Next Article in Journal
Effect of the Nonpathogenic Strain Fusarium oxysporum FO12 on Fe Acquisition in Rice (Oryza sativa L.) Plants
Next Article in Special Issue
Plant-Growth-Promoting Bacteria
Previous Article in Journal
Inequality Measure of Leaf Area Distribution for a Drought-Tolerant Landscape Plant
Previous Article in Special Issue
Plant Growth-Promoting Rhizobacteria Improve Rice Response to Climate Change Conditions
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Plants
Volume 12
Issue 17
10.3390/plants12173141
plants-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Effect of Co-Application of Azospirillum brasilense and Rhizobium pisi on Wheat Performance and Soil Nutrient Status under Deficit and Partial Root Drying Stress

by
Bushra Ahmed Alhammad
1,
Muhammad Saqlain Zaheer
2,*,
Hafiz Haider Ali
3,
Akhtar Hameed
4,
Kholoud Z. Ghanem
5 and
Mahmoud F. Seleiman
6,7,*
1
Biology Department, College of Science and Humanity Studies, Prince Sattam Bin Abdulaziz University, P.O. Box 292, Riyadh 11942, Saudi Arabia
2
Department of Agricultural Engineering, Khwaja Fareed University of Engineering and Information Technology, Rahim Yar Khan 64200, Pakistan
3
Department of Agriculture, Government College University, Lahore 54000, Pakistan
4
Institute of Plant Protection, MNS University of Agriculture Multan, Multan 61000, Pakistan
5
Department of Biological Science, College of Science and Humanities, Shaqra University, Riyadh 11961, Saudi Arabia
6
Plant Production Department, College of Food and Agriculture Sciences, King Saud University, P.O. Box 2460, Riyadh 11451, Saudi Arabia
7
Department of Crop Sciences, Faculty of Agriculture, Menoufia University, Shibin El-Kom 32514, Egypt
*
Authors to whom correspondence should be addressed.
Plants 2023, 12(17), 3141; https://doi.org/10.3390/plants12173141
Submission received: 19 July 2023 / Revised: 15 August 2023 / Accepted: 29 August 2023 / Published: 31 August 2023
(This article belongs to the Special Issue Plant Growth Promoting Bacteria)
Browse Figures
Versions Notes

Abstract

:
Water management techniques are improving at the farm level, but they are not enough to deal with the limited availability of water and increased crop yields. Soil microbes play a vital role in nitrogen fixation, improving soil fertility and enhancing plant growth hormones under drought conditions. Therefore, this study was conducted to investigate the impact of water management combined with Azospirillum brasilense and Rhizobium pisi on wheat crop productivity and soil properties in dry regions. Three water management techniques were compared, normal irrigation as a control (C), deficit irrigation (DI), and partial root drying irrigation (PRD), together with the interaction of plant-growth-promoting rhizobacteria (PGPR). Experiments were conducted with six treatments in total: T1 = C + No PGPR, T2 = C + PGPR, T3 = DI + No PGPR, T4 = DI + PGPR, T5 = PRD + No PGPR, and T6 = PRD + PGPR. The highest grain yield was achieved in the control irrigation treatment using seeds inoculated with rhizobacteria, followed by control treatment without any inoculation, and the lowest was recorded with deficit irrigation without rhizobacteria inoculated in the seeds. However, PRD irrigation resulted in significantly higher plant growth and grain yield than the DI treatment. PGPR inoculation combined with PRD resulted in a 22% and 20% higher number of grains per spike, a 19% and 21% higher grain yield, and a 25% and 22% higher crop growth rate compared to rhizobacteria inoculation combined with the DI system in 2021-22 and 2022-23, respectively. This increase was due to the higher production of growth hormones and higher leaf area index under water-limited conditions. A greater leaf area index leads to a higher chlorophyll content and higher food production for plant growth.

1. Introduction

Wheat (Triticum aestivum L.) was the first domesticated cereal and is the most important staple food worldwide. It is the most widely grown crop and fulfills the nutrient needs of more than 40% of the world’s population [1]. Wheat is a cereal crop and is severely affected by seasonal drought. It is mostly grown in the arid and semi-arid regions of the country [2]. Poor water management and the unavailability of water are the main cause of low yields in these areas. Growth parameters are affected by poor metabolism and physiological functions when crops face dry periods [3]. The reduction in crop yield due to water stress varies according to the intensity and timing of drought stress [4]. Wheat is not only the staple crop but the most important crop for the country’s economy. Its production in arid and semi-arid regions is highly restricted due to the poor availability of water and low rainfall [5]. Limited water availability and seasonal drought have intense effects on the wheat crop yield, so it is very difficult to attain the actual potential [6]. Water management techniques are improving at the farm level, but they are not enough to counter the effects of limited water availability and increase crop yield [7,8]. The cropping area and wheat crop yield will decrease day by day; on the other hand, soil salinity is increasing in arid regions [5]. Inefficient irrigation systems in arid regions are the main reason for the increasing salinity and poor plant growth. The unavailability of water is causing a decrease in the wheat cropping area under arid conditions [9]. The unreliability and inequity of rainfall and the seasonal drought conditions are also key reasons for decreasing crop yields. In general, wheat is sown on flat land and flood irrigation is applied, leading to a significant loss of water. The sowing of wheat on a bed or furrow is also useful to save water, but still not as effective under limited water availability [10].
Using a suitable irrigation method in dry regions is the main priority for farmers to obtain maximum crop yields with the available water. Water management and different agronomic practices are highly effective in increasing crop yields with the optimal utilization of the available resources, especially in dry regions [11]. The flood irrigation method is the most widely used practice for farmers, as it requires less labor and is low-cost, but farmers are now moving towards the sowing of wheat crops on beds and furrows to save irrigation water. Water management techniques in dry areas can directly affect crop yield [12]. Water deficit irrigation (DI) is an irrigation method in which less water is applied than the crop requires, but drought conditions do not exist at any growth stage. This method is effective under very low water availability, and flood irrigation leads to a loss of water [13]. Partial root-zone drying irrigation (PRDI) is another water management technique in which irrigation is first applied on one side of the roots while the other side remains dry, and the next time is applied on the other side of the roots. A water saving of 50% has been reported from the use of DI and PRDI, but Iqbal et al. [14] have recommended PRDI as more suitable irrigation method to obtain higher crop yields. It was also reported that during PRDI, plants modify their internal metabolic and physiological functions and try to close their stomata due to internal plant signaling, as irrigation water is limited or unavailable, but water is available in the soil on one side of the roots and plants can continue their metabolic functions [15].
Low soil fertility and drought are the leading threats to wheat production. The continual use of inorganic chemical fertilizers can lower soil productivity. Micro-organisms are very beneficial to crop production and nutrient availability in the soil [16]. Plant-growth-promoting rhizobacteria (PGPR) are a group of microbes that play a vital role in nitrogen fixation, improving soil fertility, enhancing nutrient uptake by plants, and increasing the amounts of growth hormones in the plants, helping to improve crop yield. PGPR also improve the tolerance of plants to water stress and pests [17]. These bacteria are naturally present in the soil and colonize the root zone, and some bacteria form nodules in leguminous crops that improve plant growth. PGPR also improve soil fertility by enhancing nutrient contents and breaking down complex nutrients into a simple form available for plant uptake [18]. Inoculation of crop seeds with PGPR during sowing improves crop biomass and production [19]. PGPR fix atmospheric nitrogen and increase soil fertility. They also increase the resistance of plants to oxidative and drought stress with the production of water-soluble vitamins, riboflavin, pantothenic acid, thiamine, cytokinins, and many other growth-promoting hormones [20]. Siddhartha et al. [21] and Cohen et al. [22] reported root enhancement and more water content in plants with the application of Azospirillum brasilense, while higher nutrient supply and growth hormone production was reported from Rhizobium pisi [23,24]. Yan et al. [25] and Nie et al. [26] reported that the different environmental conditions can affect the soil fertility and growth of different plants. Water availability and its quality can damage the whole plant physiological mechanism [27,28]. Soil fertility and soil structure also affect plant growth [4,29]. Zhang et al. [30] reported that the availability of beneficial soil microbes can produce the antibiotics to improve plant growth and root biomass. An increase in root biomass can increase nitrogen uptake [31]. Both these bacteria were also reported by many researchers to helpful for plant growth promotion under water stress condition [23,24,32,33,34], but nothing is clear about their combined application under drought stress.
Inoculation of crop seeds with PGPR is an effective method to enhance long-term soil productivity and obtain a higher crop yield [35,36]. Ecofriendly crop production is also possible with the maximum utilization of soil microbes in agricultural crop production. Different bacterial groups, such as Bacillus, Azospirillum, Enterobacter, Pseudomonas, and Agrobacterium, are used in seed inoculation [37,38], which is reported to be very beneficial for soil productivity, enhancing crop yields and also improving drought stress tolerance in wheat [39]. The interaction of PGPR with PRD and DI irrigation systems in wheat crop production is not investigated enough, and therefore there is a need to understand the soil properties and plant growth/yield improvement [40]. PGPR might modify plant growth under DI or PRDI systems, but investigations on such are limited.
Therefore, this study aimed to investigate the physiological effects of PRD, DI, and FI systems combined with the PGPR inoculation of wheat seeds under field and wirehouse conditions. Further, the current study was also designed to test the hypothesis that combining PGPR with a suitable irrigation method can improve plant growth and soil properties under limited water conditions.

