Plant-Growth-Promoting Rhizobacteria and Known Interactions with Plant Phytophagous Insects: A Meta-Analysis

Abstract

Plant-growth-promoting rhizobacteria (PGPR) influence soil fertility, plant growth, tolerance to abiotic stress, resistance to herbivorous insects, and plant interactions with other organisms. While the effects of PGPR on plant growth, fruit yield, and induced defense responses have been extensively studied, the consistent positive outcomes have fueled rapid expansion in this research field. To evaluate PGPR impacts on plant growth and interactions with phytophagous insects, we conducted a systematic meta-analysis using publications from electronic databases (e.g., PubMed, Web of Science) that reported PGPR effects on plants and insects. Effects were categorized by plant family, PGPR genus, insect feeding guild, and insect–host specialization. Our analysis revealed that PGPR generally enhanced plant growth across most plant families; however, the magnitude and direction of these effects varied significantly among PGPR genera, indicating genus-specific interactions with host plants. When assessing PGPR-mediated reductions in phytophagous insects, we found that Pseudomonas, Rhizobium, and Bacillus exhibited the weakest negative effects on insect populations. PGPR significantly reduced both monophagous and polyphagous insects, with the most pronounced negative impacts on sucking insects (e.g., aphids, whiteflies). This study highlights critical patterns in PGPR-mediated plant growth promotion across taxa and the related differential effects on phytophagous insect activity. These insights advance our understanding of PGPR applications in agroecological production systems, particularly for integrated pest management and sustainable crop productivity.

1. Introduction

All organisms within a plant–associated food web are interconnected through trophic networks [1,2], and these connections are facilitated by environmental signals [2,3]. Plant-growth-promoting rhizobacteria (PGPR) can influence soil fertility, plant growth, abiotic stress tolerance, herbivorous insect resistance, and the interactions between plants and other organisms [4,5,6,7]. Growth promotion can be based on different mechanisms, such as associations with nitrogen-fixing microorganisms, reduced tissue ethylene levels, increased production of siderophores and phytohormones, induced systemic resistance to pathogens, and nutrient solubilization. More than one of these mechanisms can be activated simultaneously, contributing to improved plant growth and affecting phytophagous insect activity [8]. Plant growth promotion by PGPR has been thought to benefit aboveground herbivorous insects by increasing the nitrogen (N) levels in plant tissues, thus providing a better food source for insects [9].

As previously mentioned, some PGPR can induce systemic resistance. This resistance response activates physical and chemical defenses in plants, which can provide increased resistance to leaf-eating insects [10,11,12,13]. However, the impact of this defense mechanism against insect pests has been scarcely studied [14]. PGPR in association with plants can trigger a cascade of effects that can increase plant growth, which has been mainly linked to increased phytohormone production and improved nutrition [15]. In contrast, the cascade can have a negative effect on growth through the production of phenolic compounds, which can act as deterrents to insect feeding, and growth inhibitors via the jasmonic acid and salicylic acid pathway [15,16,17]. For example, after treatment with PGPR, some plants become more susceptible to phytophagous insects due to improved nutritional quality, and others become more resistant when the levels of toxic metabolites increase in the leaves [18,19]. The inoculation of Solanum lycopersicum roots with a growth-promoting strain of Bacillus subtilis induces systemic resistance and significantly decreases the number of pupae from the phloem-feeding Bemisia tabaci [20]. In greenhouse experiments, treatment of seeds from a nodulating line of Trifolium repens with Rhizobium leguminosarum increased the plant biomass above and below ground; however, plants exposed to leaf-chewing larvae of Spodoptera exigua did not gain as much biomass, with and without R. leguminosarum treatment [21].

Several studies on PGPR and their interactions with plants and phytophagous insects have reported a wide range of responses across systems and taxa [11,13,14,22]. PGPR may influence both plant and insect performance through direct or indirect mechanisms. Although numerous studies have addressed these effects independently, integrated evidence evaluating both aspects concurrently remains limited. Previous meta-analyses have typically focused on either plant growth promotion or pest suppression, but not both.

