Next Article in Journal
Implementation of Proximal and Remote Soil Sensing, Data Fusion and Machine Learning to Improve Phosphorus Spatial Prediction for Farms in Ontario, Canada
Previous Article in Journal
Growth Dynamic, Productivity, Evapotranspiration, and Water-Economic Indices of Forage Cactus under Different Irrigation Depths
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Agronomy
Volume 14
Issue 4
10.3390/agronomy14040692
agronomy-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

Enhancing Drought Resistance and Yield of Wheat through Inoculation with Streptomyces pactum Act12 in Drought Field Environments

by
Bin Yang
1,†,
Hongwei Wen
1,†,
Shanshan Wang
1,2,
Jinhui Zhang
1,
Yuzhi Wang
1,
Ting Zhang
1,
Kai Yuan
1,
Lahu Lu
1,
Yutao Liu
3,
Quanhong Xue
3 and
Hao Shan
1,*
1
Institute of Wheat Research, Shanxi Agricultural University, Linfen 041000, China
2
College of Agronomy, Shanxi Agricultural University, Taiyuan 030031, China
3
College of Natural Resources and Environment, Northwest A&F University, Yangling 712100, China
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Agronomy 2024, 14(4), 692; https://doi.org/10.3390/agronomy14040692
Submission received: 26 February 2024 / Revised: 20 March 2024 / Accepted: 25 March 2024 / Published: 27 March 2024
(This article belongs to the Section Farming Sustainability)
Browse Figures
Versions Notes

Abstract

:
Drought stress is the primary abiotic factor affecting wheat growth, development, and yield formation. The application of plant growth-promoting rhizobacteria (PGPR) represents an environmentally sustainable approach to mitigate the impacts of drought stress on wheat. This study conducted field experiments using two winter wheat varieties, the drought-sensitive variety Jimai 22 and the drought-resistant variety Chang 6878, aiming to investigate the effects of Streptomyces pactum Act12 inoculation on photosynthetic characteristics, physiological parameters, and yield traits during the jointing, heading, and middle-filling stages under drought stress. The results revealed that drought stresses significantly reduced chlorophyll content, leaf area, biomass, and yield in wheat, while Act12 inoculation significantly increased chlorophyll content, photosynthetic efficiency, antioxidant enzyme activity such as superoxide dismutase (SOD) and peroxidase (POD), osmolyte content (proline and soluble proteins), and decreased malondialdehyde (MDA) content. These combined effects alleviated drought stress, resulting in increased biomass and yield in wheat. Under drought stress, an increase in leaf proline content of 13.53% to 53.23% (Jimai 22) and 17.17% to 43.08% (Chang 6878) was observed upon Act12 inoculation. Moreover, a decrease in MDA content was recorded of 15.86% to 53.61% (Jimai 22) and 13.47% to 26.21% (Chang 6878). Notably, there was a corresponding increase in yield of 11.78% (Jimai 22) and 13.55% (Chang 6878). In addition, grain quality analysis revealed a significant improvement in grain hardness with Act12 inoculation. Therefore, Act12 demonstrates the potential for enhancing the sustainable development of wheat production in arid and semi-arid regions.

1. Introduction

Wheat (Triticum aestivum L.) is one of the most important cereal crops in the world, providing approximately 20% of the total calorie intake for humans [1]. With the continuous increase in population and rising demand for wheat consumption, ensuring stable wheat yields is crucial for food security. Relying only on natural precipitation necessitates a minimum of 450 mm of rainfall throughout the wheat’s growth season to satisfy the fundamental prerequisites for yield establishment [2]. In the North China Plain, the foremost region for wheat production in China, annual rainfall varies from 400 to 1000 mm [3]. However, only 20–30% of this occurs during the winter wheat growing season [4], leading to significant drought stress in most wheat fields without irrigation. Drought stress is the primary abiotic factor that significantly affects wheat growth, development, and yield formation, leading to annual yield losses ranging from 17% to 70% [5]. In response to this agricultural challenge, extensive research efforts have been directed toward breeding techniques and cultivation practices to optimize water utilization efficiency [6,7]. For instance, strategies include breeding drought-resistant varieties [8], incorporating organic amendments or fertilizers, such as compost, to enhance soil moisture retention [9], and employing plastic mulch to diminish the evaporation of soil moisture [10]. Although some progress has been made, most existing methods to mitigate the effects of drought are time-consuming, labor-intensive, environmentally polluting, and costly [11]. Therefore, an urgent need is to explore a practical and environmentally friendly approach that can enhance drought resistance in wheat.
Plant growth-promoting rhizobacteria (PGPR) are beneficial strains that reside in the rhizosphere or colonize the root surface of plants, playing an important role in promoting plant growth. PGPR promotes the uptake of essential nutrients such as nitrogen, iron, phosphorus, potassium, and zinc in wheat through various mechanisms, including nitrogen fixation, production of iron chelators, and organic acids to dissolve mineral elements in the soil that are difficult for plants to access [12]. Additionally, they can produce plant hormones such as indole-3-acetic acid (IAA) and cytokinin (CTK), promoting wheat growth [13]. PGPR can also enhance the drought resistance of wheat. For example, Bacillus proteus promotes wheat seed germination, enhancing emergence under drought stress by producing extracellular polysaccharides [14,15]. Under drought conditions, Bacillus megaterium MU2 and Bacillus amyloliquefaciens produce 1-aminocyclopropane-1-carboxylate deaminase (ACC-deaminase), degrading the precursor substance ACC (1-aminocyclopropane-1-carboxylic acid) involved in ethylene synthesis in wheat, thus alleviating ethylene stress levels [16,17]. Burkholderia cepacia and arbuscular mycorrhizal fungi (AMF) can induce the accumulation of osmolytes such as proline and soluble proteins in wheat, enhancing its water retention and water uptake capacity under drought stress, thereby improving its water use efficiency [18]. Piriformospora indica can enhance the activity of various antioxidant enzymes in wheat, including SOD, POD, catalase (CAT), ascorbate peroxidase (APX), and glutathione reductase (GR), thereby forming an adequate antioxidant defense system. It helps to remove excessive reactive oxygen species generated under drought stress, delays the degradation of chlorophyll and thylakoid membrane proteins, maintains organelle integrity, and improves drought resistance in wheat [19]. Additionally, AMF can modify the root architecture of wheat, increasing the absorption surface area of roots and promoting the uptake of water and nutrients by the root system [20].
Research on improving drought resistance in wheat using PGPR has mainly focused on bacteria and fungi [21,22,23,24]. However, studies on using actinomycetes, the primary producers of agricultural antibiotics, to enhance wheat drought resistance have received less attention [25,26]. Yandigeri et al. found that Streptomyces coelicolor DE07 promotes the aboveground biomass and root length, tiller number, spikelet number, and yield of wheat plants under drought stress conditions [27]. Streptomyces corchorusii UCR3-16 can produce IAA and gibberellins (GA3), thus promoting the growth of wheat seedlings [28]. However, current research on PGPR’s ability to enhance drought resistance in wheat primarily occurs in laboratory settings, and there are limited successful cases of commercial application [29,30]. This could be attributed to several reasons. Firstly, adverse environmental conditions, such as drought and high temperatures, can also inhibit the growth of PGPR [31]. Secondly, some PGPR strains exhibit host specificity, displaying variations in their affinity towards different hosts, including promoting the growth of some hosts while inhibiting others [32]. Thirdly, PGPR may engage in competitive or antagonistic interactions with local soil microorganisms [33]. Lastly, current research on the role of PGPR in enhancing crop drought resistance primarily focuses on the seedling stage, with a notable lack of experimental validation during the mature plant phase. Moreover, findings from seedling-stage studies provide limited guidance for the practical application of PGPR in field conditions [34]. Consequently, PGPR products that are successfully commercialized should at least exhibit the ability to consistently and significantly enhance performance across a variety of crops or various cultivars of a specific crop. This encompasses increased yield, improved nutrient uptake efficiency, and enhanced crop resistance against adverse conditions [29]. Moreover, these products must be adaptable to a wide range of environmental conditions, including diverse soil types, climatic conditions, and crop species [30]. Additionally, the efficacy and stability of PGPR products should be validated through multi-year, multi-site field trials [35]. Hence, to improve the application of PGPR for enhancing drought resistance in wheat, it is necessary to conduct field experiments and further investigate these issues.
Our previous studies isolated a strain of Streptomyces pactum called Act12 from arid environments, which can produce ACC-deaminase, IAA, and other metabolites. Our findings indicate that Act12 promotes the growth of various plant species, such as cucumber, tomato, chili pepper, sunflower, and jujube [11,36,37]. Building on these findings, our investigation employed field experiments with the moisture-sensitive wheat variety Jimai 22 and the drought-resistant Chang 6878. The research aimed at analyzing drought-sensitive indicators such as leaf size, biomass, chlorophyll content, Fv/Fm ratio, SOD and POD enzyme activities, proline and soluble protein contents, MDA levels, and yield, to assess the impact of Act12 inoculation during critical growth stages (jointing, heading, and middle-filling) under drought stress conditions. It is hypothesized that inoculation with Streptomyces pactum Act12 will result in a significant enhancement of photosynthetic efficiency, physiological resilience, and yield of wheat under drought conditions. This would illustrate the potential of Act12 for application in improving drought resistance in wheat. Our research aims to establish a theoretical basis for the commercial utilization of Act12 in enhancing drought resistance in wheat.

