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Article

Bio-Inoculation of Tomato (Solanum lycopersicum L.) and Jalapeño Pepper (Capsicum annuum L.) with Enterobacter sp. DBA51 Increases Growth and Yields under Open-Field Conditions

by
John Paul Délano-Frier
1,
Alberto Flores-Olivas
2,* and
José Humberto Valenzuela-Soto
3,*
1
Departamento de Biotecnología y Bioquímica, Centro de Investigación y de Estudios Avanzados, Unidad Irapuato, Km 9.6 Libramiento Norte, Irapuato 36821, Guanajuato, Mexico
2
Departamento de Parasitología, Universidad Autónoma Agraria Antonio Narro, Buenavista, Saltillo 25315, Coahuila, Mexico
3
CONAHCYT-Centro de Investigación en Química Aplicada, Blvd. Enrique Reyna 104, Saltillo 25294, Coahuila, Mexico
*
Authors to whom correspondence should be addressed.
Agronomy 2024, 14(4), 702; https://doi.org/10.3390/agronomy14040702
Submission received: 29 February 2024 / Revised: 27 March 2024 / Accepted: 27 March 2024 / Published: 28 March 2024
(This article belongs to the Section Agricultural Biosystem and Biological Engineering)
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Versions Notes

Abstract

:
The rhizobacterium Enterobacter sp. DBA51 (DBA51), isolated from the semi-desert in Coahuila, Mexico, was previously found to increase the vegetative growth of tomato and tobacco plants cultivated under greenhouse conditions. The present report describes the results obtained from two independent open-field experiments performed with tomato and jalapeño pepper commercial crops inoculated with DBA51. Additionally, plants inoculated with Bacillus subtilis LPM1 (LPM1) and uninoculated plants were included as positive and negative controls, respectively. DBA51 and LPM1 significantly promoted growth at vegetative stages in the tomato plants; this effect was evident in the stem diameter (DBA51 with p < 0.0001 and LPM1 with p < 0.0001) and height (DBA51 with p < 0.0001 and LPM1 with p < 0.0001) of the tomato plants. However, no differences were detected in the jalapeño pepper plants. Additionally, DBA51 and LPM1 treatments increased tomato fruit production by 80% and 31%, respectively, compared to uninoculated plants. A similar increase in yield was recorded in DBA51- and LPM1-treated jalapeño pepper plants, which was 75% and 56% higher than uninoculated controls, respectively. These results strongly recommend the potential use of DBA51 as a biofertilizer in horticultural crops.

1. Introduction

Worldwide crop production is severely affected by numerous (a)biotic stresses, whose increased impacts have been recently associated with climate change. This tendency represents a significant challenge for sustainable agriculture and food production. Plant growth-promoting rhizobacteria (PGPR) have gained enormous importance and have been widely reported to confer several benefits to crops, including their use as biofertilizers [1,2], biocontrol agents against pathogens and pests [1,2,3], and as phyto-stimulators [1,2,4]. In the last decades, many reports have been conducted to improve crop fitness through PGPR inoculation, thereby ensuring growth promotion and increased yields under various conditions [5,6].
The interactions between host plants and beneficial rhizobacteria are also known to increase soil fertility and to improve resistance to soil pathogens by dint of the highly diverse antimicrobial compounds released by PGPR strains [7,8]. This interaction is improved by the release of root exudative compounds that recruit rhizobacteria by chemotaxis, which is frequently the case during stress conditions under which the plants often secrete organic acids, e.g., malic, fumaric, and oxalic acid, etc., that act as chemo-attractants [9,10]. For instance, the augmented root exudation of malic acid in leaves of tomato plants sprayed with benzothiadiazole (BTH) was found to be responsible for root Bacillus subtilis LPM1 colonization under in vitro conditions [11].
Successful PGPR colonization in open-field crops remains a challenge for crop growers. The soil physicochemical properties and natural soil microbiota represent limitations for PGPR establishment. Also, the different environmental conditions in which rhizobacteria are originally isolated can affect their subsequent performance and beneficial effect. In order to avoid these limitations in agricultural soils, broad strategies have been implemented to improve plant–rhizobacteria interaction. The microencapsulation of rhizobacteria has been recently reported as an eco-friendly alternative since the biopolymers can function as a protective coat for the PGPR. However, very few encapsulation techniques are suitable for microorganisms [12]. Another one, as mentioned above, is the activated exudation of root photosynthates under in vitro and in vivo conditions by the foliar application of defense response inductors; therefore, its use to improve rhizobacteria–plant interactions represents an attractive possibility to be explored. Our previous study revealed that the Enterobacter sp. DBA51 strain was capable of metabolizing 1-aminocyclopropane-1-carboxylic acid (ACC) under in vitro conditions, showed a high phosphate solubilizing index (PSI), was capable of producing indole acetic acid (IAA), and enhanced the plant height and root biomass of tomato plants [13]. In accordance with previous studies of DBA51 performance in tomato plants under greenhouse conditions, we hypothesized that tomato and jalapeño pepper commercial crops inoculated with DBA51 could improve growth and yields under open-field conditions. The main purpose of this research was to provide evidence of growth promotion and yield increase through DBA51 inoculation. Thus, the objective of this research was to evaluate the growth-promoting and yield-enhancing effects on tomato and jalapeño pepper plants sprayed with methyl salicylate (MeSA) prior to their inoculation with Enterobacter sp. DBA51 (DBA51) under open-field conditions. The results obtained indicate that this strategy improved the field performance of both solanaceous crops in terms of both vegetative growth and yield. This outcome suggests that this procedure could represent a suitable alternative to enhance the positive effect of PGPR on plant agricultural production.