2. Materials and Methods

2.1. Plant Material and Experimental Unit

This experiment was conducted at greenhouse, during 2021–2022 and 2022–2023, with a complete randomized design (CRD) to investigate the impact of water management combined with microbial inoculation on crop productivity and soil properties. The sowing date for seeds was 5th November. Three water management practices were used in the experiment: normal irrigation as a control (C), deficit irrigation (DI), and partial root drying (PRD) irrigation, all with and without the use of plant-growth-promoting rhizobacteria (PGPR). The experiments consisted of six treatments, each having three replicates: T1 = Control + No PGPR, T2 = C + PGPR, T3 = DI + No PGPR, T4 = DI + PGPR, T5 = PRD + No PGPR, T6 = PRD + PGPR. PGPR was applied as a combination of two bacterial strains, Azospirillum brasilense and Rhizobium pisi. The wheat variety Galaxy-2013 was used in the current investigation. The pot size was 2 × 2 × 2 feet with 20 kg of soil per pot, and soil analysis was performed before the start of the experiment. The mean annual temperature at the experimental site was 27 °C and the average humidity was 55%. PGPR strains of Azospirillum brasilense and Rhizobium pisi were obtained from the Government College University, Lahore. Irrigation was applied on critical growth stages (Tillering (30 days after sowing (DAS)), booting (60 DAS), anthesis (90 DAS), and grain filling stage (110 DAS)) of the wheat crop when the crop required the irrigation water. The timing of the irrigation for PRD was also the same as for the control treatment. Recommended fertilizers were applied equally to all the experimental units.
Seeds were sown with seed inoculation according to the procedure described by Fukami et al. [39]. Ten pre-germinated wheat seeds were sown in each pot. After eight days of emergence, the seedlings of the PRD treatments were uprooted, and the roots were divided in half. Wheat seedlings were repotted into special pots with partitions that allowed the roots of each plant to be separated equally between each portion. Partitioned wheat seedlings were watered for 6 days. One side was irrigated on one event, and the other side was irrigated on the next event. Deficit irrigation (DI) was applied so that the seedlings received 60% of the amount of water applied in the control treatment. Loam soil was used in the experiment and the properties of the pot are given in Table 1.

2.2. Plant Analysis: Morpho-Biochemical Traits

Plant height, spike length, the number of spikelets per spike and grains per spike, the 1000-grain weight, and yield per plant were recorded when the crop matured using standard procedures (Bhutta et al. [41]). The leaf area index (LAI), crop growth rate (CGR), and relative growth rate (RGR) were calculated according to the procedure described by Gardner et al. [42]. Leaf samples of 0.5 g were placed in distilled water for 24 h at 4 °C to determine the turgid weight, and after that the samples were oven-dried at 65 °C for 48 h to obtain the dry weight (g). The relative water content (RWC) was determined using the formula reported by Barr and Weatherley [43]:
RWC (%) = [(FW − DW)/(TW − DW)] × 100
Stomatal conductance and the photosynthesis rate were measured using an infrared gas analyzer (Cl-340 Handheld Photosynthesis System, Camas, WA, USA), and a chlorophyll meter (CL-1: Hansatech Instruments Ltd., Pentney, UK) was used to determine the chlorophyll content.

2.3. Soil Fertility Analysis

Soil samples were collected from the pots when the crop was harvested to determine the available nitrogen (N), phosphorous (P), and potassium (K) concentrations. Soil organic matter was determined using Walkley and Black’s [44] method. Extraction with sodium bicarbonate, alkaline potassium permanganate [45], and ammonium acetate [46] was carried out using standard protocols and procedures were applied to measure the available N, P, and K, respectively. Soil respiration (SR) was determined according to the procedure described by Dinesh et al. [47].

2.4. Data Interpretation

The collected data were analyzed using the computer software Statistix 8.1 at the 95% probability level. The different lowercase letters indicate the significant differences among various treatments.

3. Results

3.1. Wheat Growth Traits

The highest plant height was recorded in T2 (97.48 cm and 98.11 cm) followed by T1 (95.07 cm and 95.55 cm) and the lowest results were obtained in T3 (84.10 cm and 83.38 cm) (Table 2). The highest spike length was recorded in T2 (21.41 cm and 21.89 cm), followed by T1 (19.41 cm and 20.03 cm), and the lowest results were obtained in T3 (12.45 cm and 12.96 cm) (Table 2). Spikelets per spike were also significantly affected by all studied treatments. The highest number of spikelets per spike was recorded in T2 (30.19 and 30.65), in which control conditions were maintained and the seeds had been inoculated with plant-growth-promoting rhizobacteria (PGPR), followed by T1 (28.54 and 28.95), with control conditions and no PGPR inoculation, and the lowest results were obtained in T3 (20.22 and 20.73), in which deficit irrigation was applied without the use of PGPR (Table 2).

3.2. Wheat Yield Traits

The thousand-grain weight was significantly affected by PGRP inoculation and different irrigation systems (Table 3). The highest 1000-grain weight was recorded in T2 (44.77 g and 45.92 g) followed by T1 (42.78 g and 43.82 g). The lowest results were obtained in T3 (31.82 g and 32.90 g) (Table 3). The grain yield per plant was also significantly affected by PGRP inoculation and different irrigation systems (Table 3). The highest grain yield per plant was recorded in T2 (1.256 g and 1.393 g) followed by T1 (1.183 g and 1.316 g). The lowest results were obtained in T3 (0.693 g and 0.490 g).

3.3. Relative Growth Rate of Wheat

The crop growth rate (CGR) was significantly affected by PGPR inoculation and different irrigation methods in wheat in both the tillering and flag leaf stages (Table 4). The highest CGR was recorded in T2 (tillering stage: 2.29 g m−2 day−1 and 2.32 g m−2 day−1; flag leaf stage: 9.75 g m−2 day−1 and 9.71 g m−2 day−1) followed by T1 (tillering stage: 2.14 g m−2 day−1 and 2.17 g m−2 day−1; flag leaf stage: 9.19 g m−2 day−1 and 9.22 g m−2 day−1). The lowest results were obtained in T3 (tillering stage: 1.64 g m−2 day−1 and 1.13 g m−2 day−1; flag leaf stage: 7.09 g m−2 day−1 and 7.12 g m−2 day−1). The relative growth rate (RGR) was also significantly affected by PGPR inoculation and different irrigation methods in wheat in both the tillering and flag leaf stages (Table 5). The highest RGR was recorded in T2 (tillering stage: 0.143 g m−2 day−1 and 0.148 g m−2 day−1; flag leaf stage: 4.580 g m−2 day−1 and 4.610 g m−2 day−1) followed by T1 (tillering stage: 0.134 g m−2 day−1 and 0.139 g m−2 day−1; flag leaf stage: 4.236 g m−2 day−1 and 4.263 g m−2 day−1). The lowest results were obtained in T3 (tillering stage: 0.076 g m−2 day−1 and 0.070 g m−2 day−1; flag leaf stage: 3.543 g m−2 day−1 and 3.483 g m−2 day−1) (Table 5).