2. Materials and Methods

2.1. Plant Material and Biological Material

The wheat varieties used in this study were Jimai 22 and Chang 6878. Jimai 22 is the most widely cultivated waterland winter variety in China, while Chang 6878 is a drought-resistant dryland winter variety commonly grown in the northern regions of China.
The Streptomyces partum Act12 (GenBank: MH542148) was isolated from extreme arid and cold environments on the Qinghai-Tibet Plateau by the Microbial Resources Laboratory of the College of Natural Resources and Environment of Northwest A&F University. The concentration of viable cells in the Act12 inoculant was 4.6 × 1010 CFU·g−1.
Before planting, wheat seeds were thoroughly mixed with a sodium carboxymethyl cellulose solution of 6 g/L, ensuring an even distribution on the seed surface. Subsequently, the wheat seeds were mixed with Act12 powder, accounting for 5% of the seed mass, and gently stirred to ensure uniform coating of the seeds [38]. The treated seeds dried in a shaded area.

2.2. Field Experiment

During the 2018–2019 period, experimental materials were cultivated at the Hancun Experimental Station of the Wheat Research Institute, Shanxi Agricultural University, Shanxi Province, China, situated at an elevation of 459.00 m (111°34′36″ E, 36°8′43″ N). Located within the North China Plain, the site is characterized by a typical temperate continental semi-arid climate, receiving an average annual rainfall of 457.71 mm and maintaining an average annual temperature of 13.08 °C. The total rainfall during the wheat growing season (October 2018 to June 2019) was 93.6 mm, rainfall from the tillering to the jointing stages (November 2018 to March 2019) amounted to 34.0 mm, from jointing to heading stages (March 2019 to April 2019) was 35.2 mm, and from filling to maturity stages (May 2019 to June 2019) totaled 24.0 mm (Figure 1). The soil type is calcareous brown soil, pH 8.78, with organic matter content of 18.70 g·kg−1, total nitrogen content of 1.06 g·kg−1, available nitrogen content of 44.61 mg·kg−1, available phosphorus content of 6.78 mg·kg−1, and available potassium content of 128.02 mg·kg−1.
The experiment comprised four treatments. (1) W group: normal irrigation; (2) W+Act12 group: normal irrigation and seeds inoculated with Act12; (3) D group: reliance on natural rainfall throughout the entire growth period of wheat; and (4) D+Act12 group: reliance on natural rainfall and seeds inoculated with Act12. The W group and W+Act12 group irrigated during the overwintering, jointing, and grain-filling stage, with an irrigation amount of 700 m3·ha−1. The experimental design followed a randomized complete block design with three replications. Each plot measured 5 × 1.3 m. Before planting, the foundational fertilization for all experimental treatments included the application of 150 kg·ha−1 nitrogen (N), 105 kg·ha−1 phosphorus pentoxide (P2O5), and 50 kg·ha−1 potassium oxide (K2O). Fertilizers were not applied during the growth periods.

2.3. Plant Growth Parameters

Five wheat plants with consistent growth within each plot were randomly selected to measure leaf length, width, and fresh weight during the heading and middle-filling stages. The leaves, stems, and spikes were dried in an oven at 105 °C for 15 min and then weighed after reaching a constant weight of 80 °C.

2.4. Determination of Chlorophyll Content and Chlorophyll Fluorescence Parameters

Five wheat plants with consistent growth within each plot were randomly selected during the jointing, heading, and middle-filling stages. The chlorophyll content of the flag leaves was measured using a SPAD-502 Plus chlorophyll meter (Konica-Minolta, Tokyo, Japan) [39]. Chlorophyll fluorescence parameters were measured using a PAM-2500 chlorophyll fluorometer (Waltz, Effeltrich, Germany). Before measurement, the wheat leaves were dark-adapted for 20 min at a light intensity of 400 μmol·m−2·s−1, followed by a saturation pulse of 8000 μmol·m−2·s−1. The maximum photochemical efficiency of Photosystem II (PSII) (Fv/Fm) was calculated as (Fm − Fo)/Fm, where Fo was the initial fluorescence, Fm was the maximum fluorescence, and Fv was the variable fluorescence.

2.5. Determination of Antioxidant Enzyme Activity, MDA, and Osmolyte Content

The uppermost leaves of wheat plants from each treatment were collected during the jointing, heading, and middle-filling stages; rapidly frozen in liquid nitrogen; and stored at −80 °C. Before analysis, the samples from each treatment were ground and thoroughly mixed with three replicates. A leaf sample of 0.5 g was weighed and subsequently homogenized in 5 mL of 50 mM phosphate buffer (pH 7.0, with 0.1 mM EDTA) using a prechilled mortar and pestle. The resulting homogenate was centrifuged at 12,000 rpm for 20 min at 4 °C. The plant enzyme extract obtained was then employed in the assays to determine SOD and POD activities.
The SOD activity was measured spectrophotometrically by assessing the inhibition of photochemical reduction of NBT at 560 nm. The reaction mixture contained 33 mM NBT, 10 mM L-methionine, 0.66 mM EDTANa2, and 0.0033 mM riboflavin in 0.05 M phosphate buffer (pH 7.8) and 0.1 mL of plant enzyme extract. One unit of SOD is defined as the amount of enzyme that inhibits 50% of NBT photoreduction. Reactions were conducted at 25 °C under a light intensity of approximately 4000 flux for 20 min. The original methods were modified as described by Costa et al. [40].
The POD activity was assessed using the method described by Kochba et al. [41]. A reaction mixture comprises 0.2 mL of plant enzyme extract, 50 mM phosphate buffer (pH 7.0), guaiacol (20 mM final concentration), and H2O2 (40 mM final concentration). The reaction is initiated by the addition of H2O2, followed by the measurement of absorbance increase at 470 nm resulting from guaiacol oxidation over a period of 1–3 min at ambient temperature. The calculation of POD activity is derived from the rate of absorbance change per minute.
The extent of lipid peroxidation was determined by quantifying MDA using a colorimetric method. For this, 0.5 g of grounded leaf samples were homogenized in 5 mL of distilled water, and an equal volume of 0.5% thiobarbituric acid in 20% trichloroacetic acid (TCA) was added. The solution was incubated at 95 °C for 30 min. Subsequently, the adsorption was measured at 532 nm and then at 600 nm to subtract the value of non-specific absorption for the calculation of MDA contents [42].
The proline contents were estimated according to Bates et al. [43]. Fresh leaf samples weighing 0.2 g from each group were ground into a fine powder using liquid nitrogen in a sterilized mortar and pestle. The leaf samples were homogenized in 100 mM PBS buffer (pH 7.8) to extract crude protein. The homogenate was centrifuged at 12,000 rpm for 15 min at 4 °C, and the supernatant was aliquoted into new sterile tubes. The proline content of the leaf was obtained from the 50 µL crude plant extract added to 1 mL of the reaction mixture, followed by boiling in a water bath for 50 min at 98 °C. The reaction mixture was incubated on ice for 5 min, and 2 mL of toluene with vortexing was added. A total of 1 mL of supernatant was used to read absorbance at 520 nm.
The protein concentration was determined by Bradford’s method [44] using bovine serum albumin (BSA) as a standard.