This study sought to fill that gap by systematically analyzing the dual effects of PGPR on plant growth and herbivorous insect activity using a bias-corrected, quantitative meta-analytical framework. Beyond quantifying these effects, our findings offer valuable insights for developing integrated agroecological practices. By identifying specific PGPR genera and plant–insect interactions that consistently enhance plant performance and suppress pest activity, this research provides a foundation for designing more sustainable crop management strategies. These results are particularly relevant in the context of reducing chemical inputs, promoting soil biodiversity, and improving the resilience of agricultural systems under changing environmental conditions.

2. Results

2.1. Heterogeneity and General Effects

Among 166 studies published between 2008 and 2023, only 34 met the stringent selection criteria. After rigorous screening for methodological consistency, a robust synthesis of 176 cases for plant growth, 124 cases for phytophagous insects, and 107 cases for feeding guilds was conducted. While environmental factors (e.g., climate, soil properties) and experimental designs may influence the effects of PGPR, our use of bias-corrected random-effects models accounted for this heterogeneity, ensuring reliable effect size estimates. Specifically:

For the meta-analysis, a positive effect of PGPR was indicated by a positive value for plant growth variables and a negative value for phytophagous insect variables. Overall, PGPR had a significant effect on plant growth (effect size = 0.49930, 95% bias-corrected confidence interval (95% Bc CI) = 0.3679 to 0.6470) and phytophagous insects (effect size = –0.44110, (95% Bc CI) = –0.54979 to –0.32370) (Figure 1 and

Table 1. Heterogeneity statistics for the effect of PGPR on plant growth and phytophagous insect activity were analyzed using three different models. Df: degrees of freedom; QB: variation in effect size explained by the model.

Model	Plant growth			Phytophagous insect activity
	Df	QB	p-Value	Df	QB	p-Value
Full model	297	9612.85	<0.0001	297	4793.1536	<0.0001
Bacterial genus	6	308.27	<0.0001	8	75.14	<0.0001
Plant family	4	264.35	<0.0001	6	135.46	<0.0001

).

2.2. Plant Growth

Five Rhizobacteria families significantly affected plant growth; the exceptions were Bradyrhizobium and Rothia. These results are robust only for Pseudomonas, Rhizobium, Bacillus, and mixtures (QB = 6137.11, df = 81, p < 0.0001). When the effect was analyzed by plant family, PGPR had a positive impact on plant growth for six of the analyzed families (QB = 4775.21, df = 81, p < 0.0001) (Figure 2).

2.3. Phytophagous Insect Activity

Analyses by bacterial genus and plant family indicated that phytophagous insect activity tends to decrease on PGPR-treated plants. The effects of Pseudomonas, Bacillus, and Rhizobium on phytophagous insect activity were significant and robust (QB = 3927.53, df = 59, p < 0.0001). Similarly, only PGPR associated with plant families Cannabaceae, Cucurbitaceae, and Brassicaceae significantly affected phytophagous insect activity (Figure 3) (QB = 3848.59, df = 60, p < 0.0001). In addition, when we tested the effects of PGPR on host specialization by monophagous and polyphagous insects, both showed significant effects (Figure 4) (QB = 3858.31, df = 60, p < 0.0001).

2.4. Variation in the Effects of PGPR on Phytophagous Insect Activity Based on Feeding Guild

The negative effect of PGPR on phytophagous insect activity was then analyzed by feeding guild: chewing insects and phloem-feeding insects (QB = 4775.21, df = 119, p < 0.0001). The PGPR had robust and significant negative effects on phloem-feeding insects and those with leaf chewing activity, with an effect size of −0.4376 ((95% Bc CI) = −0.4376 to −0.5497) for the sucking group, and effect size of −0.5712 ((95% Bc CI) = −1.0255 to −0.1595) for chewing insects (Figure 5).