3.4. Gas Exchange Rate and Photosynthetic Capacity

The net assimilation rate (NAR) was significantly affected by PGPR inoculation and different irrigation methods in wheat in both the tillering and flag leaf stages (Table 6). The highest NAR was recorded in T2 (tillering stage: 1.530 g m−2 day−1 and 1.527 g m−2 day−1; flag leaf stage: 4.620 g m−2 day−1 and 4.643 g m−2 day−1) followed by T1 (tillering stage: 1.423 g m−2 day−1 and 1.431 g m−2 day−1; flag leaf stage: 4.433 g m−2 day−1 and 4.446 g m−2 day−1). The lowest results were obtained in T3 (tillering stage: 1.042 g m−2 day−1 and 1.020 g m−2 day−1; flag leaf stage: 3.633 g m−2 day−1 and 3.640 g m−2 day−1).
The leaf area index (LAI) was significantly affected by PGPR inoculation and different irrigation methods in wheat in both the tillering and flag leaf stages (Table 7). The highest LAI was recorded in T2 (tillering stage: 2.51 and 2.63; flag leaf stage: 7.35 and 7.43) followed by T1 (tillering stage: 2.32 and 2.41; flag leaf stage: 7.06 and 7.12) and the lowest results were obtained in T3 (tillering stage: 1.81 and 1.89; flag leaf stage: 6.01 and 6.14) in both years of the experiment.
Data regarding the transpiration rate, proline contents, chlorophyll contents, stomatal conductance, and relative water content were also significantly affected by the application of PGPR and by the different irrigation methods (Figure 1, Figure 2, Figure 3, Figure 4, Figure 5 and Figure 6). The highest values were recorded in T2, followed by T1, and the lowest results were noticed in T3 in both years.

3.5. Soil Fertility Indices

Soil properties such as available soil nitrogen, phosphorus, and potassium, the soil organic matter content, and soil respiration were significantly affected by all the treatments (Table 8). The highest soil N, P, and K concentrations, organic matter contents, and soil respiration were recorded in T2 followed by T1 and the lowest results were observed in T3. PRD irrigation resulted in higher values than DI irrigation, but we observed even higher values with PGPR inoculation.

4. Discussion

Availability of water is one of the serious challenges for the present and future of the world. Drought-dominant areas are increasing day by day in the world, which limits crop production [48]. One of the methods for water saving is deficit irrigation (DI) of the plants. It reduces the vegetative growth of plants and subsequently reduces their competitiveness with other plants and significantly reduces the cost of agricultural management practices [49]. However, partial root drying (PRD) is a changed type of deficit irrigation system [50]. In this method, during each irrigation, we apply irrigation to only half of the plant root, and in this way one part of the root absorbs water and the other remains dry for the next irrigation. Therefore, the partial root drying technique is considered an imperative irrigation strategy. Further, it has also been studied that exogenous application of PGRs like SA and PN along with medium levels of DI can help in rational utilization of water resources and could effectively improve crop yield under water-scarce conditions [51].
In the current research, plant height was significantly affected by the application of plant-growth-promoting rhizobacteria. The production of different growth hormones is also reported in the seed inoculation of wheat with Azospirillum brasilense [4]. Higher growth hormones can also improve plant growth through various physiological mechanisms [52]. Similar to our findings, Ahmad et al. [53] also reported that the application of PGPR produced more plant leaves for photosynthesis under water deficit conditions. A 5% greater plant height was also observed with the application of plant-growth-promoting rhizobacteria. The partial root-zone drying (PRD) system has been found to be more effective in increasing plant height than deficit irrigation. However, it was also stated that water deficit conditions also affected plant height [54], but the application of PGPR significantly enhanced plant height, as it increased the availability of nutrients for plant growth [4,24]. Previously, Stikić et al. [55] also reported greater plant height in PRD treatments as compared to deficit irrigation conditions [51]. In this study, the spike length, number of grains per spike, and grain weight of the wheat crop improved with the application of PGPR. This improvement might be due to the fact that PGPR produces the enzyme ACC deaminase, which helps to improve nutrient availability and reduce the extra ethylene, so there is greater photosynthetic production that improves the spike length in plants [4,24]. Water is essential to maintain all physiological functions of the plant, so water-deficient conditions severely reduce all the growth-related parameters of wheat plants [56]. Recently, Iqbal et al. [57] also proved that PRD irrigation is more beneficial to plant growth than the DI irrigation system. In PRD irrigation, more photosynthates are produced as compared to DI because of the plant’s stomatal size and internal signaling [58].
Water availability under PRD irrigation is more beneficial compared to DI, and the findings of the present study for the irrigation system are in line with those of Iqbal et al. [57] and Ahmad et al. [59]. The PRD irrigation system with the application of PGPR has been found to be more beneficial than the same system with non-inoculated wheat seeds [50]. Previously, Mayak et al. [60] reported that ACC enzyme production by PGPR-inoculated plants enhances nutrient uptake and increases the root and shoot length, which helps to improve plant growth- and yield-related parameters. Further, it was reported that PGPR inoculation in wheat seeds enhances plant growth by improving the organic entities for plant growth [61,62]. Recently, Zaheer et al. [63] also proved that application of PGPR produced more growth hormones such as cytokinin, which can improve cell division and, ultimately, growth- and yield-related parameters. The higher spike length, number of grains per spike, and 1000-grain weight directly help to increase the grain yield of the wheat crop [4]. It has been reported that PGPR produces the phytohormone indole-3-acetic acid (IAA), which can help to improve the surface area and adventitious root formation, thereby enhancing nutrient uptake and improving plant growth and yield [64,65]. Our study observed the same response with the PGPR-inoculated treatments in the FI, PRD, and DI irrigation systems, i.e., better plant growth and yields.
Previously, Bashan et al. [66] reported that inoculation of wheat seeds with A. brasilense enhanced photosynthesis, thus improving the plant growth rate and other physiological parameters. The application of PGPR also increased the leaf area index, and greater nutrient uptake was observed. Moreover, higher hormonal levels in crops have been observed after inoculation with PGPR, especially under water-limited conditions [14,67,68]. Ha et al. [69] also reported that cell division, nutrient uptake, and the leaf area index were higher following PGPR inoculation. In the PRD irrigation system, plant growth and yield were observed to be improved by PGPR inoculation in seeds. This study revealed that the transpiration rate in wheat plants was lower under DI and PRD irrigation systems compared to the control. However, PGPR significantly improved the transpiration rate with increased relative water content and stomatal conductance. Higher photosynthetic activities might be due to PGPR enhancing the production of cytokinin and other growth hormones, leading to improvements in plant growth, relative water content, and transpiration rate [5,70]. According to Iqbal et al. [14], water availability is essential for proper plant growth, but when water availability is restricted, the PRD irrigation system is more effective than the DI irrigation system [71].
Leaf area defines plants’ transpiration rate, stomatal conductance, and chlorophyll content, so a higher LAI leads to improved growth- and yield-related parameters. A higher LAI will be able to catch more solar energy for transpiration rate and photosynthesis [4,24,70]. Lazauskas et al. [72] reported that a lower LAI was observed under limited water availability, leading to poor leaf turgidity and leaf expansion. Concerning PRD and DI irrigation systems, the present findings are in line with those of Stikić et al. [55] and Elhani et al. [13]. Proline is also an important osmolyte in wheat plants, as it stabilizes the different organelles and molecules in the cell [73]. Szepesi and Szőllősi [74] reported lower proline contents in plants under limited water availability due to the breakdown of the protein molecule. Moreover, ABA regulates P5CS gene expression, increasing proline synthesis when water availability is lower [75]. Soil moisture is essential for the availability of soil nutrients. Higher concentrations of available soil N, P, and K were observed in the PRD irrigation system compared to the DI irrigation system. Iqbal et al. [14] reported that an appropriate soil moisture content is essential to enhance the availability of N, P, and K. PGPR fixes atmospheric nitrogen and enhances the availability of the nutrients by breaking down the complex molecules from the soil and enhancing the organic matter content [54,76]. Soil respiration is very suitable for plant growth and microorganisms, and it also indicates the soil’s microbial activity and organic matter content [63]. The present findings are aligned with those of Skopp et al. [76], who reported that limited soil moisture decreases microbial activity, organic matter content, and availability of soil nutrients. Greater microbial activity enhances soil respiration and organic matter, improving nutrient availability and source–sink linkage between soil nutrients [77].
Soil moisture affects the mineralization of soil nutrients. Under limited water conditions, more nitrogen is lost because of the increasing asynchronicity between nitrogen uptake and mineralization [78]. Hailegnaw et al. [79] and Elkhlifi et al. [80] reported that any soil amendment that can enhance the organic matter content of the soil could enhance soil nutrient availability. Further, application of PGPR has been shown to increase soil nutrients by breaking down the chelate compounds and increasing the amount of organic matter [63]. According to Al-Wabel et al. [81], PGPR enhances soil microbial activity, enhancing soil respiration. A higher organic matter content can also help to increase soil respiration. Limited water conditions decrease the soil’s microbial activity and organic matter content [14,63]. Our study also demonstrated that the PRD irrigation system with PGPR inoculation in seeds is more beneficial than the DI irrigation system with PGPR. The PRD irrigation system is more beneficial than the DI irrigation system, as soil nutrients are more available for plant uptake [14].