2.6. Determination of Yield-Related Traits

After maturity, five wheat plants with similar heights were randomly selected from each plot. The plant height, spike length, number of effective spikes, number of grains per spike, and thousand-grain weight were measured. Subsequently, the yield of each plot was harvested and recorded.

2.7. Analysis of Grain Quality Traits

A multi-functional near-infrared grain quality analyzer (DA7200, Perten, Stockholm, Sweden) was employed to measure grain hardness, test weight, protein content, wet gluten content, sedimentation, dough development time, and dough stability time.

2.8. Statistical Analysis

All data were analyzed using the SPSS 20.0 software (SPSS Inc., Chicago, IL, USA) with an LSD test (p < 0.05). Graphs were generated using Origin2018 software (OriginLab, Northampton, MA, USA).

3. Results

3.1. Effects of Act12 Inoculation on Wheat Plant Growth Parameters under Drought Stress

Compared to normal irrigation conditions, drought stress significantly reduced the plant height, leaf length, leaf width, and leaf area, as well as the fresh and dry weights of leaves, stems, and spikes in both wheat varieties (p < 0.05) (Figure 2). However, under both water conditions, inoculation with Act12 significantly enhanced the leaf length and biomass, indicating a growth-promoting effect of Act12 on wheat. This promoting effect was particularly pronounced under drought stress. During the heading and middle-filling stages, the dry weight of Jimai 22 and Chang 6878 inoculated with Act12 increased by 65.88% and 61.85%, respectively (Figure 2k), as well as 42.86% and 44.36% (Figure 2l), suggesting that Act12 may have a more substantial growth-promoting effect on drought-sensitive variety compared to drought-resistant one.

3.2. Effects of Act12 Inoculation on Leaf Photosynthetic Characteristics under Drought Stress

During the jointing, heading, and middle-filling stages, drought stress significantly reduced the chlorophyll content in the leaves of both wheat varieties. However, inoculation with Act12 significantly increased the chlorophyll content during all three stages (Figure 3a,b). Specifically, Jimai 22 exhibited an increase of 4.09%, 5.87%, and 11.06% in chlorophyll content during the 3 stages (Figure 3a), while Chang 6878 showed increases of 2.07%, 4.10%, and 5.10% (Figure 3b). These results indicate that Act12 inoculation effectively alleviates the degradation of chlorophyll under drought stress.
Chlorophyll fluorescence kinetics parameters are essential indicators reflecting the level of plant stress. Fv/Fm is considered one of the most sensitive indicators [45]. Under drought stress, the Fv/Fm values of the leaves at different developmental stages generally decreased (Figure 3c,d), especially during the middle-filling stage. Jimai 22 and Chang 6878 experienced significant reductions of 10.31% and 8.25% in their Fv/Fm values, respectively. Under conditions of drought stress, the middle-filling stages of Jimai 22 and Chang 6878 inoculated with Act12 exhibited a significant enhancement in Fv/Fm values by 5.05% and 5.98%, respectively, in comparison to their uninoculated counterparts. This increase markedly mitigated the adverse effects of drought stress on Photosystem II.

3.3. Effects of Act12 Inoculation on Leaf Antioxidant Enzyme Activity under Drought Stress

Under drought stress conditions, compared to normal irrigation, the activity of SOD and POD enzymes in the leaves of both wheat varieties significantly increased during the jointing, heading, and middle-filling stages (Figure 4). Specifically, during three distinct periods, the SOD activity of Jimai 22 exhibited significant enhancements of 5.23%, 12.01%, and 20.76%, respectively (Figure 4a), while Chang 6878 showed significant increases of 13.79%, 6.17%, and 7.11% (Figure 4b). Similarly, the POD activity of Jimai 22 demonstrated significant gains of 26.71%, 39.09%, and 11.59% across these intervals (Figure 4c), while Chang 6878, which revealed notable enhancements of 23.67%, 7.33%, and 36.74%, respectively (Figure 4d).
Under drought stress, Jimai 22 inoculated with Act12 exhibited a significant increase in SOD activity ranging from 7.13% to 24.60% across the three stages (Figure 4a), and POD activity increased significantly by 10.20% to 11.73% (Figure 4c). Similarly, Chang 6878 inoculated with Act12 showed enhancements in SOD activity ranging from 7.38% to 11.12% (Figure 4b) and an increase in POD activity ranging from 4.26% to 14.47% (Figure 4d). These results indicate that Act12 inoculation effectively enhances the antioxidant enzyme activity in the leaves, mitigating oxidative damage caused by drought stress and strengthening wheat’s drought resistance capability.

3.4. Effects of Act12 Inoculation on MDA and Osmolyte Content in Wheat under Drought Stress

Under drought stress conditions, the MDA content in the Jimai 22 and Chang 6878 leaves significantly increased during the jointing, heading, and middle-filling stages, indicating membrane damage caused by drought stress. It is noteworthy that during the middle-filling stage, the MDA content in the leaves of Chang 6878 was lower than that of Jimai 22, suggesting milder membrane damage and more excellent drought resistance in Chang 6878. Act12 inoculation significantly reduced the MDA content in the leaves of both varieties during all three stages. Specifically, the MDA content in Jimai 22 decreased by 15.86% to 53.61%, while in Chang 6878, it decreased by 13.47% to 26.21% (Figure 5a,b), demonstrating the significant effect of Act12 in alleviating membrane damage caused by drought stress.
Drought stress also significantly increased the leaves’ osmolyte content (proline and soluble proteins). Act12 inoculation further significantly enhanced the content of proline and soluble proteins during the jointing, heading, and middle-filling stages. Specifically, the proline content in the leaves of Jimai 22 increased by 53.23%, 21.61%, and 13.53%, respectively, while in Chang 6878, it increased by 43.08%, 40.19%, and 17.17% (Figure 5c,d). These findings indicate that Act12 inoculation can produce more osmolytes in wheat leaves, enabling better adaptation to drought stress.

3.5. Effects of Act12 Inoculation on Wheat Yield and Related Traits under Drought Stress

Compared to normal irrigation, drought stress significantly reduced spike length, the number of effective spikes, grains per spike, thousand-grain weight, and yield in Jimai 22 and Chang 6878, with yield decreases of 75.91% and 64.60%, respectively (Figure 6). Except for spike length and thousand-grain weight, inoculation with Act12 had a significant positive effect on the yield and its related traits under drought stress. Under drought conditions, yields of Act12-inoculated Jimai 22 and Chang 6878 increased by 11.78% and 13.55%, respectively, compared to the uninoculated controls (Figure 6e,j). It is worth noting that although the impact of Act12 on thousand-grain weight was insignificant, it led to a significant increase in overall yield by increasing the effective spike number and grain number per spike. This finding demonstrates the critical role of Act12 in enhancing wheat yield and its components under drought conditions.

3.6. Effects of Act12 Inoculation on Quality Traits under Drought Stress

Under both water conditions, the impact of Act12 inoculation on protein content, wet gluten content, sedimentation, dough development time, and dough stability time of Jimai 22 and Chang 6878 was insignificant. Under drought stress conditions, a significant decrease in grain hardness and test weight was observed. However, both varieties inoculated with Act12 significantly improved grain hardness, with an increase of 30.76% in Jimai 22 and 14.81% in Chang 6878 (Table 1).