When individual variables of phytophagous insects were analyzed, the three variables, weight, leaf consumption, and individuals per plant, showed a significant effect for the chewing insects. Surprisingly, only individuals per plant, showed a significant but null response for sucking insects when plants were treated with PGPR (Figure 5).

3. Discussion

The main findings of this meta-analysis are (1) PGPR enhanced plant growth, with the strength depending on the PGPR genus, and (2) PGPR reduced phytophagous insect activity, with the strength depending on the PGPR genus, plant family, and insect feeding guild. (3) Specifically, PGPR reduced leaf consumption and individuals per plant and enhanced the weight of phloem feeders.

3.1. Plant Growth

Detailed analyses of the effects of PGPR on plant growth showed that the effect was robust and significant for PGPR species in the genera Pseudomonas, Rhizobium, Bacillus, Enterobacter, and mixtures. In addition, the effects of PGPR on plant growth were significant and robust for six of the plant families analyzed: Piperaceae, Cannbaceae, Solanaceae, Poaceae, Fabaceae, and Brassicaceae. These results might be explained by the genera Pseudomonas, Bacillus, and Rhizobium, which are the most studied among the PGPR for promoting plant growth [23]. Increased plant growth has been mainly related to improved production of phytohormones, which improves nutrition [15]. In addition, as we expected, of the families studied, Fabaceae and Poaceae (legumes and grasses) had the greatest positive, most robust effects. These families exhibit a high affinity and capacity for biological nitrogen fixation (N₂), which contributes to enhanced nutrient uptake and overall plant vigor. This physiological trait likely makes these families more responsive to PGPR inoculation, as these bacteria often enhance nitrogen availability and root system development, thereby amplifying the growth-promoting effects in host plants with an inherent capacity for nitrogen assimilation [11,24]. Our results for the plant family showed that this effectiveness in promoting plant growth can occur similarly with equal magnitude in different crops of economic importance [24,25].

3.2. Phytophagous Insect Activity

Overall, this meta-analysis also showed that PGPR negatively impacted phytophagous insect activity, mainly monophagous, and that the effects varied depending on the bacterial genus and plant family. The effects were significant and robust for Pseudomonas, Bacillus, and Rhizobium. Our study found a tendency for phytophagous insect activity to decrease after plant inoculation, in line with the growth promotion and the chemical changes induced in plants after inoculation with species of PGPR, which also affect other natural enemies and insect herbivores [26,27]. The fact that Bacillus decreased phytophagous insect activity more strongly than the others was expected because Bacillus have been shown to suppress insect pest populations in the laboratory and field. Based on existing literature, Bacillus may suppress herbivorous insects through two key mechanisms. First, Bacillus produces toxins that harm insect digestive systems, leading to high mortality rates (e.g., 91.3% in Spodoptera exigua larvae) [12]. Second, Bacillus enhances plant defenses by triggering the production of compounds like protease inhibitors, which reduce leaf consumption by insects (e.g., Plutella xylostella feeding reduced by 40% in Brassica oleracea), and volatiles, like β-caryophyllene, which attract natural predators such as parasitic wasps targeting Helicoverpa armigera in tomato crops [12,20,25,28,29]. After inoculation with various species of Bacillus, the defense signaling pathways in the Brassica oleracea plant were activated, which reduced the population of the aphid Brevicoryne brassicae. These combined effects reduce feeding, delay development, increase mortality, and suppress reproduction in herbivores. Meta-analysis findings suggest Bacillus is the most effective genus (QB = −0.68; 95% CI = −0.82 to −0.54), particularly against chewing insects due to its synergy with jasmonic acid-mediated plant defenses [30,31]. Our results showed a negative effect on phytophagous insect activity, and interestingly, when we separated the results by feeding specialization, this negative effect was due mainly to monophagous insects. Systemic resistance induced by PGPR against sucking and chewing insects is plant- or beneficial-microbe-specific. This effect also depends on whether the targeted insects are specialist or generalist feeders. In this way, herbivorous insects were also negatively affected after inoculation with PGPR Bacillus [20,28]; likely due to Bacillus-mediated modulation of host–plant resistance via jasmonic acid levels [20,31]. The differing effects on the phytophagous insect activity in different genera can be explained by the differential expression of insect-responsive genes and insect-derived volatiles that trigger plant defense priming [32]. For example, Van Oosten et al. [33] reported that inoculation with Pseudomonas fluorescens did not improve the resistance of Arabidopsis against the specialist Pieris rapae L. In addition, Pineda et al. [34] found that PGPR can affect the production of root exudates, such as jasmonic acid, abscisic acid, and salicylic acid, which can enhance plant growth and induce systemic resistance against different attackers [33,35]. Interestingly, the results of these studies show that P. fluorescens primes Arabidopsis plants for expression of the LOX2 gene, which activates jasmonic acid when the generalist Myzus persicae damages them through phloem sucking. However, this pattern is inconsistent in the specialist Brevicoryne brassicae [36,37,38].