5. Conclusions

Plant-growth-promoting rhizobacteria (PGPR) improved wheat growth and physiology, particularly in conditions of water scarcity. Among the irrigation methods, partial root-zone Ddying (PRD) emerges as a promising approach compared to deficit irrigation (DI). PGPR inoculation showcases consistent efficacy within both PRD and DI irrigation systems, fostering improved wheat growth, yield characteristics, and soil fertility dynamics. The integration of PGPR inoculation with diverse irrigation strategies warrants further investigation for its synergistic benefits and optimal agricultural outcomes.

Author Contributions

Conceptualization, M.S.Z. and H.H.A.; data curation, H.H.A. and B.A.A.; formal analysis, M.S.Z. and K.Z.G.; funding acquisition, M.S.Z. and M.F.S.; investigation, M.S.Z.; methodology, M.F.S.; project administration, H.H.A., A.H., and M.S.Z.; resources, M.S.Z., A.H., and M.F.S.; software, M.S.Z.; supervision, H.H.A.; validation, M.F.S. and A.H.; visualization, M.S.Z.; writing—original draft, M.S.Z., B.A.A., and K.Z.G.; writing—review and editing, H.H.A. and M.F.S. All authors have read and agreed to the published version of the manuscript.

Funding

The authors extend their appreciation to Prince Sattam bin Abdulaziz University for funding this research work through the project number (PSAU/2023/01/23356).

Data Availability Statement

The data is contained within the article.

Acknowledgments

The authors extend their appreciation to Prince Sattam bin Abdulaziz University for funding this research work through the project number (PSAU/2023/01/23356).

Conflicts of Interest

The authors declare that there are no conflict of interest.