4. Discussion

The North China Plain is distinguished as a crucial agricultural region in China, contributing over three-quarters of the nation’s wheat production [46]. Despite the annual rainfall being between 400 mm and 1000 mm, the precipitation during the wheat’s growing season only accounts for 20–30%, which cannot meet the requirements for the normal formation of wheat yield. [4]. As a result, the repercussions of drought stress on wheat development are profound and pervasive throughout the North China Plain. Drought is recognized as a crucial factor that adversely affects wheat growth and development. During the wheat growth stages, drought stress adversely affects photosynthesis and assimilation processes, causing oxidative damage to cell membranes, restricted mineral nutrient uptake, and disrupted hormone metabolism, ultimately severely impairing biomass accumulation and yield formation [47,48].
Enhancing wheat drought resistance through PGPR has been widely acknowledged as a promising eco-friendly and cost-effective sustainable agricultural approach [49]. Generally, PGPR strains isolated from harsh environments such as drought exhibit the potential to assist crops in stress resistance [17]. Previously, we isolated a drought-resistant actinomycete strain, Act12, from the extremely arid and cold environment of the Qinghai-Tibet Plateau. Biological characterization revealed that Act12 produces IAA, ACC-deaminase, and iron-chelating compounds and possesses phosphate and iron solubilization abilities [50]. In a pot experiment, inoculating Act12 improved the early-stage drought resistance of the water-sensitive wheat variety XN979 [47]. Based on this finding, a subsequent field experiment was carried out in this study, where two wheat varieties with different water sensitivity were subjected to inoculation with Act12. The focus of our research is not merely to highlight the growth-promotional activities of Streptomyces pactum Act12, but more importantly, to elucidate its significant contribution to enhancing wheat’s drought resistance.

4.1. Act12’s Role in Enhancing Drought Resistance of Wheat

Under drought stress, this study found significant reductions in wheat’s flag leaf dimensions and a notable decrease in leaf area (Figure 2). Chlorophyll content and Fv/Fm ratios also significantly dropped across various growth stages (Figure 3). However, Act12 inoculation markedly improved flag leaf area, chlorophyll content, and Fv/Fm (middle-filling stage) under drought stress conditions. These benefits can be attributed to Act12’s ability to produce ACC-deaminase and IAA and to solubilize phosphorus [50]. ACC-deaminase transforms ACC into NH3 and α-ketobutyrate, providing nitrogen nutrition to wheat and reducing ethylene’s harmful effects on cellular membranes and chloroplasts, thus preserving leaf photosynthesis and delaying senescence [51,52]. IAA and phosphorus enhance root system development, root hair growth, and nutrient and water absorption, promoting overall plant health [53,54]. The synergistic effect of ACC-deaminase and IAA notably supports root elongation [55]. Supporting evidence shows that the co-application of Bacillus amyloliquefaciens and Agrobacterium fabrum, both producing ACC-deaminase, significantly enhanced photosynthetic rate, transpiration rate, stomatal conductance, as well as chlorophyll a and chlorophyll b content under drought stress [16]. Similarly, Enterobacter bugandensis WRS7, which produces ACC-deaminase, increased leaf chlorophyll content under drought stress, indirectly improving leaf photosynthetic efficiency and energy metabolism [22].

4.2. Physiological Improvements by Act12 Inoculation under Drought Stress

Drought stress induces an increase in reactive oxygen species (ROS) production, disrupting cellular membranes and organelles and impairing plant metabolism. In response, plants deploy a comprehensive antioxidant defense system that merges osmotic regulation with antioxidant enzymes to scavenge ROS and mitigate oxidative damage [56]. Antioxidant enzymes play a key role in neutralizing ROS, thereby protecting cellular structures from oxidative harm [57]. Concurrently, osmolytes such as proline and soluble proteins are pivotal for osmotic adjustment and safeguarding the integrity of cells under stress conditions [58]. These adaptations are crucial in the plant’s defense against drought stress, offering dual protection mechanisms. As drought stress intensifies, wheat commonly demonstrates elevated MDA concentrations, signaling increased lipid peroxidation and cellular injury. Although antioxidant enzyme activities and osmolyte levels are enhanced, such adjustments fall short of effectively mitigating oxidative stress [59,60].
Our investigation revealed that, at different developmental stages, drought stress significantly elevated the levels of antioxidant enzymes and osmolytes in leaves, alongside a marked increase in MDA levels, indicative of damage to leaf cell membranes. Relative to drought controls, Act12 inoculation markedly improved wheat’s drought resistance by enhancing physiological responses, notably through the upregulation of antioxidant enzyme (SOD and POD) activities and the augmentation of osmolytes (proline and soluble proteins) concentrations under drought stress conditions. This adjustment significantly mitigates the drought-induced oxidative stress, as evidenced by the reduced MDA levels in wheat leaves, which signifies diminished lipid peroxidation and less cellular damage.

4.3. Act12 Inoculation Promotes Yield Formation under Drought Stress

This research demonstrates a pronounced decline in biomass and yield of wheat when subjected to drought stress as opposed to conditions of normal irrigation. Under drought conditions, wheat inoculated with Act12 is observed to possess significantly higher antioxidant enzyme activities and levels of osmoregulatory compounds compared to its drought-stressed counterparts. Such augmentation leads to reduced peroxidative damage to the leaves, enhanced content of chlorophyll, increased photosynthetic efficiency, and enlarged leaf size, which collectively contribute to a substantial increase in biomass and yield.
The administration of Act12 was found to enhance both biomass and yield in wheat across varied moisture conditions. Notably, the growth-promoting impact of Act12 under conditions of drought stress was observed to be markedly superior compared to that under normal irrigation conditions. Meta-analysis of research data on PGPR inoculation in multiple crops by Zhao et al. confirms that PGPR is more effective in increasing plant biomass and yield, enhancing photosynthesis, and suppressing oxidative damage under drought conditions [48]. It indicates a shift in the interaction between plants and PGPR under drought stress. Root exudates, which are messengers between plants and PGPR, can provide a nutrient supply to PGPR. Under drought stress, there are changes in the quantity and composition of root exudates, including a significant increase in the content of assimilation products of photosynthesis [61]. It provides nutrients to PGPR, thus enhancing their ability to assist plants in drought resistance and growth promotion, and helps to recruit more beneficial bacteria in the soil to enhance plant drought resistance synergistically. Therefore, under drought stress conditions, this interaction promotes yield formation [62].
The number of effective spikes, number of grains per spike, and thousand-grain weight are the three essential factors influencing wheat yield formation, with thousand-grain weight having the highest heritability and less affected by the environment [63]. Previous studies have demonstrated that PGPR inoculation under drought stress conditions significantly increases the thousand-grain weight of wheat, thereby increasing yield [64]. However, in this study, it was observed that drought stress significantly reduced the number of effective spikes, number of grains per spike, and thousand-grain weight. Remarkably, Act12 inoculation led to a notable enhancement in the number of effective spikes, grains per spike, and an increase in yield under drought-stress conditions. However, no significant impact was observed on the thousand-grain weight. Consequently, the increase in yield can be attributed primarily to the amplified number of effective spikes and grains per spike facilitated by Act12 inoculation under drought-stress conditions (Figure 6). This phenomenon may be attributed to different PGPR strains having distinct growth-promoting functions, leading to variations in their mechanisms and effects on plants [48].
Under drought conditions, the available nitrogen content in the soil decreases, severely affecting the nitrogen uptake by wheat roots [65], thereby limiting grain protein synthesis. PGPR strains with nitrogen-fixing capabilities can provide nitrogen to wheat under drought conditions, significantly increasing grain protein content [66]. However, in this study, it was observed that inoculation with Act12 significantly increased grain hardness under drought stress but had no significant effect on indicators such as grain protein content. It may be attributed to Act12’s lack of nitrogen-fixing ability, thus making it unable to provide additional nitrogen nutrients to wheat.

