3.2.1. Chemical Characteristics of Soil

The assessment of experimental soil chemistry (Table 2) revealed that the organic matter rate was low (0.1%) and that of nitrogen (0.1%). The content (6, 91 ppm) of phosphorus is average in soil. The sum of the bases (3.3 meq/100 g soil) and cation exchange capacity (6.06 meq) are low. The pH values (pH-water = 6.01 and pH-KCl = 5.5) showed that the study soil was moderately acidic. These recorded chemical properties reflect a limited fertility of the study soil due to its low mineral reserves with a fairly pronounced phosphorus deficiency. This soil has been classified in the agroecology zone III (food cultivation area south of Borgou) with a low level of fertility [42] responsible for declining crops yields such as maize.

Table 2. Chemical characteristic of the study soil.

3.2.2. Growth Parameters (Height, Collar Diameter and Leaf Area of Plants)

From the analysis in Table 3, it is apparent that the bacterial strains tested have a very highly significant effect (P < 0.001) on the height of the seedlings at 30th day after sowing. The maximum heights of the seedlings were induced by seedlings inoculated with S. marcescens, an increase of 58.83% in comparison with the control plants followed by plants treated with P. cichorii and P. putida, respectively, with increases of 53.91% and 45.64% compared to control plants. On the other hand, the effect expressed at the circumference of the seedling collar by the PGPR and their combination indicates that there is no significant difference (P < 0.05) between treatments. In contrast, inoculation of maize seeds by PGPR had a stimulating effect on the leaf area of the seedlings. The best leaf surfaces were obtained with the inoculation of S. marcescens followed by P. putida, a percentage improvement of 108.43% and 107.90%, respectively, compared with the control plants.

3.3. Effect of PGPR on Yield Parameters (Fresh Aboveground and Underground Biomass and Dry Matter)

At the reading of Figure 1(a), the plants inoculated with P. putida followed by S. marcescens produced the most important fresh aerial biomass, with increases of 161.60% and 94.37% compared to controls. In fact, according to the results of the analysis of variance, a very highly significant difference (P < 0.001) between the different treatments was noted. In addition, a similar improvement (P < 0.001) was also observed for some strains on the fresh underground biomass of seedlings. This is the case of S. marcescens, B. panthothenicus and P. cichorii, which induced an increase of the fresh underground biomass up to 59.16%; 52.08% and 47.45%, respectively compared with control plants. The lowest value of fresh underground biomass was recorded with plants treated with B. circulans. Rather, the analysis in Figure 1(b) indicates that the inoculation of PGPR and their combination has had a positive impact not only on air dry matter but also on the underground dry matter of plants. The highest significant values (P < 0.001) of air dry matter were obtained with P. putida treatments followed by S. marcescens, which induced an increase of 78.83% and 78.09% respectively. For the underground dry matter, the best productions were recorded at the “P. putida-S. marcescens” combination followed by “B. thuringiensis-P. cichorii”. The underground dry matter developed with the inoculation of P. syringae experienced an increase of 57% over the control plants.

Table 3. Effect of PGPR on growth parameters.

NS = P > 0.05 (not significant). m = means and cv = coefficient of variation. The averages followed by the same letter are not significantly different by the Newman-Keuls test at the 0.05 probability level.

(a) (b)

Figure 1. Fresh biomass of corn plants based on different treatments (a) Dry matter produced by maize plants according to different treatments (b). CTL: Control without bacteria, Bacillus polymysa, B2: Bacillus anthracis, B3: Bacillus circulans, B4: Bacillus thuringiensis, B5: Bacillus panthothenicus, P1: Pseudomonas cichori, P2: Pseudomonas putida, P3: Pseudomonas syringae, Sm: Serratia marcescens, B1B2B3B4B5: Bacillus polymysa-Bacillus anthracis-Bacillus circulans-Bacillus thuringiensis-Bacillus panthothenicus, B4B5Sm: Bacillus thuringiensis-Bacillus Panthothenicus-Serratia marcescens, P1P2P3: Pseudomonas cichorii-Pseudomonas putida-Pseudomonas syringae, P2Sm: Pseudomonas putida-Serratia marcescens, B4P1: Pseudomonas cichorii-Bacillus thuringiensis, P2B4Sm: Pseudomonas putida-Bacillus thuringiensis-Serratia marcescens.