References

  1. Giraldo, P.; Benavente, E.; Manzano-Agugliaro, F.; Gimenez, E. Worldwide Research Trends on Wheat and Barley: A Bibliometric Comparative Analysis. Agronomy 2019, 9, 352. [Google Scholar] [CrossRef]
  2. Akram, M. Growth and Yield Components Of Wheat Under Water Stress Of Different Growth Stages. Bangladesh J. Agric. Res. 2011, 36, 455–468. [Google Scholar] [CrossRef]
  3. Shahid, R.; Ren, M.; Mora-Poblete, F.; Arnao, M.B.; Naz, S.; Anwar, M.; Altaf, M.M.; Shahid, S.; Shakoor, A.; Sohail, H.; et al. Phytomelatonin: An overview of the importance and mediating functions of melatonin against environmental stresses. Physiol. Plant. 2020, 172, 820–846. [Google Scholar] [CrossRef]
  4. Seleiman, M.F.; Al-Suhaibani, N.; Ali, N.; Akmal, M.; Alotaibi, M.; Refay, Y.; Dindaroglu, T.; Abdul-Wajid, H.H.; Battaglia, M.L. Drought Stress Impacts on Plants and Different Approaches to Alleviate Its Adverse Effects. Plants 2021, 10, 259. [Google Scholar] [CrossRef]
  5. Ahmadi, S.H.; Andersen, M.N.; Plauborg, F.; Poulsen, R.T.; Jensen, C.R.; Sepaskhah, A.R.; Hansen, S. Effects of irrigation strategies and soils on field-grown potatoes: Gas exchange and xylem [ABA]. Agric. Water Manag. 2010, 97, 1486–1494. [Google Scholar] [CrossRef]
  6. Hamdy, A.; Ragab, R.; Scarascia-Mugnozza, E. Coping with water scarcity: Water saving and increasing water productivity. Irrig. Drain. 2003, 52, 3–20. [Google Scholar] [CrossRef]
  7. Gill, S.S.; Tuteja, N. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol. Biochem. 2010, 48, 909–930. [Google Scholar] [CrossRef] [PubMed]
  8. Qiu, D.; Zhu, G.; Lin, X.; Jiao, Y.; Lu, S.; Liu, J.; Liu, J.; Zhang, W.; Ye, L.; Li, R.; et al. Dissipation and movement of soil water in artificial forest in arid oasis areas: Cognition based on stable isotopes. CATENA 2023, 228, 107178. [Google Scholar] [CrossRef]
  9. Tanji, K.K. Agricultural Salinity Assessment and Management; Scientific Publishers: New York, NY, USA, 2012; ISBN 9388812832. [Google Scholar]
  10. Ahmed, A.; Hussain, I.; Khalil, I.A.; Subhanulla, S.; Ahmed, G.; Ahmad, I.; Imtiaz, M. Effect of Bed Planting and Zero Tillage on Productivity and Water Use of Irrigated Maize Wheat Cropping System in Khyber Pakhtunkhwa Province of Pakistan. Sarhad J. Agric. 2018, 34, 696–704. [Google Scholar] [CrossRef]
  11. Seleiman, M.F.; Kheir, A.M.S.; Al-Dhumri, S.; Alghamdi, A.G.; Omar, E.S.H.; Aboelsoud, H.M.; Abdella, K.A.; Abou El Hassan, W.H. Exploring optimal tillage improved soil characteristics and productivity of wheat irrigated with different water qualities. Agronomy 2019, 9, 233. [Google Scholar] [CrossRef]
  12. Chen, X.; Feng, S.; Qi, Z.; Sima, M.W.; Zeng, F.; Li, L.; Cheng, H.; Wu, H. Optimizing Irrigation Strategies to Improve Water Use Efficiency of Cotton in Northwest China Using RZWQM2. Agriculture 2022, 12, 383. [Google Scholar] [CrossRef]
  13. Elhani, S.; Haddadi, M.; Csákvári, E.; Zantar, S.; Hamim, A.; Villányi, V.; Douaik, A.; Bánfalvi, Z. Effects of partial root-zone drying and deficit irrigation on yield, irrigation water-use efficiency and some potato (Solanum tuberosum L.) quality traits under glasshouse conditions. Agric. Water Manag. 2019, 224, 105745. [Google Scholar] [CrossRef]
  14. Iqbal, R.; Raza, M.A.S.; Toleikiene, M.; Ayaz, M.; Hashemi, F.; Habib-Ur-Rahman, M.; Zaheer, M.S.; Ahmad, S.; Riaz, U.; Ali, M.; et al. Partial root-zone drying (PRD), its effects and agricultural significance: A review. Bull. Natl. Res. Cent. 2020, 44, 159. [Google Scholar] [CrossRef]
  15. Yactayo, W.; Ramírez, D.A.; Gutiérrez, R.; Mares, V.; Posadas, A.; Quiroz, R. Effect of partial root-zone drying irrigation timing on potato tuber yield and water use efficiency. Agric. Water Manag. 2013, 123, 65–70. [Google Scholar] [CrossRef]
  16. Babur, E.; Dindaroğlu, T.; Roy, R.; Seleiman, M.F.; Ozlu, E.; Battaglia, M.L.; Uslu, Ö.S. Relationship between organic matter and microbial biomass in different vegetation types. In Microbial Syntrophy-Mediated Eco-Enterprising; Elsevier: Amsterdam, The Netherlands, 2022; pp. 225–245. [Google Scholar]
  17. Saad, M.M.; Eida, A.A.; Hirt, H. Tailoring plant-associated microbial inoculants in agriculture: A roadmap for successful application. J. Exp. Bot. 2020, 71, 3878–3901. [Google Scholar] [CrossRef] [PubMed]
  18. Kashif, M.; Sang, Y.; Mo, S.; Rehman, S.U.; Khan, S.; Khan, M.R.; He, S.; Jiang, C. Deciphering the biodesulfurization pathway employing marine mangrove Bacillus aryabhattai strain NM1-A2 according to whole genome sequencing and transcriptome analyses. Genomics 2023, 115, 110635. [Google Scholar] [CrossRef]
  19. Seleiman, M.F.; Abdelaal, M.S. Effect of organic, inorganic and bio-fertilization on growth, yield and quality traits of some chickpea (Cicer arietinum L.) varieties. Egypt. J. Agron. 2018, 40, 105–117. [Google Scholar] [CrossRef]
  20. McGuire, A.V.; Northfield, T.D. Tropical Occurrence and Agricultural Importance of Beauveria bassiana and Metarhizium anisopliae. Front. Sustain. Food Syst. 2020, 4, 6. [Google Scholar] [CrossRef]
  21. Siddhartha, P.S.; Debashish, B.; Adrita, G.; Kalpataru, D.M.; Animesh, G. A review on the role of Azospirillum in the yield improvement of non leguminous crops. Afr. J. Microbiol. Res. 2012, 6, 1085–1102. [Google Scholar] [CrossRef]
  22. Cohen, A.C.; Bottini, R.; Pontin, M.; Berli, F.J.; Moreno, D.; Boccanlandro, H.; Travaglia, C.N.; Piccoli, P.N. Azospirillum brasilense ameliorates the response of Arabidopsis thaliana to drought mainly via enhancement of ABA levels. Physiol. Plant. 2014, 153, 79–90. [Google Scholar] [CrossRef] [PubMed]
  23. Wdowiak-Wróbel, S.; Marek-Kozaczuk, M.; Kalita, M.; Karaś, M.; Wójcik, M.; Małek, W. Diversity and plant growth promoting properties of rhizobia isolated from root nodules of Ononis arvensis. Antonie Leeuwenhoek 2017, 110, 1087–1103. [Google Scholar] [CrossRef] [PubMed]
  24. Zaheer, M.S.; Raza, M.A.S.; Saleem, M.F.; Khan, I.H.; Ahmad, S.; Iqbal, R.; Manevski, K. Investigating the effect of Azospirillum brasilense and Rhizobium pisi on agronomic traits of wheat (Triticum aestivum L.). Arch. Agron. Soil Sci. 2019, 65, 1554–1564. [Google Scholar] [CrossRef]
  25. Yan, Y.; Jarvie, S.; Liu, Q.; Zhang, Q. Effects of fragmentation on grassland plant diversity depend on the habitat specialization of species. Biol. Conserv. 2022, 275, 109773. [Google Scholar] [CrossRef]
  26. Nie, S.; Mo, S.; Gao, T.; Yan, B.; Shen, P.; Kashif, M.; Zhang, Z.; Li, J.; Jiang, C. Coupling effects of nitrate reduction and sulfur oxidation in a subtropical marine mangrove ecosystem with Spartina alterniflora invasion. Sci. Total. Environ. 2023, 862, 160930. [Google Scholar] [CrossRef] [PubMed]
  27. Zhu, G.; Liu, Y.; Shi, P.; Jia, W.; Zhou, J.; Liu, Y.; Ma, X.; Pan, H.; Zhang, Y.; Zhang, Z.; et al. Stable water isotope monitoring network of different water bodies in Shiyang River basin, a typical arid river in China. Earth Syst. Sci. Data 2022, 14, 3773–3789. [Google Scholar] [CrossRef]
  28. Zhang, T.; Song, B.; Han, G.; Zhao, H.; Hu, Q.; Zhao, Y.; Liu, H. Effects of coastal wetland reclamation on soil organic carbon, total nitrogen, and total phosphorus in China: A meta-analysis. Land Degrad. Dev. 2023, 34, 3340–3349. [Google Scholar] [CrossRef]
  29. Ran, C.; Bai, X.; Tan, Q.; Luo, G.; Cao, Y.; Wu, L.; Chen, F.; Li, C.; Luo, X.; Liu, M.; et al. Threat of soil formation rate to health of karst ecosystem. Sci. Total. Environ. 2023, 887, 163911. [Google Scholar] [CrossRef] [PubMed]
  30. Zhang, G.; Zhao, Z.; Yin, X.-A.; Zhu, Y. Impacts of biochars on bacterial community shifts and biodegradation of antibiotics in an agricultural soil during short-term incubation. Sci. Total. Environ. 2021, 771, 144751. [Google Scholar] [CrossRef]
  31. Li, W.; Shi, Y.; Zhu, D.; Wang, W.; Liu, H.; Li, J.; Shi, N.; Ma, L.; Fu, S. Fine root biomass and morphology in a temperate forest are influenced more by the nitrogen treatment approach than the rate. Ecol. Indic. 2021, 130, 108031. [Google Scholar] [CrossRef]
  32. Arzanesh, M.H.; Alikhani, H.A.; Khavazi, K.; Rahimian, H.A.; Miransari, M. Wheat (Triticum aestivum L.) growth enhancement by Azospirillum sp. under drought stress. World J. Microbiol. Biotechnol. 2010, 27, 197–205. [Google Scholar] [CrossRef]