4.4. Act12 Has Potential for Commercial Applications

This study revealed that inoculation with Act12 significantly improved drought resistance at different stages of development and ultimately increased yield in various wheat varieties under field conditions. It indicates that Act12 can withstand environmental stress and exhibits a consistent drought-resistant and growth-promoting effect across different wheat cultivars. Extensive prior research has also confirmed the stress-resistant and growth-promoting roles of Act12 in various plants, including wheat, tomato, pepper, sunflower, and jujube [11,36,47,67,68]. It seems Act12 has significant commercialization potential and application value. However, extensive multi-year and multi-site field experiments are still required before commercial application to validate its efficacy. Further studies delving into the molecular mechanisms by which Act12 enhances wheat drought resistance will better understand the interaction between Act12 and wheat, offering scientific insights for optimization and application.

5. Conclusions

This study investigated the impact of Act12 inoculation on wheat subjected to drought stress. Observations indicated significant enhancements in chlorophyll content, photosynthetic efficiency, antioxidant enzyme activity, and osmolyte levels, alongside reduced MDA levels. Resulting enhancements in biomass and yield highlight Act12’s ability to mitigate drought stress in wheat. This research stands out by leveraging microbial technology to enhance wheat’s drought resistance and productivity, diverging from traditional water management and soil improvement methods.
However, the precise molecular mechanisms by which Act12 functions are still unknown. Future research should aim to elucidate the signal transduction pathways and gene expression changes induced by Act12 inoculation. Confirming these results via comprehensive field trials in varied climatic conditions is essential.

Author Contributions

Conceptualization, B.Y., L.L., Y.L., Q.X. and H.S.; data curation, S.W. and Y.W.; formal analysis, S.W. and J.Z.; methodology, B.Y., H.W., T.Z., Y.L. and Q.X.; software, S.W., J.Z. and K.Y.; visualization, J.Z., T.Z. and K.Y.; validation, H.W., L.L., Q.X. and H.S.; investigation, H.W., Y.W., T.Z. and K.Y.; resources, Y.W. and Y.L.; writing—original draft preparation, B.Y. and H.W.; writing—review and editing, B.Y., H.W., S.W., J.Z., Y.W., T.Z., K.Y., L.L., Y.L., Q.X. and H.S.; supervision, L.L. and H.S.; funding acquisition, B.Y. and H.S. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Central Leading Local Technology Development Fund Project of Shanxi Province, grant numbers YDZJSX2022A033 and YDZJSX20231A039, and the Technology Innovation and Enhancement Program of Shanxi Agricultural University, grant number CXGC2023058.

Data Availability Statement

Data are contained within the article.