It has been well documented that PGPR benefits plant species such as Capsicum annuum L. [39], Brassica oleracea [40], Lactuca sativa L. [30], and Glycine max [41]. Also, Bacillus and Rhizobium greatly improve soil fertility and the growth and phytophagous activity of important agronomic crops [30,37,39,41]. The mixtures also showed significance in our results. A mixed inoculum of either Bacillus or Pseudomonas with Rhizobium can also improve plant growth [42,43,44,45]. Although the benefits conferred by PGPR can differ in magnitude, in all cases, the improvements result from a synergy among plant species, the bacterial strains, climatic conditions, soil, and stage of crop development [46,47]. In addition, each PGPR species differs in its effect on indole acetic acid production, phosphate solubilization, ammonia production, and siderophore production [48].

PGPR significantly affected the activity of phytophagous insects on the plant families Cannabaceae, Cucurbitaceae, and Brassicaceae, but not on Fabaceae, Solanaceae, and Poaceae. This variation might be explained by ecological factors unique to each plant family. For example, Solanaceae plants like Capsicum annuum produce natural alkaloids, such as capsaicin, which repel herbivores and may reduce the need for defenses triggered by PGPR. In Fabaceae plants like Glycine max, native rhizobia symbionts enhance salicylic acid (SA)-mediated resistance, which could interfere with PGPR signaling. Meanwhile, Poaceae plants like maize have root microbiomes dominated by mycorrhizae, which might compete with PGPR and weaken their impact on insect activity [44,45,49,50]. Metabolic processes, such as the production of primary and secondary metabolites, can vary among species and families and be further modulated by PGPR, other herbivores, pathogens, and predators/parasitoids, microclimatic conditions, and plant architecture [49,50,51]. Interestingly, among the results for insect activity by plant family, activity on Fabaceae and Poaceae was not significantly affected by PGPR despite members of Fabaceae having a high frequency of association with fixing bacteria [52]. We believe these associations improve growth and nutritional quality, thus influencing their suitability as a food resource for herbivores [53]. Different studies have shown the benefits of PGPR in association with legumes, such as N₂ fixation by the bacteria and increased N content in the host tissue, a crucial component that determines the quality of the food source for herbivorous insects. In addition, these effects can be linked to secondary chemicals and the plant species/culture and bacterial strain [21,54,55].

3.3. Variation in the Effects of PGPR on Phytophagous Insect Activity Based on Feeding Guild

We also found that the effects of PGPR on phytophagous insect activity decreased for the insect feeding guilds. The effects of PGPR on phloem-feeding insects were significant and robustly negative, in particular on leaf consumption and individuals per plant. However, in chewing insects, only the individuals per plant were robust, but with a null response. PGPR decreased the phytophagous insect activity, particularly for sucking insects, which is consistent with the plant defense mechanisms against herbivores. Feeding in herbivores causes mechanical damage, but the degree of damage can vary greatly depending on the feeding guild [56]. The difference between the feeding guilds may be due to the production of hormones such as jasmonic acid or salicylic acid, which are involved in the induced plant defenses [57,58,59]. Although chewing insects and phloem-sucking insects are adversely affected by defenses mediated by jasmonic acid, the phloem feeder’s suckers also seem to activate signaling pathways for salicylic acid, which can counteract the effects of jasmonic acid defenses through crosstalk, and, thus, increase the phytophagous insect activity of the phloem feeder’s suckers [60,61]. Thus, these variations in plants and the defenses that are differentially triggered by the different types of feeding lead to variations in phytophagous insect activity. We also found that the use of PGPR diminishes the population of sucking insects. Growth of Fabaceae and Solanaceae plants is negatively correlated with biological N-fixation by PGPR and the activity and abundance of aphids [62,63,64]. Our results also showed a negative tendency for chewing insects. Nevertheless, the guild of chewing insects is negatively affected by PGPR, in agreement with other reports [33,65,66]. The negative effect on the activity of phytophagous insects in the presence of PGPR-inoculated plants is mainly due to the different effects on plant growth, plant volatile organic compounds, emission, and total phenolic content. In addition, some phenolic compounds negatively affect insects by acting as feeding deterrents and growth inhibitors, as the jasmonic acid pathway is activated in response to chewing herbivores [22,67,68]. The effects of PGPR on phytophagous insects vary markedly between sucking (e.g., aphids) and chewing guilds (e.g., caterpillars), driven by distinct plant defense pathways. For sucking insects like Myzus persicae (aphid), Pseudomonas simiae induces phenolic compounds (e.g., chlorogenic acid) and repellent volatiles (e.g., limonene), reducing aphid survival by 45% in Arabidopsis [69]. In contrast, chewing insects like Plutella xylostella (caterpillar) are suppressed via PGPR-mediated activation of the jasmonic acid pathway. For example, Bacillus in Brassica oleracea boosts protease inhibitors, reducing leaf consumption by 40% [17]. However, sucking insects often evade jasmonic acid-mediated defenses by triggering the antagonistic salicylic acid pathway. Notably, some PGPR, like Rhizobium in soybean (Glycine max), enhance parasitoid attraction (e.g., Cotesia marginiventris), increasing Spodoptera frugiperda mortality by 50% regardless of guild [45]. A study on Capsicum annuum highlighted this contrast: Bacillus reduced aphid (Aphis gossypii) populations by 70% but only 30% in caterpillars (Spodoptera litura), underscoring the sensitivity of sucking insects to PGPR-induced phenols [44]. On the other hand, sucking insects are activators of the salicylic acid pathway, which is activated when the plant is attacked by phloem-sucking insects [17].

However, it is essential to note that while this information is highly relevant, certain limitations must be considered. As with any meta-analysis, our findings are subject to some constraints. Variability in experimental conditions, plant species, soil types, and environmental contexts across studies may contribute to the heterogeneity of effect sizes. These considerations underscore the importance of cautious extrapolation and highlight the need for complementary experimental validation under both controlled and field conditions.

4. Materials and Methods

4.1. Data Selection

This research is a type of meta-analysis, which evaluates previous studies that can be analyzed statistically [69,70]. The Google Scholar, Science Direct, Springer Journal, Taylor & Francis, and Wiley Online Library databases were searched for data sources, using individual search terms, including Rhizobacteria, plant growth promotion, insect resistance, phytophagous insects, defense induction, plant defense, insect deterrence, and herbivorous insects. The Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) model was used to select data sources (Figure 6) [71]. The citations for the studies included in the meta-analysis search are provided in the Supplementary Materials (see Supplementary Table S1) [72,73,74,75,76,77,78,79,80,81,82,83,84,85,86,87,88,89,90,91,92,93,94,95,96,97,98,99,100,101]. A study had to meet four criteria to include the primary literature for the meta-analysis: (1) The study was published between 2000 and 2023. (2) The study evaluated the effect of plant inoculation on plant growth and phytophagous insects. (3) The study reported data on growth, leaf consumption, pest incidence, leaf damage, leaf area, leaf biomass, root biomass, total biomass, number of leaves, or root length. (4) The study provided means, sample sizes, and measures of variance (standard deviation or standard error) for a control group and an experimental group. When one article reported data for more than one plant family, PGPR genus, growth variable, leaf damage type, or insect type, the data for the different factors were considered independent studies. Plant growth was assessed using at least one of the following variables: length or height of plants (cm), length of roots (cm), dry mass (g), dry mass of root (g), dry mass of nodules (g), fresh biomass (g), leaf area (cm²), number of leaves, specific leaf area (cm² g⁻¹), and number of seeds and fruits. Phytophagous insects were assessed using at least one of the following variables: leaf consumption (amount of leaf area consumed or affected by the insect), individuals per plant (number of individuals on the plants with PGPR), and weight (mg); for the weight experiments, insects were allowed to feed on plants inoculated with PGPR.

4.2. Effect Sizes

The mean, sample size, and deviation were obtained for the control and experimental groups in each study to calculate the effect size of each variable. If a study did not provide this information, univariate statistical data (F, t, and p) from the study were used to calculate the effect size [102]. All standard errors were converted to the standard deviation using the equation: SD = SE √n, where SD is the standard deviation, SE is the standard error, and n is the sample size.

The effect size was calculated as the difference between the means of the experimental and control data divided by the pooled standard deviation and weighted by sample size Hedges d: d = $d=\left[\left({\overline{x}}_0-{\overline{x}}_y\right)∕s\right]J,$ where ${\overline{x}}_0$ is the average of the control group, and $x_y$ is the average response of the experimental group, s is the combined SD, and J is a factor to correct for bias due to small sample size [10].

4.3. Statistical Analyses

The variables analyzed were the influence of PGPR on plant growth and the activity of phytophagous insects. In addition, we tested whether the effects depended on PGPR genus, plant family, insect guilds, and host specializations (monophagous vs. polyphagous). The data were analyzed using the statistical program Meta Win 2.1 and a fixed-effects model [102]. For all effect sizes with 999 iterations, 95% confidence intervals were generated (bootstrap with correction of bias). The effects were considered significant if the confidence intervals did not overlap with zero.

To evaluate whether the categorical groups (phytophagous insect activity and plant growth) were homogeneous with respect to the effect size, the heterogeneity within each group (Qw) and among groups (QB) was calculated, and the significance was evaluated using the x² test.

The risk of bias in the data set was assessed by the security number (n_fs) using the Rosenberg method [103,104]; n_fs indicates the number of non-significant, unpublished, or missing studies that should be added to the meta-analysis to change the results from significant to non-significant. The results are considered robust when n_fs is greater than 5n + 10, where n is the number of studies [103].

5. Conclusions

Our study demonstrated that most of the studied PGPR genera (with the exception of Rothia and Bradyrhizobium) promoted plant growth in the majority of the plant families analyzed. Bacteria in the genera Pseudomonas, Rhizobium, and Bacillus decreased the activity of phytophagous insects, mainly phloem-sucking insects. Plants in the families Cannabaceae, Cucurbitaceae, and Brassicaceae showed the strongest negative effects on phytophagous insect activity. Furthermore, we found that the use of PGPR, especially, negatively affected the sucking insect guild and monophagous insects. Our study revealed critical patterns in the effects of PGPR on the growth of different plant species and taxonomic families, as well as on phytophagous insect activity. These findings provide a scientific basis for integrating PGPR into agroecological systems, with implications for pest regulation and plant productivity within the sustainable agricultural framework.