  33. Pereyra, M.A.; Ballesteros, F.M.; Creus, C.M.; Sueldo, R.J.; Barassi, C.A. Seedlings growth promotion by Azospirillum brasilense under normal and drought conditions remains unaltered in Tebuconazole-treated wheat seeds. Eur. J. Soil Biol. 2009, 45, 20–27. [Google Scholar] [CrossRef]
  34. Nguyen, M.L.; Spaepen, S.; du Jardin, P.; Delaplace, P. Biostimulant effects of rhizobacteria on wheat growth and nutrient uptake depend on nitrogen application and plant development. Arch. Agron. Soil Sci. 2018, 65, 58–73. [Google Scholar] [CrossRef]
  35. El-Saadony, M.T.; Saad, A.M.; Soliman, S.M.; Salem, H.M.; Ahmed, A.I.; Mahmood, M.; El-Tahan, A.M.; Ebrahim, A.A.M.; El-Mageed, T.A.A.; Negm, S.H.; et al. Plant growth-promoting microorganisms as biocontrol agents of plant diseases: Mechanisms, challenges and future perspectives. Front. Plant Sci. 2022, 13, 923880. [Google Scholar] [CrossRef]
  36. El-Mageed, T.A.A.; Gyushi, M.A.H.; Hemida, K.A.; El-Saadony, M.T.; El-Mageed, S.A.A.; Abdalla, H.; AbuQamar, S.F.; El-Tarabily, K.A.; Abdelkhalik, A. Coapplication of Effective Microorganisms and Nanomagnesium Boosts the Agronomic, Physio-Biochemical, Osmolytes, and Antioxidants Defenses Against Salt Stress in Ipomoea batatas. Front. Plant Sci. 2022, 13, 883274. [Google Scholar] [CrossRef]
  37. Islam, F.; Yasmeen, T.; Arif, M.S.; Ali, S.; Ali, B.; Hameed, S.; Zhou, W. Plant growth promoting bacteria confer salt tolerance in Vigna radiata by up-regulating antioxidant defense and biological soil fertility. Plant Growth Regul. 2016, 80, 23–36. [Google Scholar] [CrossRef]
  38. Imran, M.; Shahzad, S.M.; Arif, M.S.; Yasmeen, T.; Ali, S.; Ali, B.; Tanveer, A.; Ghani, M.A.; Nadeem, M.; Javed, M.A. Inoculation of Potassium Solubilizing Bacteria with Different Potassium Fertilization Sources Mediates Maize Growth and Productivity. Pak. J. Agric. Sci. 2020, 57, 1045–1055. [Google Scholar]
  39. Fukami, J.; Nogueira, M.A.; Araujo, R.S.; Hungria, M. Accessing inoculation methods of maize and wheat with Azospirillum brasilense. AMB Express 2016, 6, 3. [Google Scholar] [CrossRef]
  40. Liu, D.; Hu, L.Y.; Ali, B.; Yang, A.G.; Wan, G.L.; Xu, L.; Zhou, W.J. Influence of 5-aminolevulinic acid on photosynthetically related parameters and gene expression in Brassica napus L. under drought stress. Soil Sci. Plant Nutr. 2016, 62, 254–262. [Google Scholar] [CrossRef]
  41. Bhutta, S.K.; Bhutta, K.N.; Aslam, M.N.; Nasir, I.R.; Ali, M.A. Evaluation of Growth and Yield Attributes of Some Wheat Varieties under Local Conditions of Southern Punjab, Pakistan. J. Plant Breed. Genet. 2019, 7, 19–25. [Google Scholar] [CrossRef]
  42. Gardner, F.P.; Pearce, R.B.; Mitchell, R.L. Physiology of Crop Plants; Iowa State University Press: Ames, IA, USA, 1985. [Google Scholar]
  43. Barrs, H.D.; Weatherley, P.E. A Re-Examination of the Relative Turgidity Technique for Estimating Water Deficits in Leaves. Aust. J. Biol. Sci. 1962, 15, 413–428. [Google Scholar] [CrossRef]
  44. Walkley, A.; Black, I.A. An examination of the Degtjareff method for determining soil organic matter, and a proposed modification of the chromic acid titration method. Soil Sci. 1934, 37, 29–38. [Google Scholar] [CrossRef]
  45. Subbaiah, V.V.; Asija, G.K. A Rapid Procedure for Utilization of Available Nitrogen in Soil. Curr. Sci. 1956, 26, 258–260. [Google Scholar]
  46. Nelson, L.B.; Heidel, H. Soil Analysis Methods as Used in the Iowa State College Soil Testing Laboratory; Science and Education Publishing: Cagayan de Oro City, Philippines, 1952. [Google Scholar]
  47. Dinesh, R.; Anandaraj, M.; Kumar, A.; Srinivasan, V.; Bini, Y.K.; Subila, K.P.; Aravind, R.; Hamza, S. Effects of Plant Growth-Promoting Rhizobacteria and NPK Fertilizers on Biochemical and Microbial Properties of Soils Under Ginger (Zingiber officinale) Cultivation. Agric. Res. 2013, 2, 346–353. [Google Scholar] [CrossRef]
  48. Fathian, F.; Morid, S.; Kahya, E. Identification of trends in hydrological and climatic variables in Urmia Lake basin, Iran. Theor. Appl. Clim. 2015, 119, 443–464. [Google Scholar] [CrossRef]
  49. Chalmers, D.J.; Mitchell, P.D.; van Heek, L. Control of Peach Tree Growth and Productivity by Regulated Water Supply, Tree Density, and Summer Pruning1. J. Am. Soc. Hortic. Sci. 1981, 106, 307–312. [Google Scholar] [CrossRef]
  50. English, M.; Raja, S.N. Perspectives on deficit irrigation. Agric. Water Manag. 1996, 32, 1–14. [Google Scholar] [CrossRef]
  51. Wakchaure, G.; Minhas, P.; Meena, K.K.; Kumar, S.; Rane, J. Effect of plant growth regulators and deficit irrigation on canopy traits, yield, water productivity and fruit quality of eggplant (Solanum melongena L.) grown in the water scarce environment. J. Environ. Manag. 2020, 262, 110320. [Google Scholar] [CrossRef]
  52. Seleiman, M.F.; Ahmad, A.; Alshahrani, T.S. Integrative Effects of Zinc Nanoparticle and PGRs to Mitigate Salt Stress in Maize. Agronomy 2023, 13, 1655. [Google Scholar] [CrossRef]
  53. Ahmad, S.; Raza, M.A.S.; Saleem, M.F.; Zahra, S.S.; Khan, I.H.; Ali, M.; Shahid, A.M.; Iqbal, R.; Zaheer, M.S. Mulching Strategies for Weeds Control and Water Conservation in Cotton. J. Agric. Biol. Sci. 2015, 8, 299–306. [Google Scholar]
  54. Farooq, M.; Basra, S.M.A.; Wahid, A.; Cheema, Z.A.; Cheema, M.A.; Khaliq, A. Physiological Role of Exogenously Applied Glycinebetaine to Improve Drought Tolerance in Fine Grain Aromatic Rice (Oryza sativa L.). J. Agron. Crop. Sci. 2008, 194, 325–333. [Google Scholar] [CrossRef]
  55. Stikić, R.; Popović, S.; Srdić, M.; Savić, D.; Jovanović, Z.; Prokić, L.; Zdravković, J. Partial Root Drying (PRD): A New Technique for Growing Plants That Saves Water and Improves the Quality of Fruit. Bulg. J. Plant Physiol. 2003, 29, 3–4. [Google Scholar]
  56. Posadas, A.; Rojas, G.; LMalaga, M.; Mares, V.; Quiroz, R.A. Partial Root-Zone Drying: An Alternative Irrigation Management to Improve the Water Use Efficiency of Potato Crops; International Potato Center: Lima, Peru, 2008. [Google Scholar]
  57. Iqbal, R.; Raza, M.A.S.; Saleem, M.F.; Khan, I.H.; Ahmad, S.; Zaheer, M.S.; Aslam, M.U.; Haider, I. Physiological and biochemical appraisal for mulching and partial rhizosphere drying of cotton. J. Arid. Land 2019, 11, 785–794. [Google Scholar] [CrossRef]
  58. Raza, M.A.S.; Ahmad, S.; Saleem, M.F.; Khan, I.H.; Iqbal, R.; Zaheer, M.S.; Haider, I.; Ali, M. Physiological and biochemical assisted screening of wheat varieties under partial rhizosphere drying. Plant Physiol. Biochem. 2017, 116, 150–166. [Google Scholar] [CrossRef]
  59. Ahmad, S.; Zaheer, M.S.; Ali, H.H.; Erinle, K.O.; Wani, S.H.; Iqbal, R.; Okone, O.G.; Raza, A.; Waqas, M.M.; Nawaz, M. Physiological and biochemical properties of wheat (Triticum aestivum L.) under different mulching and water management systems in the semi-arid region of Punjab, Pakistan. Arid. Land Res. Manag. 2022, 36, 181–196. [Google Scholar] [CrossRef]
  60. Mayak, S.; Tirosh, T.; Glick, B.R. Plant growth-promoting bacteria confer resistance in tomato plants to salt stress. Plant Physiol. Biochem. 2004, 42, 565–572. [Google Scholar] [CrossRef]
  61. Xie, H.; Pasternak, J.J.; Glick, B.R. Isolation and Characterization of Mutants of the Plant Growth-Promoting Rhizobacterium Pseudomonas putida GR12-2 That Overproduce Indoleacetic Acid. Curr. Microbiol. 1996, 32, 67–71. [Google Scholar] [CrossRef]
  62. Mustafa, A.; Naveed, M.; Saeed, Q.; Nadeem Ashraf, M.; Hussain, A.; Abbas, T.; Kamran, M.; Minggang, X. Application potentials of plant growth promoting rhizobacteria and fungi as an alternative to conventional weed control methods. In Sustainable Crop Production; IntechOpen: London, UK, 2019; Available online: https://www.intechopen.com/chapters/67546 (accessed on 1 January 2023).
  63. Zaheer, M.S.; Ali, H.H.; Soufan, W.; Iqbal, R.; Habib-ur-Rahman, M.; Iqbal, J.; Israr, M.; El Sabagh, A. Potential Effects of Biochar Application for Improving Wheat (Triticum aestivum L.) Growth and Soil Biochemical Properties under Drought Stress Conditions. Land 2021, 10, 1125. [Google Scholar] [CrossRef]
  64. Mohite, B. Isolation and characterization of indole acetic acid (IAA) producing bacteria from rhizospheric soil and its effect on plant growth. J. Soil Sci. Plant Nutr. 2013, 13, 638–649. [Google Scholar] [CrossRef]