Acknowledgments

The authors would like to thank their colleagues, whose suggestions helped improve the manuscript’s contents.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. Qu, P.; Wang, J.; Wen, W.; Gao, F.; Liu, J.; Xia, X.; Peng, H.; Zhang, L. Construction of consensus genetic map with applications in gene mapping of wheat (Triticum aestivum L.) using 90K SNP array. Front. Plant Sci. 2021, 12, 727077. [Google Scholar] [CrossRef]
  2. Xiao, D.P.; Shen, Y.J.; Qi, Y.Q.; Moiwo, J.P.; Min, L.L.; Zhang, Y.C.; Guo, Y.; Pei, H.W. Impact of alternative cropping systems on groundwater use and grain yields in the North China Plain Region. Agric. Syst. 2017, 153, 109–117. [Google Scholar] [CrossRef]
  3. Xiao, D.P.; Liu, D.L.; Wang, B.; Feng, P.Y.; Bai, H.Z.; Tang, J.Z. Climate change impact on yields and water use of wheat and maize in the North China Plain under future climate change scenarios. Agric. Water Manag. 2020, 238, 106238. [Google Scholar] [CrossRef]
  4. Meng, Q.F.; Sun, Q.P.; Chen, X.P.; Cui, Z.L.; Yue, S.C.; Zhang, F.S.; Römheld, V. Alternative cropping systems for sustainable water and nitrogen use in the North China Plain. Agric. Ecosyst. Environ. 2012, 146, 93–102. [Google Scholar] [CrossRef]
  5. Nouri-Ganbalani, A.; Nouri-Ganbalani, G.; Hassanpanah, D. Effects of drought stress condition on the yield and yield components of advanced wheat genotypes in Ardabil, Iran. J. Food Agric. Environ. 2009, 7, 228–234. [Google Scholar]
  6. Passioura, J. The drought environment: Physical, biological and agricultural perspectives. J. Exp. Bot. 2007, 58, 113–117. [Google Scholar] [CrossRef] [PubMed]
  7. Ngumbi, E.; Kloepper, J. Bacterial-mediated drought tolerance: Current and future prospects. Appl. Soil. Ecol. 2016, 105, 109–125. [Google Scholar] [CrossRef]
  8. Ayalew, H.; Ma, X.; Yan, G. Screening wheat (Triticum spp.) genotypes for root length under contrasting water regimes: Potential sources of variability for drought resistance breeding. J. Agron. Crop Sci. 2015, 201, 189–194. [Google Scholar] [CrossRef]
  9. Amirahmadi, E.; Ghorbani, M.; Moudry, J.; Bernas, J.; Mukosha, C.E.; Hoang, T.N. Environmental assessment of dryland and irrigated winter wheat cultivation under compost fertilization strategies. Plants 2024, 13, 509. [Google Scholar] [CrossRef]
  10. Qi, Y.L.; Yang, X.M.; Pelaez, A.M.; Lwanga, E.H.; Beriot, N.; Gertsen, H.; Garbeva, P.; Geissen, V. Macro- and micro- plastics in soil-plant system: Effects of plastic mulch film residues on wheat (Triticum aestivum) growth. Sci. Total Environ. 2018, 645, 1048–1056. [Google Scholar] [CrossRef]
  11. Li, Y.; Li, H.; Han, X.; Han, G.; Xi, J.; Liu, Y.; Zhang, Y.; Xue, Q.; Guo, Q.; Lai, H. Actinobacterial biofertilizer improves the yields of different plants and alters the assembly processes of rhizosphere microbial communities. Appl. Soil. Ecol. 2022, 171, 104345. [Google Scholar] [CrossRef]
  12. Ijaz, M.; Tahir, M.; Shahid, M.; Ul-Allah, S.; Sattar, A.; Sher, A.; Mahmood, K.; Hussain, M. Combined application of biochar and PGPR consortia for sustainable production of wheat under semiarid conditions with a reduced dose of synthetic fertilizer. Braz. J. Microbiol. 2019, 50, 449–458. [Google Scholar] [CrossRef] [PubMed]
  13. Sokolova, M.G.; Akimova, G.P.; Vaishlya, O.B. Effect of phytohormones synthesized by rhizosphere bacteria on plants. Appl. Biochem. Microbiol. 2011, 47, 274–278. [Google Scholar] [CrossRef]
  14. Etesami, H.; Beattie, G.A. Mining halophytes for plant growth-promoting halotolerant bacteria to enhance the salinity tolerance of non-halophytic crops. Front. Microbiol. 2018, 9, 148. [Google Scholar] [CrossRef] [PubMed]
  15. Kumar, A.; Maurya, B.; Raghuwanshi, R. Isolation and characterization of PGPR and their effect on growth, yield and nutrient content in wheat (Triticum aestivum L.). Biocatal. Agric. Biotechnol. 2014, 3, 121–128. [Google Scholar] [CrossRef]
  16. Zafar-Ul-Hye, M.; Danish, S.; Abbas, M.; Ahmad, M.; Munir, T.M. ACC deaminase producing PGPR Bacillus amyloliquefaciens and Agrobacterium fabrum along with biochar improve wheat productivity under drought stress. Agronomy 2019, 9, 343. [Google Scholar] [CrossRef]
  17. Rashid, U.; Yasmin, H.; Hassan, M.N.; Naz, R.; Nosheen, A.; Sajjad, M.; Ilyas, N.; Keyani, R.; Jabeen, Z.; Mumtaz, S.; et al. Drought-tolerant Bacillus megaterium isolated from semi-arid conditions induces systemic tolerance of wheat under drought conditions. Plant Cell Rep. 2022, 41, 549–569. [Google Scholar] [CrossRef] [PubMed]
  18. Naveed, M.; Hussain, M.B.; Zahir, Z.A.; Mitter, B.; Sessitsch, A. Drought stress amelioration in wheat through inoculation with Burkholderia phytofirmans strain PsJN. Plant Growth Regul. 2014, 73, 121–131. [Google Scholar] [CrossRef]
  19. Sun, C.; Johnson, J.M.; Cai, D.; Sherameti, I.; Oelmuller, R.; Lou, B. Piriformospora indica confers drought tolerance in Chinese cabbage leaves by stimulating antioxidant enzymes, the expression of drought-related genes and the plastid-localized CAS protein. J. Plant Physiol. 2010, 167, 1009–1017. [Google Scholar] [CrossRef]
  20. Luo, W.; Li, J.; Ma, X.; Niu, H.; Hou, S.; Wu, F. Effect of arbuscular mycorrhizal fungi on uptake of selenate, selenite, and selenomethionine by roots of winter wheat. Plant Soil. 2019, 438, 71–83. [Google Scholar] [CrossRef]
  21. Alaskar, A.A.; Al-Shwaiman, H.A. The effect of plant growth-promoting rhizobacteria on soil properties and the physiological and anatomical characteristics of wheat under water-deficit stress conditions. Agriculture 2023, 13, 2042. [Google Scholar] [CrossRef]
  22. Arora, S.; Jha, P.N. Drought-tolerant Enterobacter bugandensis WRS7 induces systemic tolerance in Triticum aestivum L. (wheat) under drought conditions. J. Plant Growth Regul. 2023, 42, 7715–7730. [Google Scholar] [CrossRef]
  23. Guzel, K.; Tatiana, A.; Dmitriy, V. Water relations in plants treated with growth promoting rhizosphere bacteria. Plant Soil 2023, 494, 51–72. [Google Scholar]
  24. Ikan, C.; Ben-Laouane, R.; Ouhaddou, R.; Ghoulam, C.; Meddich, A. Co-inoculation of arbuscular mycorrhizal fungi and plant growth-promoting rhizobacteria can mitigate the effects of drought in wheat plants (Triticum durum). Plant Biosyst. 2023, 157, 907–919. [Google Scholar] [CrossRef]
  25. Viaene, T.; Langendries, S.; Beirinckx, S.; Maes, M.; Goormachtig, S. Streptomyces as a plant’s best friend? Fems Microbiol. Ecol. 2016, 92, fiw119. [Google Scholar] [CrossRef] [PubMed]
  26. Seipke, R.F.; Kaltenpoth, M.; Hutchings, M.I. Streptomyces as symbionts: An emerging and widespread theme? Fems Microbiol. Rev. 2012, 36, 862–876. [Google Scholar] [CrossRef] [PubMed]
  27. Yandigeri, M.S.; Meena, K.K.; Singh, D.; Malviya, N.; Singh, D.P.; Solanki, M.K.; Yadav, A.K.; Arora, D.K. Drought-tolerant endophytic actinobacteria promote growth of wheat (Triticum aestivum) under water stress conditions. Plant Growth Regul. 2012, 68, 411–420. [Google Scholar] [CrossRef]
  28. Tamreihao, K.; Ningthoujam, D.S.; Nimaichand, S.; Singh, E.S.; Reena, P.; Singh, S.H.; Nongthomba, U. Biocontrol and plant growth promoting activities of a Streptomyces corchorusii strain UCR3-16 and preparation of powder formulation for application as biofertilizer agents for rice plant. Microbiol. Res. 2016, 192, 260–270. [Google Scholar] [CrossRef]
  29. Tabassum, B.; Khan, A.; Tariq, M.; Ramzan, M.; Khan, M.S.I.; Shahid, N.; Aaliya, K. Bottlenecks in commercialisation and future prospects of PGPR. Appl. Soil. Ecol. 2017, 121, 102–117. [Google Scholar] [CrossRef]
  30. Aloo, B.N.; Makumba, B.A.; Mbega, E.R. Status of biofertilizer research, commercialization, and practical applications: A global perspective. In Biofertilizers; Elsevier Press: Amsterdam, The Netherlands, 2021; pp. 191–208. ISBN 978-012-821-667-5. [Google Scholar]
  31. Essahibi, A.; Benhiba, L.; Babram, M.A.; Ghoulam, C.; Qaddoury, A. Influence of arbuscular mycorrhizal fungi on the functional mechanisms associated with drought tolerance in carob (Ceratonia siliqua L.). Trees 2017, 32, 87–97. [Google Scholar] [CrossRef]
  32. Ilangumaran, G.; Smith, D.L. Plant growth promoting rhizobacteria in amelioration of salinity stress: A systems biology perspective. Front. Plant Sci. 2017, 8, 1768. [Google Scholar] [CrossRef] [PubMed]
  33. Hamedi, J.; Mohammadipanah, F. Biotechnological application and taxonomical distribution of plant growth promoting actinobacteria. J. Ind. Microbiol. Biotechnol. 2015, 42, 157–171. [Google Scholar] [CrossRef] [PubMed]
  34. Rho, H.; Hsieh, M.; Kandel, S.L.; Cantillo, J.; Doty, S.L.; Kim, S.H. Do endophytes promote growth of host plants under stress? A meta-analysis on plant stress mitigation by endophytes. Microb. Ecol. 2018, 75, 407–418. [Google Scholar] [CrossRef] [PubMed]
  35. Backer, R.; Rokem, J.S.; Ilangumaran, G.; Lamont, J.; Praslickova, D.; Ricci, E.; Subramanian, S.; Smith, D.L. Plant growth-promoting rhizobacteria: Context, mechanisms of action, and roadmap to commercialization of biostimulants for sustainable agriculture. Front. Plant Sci. 2018, 9, 1473. [Google Scholar] [CrossRef]
  36. Li, Y.; Guo, Q.; Li, Y.; Sun, Y.; Xue, Q.; Lai, H. Streptomyces pactum Act12 controls tomato yellow leaf curl virus disease and alters rhizosphere microbial communities. Biol. Fertil. Soils 2019, 55, 149–169. [Google Scholar]
  37. Zhang, Y.; Zhang, T.; Xue, Z.; Liu, Y.; Li, Y.; Li, Y.; Chen, Q. Streptomyces application triggers reassembly and optimization of the rhizosphere microbiome of cucumber. Diversity 2021, 13, 413. [Google Scholar] [CrossRef]
  38. Liu, Y.; Zhang, K.; Ma, J.; Lai, H.; Xue, Q. Effects of two Streptomyces strains on growth and induced resistance of wheat seedings. Acta Agric. Boreali-Occident. Sinica 2018, 27, 658–666. [Google Scholar]
  39. Yang, B.; Yan, X.; Wang, H.Y.; Li, X.Y.; Ma, H.X.; Wang, S.G.; Sun, D.Z.; Jing, R.L. Dynamic QTL analysis of chlorophyll content during grain filling stage in winter wheat (Triticum aestivum L.). Rom. Agric. Res. 2016, 33, 77–85. [Google Scholar]
  40. Costa, M.A.; Pinheiro, H.A.; Shimizu, E.S.C.; Fonseca, F.T.; Dos Santos Filho, B.G.; Moraes, F.K.C.; De Figueiredo, D.M. Lipid peroxidation, chloroplastic pigments and antioxidant strategies in Carapa guianensis (Aubl.) subjected to water-deficit and short-term rewetting. Trees 2009, 24, 275–283. [Google Scholar] [CrossRef]
  41. Kochba, J.; Lavee, S.; Spiegelroy, P. Differences in peroxidase-activity and isoenzymes in embryogenic and non-embryogenic ‘Shamouti orange’ ovular callus lines. Plant Cell Physiol. 1977, 18, 463–467. [Google Scholar] [CrossRef]
  42. Stewart, R.R.C.; Bewley, J.D. Lipid peroxidation associated with accelerated aging of soybean axes. Plant Physiol. 1980, 65, 245–248. [Google Scholar] [CrossRef]
  43. Bates, L.S.; Waldren, R.A.; Teare, I. Rapid determination of free proline for water-stress studies. Plant Soil. 1973, 39, 205–207. [Google Scholar] [CrossRef]
  44. Bradford, M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72, 248–254. [Google Scholar] [CrossRef] [PubMed]
  45. Maxwell, K.; Johnson, G.N. Chlorophyll fluorescence—A practical guide. J. Exp. Bot. 2000, 51, 659–668. [Google Scholar] [CrossRef] [PubMed]
  46. Ma, J.; Lin, X.; Luo, L.; Zhang, W.; Xu, Y.; Xie, H.; Xu, X.; Li, Q.; Li, X. China Statistics Yearbook; National Bureau of Statistics of China Press: Beijing, China, 2009; ISBN 978-750-375-800-3.
  47. Li, H.; Guo, Q.; Jing, Y.; Liu, Z.; Zheng, Z.; Sun, Y.; Xue, Q.; Lai, H. Application of Streptomyces pactum Act12 enhances drought resistance in wheat. J. Plant Growth Regul. 2019, 39, 122–132. [Google Scholar] [CrossRef]