2. Materials and Methods

2.1. Location of the Field Experiments and Vegetal Material

The experiment was performed under open-field conditions in the municipality of Irapuato, Guanajuato, Mexico (20°34′34.3″ N 101°23′24.3″ W masl), from March (seedling transplanting to soil) to July 2021 (last harvest), with yearly high and low temperatures, relative humidity, and rainfall in the March–July period ranging between 25.8 and 30.8 °C, 9.7 and 16.1 °C, 35 and 73%, and 11 and 114 mm, respectively (https://www.weather-atlas.com, accessed on 25 February 2024). The soil beds had a 1.5 m separation from center to center. Drip irrigation was placed at the center of each bed with emitters spaced at 10 cm. The seeds of a hybrid commercial tomato (Solanum lycopersicum L., DRD8550, SEMINIS, CA, USA) and of a hybrid commercial jalapeño pepper (Capsicum annuum L., PS11435807, SEMINIS, Saint Louis, MO, USA) were germinated at INVERNADEROS APATZEO, Apaseo El Grande, Guanajuato, Mexico. Soil and underground water samples were collected for physicochemical analysis by an external service at FERTILAB laboratories, located in Celaya, Guanajuato, Mexico.

2.2. Water and Soil Physicochemical Properties

The physicochemical properties from the groundwater analysis are presented in Table 1. Values indicate moderately high salinity/sodicity as manifested by elevated EC, pH, and hardness. High K cation values were detected, while Ca, Mg, and Na levels were moderately high. Carbonate anions were absent, nitrates were very low, and sulfate and chlorides were low to moderately low, while bicarbonate levels were very high. Low levels of heavy metals, i.e., B, Fe, Mn, Cu, Zn, and As, were found.
The soil properties are presented in Table 2. The soil texture of the experimental location was sandy clay loam, with a moderately alkaline pH value of 7.38. Total carbonate percentages were very low, with a moderately low electric conductivity and a bulk density value of 1.13. The measurement of soil fertility parameters indicated that organic matter, total N, and available P were high, at 2.06%, 202.71 kg/ha, and 375.18 kg/ha, respectively. K, Ca, Mg, and S levels were also elevated, at 1645.68, 24,195.51, 5704.55, and 177.97 kg/ha, respectively. Other elements, such as Na, Fe, Zn, Mn, Cu, and B, were detected at moderately high levels. Additionally, the very high level of CO2 detected, at 309 mg CO2/kg, was indicative of healthy soil conditions.