  65. Qin, X.; Zhang, K.; Fan, Y.; Fang, H.; Nie, Y.; Wu, X.-L. The Bacterial MtrAB Two-Component System Regulates the Cell Wall Homeostasis Responding to Environmental Alkaline Stress. Microbiol. Spectr. 2022, 10, e0231122. [Google Scholar] [CrossRef]
  66. Bashan, Y.; Bustillos, J.J.; Leyva, L.A.; Hernandez, J.-P.; Bacilio, M. Increase in auxiliary photoprotective photosynthetic pigments in wheat seedlings induced by Azospirillum brasilense. Biol. Fertil. Soils 2006, 42, 279–285. [Google Scholar] [CrossRef]
  67. Vacheron, J.; Desbrosses, G.; Bouffaud, M.-L.; Touraine, B.; Moënne-Loccoz, Y.; Muller, D.; Legendre, L.; Wisniewski-Dyé, F.; Prigent-Combaret, C. Plant growth-promoting rhizobacteria and root system functioning. Front. Plant Sci. 2013, 4, 356. [Google Scholar] [CrossRef]
  68. Sadak, M.S.; Abdalla, A.M.; Elhamid, E.M.A.; Ezzo, M.I. Role of melatonin in improving growth, yield quantity and quality of Moringa oleifera L. plant under drought stress. Bull. Natl. Res. Cent. 2020, 44, 18. [Google Scholar] [CrossRef]
  69. Ha, S.; Vankova, R.; Yamaguchi-Shinozaki, K.; Shinozaki, K.; Tran, L.-S.P. Cytokinins: Metabolism and function in plant adaptation to environmental stresses. Trends Plant Sci. 2012, 17, 172–179. [Google Scholar] [CrossRef] [PubMed]
  70. Zaheer, M.S.; Ali, H.H.; Erinle, K.O.; Wani, S.H.; Okon, O.G.; Nadeem, M.A.; Nawaz, M.; Bodlah, M.A.; Waqas, M.M.; Iqbal, J.; et al. Inoculation of Azospirillum brasilense and exogenous application of trans-zeatin riboside alleviates arsenic induced physiological damages in wheat (Triticum aestivum). Environ. Sci. Pollut. Res. 2022, 29, 33909–33919. [Google Scholar] [CrossRef] [PubMed]
  71. Wakrim, R.; Wahbi, S.; Tahi, H.; Aganchich, B.; Serraj, R. Comparative effects of partial root drying (PRD) and regulated deficit irrigation (RDI) on water relations and water use efficiency in common bean (Phaseolus vulgaris L.). Agric. Ecosyst. Environ. 2005, 106, 275–287. [Google Scholar] [CrossRef]
  72. Lazauskas, S.; Povilaitis, V.; Antanaitis, Š.; Sakalauskaite, J.; Sakalauskiene, S.; Pšibišauskiene, G.; Auškalniene, O.; Raudonius, S.; Duchovskis, P. Winter Wheat Leaf Area Index under Low and Moderate Input Management and Climate Change. J. Food Agric. Environ. 2012, 10, 588–593. [Google Scholar]
  73. Shahid, M.A.; Sarkhosh, A.; Khan, N.; Balal, R.M.; Ali, S.; Rossi, L.; Gómez, C.; Mattson, N.; Nasim, W.; Garcia-Sanchez, F. Insights into the Physiological and Biochemical Impacts of Salt Stress on Plant Growth and Development. Agronomy 2020, 10, 938. [Google Scholar] [CrossRef]
  74. Szepesi, Á.; Szőllősi, R. Mechanism of Proline Biosynthesis and Role of Proline Metabolism Enzymes Under Environmental Stress in Plants. In Plant Metabolites and Regulation under Environmental Stress; Academic Press: Cambridge, MA, USA, 2018; pp. 337–353. [Google Scholar] [CrossRef]
  75. Peng, C.; Hong-Yan, W.; Zheng, R.-L.; Zhang, B.; Guo-Xin, S.U.N. Long-Term Effects of Biochar on Rice Production and Stabilisation of Cadmium and Arsenic Levels in Contaminated Paddy Soils. Earth Environ. Sci. Trans. R. Soc. Edinb. 2018, 109, 415–420. [Google Scholar]
  76. Skopp, J.; Jawson, M.D.; Doran, J.W. Steady-State Aerobic Microbial Activity as a Function of Soil Water Content. Soil Sci. Soc. Am. J. 1990, 54, 1619–1625. [Google Scholar] [CrossRef]
  77. Marschner, P.; Hatam, Z.; Cavagnaro, T. Soil respiration, microbial biomass and nutrient availability after the second amendment are influenced by legacy effects of prior residue addition. Soil Biol. Biochem. 2015, 88, 169–177. [Google Scholar] [CrossRef]
  78. Bond-Lamberty, B.; Bolton, H.; Fansler, S.; Heredia-Langner, A.; Liu, C.; McCue, L.A.; Smith, J.; Bailey, V. Soil Respiration and Bacterial Structure and Function after 17 Years of a Reciprocal Soil Transplant Experiment. PLoS ONE 2016, 11, e0150599. [Google Scholar] [CrossRef] [PubMed]
  79. Hailegnaw, N.S.; Mercl, F.; Pračke, K.; Száková, J.; Tlustoš, P. Mutual Relationships of Biochar and Soil PH, CEC, and Exchangeable Base Cations in a Model Laboratory Experiment. J. Soils Sediments 2019, 19, 2405–2416. [Google Scholar] [CrossRef]
  80. Elkhlifi, Z.; Kamran, M.; Maqbool, A.; El-Naggar, A.; Ifthikar, J.; Parveen, A.; Bashir, S.; Rizwan, M.; Mustafa, A.; Irshad, S.; et al. Phosphate-lanthanum coated sewage sludge biochar improved the soil properties and growth of ryegrass in an alkaline soil. Ecotoxicol. Environ. Saf. 2021, 216, 112173. [Google Scholar] [CrossRef] [PubMed]
  81. Al-Wabel, M.I.; Hussain, Q.; Usman, A.R.; Ahmad, M.; Abduljabbar, A.; Sallam, A.S.; Ok, Y.S. Impact of biochar properties on soil conditions and agricultural sustainability: A review. Land Degrad. Dev. 2018, 29, 2124–2161. [Google Scholar] [CrossRef]
Plants 12 03141 g001
Figure 1. Effects of PGPR on the transpiration rate of wheat under different irrigation systems. The different letters show a significant difference in treatments at 5% probability level. PGPR (plant-growth-promoting rhizobacteria), C (control), DI (deficit irrigation), PRD (partial root drying).
Figure 1. Effects of PGPR on the transpiration rate of wheat under different irrigation systems. The different letters show a significant difference in treatments at 5% probability level. PGPR (plant-growth-promoting rhizobacteria), C (control), DI (deficit irrigation), PRD (partial root drying).
Plants 12 03141 g001
Plants 12 03141 g002
Figure 2. Effects of PGPR on the proline contents of wheat under different irrigation systems. The different letters show a significant difference in treatments at 5% probability level. PGPR (plant-growth-promoting rhizobacteria), C (control), DI (deficit irrigation), PRD (partial root drying).
Figure 2. Effects of PGPR on the proline contents of wheat under different irrigation systems. The different letters show a significant difference in treatments at 5% probability level. PGPR (plant-growth-promoting rhizobacteria), C (control), DI (deficit irrigation), PRD (partial root drying).
Plants 12 03141 g002
Plants 12 03141 g003
Figure 3. Effects of PGPR on the chlorophyll contents of wheat under different irrigation systems. The different letters show a significant difference in treatments at 5% probability level. PGPR (plant-growth-promoting rhizobacteria), C (control), DI (deficit irrigation), PRD (partial root drying).
Figure 3. Effects of PGPR on the chlorophyll contents of wheat under different irrigation systems. The different letters show a significant difference in treatments at 5% probability level. PGPR (plant-growth-promoting rhizobacteria), C (control), DI (deficit irrigation), PRD (partial root drying).
Plants 12 03141 g003
Plants 12 03141 g004
Figure 4. Effects of PGPR on the stomatal conductance at tillering stage of wheat under different irrigation systems. The different letters show a significant difference in treatments at 5% probability level. PGPR (plant-growth-promoting rhizobacteria), C (control), DI (deficit irrigation), PRD (partial root drying).
Figure 4. Effects of PGPR on the stomatal conductance at tillering stage of wheat under different irrigation systems. The different letters show a significant difference in treatments at 5% probability level. PGPR (plant-growth-promoting rhizobacteria), C (control), DI (deficit irrigation), PRD (partial root drying).
Plants 12 03141 g004
Plants 12 03141 g005
Figure 5. Effects of PGPR on the stomatal conductance at flag leaf stage of wheat under different irrigation systems. The different letters show a significant difference in treatments at 5% probability level. PGPR (plant-growth-promoting rhizobacteria), C (control), DI (deficit irrigation), PRD (partial root drying).
Figure 5. Effects of PGPR on the stomatal conductance at flag leaf stage of wheat under different irrigation systems. The different letters show a significant difference in treatments at 5% probability level. PGPR (plant-growth-promoting rhizobacteria), C (control), DI (deficit irrigation), PRD (partial root drying).
Plants 12 03141 g005
Plants 12 03141 g006