  48. Zhao, X.W.; Yuan, X.M.; Xing, Y.J.; Dao, J.C.; Zhao, D.Q.; Li, Y.Z.; Li, W.W.; Wang, Z.T. A meta-analysis on morphological, physiological and biochemical responses of plants with PGPR inoculation under drought stress. Plant Cell Environ. 2023, 46, 199–214. [Google Scholar] [CrossRef] [PubMed]
  49. Al-Turki, A.; Murali, M.; Omar, A.F.; Rehan, M.; Sayyed, R.Z. Recent advances in PGPR-mediated resilience toward interactive effects of drought and salt stress in plants. Front. Microbiol. 2023, 14, 1214845. [Google Scholar] [CrossRef] [PubMed]
  50. Cao, S. Actinomycetes Enhance Phytoremediation of Lead and Cadmium Contaminated Soil and Its Mechanisms. Ph.D. Thesis, Chang’an University, Xi’an, China, 2016. [Google Scholar]
  51. Danish, S.; Zafar-Ul-Hye, M. Co-application of ACC-deaminase producing PGPR and timber-waste biochar improves pigments formation, growth and yield of wheat under drought stress. Sci. Rep. 2019, 9, 5999. [Google Scholar] [CrossRef]
  52. Chandra, D.; Srivastava, R.; Gupta, V.; Franco, C.M.M.; Sharma, A.K. Evaluation of ACC-deaminase-producing rhizobacteria to alleviate water-stress impacts in wheat (Triticum aestivum L.) plants. Can. J. Microbiol. 2019, 65, 387–403. [Google Scholar] [CrossRef]
  53. 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]
  54. Vaishnav, A.; Choudhary, D.K. Regulation of drought-responsive gene expression in Glycine max L. merrill is mediated through Pseudomonas simiae strain AU. J. Plant Growth Regul. 2019, 38, 333–342. [Google Scholar] [CrossRef]
  55. Noreen, S.; Ali, B.; Hasnain, S. Growth promotion of Vigna mungo (L.) by Pseudomonas spp. exhibiting auxin production and ACC-deaminase activity. Ann. Microbiol. 2012, 62, 411–417. [Google Scholar] [CrossRef]
  56. Miller, G.; Suzuki, N.; Ciftci-Yilmaz, S.; Mittler, R. Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ. 2010, 33, 453–467. [Google Scholar] [CrossRef] [PubMed]
  57. Tanveer, S.; Ilyas, N.; Akhtar, N.; Sayyed, R.Z.; Almalki, W.H. Induction of regulatory mechanisms by plant growth promoting rhizobacteria in crops facing drought stress. Crop Pasture Sci. 2023, 74, 856–870. [Google Scholar] [CrossRef]
  58. Mansoor, S.; Wani, O.A.; Lone, J.K.; Manhas, S.; Kour, N.; Alam, P.; Ahmad, A.; Ahmad, P. Reactive oxygen species in plants: From source to sink. Antioxidants 2022, 11, 225. [Google Scholar] [CrossRef] [PubMed]
  59. Gontia-Mishra, I.; Sapre, S.; Sharma, A.; Tiwari, S. Amelioration of drought tolerance in wheat by the interaction of plant growth-promoting rhizobacteria. Plant Biol. 2016, 18, 992–1000. [Google Scholar] [CrossRef]
  60. Akhtar, N.; Ilyas, N.; Mashwani, Z.U.R.; Hayat, R.; Yasmin, H.; Noureldeen, A.; Ahmad, P. Synergistic effects of plant growth promoting rhizobacteria and silicon dioxide nano-particles for amelioration of drought stress in wheat. Plant Physiol. Biochem. 2021, 166, 160–176. [Google Scholar] [CrossRef] [PubMed]
  61. De Vries, F.T.; Griffiths, R.I.; Knight, C.G.; Nicolitch, O.; Williams, A. Harnessing rhizosphere microbiomes for drought-resilient crop production. Science 2020, 368, 270–274. [Google Scholar] [CrossRef] [PubMed]
  62. Williams, A.; De Vries, F.T. Plant root exudation under drought: Implications for ecosystem functioning. New Phytol. 2020, 225, 1899–1905. [Google Scholar] [CrossRef]
  63. Zhang, J.J.; She, M.Y.; Yang, R.C.; Jiang, Y.J.; Qin, Y.B.; Zhai, S.N.; Balotf, S.; Zhao, Y.; Anwar, M.; Alhabbar, Z.; et al. Yield-related QTL clusters and the potential candidate genes in two wheat DH populations. Int. J. Mol. Sci. 2021, 22, 11934. [Google Scholar] [CrossRef]
  64. 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. 2011, 27, 197–205. [Google Scholar] [CrossRef]
  65. Frechilla, S.; González, E.M.; Royuela, M.; Minchin, F.R.; Aparicio-Tejo, P.M.; Arrese-Igor, C. Source of nitrogen nutrition (nitrogen fixation or nitrate assimilation) is a major factor involved in pea response to moderate water stress. J. Plant Physiol. 2000, 157, 609–617. [Google Scholar] [CrossRef]
  66. Sedri, M.H.; Niedbala, G.; Roohi, E.; Niazian, M.; Szulc, P.; Rahmani, H.A.; Feiziasl, V. Comparative analysis of plant growth-promoting rhizobacteria (PGPR) and chemical fertilizers on quantitative and qualitative characteristics of rainfed wheat. Agronomy 2022, 12, 1524. [Google Scholar] [CrossRef]
  67. Cao, S.; Wang, W.; Wang, F.; Zhang, J.; Wang, Z.; Yang, S.; Xue, Q. Drought-tolerant Streptomyces pactum Act12 assist phytoremediation of cadmium-contaminated soil by Amaranthus hypochondriacus: Great potential application in arid/semi-arid areas. Environ. Sci. Pollut. Res. Int. 2016, 23, 14898–14907. [Google Scholar] [CrossRef]
  68. Zhao, Y.; Sun, C.; Wang, S.; Zhang, M.; Li, Y.; Xue, Q.; Guo, Q.; Lai, H. Widely targeted metabolomic, transcriptomic, and metagenomic profiling reveal microbe-plant-metabolic reprogramming patterns mediated by Streptomyces pactum Act12 enhance the fruit quality of Capsicum annuum L. Food Res. Int. 2023, 166, 112587. [Google Scholar] [CrossRef]
Agronomy 14 00692 g001
Figure 1. Variation in monthly rainfall and average temperature throughout the entire wheat growth period.
Figure 1. Variation in monthly rainfall and average temperature throughout the entire wheat growth period.
Agronomy 14 00692 g001
Agronomy 14 00692 g002aAgronomy 14 00692 g002b
Figure 2. Effects of Act12 inoculation on plant height (a,e), leaf length (b,f), leaf width (c,g), leaf area (d,h), fresh weight of leaves, stems, and spikes (i,j), and dry weight of leaves, stems, and spikes (k,l) in two wheat varieties ((a–d,i,k) Jimai 22; (e–h,j,l) Chang 6878) at the heading and middle-filling stages under different water conditions. Data are presented as mean ± standard deviation (SD) with n = 5. Statistically significant differences are denoted by distinct alphabetical letters (p < 0.05).
Figure 2. Effects of Act12 inoculation on plant height (a,e), leaf length (b,f), leaf width (c,g), leaf area (d,h), fresh weight of leaves, stems, and spikes (i,j), and dry weight of leaves, stems, and spikes (k,l) in two wheat varieties ((a–d,i,k) Jimai 22; (e–h,j,l) Chang 6878) at the heading and middle-filling stages under different water conditions. Data are presented as mean ± standard deviation (SD) with n = 5. Statistically significant differences are denoted by distinct alphabetical letters (p < 0.05).
Agronomy 14 00692 g002aAgronomy 14 00692 g002b
Agronomy 14 00692 g003
Figure 3. Effects of Act12 inoculation on leaf chlorophyll content (a,b) and photosynthetic efficiency (Fv/Fm) (c,d) in two wheat varieties ((a,c) Jimai 22; (b,d) Chang 6878) across jointing, heading, and middle-filling stages under different water conditions. Data are presented as mean ± standard deviation (SD) with n = 5. Statistically significant differences are denoted by distinct alphabetical letters (p < 0.05).
Figure 3. Effects of Act12 inoculation on leaf chlorophyll content (a,b) and photosynthetic efficiency (Fv/Fm) (c,d) in two wheat varieties ((a,c) Jimai 22; (b,d) Chang 6878) across jointing, heading, and middle-filling stages under different water conditions. Data are presented as mean ± standard deviation (SD) with n = 5. Statistically significant differences are denoted by distinct alphabetical letters (p < 0.05).
Agronomy 14 00692 g003
Agronomy 14 00692 g004
Figure 4. Effects of Act12 inoculation on the activities of antioxidant enzymes SOD (a,b) and POD (c,d) in two wheat varieties ((a,c) Jimai 22; (b,d) Chang 6878) across jointing, heading, and middle-filling stages under different water conditions. Data are presented as mean ± standard deviation (SD) with n = 3. Statistically significant differences are denoted by distinct alphabetical letters (p < 0.05).
Figure 4. Effects of Act12 inoculation on the activities of antioxidant enzymes SOD (a,b) and POD (c,d) in two wheat varieties ((a,c) Jimai 22; (b,d) Chang 6878) across jointing, heading, and middle-filling stages under different water conditions. Data are presented as mean ± standard deviation (SD) with n = 3. Statistically significant differences are denoted by distinct alphabetical letters (p < 0.05).
Agronomy 14 00692 g004
Agronomy 14 00692 g005
Figure 5. Effects of Act12 inoculation on MDA (a,b), proline (c,d), and soluble protein (e,f) content in two wheat varieties ((a,c,e) Jimai 22; (b,d,f) Chang 6878) across jointing, heading, and middle-filling stages under different water conditions. Data are presented as mean ± standard deviation (SD) with n = 3. Statistically significant differences are denoted by distinct alphabetical letters (p < 0.05).
Figure 5. Effects of Act12 inoculation on MDA (a,b), proline (c,d), and soluble protein (e,f) content in two wheat varieties ((a,c,e) Jimai 22; (b,d,f) Chang 6878) across jointing, heading, and middle-filling stages under different water conditions. Data are presented as mean ± standard deviation (SD) with n = 3. Statistically significant differences are denoted by distinct alphabetical letters (p < 0.05).
Agronomy 14 00692 g005
Agronomy 14 00692 g006
Figure 6. Effects of Act12 inoculation on spike length (a,f), effective spike number (b,g), grain number per spike (c,h), thousand-grain weight (d,i), and yield (e,j) in two wheat varieties ((a–e) Jimai 22; (f–j) Chang 6878) under different water conditions. Data presentation: mean ± standard deviation (SD). For spike length, effective spike number, grain number per spike, and thousand-grain weight (n = 5), yield data (n = 3). Statistically significant differences are denoted by distinct alphabetical letters (p < 0.05).
Figure 6. Effects of Act12 inoculation on spike length (a,f), effective spike number (b,g), grain number per spike (c,h), thousand-grain weight (d,i), and yield (e,j) in two wheat varieties ((a–e) Jimai 22; (f–j) Chang 6878) under different water conditions. Data presentation: mean ± standard deviation (SD). For spike length, effective spike number, grain number per spike, and thousand-grain weight (n = 5), yield data (n = 3). Statistically significant differences are denoted by distinct alphabetical letters (p < 0.05).
Agronomy 14 00692 g006
Table 1. Effects of Act12 inoculation on wheat quality indices under different water conditions.
Table 1. Effects of Act12 inoculation on wheat quality indices under different water conditions.
VarietyTreatmentHardness (%)Test Weight (g/L)Protein (%)Wet Gluten (%)Sedimentation (mL)Dough Development Time (min)Dough Stability (min)
Jimai 22W53.51 ± 1.67 a796.33 ± 6.35 a13.65 ± 0.25 a32.14 ± 0.48 a27.07 ± 0.59 a3.90 ± 0.10 a3.43 ± 0.15 a
W+Act1254.66 ± 1.40 a801.00 ± 1.73 a13.87 ± 0.25 a32.35 ± 0.51 a28.83 ± 0.64 a4.20 ± 0.10 a4.00 ± 0.17 a
D35.30 ± 0.75 c771.00 ± 12.49 b14.95 ± 1.80 a33.93 ± 4.18 a30.07 ± 4.74 a4.10 ± 0.78 a4.37 ± 1.12 a
D+Act1246.16 ± 0.94 b771.33 ± 12.01 b15.03 ± 0.86 a34.55 ± 1.64 a31.07 ± 4.16 a4.13 ± 0.35 a4.63 ± 0.95 a
Chang 6878W43.84 ± 1.66 ab809.00 ± 6.00 a13.65 ± 0.13 a31.16 ± 0.44 a24.60 ± 1.22 a3.40 ± 0.10a2.87 ± 0.15 a
W+Act1245.42 ± 1.61 a809.00 ± 2.00 a13.77 ± 0.15 a31.30 ± 0.26 a24.63 ± 1.34 a3.47 ± 0.12 a2.90 ± 0.26 a
D36.49 ± 0.52 c765.00 ± 6.56 b13.51 ± 0.30 a30.96 ± 1.02 a24.37 ± 5.03 a3.17 ± 0.40 a3.33 ± 1.00 a
D+Act1241.90 ± 0.52 b767.00 ± 8.72 b13.60 ± 0.19 a31.10 ± 0.81 a25.27 ± 4.65 a3.20 ± 0.44 a3.33 ± 0.98 a
Statistically significant differences are denoted by distinct alphabetical letters (p < 0.05).
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

Yang, B.; Wen, H.; Wang, S.; Zhang, J.; Wang, Y.; Zhang, T.; Yuan, K.; Lu, L.; Liu, Y.; Xue, Q.; et al. Enhancing Drought Resistance and Yield of Wheat through Inoculation with Streptomyces pactum Act12 in Drought Field Environments. Agronomy 2024, 14, 692. https://doi.org/10.3390/agronomy14040692

AMA Style

Yang B, Wen H, Wang S, Zhang J, Wang Y, Zhang T, Yuan K, Lu L, Liu Y, Xue Q, et al. Enhancing Drought Resistance and Yield of Wheat through Inoculation with Streptomyces pactum Act12 in Drought Field Environments. Agronomy. 2024; 14(4):692. https://doi.org/10.3390/agronomy14040692

Chicago/Turabian Style

Yang, Bin, Hongwei Wen, Shanshan Wang, Jinhui Zhang, Yuzhi Wang, Ting Zhang, Kai Yuan, Lahu Lu, Yutao Liu, Quanhong Xue, and et al. 2024. "Enhancing Drought Resistance and Yield of Wheat through Inoculation with Streptomyces pactum Act12 in Drought Field Environments" Agronomy 14, no. 4: 692. https://doi.org/10.3390/agronomy14040692

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