2.3. Inoculation of Tomato and Jalapeño Pepper Seedlings with Rhizobacteria

Bacillus subtilis strain LPM1 (LPM1), previously isolated from the rhizosphere of apple trees, was used as a positive control [13,14] and was compared to Enterobacter sp. DBA51 (DBA51), previously isolated from a semi-desertic habitat in Coahuila, Mexico [13]. Both strains were grown routinely in liquid Luria–Bertani (LB) medium on a rotary shaker (150 rpm) for 12 h at 30 °C. Healthy DRD8551 and PS11435807 seedlings were transplanted to recently water-irrigated soil plots, and after 48 h they were drench-inoculated with a manual agricultural sprayer (16 L, TRUPER, Mexico City, Mexico) with approximately 10 mL/plant of LPM1 or DBA51 suspensions (previously counted in LB plates) at 1 × 107 and 1 × 108 CFU/mL, respectively. Control plants were not inoculated with rhizobacteria.

2.4. Plant Growth Conditions

Two independent experiments were performed with a 21-day difference between them. First, tomato DRD8550 seedlings were transplanted using 225 plants/bed, spaced at 40 cm (6 March 2021), whereas jalapeño pepper PS11435807 seedlings were transplanted using 450 plants/bed, spaced at 30 cm (27 March 2021). For the growing season, tomato and jalapeño pepper plants were fertigated through a drip irrigation system totaling 300–200–300 kg/ha NPK, and micronutrients were applied via foliar spraying (AgroScience, Jalisco, Mexico). For the tomato DRD8551 and jalapeño pepper PS11435807 field experiments, two beds each were used for the uninoculated control, DBA51, and LPM1 inoculation treatments (Figures S1 and S2, respectively). For each experimental plot, three plots (experimental units) per treatment (control, DBA51, and LPM1), each 30 m in length, were completely randomized along the 90 m bed (Figures S1D and S2D). To test the possibility of improving PGPR–root interactions, the leaves of all tomato and jalapeño pepper plants were sprayed with 0.15 mM of methyl salicylate (MeSA) (SIGMA-ALDRICH; St. Louis, MO, USA) using a manual agricultural sprayer (16 L, TRUPER). No MeSA-free control plants were included because the close association of the different plant treatment groups in the randomized experimental design highly increased the possibility of plant–plant communication via volatile MeSA. Tomato and jalapeño leaves were sprayed 25 and 34 days after transplanting (DAT), respectively.

2.5. Disease Incidence and Insect Pest Monitoring in Tomato and Jalapeño Pepper Plants

The disease incidence was monitored by inspecting the plants for typical bacterial and fungal symptoms in tomato leaves from different plant treatments, 85 DAT. Bacterial infection symptoms such as chlorosis, flower abortion, and upward rolling of leaves were detected. The fungal and oomycete infection symptoms observed were early blight, vascular wilt, and powdery mildew. For insect monitoring in tomato plants, ten plants were randomly selected for each treatment to measure the number of thrips in the flowers of individual plants. Meanwhile, four blue traps (GREENVASS, Guadalajara, Mexico) were placed in a zig-zag distribution in each of the jalapeño pepper experimental plots; these were evaluated 64 DAT.

2.6. Growth Promotion and Yields in Tomato and Jalapeño Pepper Plants

In order to evaluate differences between treatments, plant size and stem diameter parameters were assessed in both experiments. Tomato plant height and stem diameter were measured at 44 DAT (control, DBA51, and LPM1 with n = 165, n = 217, and n = 214 plants, respectively). Jalapeño pepper plants were similarly evaluated 75 DAT (control, DBA51, and LPM1 with n = 50 plants per treatment). In both experiments, the combined yields of tomato and jalapeño pepper were evaluated at the end of three different harvests. The yields derived from each treatment were obtained from harvesting approximately 450 plants grown in an area of 225 m2. Plant size was obtained with a Gripper measuring tape (TRUPER), whereas stem diameter was measured using a Karlen digital Vernier (Gimbel Mexicana S.A., Mexico City, Mexico).

2.7. Data Analysis

All biometric parameter data in both experiments were analyzed (except yields) to compare the means and significant differences using analysis of variance (one-way ANOVA) followed by the Kruskal–Wallis test at p ≤ 0.05, and graphics were obtained using the GraphPad Prism version 8 for Windows (GraphPad Software, La Jolla, CA, USA).

3. Results

3.1. Potential Phytopathogen Detection in the Experimental Soil

The results of the phytopathogen soil survey diagnostic performed in the soil sample are shown in Table 3. No phytopathogenic bacteria were detected, whereas Colletotrichum sp. (4.1 × 103 CFU/g soil) and Fusarium sp. (1.3 × 103 CFU/g soil) phytopathogenic fungi were found in high levels. Moderate Pythium sp. oomycete titers were also detected (3 × 102 CFU/g soil). Nematode populations, determined as individuals per 100 g of soil, were elevated in the soil sample analyzed: Pratylenchus sp., 11; Tylenchulus sp., 33; Tylenchus sp., 99; and Nacobbus sp., 22.

3.2. Vegetative Growth Promotion by PGPR Treatments in Tomato and Jalapeño Pepper Plants

Biometric parameters were evaluated to compare the effects of Enterobacter sp. DBA51 and Bacillus subtilis LPM1 treatments on the tomato DRD8550 and jalapeño pepper PS11435807 plants at 44 and 75 DAT, respectively. In the tomato plants, DBA51 and LPM1 treatments led to highly significant differences (p < 0.0001 ****) in stem diameter compared to the uninoculated control plants (Figure 1A). Highly significant differences (p < 0.0001 ****) in plant height were also detected in the DBA51- and LPM1-treated tomato DRD8550 plants compared to the uninoculated plants (Figure 1B).
Interestingly, the biometric stem diameter and plant height parameters evaluated in the jalapeño pepper PS11435807 plants at 75 DAT did not reveal significant differences between the DBA51 and LPM1 treatments and the uninoculated control (Figure 2A,B).

3.3. Disease Incidence in Tomato Plants and Pest Monitoring in Jalapeño Pepper Plants

The disease incidence of bacterial and fungal pathogens was monitored in the tomato plants treated with DBA51 and LPM1 and in the uninoculated control plants. Typical bacterial infection symptoms were observed in 23 control plants (10%), whereas only six (2.6%) and seven (3.1%) DBA51- and LPM1-treated plants showed bacterial infection symptoms, respectively. Similar effects were observed when fungal infection was monitored; thus, 52 control plants (23.1%) showed fungal infection symptoms, while these were observed in only 27 (12%) and 18 (8%) DBA51- and LPM1-treated plants, respectively (Figure 3).
Additionally, the DRD8550 tomato plant experimental plot was monitored for the presence of phytophagous insects. This consisted of counting the number of thrips per flower in the plant population evaluated for each treatment. LPM1-inoculated tomato plants showed a significantly reduced thrip population (at p < 0.005) compared to uninoculated controls and plants inoculated with DBA51. No statistically significant differences were detected between the DBA51-treated and uninoculated control plants (Figure 4).
For pest monitoring in jalapeño plants, the number of thrips captured in the blue traps placed in the different experimental plots was evaluated. Interestingly, the number of thrips counted in the traps placed within the plots corresponding to the uninoculated control plants was lower than in those placed in the plots corresponding to the DBA51 and LPM1 treatments. The difference in thrips numbers between the uninoculated and LPM1 treatments was statistically significant (at p < 0.05) (Figure 5).

3.4. Increased Crop Yield in Tomato and Jalapeño Pepper by PGPR Treatments

The total yields of the tomato DRD8550 and jalapeño pepper PS11435807 plants were evaluated during an extended three-stage harvest period. The tomato fruit yields produced by each of the experimental treatments were the following: DBA51- and LPM1-inoculated plants produced 187.595 and 136.852 kg, respectively, while uninoculated controls yielded 104.050 kg. The percentage increase in fruit yield compared to the uninoculated controls was 80.3% for the DBA51-inoculated plants; LPM1-inoculated plants also produced higher yields than the uninoculated control plants, although the yield was only increased by 31.5% (Figure 6A). The increase in yield was much higher in the PGPR-treated jalapeño pepper plants, as evidenced by the 334.404 and 298.310 kg produced by the DBA51- and LPM1-inoculated plants, which were ca. 56 to 76% higher, respectively, than the 190.440 kg yielded by the uninoculated control plants (Figure 6B).

4. Discussion

In this study, we report the effects resulting from the inoculation of the Enterobacter sp. DBA51 rhizobacterium on MeSA-treated tomato DRD8550 and jalapeño pepper PS11435807 commercial varieties cultivated under open-field conditions. Physicochemical assessments of the site’s groundwater and soil were obtained prior to the start of the field experiment in order to make adjustments to the fertilization regime of the tomato and jalapeño pepper plants. The soil analysis data were indicative of very high biological activity, comparable to that usually present in healthy, dark soils able to support high microbial metabolism; in the analyzed soil sample, the enhanced microbiological activity could have been sustained by the degradation of organic matter incorporated from previous crops. In consequence, the majority of the nutrients measured in the soil were elevated, which was consistent with the properties of a rich soil. Also, the sandy clay loam soil texture was a favorable factor for the proper establishment of the tomato and jalapeño crops in the experimental plots.
Studies of PGPR interacting with commercial crops have increased dramatically during the last 20 years. This tendency represents a confirmation of the demonstrated efficacy that PGPR use was found to have on plant performance when tested under controlled laboratory conditions [15]. The drench inoculation with DBA51 and LPM1 tested in the tomato field experiment was shown to promote growth at the vegetative stage, as demonstrated by the evident increase in the stem diameter and height of the experimental tomato plants (Figure 1). The lack of destructive sampling in the experimental design prevented the evaluation of other growth promotion-related parameters such as root and shoot dry biomass, foliar area, and chlorophyll content, among others, which will be considered in a future replication of this field experiment. Nevertheless, the growth promotion effects produced in the tomato plants cultivated in the present study were similar to those previously reported in tomato plants inoculated with Pseudomonas fluorescens and Pseudomonas sp., in combination with arbuscular mycorrhizal fungi colonization, which increased their fruit weight by 35% under open-field conditions [16]. Similarly, Enterobacter cloacae subsp. dissolvens promoted growth and increased yields of soybean and wheat under open-field conditions [17], whereas bell pepper plants that were inoculated with the PGPR Bacillus velezensis strain BBC047 improved growth at different phenological stages under greenhouse conditions [18]. Also, studies in bell and jalapeño pepper plants inoculated with Pseudomonas tolaasii and Bacillus pumilus PGPR strains showed growth promotion compared to uninoculated plants under climatic chamber conditions [19]. Similarly, a recent study reported the growth-promoting effect produced by the inoculation of the B. subtilis strain LPM1 on bell pepper commercial varieties at both vegetative and productive stages under shade house conditions using plastic mulches [14]. Likewise, the DBA51 strain was recently reported as a plant growth-promoting rhizobacterium [13]. The improved growth rate was reflected by increased tomato and tobacco root biomass, an effect that has been associated with the inhibition of primary root growth by PGPR-enhanced ethylene biosynthesis via ACC deaminase. Ethylene exerts this effect predominantly by affecting the auxin signaling pathway in the root, mostly through its influence on auxin biosynthesis and transport, although cross-talk with other phytohormones, such as abscisic acid, gibberellin, cytokinins, jasmonic acid, and brassinosteroids, is also biologically relevant [20,21,22,23,24]. DBA51 is also known to stimulate the synthesis of IAA and has a high PSI. These two properties have been reported to enhance plant traits closely related to optimized plant growth under greenhouse and open-field conditions.
Studies performed in canola plants treated with a combination of salicylic acid and PGPR produced positive effects on plant stress relief [25]. This study demonstrated that PGPR, acting in combination with other ingredients, could have a synergistic effect on crop development. Several other studies have tested the effect of using different microbial populations, either in combination with other bacterial species, as a bacterial consortium, or in association with mycorrhizal species [15]. In this work, exogenous foliar applications of MeSA at 25 DAT were tested in order to determine whether this defense response inducer could contribute to improve root colonization by the DBA51 and LPM1 strains. This experimental factor was introduced based on several other reports in which the activation of the SA-regulated defense pathway promoted the release of root exudative compounds, mainly organic acids that acted as chemo-attractants for PGPRs [26,27]. Based on this evidence, we proposed that SA treatment could not only enhance the interaction of DBA51 or LPM1 with the rhizosphere of tomato plants but could also activate a priming response. The latter was strongly suggested by the reduced incidence of bacterial and fungal disease symptoms in the MeSA-treated plants inoculated with DBA51 and LPM1 treatments compared to the uninoculated controls. Moreover, the significant reduction in thrips number in the DBA51- or LPM1-inoculated plants was indicative of a probable widespread activation of an induced systemic resistance response effective against bacterial and fungal phytopathogens and phytophagous insects in tomato plants.
No growth promotion at the vegetative growth stage was detected in the DBA51- and LPM1-inoculated jalapeño pepper plants. However, this result was not conclusive considering that stem diameter and plant height were the only biometric parameters evaluated. Therefore, the detection of enhanced growth effects in these plants may result from the measurement of other growth-related parameters that were not considered in this study. Nevertheless, an interesting reduction in the number of thrips immobilized in the blue traps used to monitor insect populations was recorded in the plots where uninoculated jalapeño plants were cultivated. The thrip counts were lower than those recorded in the blue traps placed around the plots corresponding to the DBA51- and LPM1-inoculated plants. We speculate that the difference in thrip counts obtained in the tomato experimental plots could have been a consequence of the jalapeño pepper plants releasing a particular blend of volatile organic compounds that could have acted as an attractant for thrips in open-field conditions. This possibility remains to be determined by further experimentation.
The Enterobacter DBA51 strain was previously isolated in a soil sample obtained from the semi-desert in Coahuila, México [13]. This strain possesses several plant growth-promoting traits and was found to increase the vegetative growth of tomato and tobacco plants under greenhouse conditions, a property that was confirmed by the open-field experiment reported here. It may be pertinent to add that the significantly increased yields recorded in the DBA51- and LPM1-inoculated tomato and pepper plants could have been even higher, considering that only a third of the total harvest was reported in this study due to the fact that the prevailing climatic conditions extended the harvest times beyond the period destined for this stage in the field experiment design. In general, the above findings were in agreement with several other studies that have reported the positive growth promotion effect produced by different Enterobacter strains under both controlled and open-field experimental conditions [28,29,30,31,32]. Finally, this study strongly suggests the possibility of using the DBA51 strain as an efficient biofertilizer in horticultural crops.

5. Conclusions

This study’s results indicated that the inoculation of commercial tomato and jalapeño pepper crops with Enterobacter sp. DBA51 markedly increased yields under open-field conditions. However, the growth promotion effects produced by DBA51 inoculation were only recorded in tomato plants and not in pepper plants examined at the same phenological stages. Moreover, Enterobacter sp. DBA51 treatment reduced the incidence of phytopathogens and also decreased the number of phytophagous pests in the tomato experiment. The positive effects observed strongly suggest that the use of Enterobacter sp. DBA51 in the field represents an attractive and cost-effective alternative to the utilization of agrochemicals to increase productivity and reinforce protection against biotic stressors. Hence, we propose that Enterobacter sp. DBA51 could be used as a suitable biofertilizer to enhance the productivity of horticultural and perhaps other agronomic crops, within a sustainable agriculture context, similar to the growth promotion and abiotic stress tolerance conferred to commercially relevant monocot plants by other Enterobacter strains.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/agronomy14040702/s1, Figure S1: Different views of the experimental plots employed to cultivate tomato DRD8551 plants under the open field conditions; Figure S2: Different views of the experimental plots employed to cultivate pepper PS11438507 plants under the open field conditions.

Author Contributions

J.P.D.-F., A.F.-O. and J.H.V.-S.: conceptualization, planned the work, and wrote the manuscript; J.H.V.-S.: performed open-field experiments and biometric measurements; J.P.D.-F. and J.H.V.-S.: supervised and data analysis. All authors have read and agreed to the published version of the manuscript.

Funding

This work was partially supported by the Program “Investigadoras e Investigadores por México” from the Consejo Nacional de Humanidades, Ciencias y Tecnologías (CONAHCyT) (Project No. 1333 to J.H.V.-S.).

Data Availability Statement

The data obtained during the bioassays are available from the corresponding author upon reasonable request.

Acknowledgments

We thank Alberto Flores Olivas (Departamento de Parasitología, Universidad Autónoma Agraria Antonio Narro, Saltillo, México) for providing the Bacillus subtilis strain LPM1.

Conflicts of Interest

The authors declare that they have no conflicts of interest.

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Figure 1. Vegetative plant growth promotion in tomato plants (DRD8550, SEMINIS) inoculated with Enterobacter sp. DBA51 (DBA51) and Bacillus subtilis LPM1 (LPM1) compared to uninoculated plants (control) under field conditions. (A) Stem diameter, in mm, and (B) plant size, in cm. Bars represent the mean values ± SE; level of significance: **** p < 0.0001. ANOVA, Kruskal–Wallis test with p < 0.05 (control, DBA51, and LPM1 with n = 165, n = 217, and n = 214 plants, respectively).
Figure 1. Vegetative plant growth promotion in tomato plants (DRD8550, SEMINIS) inoculated with Enterobacter sp. DBA51 (DBA51) and Bacillus subtilis LPM1 (LPM1) compared to uninoculated plants (control) under field conditions. (A) Stem diameter, in mm, and (B) plant size, in cm. Bars represent the mean values ± SE; level of significance: **** p < 0.0001. ANOVA, Kruskal–Wallis test with p < 0.05 (control, DBA51, and LPM1 with n = 165, n = 217, and n = 214 plants, respectively).
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Figure 2. Vegetative plant growth promotion in pepper plants (PS11435807, SEMINIS) inoculated with Enterobacter sp. DBA51 (DBA51) and Bacillus subtilis LPM1 (LPM1) compared to uninoculated plants (control) under field conditions. (A) Stem diameter, in mm, and (B) plant size, in cm. Bars represent the mean values ± SE; ns, non-significant. ANOVA, Kruskal–Wallis test with p < 0.05 (control, DBA51, and LPM1 with n = 50).
Figure 2. Vegetative plant growth promotion in pepper plants (PS11435807, SEMINIS) inoculated with Enterobacter sp. DBA51 (DBA51) and Bacillus subtilis LPM1 (LPM1) compared to uninoculated plants (control) under field conditions. (A) Stem diameter, in mm, and (B) plant size, in cm. Bars represent the mean values ± SE; ns, non-significant. ANOVA, Kruskal–Wallis test with p < 0.05 (control, DBA51, and LPM1 with n = 50).
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Figure 3. Disease incidence in DRD8551 tomato plants. (A) Number of plants showing indicative symptoms of bacterial infection. (B) Number of plants showing indicative symptoms of fungal infection. Control, uninoculated plants; DBA51, plants treated with Enterobacter sp. DBA51; and LPM1, plants treated with Bacillus subtilis LPM1.
Figure 3. Disease incidence in DRD8551 tomato plants. (A) Number of plants showing indicative symptoms of bacterial infection. (B) Number of plants showing indicative symptoms of fungal infection. Control, uninoculated plants; DBA51, plants treated with Enterobacter sp. DBA51; and LPM1, plants treated with Bacillus subtilis LPM1.
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Figure 4. Thrips number in tomato DRD8550 flowers. Control, uninoculated plants; DBA51, plants inoculated with Enterobacter sp. DBA51; and LPM1, plants inoculated with Bacillus subtilis LPM1. Bars represent mean values ± SE, n = 10, significance level = *, ns = non-significant. ANOVA, Kruskal–Wallis test at p < 0.05.
Figure 4. Thrips number in tomato DRD8550 flowers. Control, uninoculated plants; DBA51, plants inoculated with Enterobacter sp. DBA51; and LPM1, plants inoculated with Bacillus subtilis LPM1. Bars represent mean values ± SE, n = 10, significance level = *, ns = non-significant. ANOVA, Kruskal–Wallis test at p < 0.05.
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Figure 5. Thrips number in traps localized within pepper PS11435807 plots. Control, uninoculated plants; DBA51, plants inoculated with Enterobacter sp. DBA51; and LPM1, plants inoculated with Bacillus subtilis LPM1. Bars represent mean values ± SE, n = 12, significance level = *, ns = non-significance. ANOVA, Kruskal–Wallis test at p < 0.05.