Figure 6. Effect of PGPR on the relative water contents (RWC) at flag leaf stage of wheat under different irrigation systems. The different letters show a significant difference in treatments at 5% probability level. PGPR (plant-growth-promoting rhizobacteria), C (control), DI (deficit irrigation), PRD (partial root drying).
Figure 6. Effect of PGPR on the relative water contents (RWC) at flag leaf stage of wheat under different irrigation systems. The different letters show a significant difference in treatments at 5% probability level. PGPR (plant-growth-promoting rhizobacteria), C (control), DI (deficit irrigation), PRD (partial root drying).
Plants 12 03141 g006
Table 1. Properties of the soil used for the experiment.
Table 1. Properties of the soil used for the experiment.
Parameters2021-222022-23
Organic matter (%)0.980.71
pH7.427.57
EC (µS/cm)226231
T.S.S. (%)0.470.57
Available-P (ppm)6.095.21
Available-P (ppm)116111
Saturation percentage3732
Soil separates
Sand (%)3536
Sand (%)4139
Sand (%)2425
Texture of SoilLoam SoilLoam Soil
Table 2. Effects of plant-growth-promoting rhizobacteria on the plant height, spike length, and number of spikelets per spike of wheat under different irrigation systems.
Table 2. Effects of plant-growth-promoting rhizobacteria on the plant height, spike length, and number of spikelets per spike of wheat under different irrigation systems.
TreatmentPlant Height (cm)Spike Length (cm)Number of Spikelets per Spike
2021-222022-232021-222022-232021-222022-23
T1 = Control + No PGPR95.07 b95.55 b19.41 b20.03 b28.54 b28.95 b
T2 = C + PGPR97.48 a98.11 a21.41 a21.89 a30.19 a30.65 a
T3 = DI + No PGPR84.10 f83.38 f12.45 f12.96 f20.22 e20.73 f
T4 = DI + PGPR90.74 d91.78 d16.45 d16.90 d24.32 c24.77 d
T5 = PRD + No PGPR87.70 e89.00 e14.52 e15.00 e22.23 d22.66 e
T6 = PRD + PGPR92.78 c93.48 c17.11 c17.53 c26.23 c26.70 c
The different letters show a significant difference in treatments at 5% probability level. PGPR (plant-growth-promoting rhizobacteria); C (control); DI (deficit irrigation); and PRD (partial root drying).
Table 3. Effects of PGPR on the thousand-grain weight and grain yield per plant of wheat under different irrigation systems.
Table 3. Effects of PGPR on the thousand-grain weight and grain yield per plant of wheat under different irrigation systems.
Treatment1000 GWYield per Plant
2021-222022-232021-222022-23
T1 = Control + No PGPR42.78 b43.81 b1.183 b1.316 b
T2 = C + PGPR44.77 a45.92 a1.256 a1.393 a
T3 = DI + No PGPR31.82 f32.90 f0.693 f0.490 f
T4 = DI + PGPR37.66 d38.84 d0.913 d0.890 d
T5 = PRD + No PGPR34.32 e35.25 e0.816 e0.753 e
T6 = PRD + PGPR39.74 c40.66 c1.030 c1.090 c
The different letters show a significant difference in treatments at 5% probability level. PGPR (plant-growth-promoting rhizobacteria); C (control); DI (deficit irrigation); and PRD (partial root drying).
Table 4. Effects of PGPR on the crop growth rate (CGR) of wheat under different irrigation systems.
Table 4. Effects of PGPR on the crop growth rate (CGR) of wheat under different irrigation systems.
TreatmentCrop Growth Rate at Tillering
(g m−2 day−1)		Crop Growth Rate at the Flag Leaf Stage
(g m−2 day−1)
2021-222022-232021-222022-23
T1 = Control + No PGPR2.14 b2.17 b9.19 b9.22 b
T2 = C + PGPR2.29 a2.32 a9.75 a9.71 a
T3 = DI + No PGPR1.64 f1.13 f7.09 f7.12 f
T4 = DI + PGPR1.84 d1.15 d8.19 d8.22 d
T5 = PRD + No PGPR1.74 e1.77 e7.69 e7.71 e
T6 = PRD + PGPR1.94 c1.97 c8.69 c8.72 c
The different letters show a significant difference in treatments at 5% probability level. PGPR (plant-growth-promoting rhizobacteria); C (control); DI (deficit irrigation); and PRD (partial root drying).
Table 5. Effects of PGPR on the relative growth rate (RGR) of wheat under different irrigation systems.
Table 5. Effects of PGPR on the relative growth rate (RGR) of wheat under different irrigation systems.
TreatmentRelative Growth Rate at Tillering (g m−2 day−1)Relative Growth Rate at the Flag Leaf Stage
(g m−2 day−1)
2021-222022-232021-222022-23
T1 = Control + No PGPR0.134 b0.139 b4.236 b4.263 b
T2 = C + PGPR0.143 a0.148 a4.580 a4.610 a
T3 = DI + No PGPR0.076 f0.074 f3.543 f3.483 f
T4 = DI + PGPR0.104 d0.108 d3.856 d3.826 d
T5 = PRD + No PGPR0.086 e0.085 e3.676 e3.680 e
T6 = PRD + PGPR0.122 c0.127 c4.016 c4.076 c
The different letters show a significant difference in treatments at 5% probability level. PGPR (plant-growth-promoting rhizobacteria); C (control); DI (deficit irrigation); and PRD (partial root drying).
Table 6. Effects of PGPR on the net assimilation rate (NAR) of wheat under different irrigation systems.
Table 6. Effects of PGPR on the net assimilation rate (NAR) of wheat under different irrigation systems.
TreatmentsNAR at Tillering (g m−2 day−1)NAR at the Flag Leaf Stage (g m−2 day−1)
2021-222022-232021-222022-23
T1 = Control + No PGPR1.423 b1.431 b4.433 b4.446 b
T2 = C + PGPR1.530 a1.527 a4.620 a4.643 a
T3 = DI + No PGPR1.042 f1.020 f3.633 f3.640 f
T4 = DI + PGPR1.234 d1.224 d4.023 d4.036 d
T5 = PRD + No PGPR1.125 e1.129 e3.830 e3.846 e
T6 = PRD + PGPR1.320 c1.318 c4.243 c4.263 c
The different letters show a significant difference in treatments at 5% probability level. PGPR (plant-growth-promoting rhizobacteria); C (control); DI (deficit irrigation); and PRD (partial root drying).
Table 7. Effects of PGPR on the leaf area index (LAI) of wheat under different irrigation systems.
Table 7. Effects of PGPR on the leaf area index (LAI) of wheat under different irrigation systems.
TreatmentLeaf Area Index at TilleringLeaf Area Index at the Flag Leaf Stage
2021-222022-232021-222022-23
T1 = Control + No PGPR2.32 b2.41 b7.06 b7.12 b
T2 = C + PGPR2.51 a2.63 a7.35 a7.43 a
T3 = DI + No PGPR1.70 f1.83 f6.01 f6.14 f
T4 = DI + PGPR1.98 d1.99 d6.57 d6.65 d
T5 = PRD + No PGPR1.81 e1.89 e6.31 e6.47 e
T6 = PRD + PGPR2.12 c2.21 c6.86 c6.95 c
The different letters show a significant difference in treatments at 5% probability level. PGPR (plant-growth-promoting rhizobacteria); C (control); DI (deficit irrigation); and PRD (partial root drying).
Table 8. Effects of PGPR on the available soil N, P, and K, organic matter content, and soil respiration of wheat under different irrigation systems.
Table 8. Effects of PGPR on the available soil N, P, and K, organic matter content, and soil respiration of wheat under different irrigation systems.
TreatmentAvailable Soil Nitrogen (mg kg−1)Available Soil Phosphorus (mg kg−1)Available Soil Potassium (mg kg−1)Soil Organic Matter (%)Soil Respiration (SR)
(µg CO2-C g−1 day−1)
2021-222022-232021-222022-232021-222022-232021-222022-232021-222022-23
T1 = Control + No PGPR30.14 b29.15 b14.30 b13.21 b60.37 b58.26 b1.31 b1.12 b24.11 b25.21 b
T2 = C + PGPR32.33 a31.35 a15.42 a14.33 a62.57 a60.46 a1.42 a1.23 a25.18 a26.34 a
T3 = DI + No PGPR22.21 f21.23 f10.42 f09.33 f52.45 f50.34 f0.98 f0.71 f20.14 f21.34 f
T4 = DI + PGPR26.32 d25.36 d12.31 d11.22 d56.58 d54.47 d1.17 d0.94 d22.16 d23.34 d
T5 = PRD + No PGPR24.12 e23.15 e11.41 e10.32 e54.37 e52.26 e1.09 e0.83 e21.47 e22.31 e
T6 = PRD + PGPR28.21 c27.26 c13.33 c12.24 c58.48 c56.37 c1.25 c1.02 c23.34 c24.45 c
The different letters show a significant difference in treatments at 5% probability level. PGPR (plant-growth-promoting rhizobacteria), C (control), DI (deficit irrigation), PRD (partial root drying).
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Alhammad, B.A.; Zaheer, M.S.; Ali, H.H.; Hameed, A.; Ghanem, K.Z.; Seleiman, M.F. Effect of Co-Application of Azospirillum brasilense and Rhizobium pisi on Wheat Performance and Soil Nutrient Status under Deficit and Partial Root Drying Stress. Plants 2023, 12, 3141. https://doi.org/10.3390/plants12173141

AMA Style

Alhammad BA, Zaheer MS, Ali HH, Hameed A, Ghanem KZ, Seleiman MF. Effect of Co-Application of Azospirillum brasilense and Rhizobium pisi on Wheat Performance and Soil Nutrient Status under Deficit and Partial Root Drying Stress. Plants. 2023; 12(17):3141. https://doi.org/10.3390/plants12173141

Chicago/Turabian Style

Alhammad, Bushra Ahmed, Muhammad Saqlain Zaheer, Hafiz Haider Ali, Akhtar Hameed, Kholoud Z. Ghanem, and Mahmoud F. Seleiman. 2023. "Effect of Co-Application of Azospirillum brasilense and Rhizobium pisi on Wheat Performance and Soil Nutrient Status under Deficit and Partial Root Drying Stress" Plants 12, no. 17: 3141. https://doi.org/10.3390/plants12173141

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop