Triticum aestivum L. cv. Sakha 95). Over two growing seasons (2016/2017 and 2017/2018) field experiments were conducted to examine eight combinations of two water treatments (water deficit and well-watered) with four soil and foliar treatments (control, PGPR, SA, and combination of PGPR + SA). The application of PGPR increased soil microbial activity resulting in increased field capacity and available soil water. Likewise, the application of the combined treatment of PGPR and SA significantly increased chlorophyll content, relative water content, stomatal conductance, soil microbial population, and showed inhibitory impacts on proline content, thus improving yield-related traits, productivity, and nutrient uptake (N, P, K) under water deficit compared to the control treatment. The results show that the integrative use of PGPR in association with SA may achieve an efficacious strategy to attenuate the harmful effects of water deficit as well as the amelioration of productivity and nutrient uptake of wheat under water-deficient conditions.

1. Introduction

Wheat (Triticum aestivum L.) is one of the most strategic crops for food, feed, and biofuel security worldwide [1]. It is grown yearly on about 215 M ha worldwide with a production of 733.40 Mt in 2018 [2]. In Egypt, the cultivated area of wheat grown during 2018 was 1.28 M ha with a production of 9.00 Mt, which is about 20% of the total cultivated agricultural land [2]. Wheat is providing as much as half of all calories consumed in the region. By 2050 consumers will require 60% more wheat than today [3]. Rapid population growth is applying great pressure to increase wheat production. Wheat productivity can be enhanced through better management of soil, water, and plants [4]. It is for these reasons that increasing wheat productivity is an extremely crucial area of research.
Water deficit has been, for a long time, the main environmental factor that impedes plant growth and crop productivity globally [5]. Roughly 1.2 billion people are living with severe water deficit, and the water-limited regions are constantly expanding [6]. Out of the total water use in the world, about 70% is used by the agricultural sector. In Africa, about 90% of the water goes towards agriculture [7]. Water deficit is detrimental to plant growth and yield productivity, which rely substantially on irrigated ecosystems [8]. Therefore, there is an imminent need to increase wheat production under water deficit. At present and more so in the future, the increment of water deficit will result in a greater focus on ameliorating excessive water use by introducing more efficient farming practices that will increase wheat production [9,10,11]. Therefore, good agricultural operation along with effective inputs and technology use, such as seed inoculation by PGPR and/or foliar spraying by salicylic acid, is one of the best tools to improve physiological processes and plant performance under water deficit conditions.
Over the last few decades, a cascade of debate has focused on excess dosages of chemical fertilizers, which has a detrimental impact on ecosystems and human health [12]. Nutrients uptake was also found to be closely related to water uptake. Water deficit conditions diminish leaf relative water content, resulting in a decline in nutrient uptake and wheat productivity [13]. We can lessen the negative impact of water deficit and thereby, help to make production more eco-friendly through the use of plant growth promoting rhizobacteria (PGPR). PGPR are the inhabitant microorganisms in the rhizosphere, improving many functions related to plant growth and development [12,13]. When the PGPR are inoculated into the soil, they enhance the plant’s tolerance to water deficit, hasten nutrient uptake, and increase soil moisture content [14]. PGPR are also an economically viable and cost-effective strategy [15].
Salicylic acid (SA) is a synthetic plant growth regulator which is important for growth and productivity [16]. SA is the major solute involved in cell osmotic water uptake [17], the maintenance of cell turgor pressure, and the regulation of stomatal opening [18]. A main physiological impact of SA is increasing internal CO2 exchange during photosynthesis. Reasonable SA application can improve a crop’s tolerance to water deficit [13]. It has also been proved that SA decreases the plant’s susceptibility to water deficit and that plants with adequate internal SA levels have better-hydrated tissues than those with SA deficiency [19]. The role of SA in increasing the drought tolerance of crops has raised considerable interest during recent decades [20]. Foliar application of salicylic acid was stimulatory to improve nutritional status in wheat and further strengthen the efficacious impact of PGPR on shoot growth [19]. Hence, the integrative use of PGPR in association with SA could be a sustainable alternative to alleviate water deficient-induced damage and increase crop productivity to wheat plants. Consequently, this research was implemented to estimate the individual role of PGPR and SA as well as the combination of PGPR and SA on soil moisture constants, physiological modifications, nutrient uptake, yield traits, and productivity in water-stressed wheat.

2. Materials and Methods

Two field experiments were conducted at the experimental farm of the Faculty of Agriculture, Kafrelsheikh University, Egypt, during growing seasons 2016/2017 and 2017/2018 to study the effects of inoculation with plant growth promoting rhizobacteria (Azospirillum brasilense SARS 1001 and Azotobacter chrococcum SARS 302) and foliar spray of salicylic acid on physiological modifications and productivity in wheat plants under water-deficient conditions. The meteorological data of the study area during the growing seasons are presented in Table 1. Clayey soil was used, and some physicochemical properties are shown in Table 2.
The experiment was conducted as a split-plot randomized complete block design with three replicates during both seasons. Irrigation treatments were considered as main-plots with inoculation and foliar spray treatments as sub-plots. Main-plots were water deficit (irrigation twice at sowing and stem elongation stages) and well-watered (irrigation four times at sowing, stem elongation, booting, and reproductive stages) treatments. Sub-plots were inoculated with PGPR (Azospirillum brasilense SARS 1001 and Azotobacter chrococcum SARS 302), foliar spraying treatment of salicylic acid (SA) at the rate of 200 mg L−1 twice using hand atomizers and wetting agents at 45 and 60 days after sowing, or the combination treatment of PGPR plus SA.
Wheat seeds (Triticum aestivum L. cv. Sakha 95) from the Wheat Research Department, Field Crops Research Institute, Agricultural Research Centre, Giza, Egypt, were sown using a drilling method on 30 November during 2016/2017 and 1 December during 2017/2018. Each plot consisted of 20 rows, 3 m width, 3.5 m length, row spacing of 15 cm and a seeding rate 140 kg ha−1. Plots and blocks were separated by 1 m unplanted distances. The preceding cultivated crop was maize (Zea mays L.) in both seasons.
Phosphorus fertilizer was added at a rate of 360 kg ha−1 as calcium superphosphate (15.5% P2O5), and potassium fertilizer was added at a rate of 120 kg ha−1 as potassium sulfate (48% K2O) during soil tillage. Nitrogen fertilizer was added in the form of urea (46.5% N) at two different rates; 2/3 of full dose (240 kg ha−1) split into two equal doses (prior to first and second irrigations) for inoculation treatments with PGPR and full dose (360 kg ha−1) for all other treatments.
The inoculation treatments (provided from Bacteriology Lab., Sakha Agricultural Research Station, Kafr El-Sheikh, Egypt), were prepared as peat-based inoculums, 15 mL of 108 CFU mL−1 from each culture per 30 g of the sterilized carrier and mixed carefully with wheat seeds using a sticking material and spread away from direct sun over a plastic sheet for a short time before sowing. Weeds were hand-controlled continuously during wheat vegetative growth. No pesticides or fungicides were used during the experiments.
Total nitrogen and carbon percent were estimated using a Sumigraph NC analyzer (Sumigraph NC-95A; Sumika Chemical Analysis Service, Osaka, Japan). In addition, the biomass of the microbial community was determined by phospholipid fatty acids (PLFAs) using the modified method of [21], Table 3.
Using an auger, (Engineering Laboratory Manual, Department of Agricultural and Chemical Engineering, Colorado State University, CO, Fort Collins, USA) soil moisture constants were measured before sowing (Table 4) in both seasons. Field capacity, wilting point, bulk density, and available soil moisture were measured by a pressure membrane and pressure cooker apparatus for measuring moisture contents at pressures of 0.33 and 15 bar using cylindrical sharp-edged core samples for analyzing soil moisture constants as described in [22,23]. Bulk density is defined as the dry weight of soil per unit volume of soil [22]. The wilting point may be defined as the amount of water per unit weight in the soil, expressed as a percentage, that is held too tightly by the soil matrix that roots cannot absorb this water, and a plant will wilt [23].

2.1. Physiological Traits

Using an auger, soil moisture constants were measured after harvest in both seasons. Field capacity, wilting point, bulk density, and available soil moisture were measured by a pressure membrane and pressure cooker apparatus for measuring moisture contents at pressures of 0.33 and 15 bar using cylindrical sharp-edged core samples for analyzing soil moisture constants as described in [22,23]. A SPAD meter (Model: SPAD-502, Minolta Sensing Ltd., Hangzhou, Japan) was used for measuring chlorophyll content from the topmost fully expanded leaves on the main stem at the flowering stage (BBCH stage 61), [24]. SPAD values were recorded from ten plants within each plot, and then the readings were values averaged per plot.
Relative water content (RWC) was analyzed gravimetrically from the topmost fully expanded leaves at the flowering stage (BBCH stage 61), [24], between 10:00 to 12:00 a.m. The leaves were weighed immediately to get the fresh weight (FW). The leaves were subsequently rehydrated in distilled water for 24 h to get the turgid weight (TW) and dried at 60 °C in an oven for 48 h to get the dry weight (DW). Relative water content was measured according to the following formula:
R W C   ( % ) = [ ( F W − D W ) / ( T W − D W ) ] × 100 .
Stomatal conductance (gs) was measured on fully expanded flag leaves from the abaxial surface as mmol H2O m−2 s−1 from three plants in each plot with a dynamic diffusion porometer (Delta-T AP4, Delta-T Devices Ltd., Cambridge, UK) on fine days. Two measurements from both adaxial and abaxial surfaces of the leaf were taken. Conductance was measured on days with favorable conditions (following weather) every 4 or 7 days from booting till harvest with a porometer [25]. Measurement on the top leaf and front (ra) and back side (rb) of the center of the leaf were taken
Total leaf conductance (rl) is 1/rl = 1/ra + 1/rb.
The free proline content in the leaves was determined following the method in [26]. Leaf samples (0.5 g) were homogenized in 5 mL of sulfosalicylic acid (3%) using a mortar and pestle. About 2 mL of extract was placed in test tubes, and then 2 mL of glacial acetic acid and 2 mL of ninhydrin reagent were added. The reaction mixture was boiled at 100 °C for 60 min. After cooling the reaction mixture, 6 mL of toluene was added, and then the mixture was transferred to a separating funnel. After thorough mixing, the chromophore containing toluene was separated, and absorbance was measured at 520 nm in a spectrophotometer against a toluene blank. Proline concentration was determined using a calibration curve.

2.2. Bacteriological Analysis

Total nitrogen-fixing bacteria was determined in rhizosphere wheat plant samples at 30, 60, and 90 days after sowing as well as at harvest using combined carbon medium Free-living putative nitrogen-fixing bacteria [27], which contained: Solution I: K2HPO4, 0.8 g; KH2PO4, 0.2 g L−1; Na2Fe EDTA, 28.0 mg; Na2MoO4.2H2O, 25.0 mg; NaCl, 0.1 g; yeast extract, 0.1 g; mannitol, 5.0 g; sucrose, 5.0 g; Na-lactate (60% v = v), 0.5 mL; distilled water, 900 mL; agar, 15.0 g. Solution II: MgSO4.7H2O, 0.2 g; CaCl2, 0.06 g; distilled water, 100 mL. Solution III: Biotin, 5.0 mg mL−1; paminobenzoic acid (PABA), 10:0 mg mL−1. Solutions I and II were adjusted to pH 7 and autoclaved at 121 °C for 15 min, cooled to 48 °C and mixed thoroughly, (filter sterilized using a sterile 0.45 mm filter) 1 mL L−1 of solution III.

2.3. Yield and Related Traits

Plants 3.0 m2 from the middle of each plot were harvested, and the number of spikes from each plot were carefully counted and averaged to determine the number of spikes m−2. The average number of spikelet’s spike−1 and of grains spike−1 was determined from ten randomly selected spikes. Five random samples of 1000 grains were taken, weighed, and averaged to calculate 1000-grain weight. At harvest maturity, each plot was harvested manually, sun-dried for three days and tied into bundles. These bundles were then threshed manually, and grains were separated and weighed. Grain moisture was measured, and yield was converted into yield per hectare at a standard moisture of 14%. Leftover straw was again weighed to record straw yield. Grain and straw yields were converted into ton ha−1. Harvest index (HI) was determined as the ratio between grain and biological yield and was expressed in percentage.

2.4. Nutrient Uptake

Uptake of N, P, and K was calculated by multiplying the percentage of each element (nitrogen, phosphorus, and potassium) present in dry grain and straw biomass to calculate total nitrogen uptake (kg ha−1), total phosphorus uptake (kg ha−1), and total potassium uptake (kg ha−1). Elemental nitrogen was determined by using the Macro–Kjeldahl technique according to [28]. Whereas, elemental phosphorus and potassium were determined according to [29,30], respectively.

2.5. Statistical Analysis

Data obtained were subjected to analysis of variance (ANOVA) procedures according to [31], using the MSTAT-C Statistical Software package (https://msu.edu/~freed/mstatc.htm) significant differences (p < 0.05).

3. Results

Water deficit treatment significantly (p ≤ 0.05) decreased the yield traits and productivity of wheat plants compared to well-watered treatment in the two growing seasons (Table 5, Table 6 and Table 7). In this study, soil moisture constants, physiological modifications, yield traits, productivity, and nutrient uptake showed significant differences in response to plant growth promoting rhizobacteria (PGPR) and salicylic acid (SA) applications under water deficit (Figure 1, Figure 2, Figure 3 and Figure 4); (Table 5, Table 6 and Table 7).

3.1. Effect of Soil and Foliar Treatments on Soil Moisture Constants under Water Deficit

The findings revealed that application of PGPR, SA, and the combination of PGPR and SA led to significant impacts of the soil physical characteristics under water treatments (Figure 1). Under the water deficit irrigation treatment and for the first year, field capacity increased 18.5%, 15.3%, and 32.2% in response to PGPR, SA, and the combination of (PGPR + SA), respectively, compared to the untreated plants (control) (Figure 1). Enhanced field capacity directly affected the wilting point which decreased to 8.2%, 6.6%, and 11.9% for PGPR, SA, and PGPR + SA, respectively, compared to the untreated plants.

3.2. Effect of Soil and Foliar Treatments on Physiological Traits under Water Deficit

Chlorophyll content, relative water content, and stomatal conductance of wheat were significantly reduced while proline content increased under water deficit (Figure 2 and Figure 3). The chlorophyll content observed under the well-watered treatment was higher than the chlorophyll content observed under the water deficit treatment in both seasons (Figure 2). However, impacts of water deficit were mitigated significantly when wheat plants were treated with the PGPR, SA, or their combination (Figure 2). Under water deficit, chlorophyll content in plants treated with either the combination of SA and PGPR, just SA or just PGPR increased by 16.6%, 14.45%, and 9.09% in the first season, respectively (Figure 2). In the second season, chlorophyll content increased by 13.9%, 12.2%, and 7.1% for plants treated with either the combination of SA and PGPR, just SA, or just PGPR, respectively, compared to the untreated plants (control) under water deficit, (Figure 2).
The plants exposed to water deficit and treated with combination (PGPR + SA) did not differ significantly with regards to RWC, stomatal conductance, and proline content compared to well-watered plots without any soil or foliar treatments during either growing season (Figure 3).
Untreated plants had the lowest leaf RWC under water deficit with 62.96% and 65.35% for seasons one and two, respectively. Leaf RWC increased to 75.65% and 77.45% with the PGPR treatment, 81.22% and 85.62% with the SA treatment, and 84.65% and 87.35% with the combination treatment under water deficit. However, well-watered plants without soil and foliar treatments maintained leaf RWC of 82.55% and 85.66% in seasons one and two, respectively (Figure 3).
Furthermore, data presented in (Figure 3) indicated that stomatal conductance under water deficit was lowest 41.23 and 43.65 mmol m−2 s−1 for untreated plants (control) in both seasons. While stomatal conductance increased to 44.59 and 46.96 mmol m−2 s−1 with the PGPR treatment, 48.34 and 49.55 mmol m−2 s−1 with the SA treatment, and 50.20 and 51.66 mmol m−2 s−1 with the combination treatment. Well-watered plants without soil or foliar treatments displayed conductance rates of 48.87 and 49.36 mmol m−2 s−1 for seasons one and two, respectively (Figure 3).
On the other hand, under water deficit, proline content was highest, 41.23 and 43.65 μ mol proline g−1 FW, in untreated plants (control) in seasons one and two, respectively. Proline content decreased to 44.59 and 46.96 μ mol proline g−1 FW in the PGPR treatment, 48.34 and 49.55 μ mol proline g−1 FW in the SA treatment, and 50.20 and 51.66 μ mol proline g−1 FW in the combination treatment for seasons one and two, respectively. Well-watered plants without soil or foliar treatment maintained proline content of 48.87 and 49.36 μ mol proline g−1 FW for seasons one and two, respectively (Figure 3).

3.3. Effect of Soil and Foliar Treatments on Bacteriological Characteristics under Water Deficit

Soil microbial populations varied significantly with respect to soil and foliar treatments, water availability conditions, and at different times during the growing season. Results in Table 5 illustrate that different irrigation treatments attained differences in total counts of N2-fixing bacteria during the two growing seasons. In general, the combination treatment (inoculated with PGPR + SA) increased N2-fixing bacteria the greatest amount at all the growth stages, with recorded of 4.35, 4.98, 4.68, and 3.91 log CFU mL−1, for water deficit and 4.37, 4.89, 5.57, and 4.93 log CFU mL−1, for well-watered at 30, 60, 90 days, and harvest during the 2016/2017 growing season with a similar trend observed in the second growing season (2017/2018).
For different growth stages of the wheat plant, the higher enumeration of N2-fixing bacteria showed that 90 days after sowing recorded 4.98 and 5.57 log CFU mL−1 at 2016/2017 season and 4.69 and 5.51 log CFU mL−1 at 2017/2018 season for water deficit and well-watered irrigation treatments, respectively (Table 5).

3.4. Effect of Soil and Foliar Treatments on Yield and Related Traits under Water Deficit

Data presented in Table 6 and Table 7 indicate that yield and related traits of wheat were significantly affected by the water treatments in the two growing seasons. Water deficit treatment resulted in reduction for 1000-grain weight by 6.64% and 6.32%, number of grains spike−1 by 4.15% and 4.33%, number of spikes m−2 by 4.89% and 4.65%, and grain yield t ha−1 by 7.82% and 7.56%, straw yield t ha−1 by 3.93%and 3.87% and harvest index (%) by 3.02% and 3.16% compared to well-watered plants in both seasons (Table 6 and Table 7). However, the application of PGPR, SA, or their combination minimized the reduction in those traits when plants were exposed to water deficit. The highest 1000-grain weight, number of grains spike−1, and number of spikes m−2 were obtained by the combination treatment (PGPR + SA) with values of 46.52 g, 50.13 grains spike−1, and 350.07 spikes m−2 in the first season. SA was the next highest with values of 43.82 g, 48.67 grains spike−1, and 338.42 spikes m−2 in the first season. PGPR had the third-highest with values of 43.25 g, 48.44 grains spike−1, and 331.55 spikes m−2 in the first season. The untreated plants (control) had the lowest values with t 41.24 g, 46.72 spikes m−2, and 311.32 grains spike−1 in the first season. Data for the second growing season were consistent with those observed in the first season.
Data presented in Table 7 show that the highest grain yield t ha−1, straw yield t ha−1, and harvest index (%) were obtained by the combination treatment (PGPR or SA) with values of 7.09, 11.05, and 39.08, followed by the SA treatment with values of 6.74, 10.57, and 38.77, and then PGPR with values of 6.20, 10.12, and 38.40. The untreated plants (control) had the lowest values of 5.61, 9.59, and 36.90 for grain yield t ha−1, straw yield t ha−1, and harvest index (%), respectively in the first season. Data for the second growing season were consistent with those observed in the first season.

3.5. Effect of Soil and Foliar Treatments on Nutrient Uptake under Water Deficit

The results presented in (Figure 4) show significant influences of the water treatments and soil and foliar treatments on nitrogen, phosphorus, and potassium uptake. In this context, the combination treatment (PGPR + SA) significantly minimized the negative effects of water deficit treatment for N, P, and K uptake.
The data presented in (Figure 4) indicates that N uptake under water deficit was lowest with values of 75.68 and 78.25 kg ha−1 in untreated plants (control) for seasons one and two, respectively. Under water deficit conditions, N uptake increased to 89.75 and 90.85 kg ha−1 with the PGPR treatment, 94.65 and 97.18 kg ha−1 with the SA treatment, 105.48 and 108.35 kg ha−1 with the combination treatment for seasons one and two, respectively. Well-watered plants had values of 103.56 and 105.32 kg ha−1 without soil and foliar treatments for seasons one and two, respectively (Figure 4).
P uptake under water deficit was lowest with values of 20.35 and 20.85 kg ha−1 in untreated plants (control) for seasons one and two, respectively. Under water deficit conditions, P uptake increased to values of 26.35 and 27.04 kg ha−1 with the PGPR treatment, 30.05 and 31.22 kg ha−1 with the SA treatment, and 35.45 and 35.89 kg ha−1 with the combination treatment for seasons one and two, respectively. Well-watered plants had values of 34.88 and 35.66 kg ha−1 without soil and foliar treatments for seasons one and two, respectively (Figure 4).
The data presented also show that K uptake under water deficit was lowest with values of 90.24 and 92.45 kg ha−1 in untreated plants (control) for seasons one and two, respectively. K uptake increased to values of 118.75 and 121.36 kg ha−1 with the PGPR treatment, 124.25 and 128.63 kg ha−1 with the SA treatment, and 139.86 and 142.74 kg ha−1 with the combination treatment. Well-watered plants had values of 135.76 and 139.53 kg ha−1 without soil and foliar treatments for seasons one and two, respectively (Figure 4).

4. Discussion

Soil–plant interactions are highly complex as the soil with its edaphic and biological factors provides most of the essential nutrients and water to the plant [13]. In the changing climate, plants are continuously subjected to abiotic stress, for instance, water deficit, which is a main restricting factor for agricultural production; it hinders plant growth and diminishes productivity [32]. There is a dire need to ameliorate water deficit by the use of various nutrients, which is also cost-effective. Therefore, in this study, the potential roles of seed inoculation by plant growth promoting rhizobacteria (PGPR), foliar application of salicylic acid (SA) and their combination in regulating water deficit tolerance in wheat were discussed. Our results showed that the integrative use of PGPR in association with SA achieved an efficacious strategy to attenuate the harmful effects of water deficit as well as the amelioration of productivity and nutrient uptake of wheat higher than the individual application of SA or PGPR under water-deficient conditions. Thus, an understanding of interactions between plants and both PGPR and SA having an impact on plant development and water deficit tolerance is required.
It was found that inoculation with PGPR enhanced microbial activity, leading to improved soil physical and chemical properties as well as soil moisture constants [15]. The application of PGPR can produce an exo-polysaccharide, which can play a critical role in the improvement of soil structure, soil aggregation, and therefore, improve the soil permeability and composition. This can enhance a beneficial impact to hold more water in the soil and consequently, can maintain plant growth under water stress conditions. In addition, the application of PGPR can increase soil microbial liveliness, which can subsequently lead to a decline in the soil bulk density and an increment in the soil water holding capacity under water stress conditions [33]. Salicylic acid exhibited a slight impact on soil moisture constants because it was added in our examination as a foliar application to improve the physiological processes, yield-related traits, and productivity [18,34]. The combination treatment of soil application of PGPR before planting and foliar application of SA at 45 and 60 days after sowing led to improved soil moisture constants owing to the diverse processes and systems for each substance. Seed inoculation with PGPR enhanced soil properties as well as soil moisture constants owing to the effective microbial activity and available nutrients in the soil, which resulted in enhanced root and plant growth [35]. Plants inoculated with PGPR had greater formation of a more effective root system for water absorption [14]. Foliar application of salicylic acid was stimulatory to root and shoot growth and further strengthened the efficacy of PGPR on root and shoot growth [36]. Additionally, these findings were consistent with the observations in [13], who reported that PGPR-induction can cause alterations in root architecture as well as boost root surface area and subsequently increase nutrient and water absorption. Likewise, a positive correlation between water deficit and membrane damage were witnessed by [37], and the bacterial inoculation decreased the membrane damage compared to uninoculated plants under water deficit [32,38]. Furthermore, foliar application of SA acts as a cofactor in regulating the physiological traits and therefore, ameliorating leaf water content and photosynthetic processes which resulted in the improvement in the root hairs efficiency to uptake water and enhance plant growth. Consequently, it was found that using the combination of PGPR side-by-side with SA was efficient in mitigating water deficit conditions and improving the nutritional status of plants. The results of the present study are consistent with the results of [39], which showed that foliar spraying of salicylic acid has the capability to produce enzymatic and non-enzymatic metabolites to detoxify the detrimental impacts of reactive oxygen species, produce of antioxidant compounds, and seed inoculation by microbes that can fix the nitrogen in the soil under harsh conditions.
It is noteworthy in the present examination that the integration of PGPR (soil application) alongside SA (foliar application) greatly improved the yield-related traits and wheat productivity possibly through collaboration with auxin and/or cytokinin synthesis, the increment of cell division and photosynthesis [40]. The SA further helped the PGPR inoculated plants to improve the physiological traits and photosynthetic activity through enhanced CO2 assimilation rates due to increased stomatal conductance, relative water content, and chlorophyll content under water deficit [9,41]. Furthermore, the integration between PGPR and SA reduced the proline content that accumulates under water deficit conditions resulting in osmotic adjustment, free radical scavenging, and stabilization of subcellular structures in plant cells and mitigation of the harmful impacts of water deficit [42]. Moreover, compatible solutes, such as proline, which are produced under water deficit may help plants in osmoregulation processes. A noteworthy result is the integrated treatment of PGPR and SA were more stimulatory for physiological traits than the PGPR or SA treatment alone. These studies are in line with [13], who reported the contributory role of the integration between bacterium inoculum and salicylic acid as foliar spraying in increasing cell elongation, which owing to water flow from the xylem to the adjacent elongation cells, results in strengthened mitosis and cell enlargement leading to an increase in yield-related traits and productivity. It could be summarized that PGPR and its combination with SA increased chlorophyll content in leaves could be attributed to higher availability of nutrients and increased organic matter in the rhizosphere leading to increases in 1000-grain weight, number of grains spike−1, and number of spikes m−2 due to the pivotal impact of chlorophyll on photosynthetic activity [41]. Foliar application of SA demonstrated, in the present examination, a better capability of increasing grain and straw yield than soil application of PGPR. Various reports depicted that PGPR can assist plants in tolerating water deficit, as indicated by the incremental soil aggregation and preserving of higher water potential around the roots, which in turn increased uptake of nutrients in plants exposed to water deficit [43]. These findings are in congruence with earlier reports on the impact of PGPR on water deficit tolerance in maize, sunflower [44], and wheat [45]. Furthermore, PGPR-inoculated plants were successful in increasing the nitrogen, phosphorus, and potassium uptake into plant biomass [44,46]. Under water deficit, nutrient content (N-P-K) of plant biomass was improved when plants were treated with PGPR, perhaps owing to incremental root growth and root number that exploited more soil volume for efficient absorption of available essential nutrients [47], thus leading to higher biomass production [1]. These results agree with those obtained in [48], who found that plants inoculated with PGPR in soils with a low availability of the essential elements led to increased N, P, and K uptake due to their increased content in the soil after inoculation compared to non-inoculated plants because of the pivotal impact of root morphology and expansion of the root hairs. The findings in [49], are also in accordance with our results. Similar results were documented in [33], who stated that salicylic acid assists in translocation and uptake of essential elements in plant biomass. It is inferred from the results obtained that foliar application of SA at stem elongation and booting stage has increased the yield-related traits of wheat, whereas it has been stated that SA has a positive role in increasing relative water content, stomatal conductance, and decreasing proline content, leading to metabolic transport of photosynthetic assimilates to wheat grains through the impact on phloem flow [17]. Furthermore, this might be attributed to an increment of nitrogen uptake, phosphorus uptake, and potassium uptake, subsequently increasing the assimilation and dry matter accumulation in wheat plants. The highest grain yield, straw yield, and harvest index were achieved when the combination of PGPR and SA was applied. Our findings showed that the physiological, yield-related traits and yield of wheat were significantly higher with the integration between PGPR and SA followed by individual application of SA and PGPR compared to the untreated (control) treatment. The integrative use of PGPR with SA was found to be an effective strategy for the improvement of crop development and productivity under water deficit conditions.

5. Conclusions

The overall research has demonstrated that soil applications of plant growth promoting rhizobacteria (PGPR) is a promising approach for improving soil moisture constants. It is clear that PGPR enhances plant growth and water status, which could contribute to retaining water potential, thus encouraging water movement from the soil into the roots and consequently, restraint of water deficit in bacterial inoculated plant tissue. Second, foliar application through salicylic acid (SA) can proficiently induce systemic water deficit tolerance through improving physiological attributes, yield-related traits, and nutrient uptake. Hence, the integrative use of PGPR in association with SA could be a sustainable alternative to alleviate water deficient-induced damage and increase crop productivity in wheat plants. To the best of our knowledge, this is the first investigation elucidating the role of the combination of PGPR and SA in the recovery of water deficit in wheat crop. However, additional research studies are required to evaluate the economic feasibility on a large scale. Moreover, the possibility of using PGPR as a clean source for ecology and could diminish chemical fertilizer use.

Author Contributions

Planned and designed the experiment, E.H.; data curation, A.E.D.O.; analyzed the data, A.A.; All authors interpreted the results and contributed to the writing.

Funding

This research received no external funding.

Acknowledgments

Faculty of agriculture, Kafrelsheikh University, Egypt, is thankfully acknowledged for carrying out this work. Authors thank Department of Agricultural Microbiology, Soil, Water and Environment Research Institute, Agricultural Research for carrying out the analysis of the most traits. We are also grateful to Bill Payne, Professor of Crop Physiology and Dean of CABNR/NAES/UNCE and Steven Bristow at the University of Nevada, USA, for his kind help to edit the English language of the manuscript.

Conflicts of Interest

The authors declare that they have no conflict of interest.

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Agronomy 09 00524 g001 550
Figure 1. Effect of soil application by plant growth promoting rhizobacteria (PGPR), foliar application by salicylic acid (SA), and their combination on some soil moisture constants (FC = field capacity, WP = wilting point, BD = bulk density, and ASW = available soil water) of wheat plants under water deficit conditions during two growing seasons 2016/2017 and 2017/2018. WD = water deficit (two irrigations), WW = well-watered (four irrigations). The data are the mean ± SE of three replicates. (control) for the first season and under water deficit conditions (Figure 1). Inoculation treatments also affected the bulk density which reduced from 1.18 to 1.14 g cm−3, 1.18 to 1.16 g cm−3, and 1.18 to 1.10 g cm−3 for PGPR, SA, and PGPR + SA, respectively, compared to the untreated plants (control) in the first season and under water deficit conditions (Figure 1). Consequently, available soil water increased 51.8%, 44.5%, and 68.3% for PGPR, SA, and PGPR + SA, respectively, compared to the untreated plants (control) in the first season and under water deficit (Figure 1). Data for the second growing season were consistent with those in the first season (Figure 1); Mean values designed by the same letter in each column are not significant according to Duncan’s Multiple Range Test.
Figure 1. Effect of soil application by plant growth promoting rhizobacteria (PGPR), foliar application by salicylic acid (SA), and their combination on some soil moisture constants (FC = field capacity, WP = wilting point, BD = bulk density, and ASW = available soil water) of wheat plants under water deficit conditions during two growing seasons 2016/2017 and 2017/2018. WD = water deficit (two irrigations), WW = well-watered (four irrigations). The data are the mean ± SE of three replicates. (control) for the first season and under water deficit conditions (Figure 1). Inoculation treatments also affected the bulk density which reduced from 1.18 to 1.14 g cm−3, 1.18 to 1.16 g cm−3, and 1.18 to 1.10 g cm−3 for PGPR, SA, and PGPR + SA, respectively, compared to the untreated plants (control) in the first season and under water deficit conditions (Figure 1). Consequently, available soil water increased 51.8%, 44.5%, and 68.3% for PGPR, SA, and PGPR + SA, respectively, compared to the untreated plants (control) in the first season and under water deficit (Figure 1). Data for the second growing season were consistent with those in the first season (Figure 1); Mean values designed by the same letter in each column are not significant according to Duncan’s Multiple Range Test.
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Figure 2. Effect of soil application by PGPR, foliar application by SA, and their combination on chlorophyll content (SPAD Unit) of wheat plants under water deficit conditions during two growing seasons 2016/2017 and 2017/2018. WD = water deficit (two irrigations), WW = well-watered (four irrigations). The data are the mean ± SE of three replicates; Mean values designed by the same letter in each column are not significant according to Duncan’s Multiple Range Test.
Figure 2. Effect of soil application by PGPR, foliar application by SA, and their combination on chlorophyll content (SPAD Unit) of wheat plants under water deficit conditions during two growing seasons 2016/2017 and 2017/2018. WD = water deficit (two irrigations), WW = well-watered (four irrigations). The data are the mean ± SE of three replicates; Mean values designed by the same letter in each column are not significant according to Duncan’s Multiple Range Test.
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Agronomy 09 00524 g003 550
Figure 3. Effect of soil and foliar treatments on relative water content, stomatal conductance (gs), and proline content of wheat plants under water deficit conditions during two growing seasons 2016/2017 and 2017/2018. WD = water deficit (two irrigations), WW = well-watered (four irrigations). The data are the mean ± SE of three replicates; Mean values designed by the same letter in each column are not significant according to Duncan’s Multiple Range Test.
Figure 3. Effect of soil and foliar treatments on relative water content, stomatal conductance (gs), and proline content of wheat plants under water deficit conditions during two growing seasons 2016/2017 and 2017/2018. WD = water deficit (two irrigations), WW = well-watered (four irrigations). The data are the mean ± SE of three replicates; Mean values designed by the same letter in each column are not significant according to Duncan’s Multiple Range Test.
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Agronomy 09 00524 g004 550
Figure 4. Effect of soil and foliar treatments on nitrogen, phosphorus and potassium uptake (Kg ha−1) of wheat plants under water deficit conditions during two growing seasons 2016/2017 and 2017/ 2018. WD = water deficit (two irrigations), WW = well-watered (four irrigations). The data are the mean ± SE of three replicates; Mean values designed by the same letter in each column are not significant according to Duncan’s Multiple Range Test.
Figure 4. Effect of soil and foliar treatments on nitrogen, phosphorus and potassium uptake (Kg ha−1) of wheat plants under water deficit conditions during two growing seasons 2016/2017 and 2017/ 2018. WD = water deficit (two irrigations), WW = well-watered (four irrigations). The data are the mean ± SE of three replicates; Mean values designed by the same letter in each column are not significant according to Duncan’s Multiple Range Test.
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Table
Table 1. Meteorological data for the two winter growing seasons 2016/2017 and 2017/2018.
Table 1. Meteorological data for the two winter growing seasons 2016/2017 and 2017/2018.
Year Month2016/20172017/2018
Temperature (°C)Precipitation (mm)RH (%)Temperature (°C)Precipitation (mm)RH (%)
MaxMinMaxMin
Dec26.911.40.8030.724.910.90.6032.6
Jan23.59.43.5041.422.29.73.3043.1
Feb22.011.07.0045.120.812.77.6044.2
Mar24.016.20.0047.922.514.70.5045.4
April27.417.20.0055.425.716.10.0053.1
May31.917.80.0064.130.315.40.0065.8
RH, Relative humidity.
Table
Table 2. Some physicochemical properties of soil used in the two winter growing seasons 2016/2017 and 2017/2018.
Table 2. Some physicochemical properties of soil used in the two winter growing seasons 2016/2017 and 2017/2018.
Cations (meq L−1)Anions (meq L−1)
SeasonO.M (%)EC (dS m−1)pHNa+K+Mg++Ca++Cl−CO3−HCo3−So4−
2016/20171.301.048.057.780.734.766.5410.560.04.225.03
2017/20181.390.897.987.650.865.237.2910.210.03.677.15
O.M. Organic Matter; pH (1:2.5); EC (electrical conductivity) and ions based (1:5).
Table
Table 3. Total nitrogen, carbon, and biomass of microbial community of soil used in the two winter growing seasons 2016/2017 and 2017/2018.
Table 3. Total nitrogen, carbon, and biomass of microbial community of soil used in the two winter growing seasons 2016/2017 and 2017/2018.
SeasonTotal Nitrogen (%)Total Carbon (%)BacteriaFungiActinomycetes
(µg g Dry Soil−1)
2016/20170.53047113.5187754.57917.4253.222
2017/20180.67543814.7687358.34218.3233.876
Table
Table 4. The mean values of soil moisture constants of the experimental site before cultivation.
Table 4. The mean values of soil moisture constants of the experimental site before cultivation.
Soil Depth (cm) Field Capacity (%)Wilting Point (%)Bulk Density (g cm−3)Available Soil Water (%)
2016/20172017/20182016/20172017/20182016/20172017/20182016/20172017/2018
0–2042.2644.0122.9721.711.221.3419.2925.79
20–4039.2941.3321.3020.961.271.2717.9920.37
40–6038.0039.2120.2120.331.321.2217.7918.88
Mean39.8541.5221.4921.001.271.2718.3521.68
Table
Table 5. Total count (Log CFU mL−1) of N2-fixing bacteria as affected by inoculation with plant growth promoting rhizobacteria (PGPR) and foliar spray with salicylic acid (SA) and their combination under water deficit conditions during 2016/2017 and 2017/2018 seasons.
Table 5. Total count (Log CFU mL−1) of N2-fixing bacteria as affected by inoculation with plant growth promoting rhizobacteria (PGPR) and foliar spray with salicylic acid (SA) and their combination under water deficit conditions during 2016/2017 and 2017/2018 seasons.
Treatment2016/20172017/2018
WD 306090Harvest306090Harvest
Control3.83c4.16d3.74c2.16c3.75c4.06c3.72c2.16d
PGPR4.3b4.75b4.11b3.57b4.27b4.49b4.16b3.60b
SA3.84c4.45c3.76c2.18c3.76c4.04c3.86c3.13c
Combination4.35a4.68a4.98a3.91a4.41a4.68a4.69a3.96a
F-Test****************
WWControl3.87c4.22d4.38c3.98c3.87c4.24d4.42c3.52d
PGPR4.28b4.81b5.23b4.71b4.23b4.81b5.42b4.67b
SA3.81c4.54c4.42c4.05c3.83c4.60c4.44c4.09c
Combination4.37a4.89a5.57a4.93a4.39a4.91a5.51a4.85a
F-Test****************
Mean values designed by the same letter in each column are not significant according to Duncan’s Multiple Range Test, WD = water deficit (two irrigations), WW = well-watered (four irrigations), Control = without soil and foliar treatments, PGPR= Plant growth-promoting rhizobacteria, SA = Salicylic acid (200 mg L−1), Combination = PGPR + SA, ** = p ≤ 0.01.
Table
Table 6. Yield traits of wheat as affected by PGPR, SA, and their combination in 2016/2017 and 2017/2018 seasons.
Table 6. Yield traits of wheat as affected by PGPR, SA, and their combination in 2016/2017 and 2017/2018 seasons.
Treatments1000-Grain Weight (g)Number of Grains Spike−1Number of Spikes m−2
2016/20172017/20182016/20172017/20182016/20172017/2018
Water treatments (W)
WD42.22b42.71b47.36b47.56b324.51b324.24b
WW45.18a45.55a49.62a49.70a341.17a344.11a
F-Test************
Soil and foliar treatments (SF)
Control41.24c41.83d46.72c46.85c311.32d313.12d
PGPR43.25b43.73b48.44b48.61b331.55c334.11c
SA43.82b44.11b48.67b48.77b338.42b338.51b
Combination46.52a46.85a50.13a50.30a350.07a350.97a
F-Test************
Interaction (W × SF)******** ****
Mean values designed by the same letter in each column are not significant according to Duncan’s Multiple Range Test, WD = water deficit (two irrigations), WW = well-watered (four irrigations), Control = without soil and foliar treatments, PGPR= Plant growth-promoting rhizobacteria, SA = Salicylic acid (200 mg L−1), Combination = PGPR + SA, ** = p ≤ 0.01.
Table
Table 7. Yield of wheat as affected by PGPR, SA, and their combination in 2016/2017 and 2017/2018 seasons.
Table 7. Yield of wheat as affected by PGPR, SA, and their combination in 2016/2017 and 2017/2018 seasons.
TreatmentsGrain Yield (ton Ha−1)Straw Yield (ton Ha−1)Harvest Index (%)
2016/20172017/20182016/20172017/20182016/20172017/2018
Water treatments (W)
WD6.15b6.13b10.17b10.21b37.71b37.59b
WW6.67a6.77a10.49a10.55a38.86a39.08a
F-Test************
Soil and foliar treatments (SF)
Control5.61d5.64d9.59d9.63d36.90d36.93d
PGPR6.20c6.25c10.12c10.18c38.40c38.45c
SA6.74b6.77b10.57b10.59b38.77b38.83b
Combination7.09a7.15a11.05a11.12a39.08a39.13a
F-Test************
Interaction (W × SF)************
Mean values designed by the same letter in each column are not significant according to Duncan’s Multiple Range Test, WD = water deficit (two irrigations), WW = well-watered (four irrigations), Control = without soil and foliar treatments, PGPR = Plant growth-promoting rhizobacteria, SA = Salicylic acid (200 mg L−1), Combination = PGPR + SA, ** = p ≤ 0.01.

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Hafez, E.; Omara, A.E.D.; Ahmed, A. The Coupling Effects of Plant Growth Promoting Rhizobacteria and Salicylic Acid on Physiological Modifications, Yield Traits, and Productivity of Wheat under Water Deficient Conditions. Agronomy 2019, 9, 524. https://doi.org/10.3390/agronomy9090524

AMA Style

Hafez E, Omara AED, Ahmed A. The Coupling Effects of Plant Growth Promoting Rhizobacteria and Salicylic Acid on Physiological Modifications, Yield Traits, and Productivity of Wheat under Water Deficient Conditions. Agronomy. 2019; 9(9):524. https://doi.org/10.3390/agronomy9090524

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Hafez, Emad, Alaa El Dein Omara, and Alshaymaa Ahmed. 2019. "The Coupling Effects of Plant Growth Promoting Rhizobacteria and Salicylic Acid on Physiological Modifications, Yield Traits, and Productivity of Wheat under Water Deficient Conditions" Agronomy 9, no. 9: 524. https://doi.org/10.3390/agronomy9090524

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