Figure 5. Thrips number in traps localized within pepper PS11435807 plots. Control, uninoculated plants; DBA51, plants inoculated with Enterobacter sp. DBA51; and LPM1, plants inoculated with Bacillus subtilis LPM1. Bars represent mean values ± SE, n = 12, significance level = *, ns = non-significance. ANOVA, Kruskal–Wallis test at p < 0.05.
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Figure 6. Fruit yields produced by tomato DRD8550 (A) and jalapeño pepper PS11435807 (B) plants inoculated with Enterobacter sp. DBA51 (DBA51) and Bacillus subtilis LPM1 (LPM1) compared to those by uninoculated plants (control) under field conditions. Total fruit weight per treatment is represented in kg.
Figure 6. Fruit yields produced by tomato DRD8550 (A) and jalapeño pepper PS11435807 (B) plants inoculated with Enterobacter sp. DBA51 (DBA51) and Bacillus subtilis LPM1 (LPM1) compared to those by uninoculated plants (control) under field conditions. Total fruit weight per treatment is represented in kg.
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Table 1. Physicochemical properties of the groundwater used for irrigation.
Table 1. Physicochemical properties of the groundwater used for irrigation.
ParametersResultsmEq/Lppm
EC (dS/m)1.28--
pH7.68--
Hardness33.91--
Ca-3.7074.1
Mg-3.1237.9
Na-5.01115
K-0.8131.7
S-SO4-1.8960.5
HCO3-8.21501
Cl-2.4786.5
CO3-0.000.00
N-NO3-0.172.38
B--0.10
Fe--0.0020
Mn--1.7630
Cu--0.0010
Zn--0.0010
As--0.0005
Table 2. Soil physicochemical properties of the experimental site.
Table 2. Soil physicochemical properties of the experimental site.
ParametersResults
Soil textureSandy, clay, loam
EC (dS/m)1.15
pH7.38
Bulk density (g/cm3)1.13
Organic matter (%)2.06
Carbonates (%)1.78
Saturation point (%)55.0
Field capacity (%)29.4
Permanent wilting point (%)17.5
Hydraulic conductivity (cm/h)2.00
P-Bray (ppm)48.3
K (ppm)403
Ca (ppm)5101
Mg (ppm)1015
Na (ppm)378
Fe (ppm)18.6
Zn (ppm)6.55
Mn (ppm)19.8
Cu (ppm)3.59
B (ppm)2.12
S (ppm)17.5
N-NO3 (ppm)39.2
Health of soil (mg CO2/kg)309
Table 3. Soil phytopathogen diagnosis of the experimental soil.
Table 3. Soil phytopathogen diagnosis of the experimental soil.
Type of PathogenIdentity(CFU/g Soil)
Bacterial cell density --
Fungal cell density
Colletotrichum sp.4.1 × 103
Fusarium sp.1.3 × 103
Pythium sp.3 × 102
Nematodes density (individuals/100 g soil)
Pratylenchus sp.11
Tylenchulus sp.33
Tylenchus sp.99
Nacobbus sp.22
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Délano-Frier, J.P.; Flores-Olivas, A.; Valenzuela-Soto, J.H. Bio-Inoculation of Tomato (Solanum lycopersicum L.) and Jalapeño Pepper (Capsicum annuum L.) with Enterobacter sp. DBA51 Increases Growth and Yields under Open-Field Conditions. Agronomy 2024, 14, 702. https://doi.org/10.3390/agronomy14040702

AMA Style

Délano-Frier JP, Flores-Olivas A, Valenzuela-Soto JH. Bio-Inoculation of Tomato (Solanum lycopersicum L.) and Jalapeño Pepper (Capsicum annuum L.) with Enterobacter sp. DBA51 Increases Growth and Yields under Open-Field Conditions. Agronomy. 2024; 14(4):702. https://doi.org/10.3390/agronomy14040702

Chicago/Turabian Style

Délano-Frier, John Paul, Alberto Flores-Olivas, and José Humberto Valenzuela-Soto. 2024. "Bio-Inoculation of Tomato (Solanum lycopersicum L.) and Jalapeño Pepper (Capsicum annuum L.) with Enterobacter sp. DBA51 Increases Growth and Yields under Open-Field Conditions" Agronomy 14, no. 4: 702. https://doi.org/10.3390/agronomy14040702

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