3.4. Correlation between Growth Parameters and Yield Parameters

Figure 2 shows the dendrogram of the Hierarchical Ascending classification (ACH) of the treatments according to the variables studied. The analysis of this dendrogram shows that the 16 treatments were divided into four (4) groups. Group 1 consists of B. polymysa, B. anthracis, and P. cichorii-P. putida-P. syringae. Group 2 brings together B. panthothenicus; B. thuringiensis-P. cichorii; B. thuringiensis-B. panthothenicus-S. marcescens; P. syringae; P.cichorii; P. putida-S. marcescens; B. polymysa polymysa-B. anthracis-B. circulans-B. thuringiensis-B. Panthothenicus and B. thuringiensis-P. cichorii-S. marcescens. Group 3 includes the witness; B. anthracis and B. circulans. The treatments P. putida and S. marcescens form Group 4.

Figures 3(a) and Figures 3(b) represent the projection on the factorial plane (Dim1 and Dim2) of the data of the variables studied in greenhouse maize plants. The two axes (Dim1 and Dim2) represent 83.16% of the total variance, which is sufficient to guarantee a precision of interpretation for the identification of the main parameters and the discriminant treatments. Variables such as air dry matter (MSA), leaf area (S. Folliaire), fresh aerial biomass (BAF), circumference and height are strongly represented on the first main component (Dim1) while the underground dry matter (MSS) and the fresh underground biomass (BSF) are represented on the second main component (Dim2). With regard to the behaviour of the treatments against the different variables evaluated, four distinct major groups emerge:

- Group 4 includes strains of PGPR with significantly improved the height, circumference, fresh aerial biomass (BAF), dry underground biomass (BSF), material dry air (MSA), and leaf area of the maize plants. This group includes P. putida and S. marcescens which are well represented on the first axis (Dim1).

- Group 3 located opposite the axes of variables includes the stem B. circulans, B. anthracis and the witness with the lowest values of all the evaluated parameters.

- Group 2 brings together eight treatments that stand out particularly because of their performance at the level of the underground dry matter (MSS) developed by corn plants with P. putida-S. marcescens at the top.

- Group 1 includes treatments such as: P. cichorii-P. putida-P. syringae, B. polymysa and B. thuringiensis having mainly negatively as corn plants underground dry matter (MSS) evidenced by their position on the Dim1 axis by report to this variable.

3.5. Effect of PGPR on the Content of Macronutrients in the Dry Matter

With the exception of the content of nitrogen, the statistical analysis of the results illustrated by Table 4 indicated a significant effect of the inoculation of the seeds by PGPR on the content of phosphorus and potassium in aerial biomass of corn plants (P < 0.05) compared with controls. Indeed, aerial biomass of plants

Figure 2. Dendrogram of the hierarchical ascending classification (ACH) of the treatments according to the variables studied.

handled by S. marcescens have presented the strongest levels in phosphorus and potassium. These values exceed respectively 80% and 11.29% those obtained at the level of the plants not inoculated. It is the same for plants under influence of P. putida where an increase of 15% and 80% respectively of the potassium and phosphorus content was recorded in comparison with plants witnesses. Phosphorus in the underground biomass of plants has been significantly improved (P < 0.05) with inoculation in comparison with plants witnesses. The highest average phosphorus (0.189 ± 0.01) has been registered with the combination S. marcescens-P. putida. On the other hand, nosignificant difference was observed on the rate of nitrogen and potassium between treatments. However, the best nitrogen levels (2.04 ± 0.39) and potassium (2.38 ± 0.72) were obtained with the inoculated plants.

4. Discussion

4.1. Germination Test

The results obtained in vitro show that treatment of the seeds of corn with PGPR strains has impacted positively the germinal parameters of the maize seeds. Indeed, good (93.75% to 100%) germination of the seeds was noted whether at the level of the inoculated seed as witnesses thus attesting the good quality of the

(a) (b)

Figure 1. Factorial projection Dim1 (a) and Dim2 (b) of the data of the variables studied on greenhouse maize plants. MSS = dry underground material, MSA = aerial underground material, BAF = cool aboveground biomass, S = surface, BSF = cool underground biomass. CTL: Control without bacteria, Bacillus polymysa, B2: Bacillus anthracis, B3: Bacillus circulans, B4: Bacillus thuringiensis, B5: Bacillus panthothenicus, P1: Pseudomonas cichori, P2: Pseudomonas putida, P3: Pseudomonas syringae, Sm: Serratia marcescens, B1B2B3B4B5: Bacillus polymysa-Bacillus anthracis-Bacillus circulans-Bacillus thuringiensis-Bacillus panthothenicus, B4B5Sm: Bacillus thuringiensis-Bacillus panthothenicus-Serratia marcescens, P1P2P3: Pseudomonas cichorii-Pseudomonas putida-Pseudomonas syringae, P2Sm: Pseudomonas putida-Serratia marcescens, B4P1: Pseudomonas cichorii-Bacillus thuringiensis, P2B4Sm: Pseudomonas putida-Bacillus thuringiensis-Serratia marcescens.

seeds used in our study. However, no significant differences (P > 0.05) were observed between treatments. Note even when that seeds inoculated with S. marcescens followed by some combinations of which P. putida-S. marcescens have been best (100%) in comparison with the witnesses seeds germination rates. These observations are consistent with the work of [43] who got 100% germination after inoculation seeds of maize with P. putida. Similarly, [44] reported a germination rate of 96% in Egypt with the inoculation of S. marcescens on maize seeds. This positive effect of PGPR on the germination of seeds would be linked to the bacterial ability to produce or modify plant hormones including gibberellins which play a key role in germination [45] [46] .

All of the maize seeds treated with the PGPR showed highly significant improvements (P < 0.001) about the length of the seedling and roots. Indeed, values the highest length of seedlings were obtained with the application of P. cichorii followed by B. panthothenicus by the respective increases of 118.95% and 110.74% compared to controls. The seeds treated with B. panthothenicus and S. marcescens stimulated a significant elongation of the roots, which exceeded 58.86% and 53.74% relative to the control, respectively. These improvements in our study are confirmed by the work of [47] . These authors showed that the strains of Bacillus sp., Serratia sp. SY 5 have led to a significant increase in the length of the seedlings and roots of maize.

Table 4. Effect of PGPR on the content of macronutrients in dry matter.

NS = P > 0.05 (not significant). Value: mean ± standard deviation, **: significant difference (P < 0.05), the means followed by the same letter are not significantly different according to the Newman-Keuls test at P < 0.05. CTL: Control without bacteria, Bacillus polymysa, B2: Bacillus anthracis, B3: Bacillus circulans, B4: Bacillus thuringiensis, B5: Bacillus panthothenicus, P1: Pseudomonas cichori, P2: Pseudomonas putida, P3: Pseudomonas syringae, Sm: Serratia marcescens, B1B2B3B4B5: Bacillus polymysa-Bacillus anthracis-Bacillus circulans-Bacillus thuringiensis-Bacillus panthothenicus, B4B5Sm: Bacillus thuringiensis-Bacillus panthothenicus-Serratia marcescens, P1P2P3: Pseudomonas cichorii-Pseudomonas putida-Pseudomonas syringae, P2Sm: Pseudomonas putida-Serratia marcescens, B4P1: Pseudomonas cichorii-Bacillus thuringiensis, P2B4Sm: Pseudomonas putida-Bacillus thuringiensis-Serratia marcescens.

The effectiveness of the strains of S. marcescens, B. panthothenicus, P. cichorii observed in our study can be attributed to the ability of these isolates to produce the acid indole Acetic (AIA), a hormone that positively affects the growth and development of roots thus increasing absorption of nutrients [48] [49] . In comparison to the witness’s seeds, all treatments have led to a significant improvement of the vigor index (Table 1). The best vigor index has been achieved on the seeds inoculated with B. panthothenicus, followed by S. marcescens. These results are similar to those of [50] who observed a significant increase in the length of the roots, seedling and vigor index with strains of Pseudomonas spp., Bacillus spp. after inoculation of these strains on maize in South Africa. Moreover, the results obtained in our study corroborate those [51] [52] . These authors reported that inoculation of spinach (Spinacia oleracea L.) and wheat by the rhizobacteria increases germinative parameters such as the length of the seedlings, the length of the roots and the vigor index during the germination period.

4.2. Test in Greenhouse Condition

The importance of PGPR strains on crops has been highlighted by [53] that corn plants inoculated by Actinomycete sp. H7 have recorded a significant increase up to 19.3% in height growth compared to the witnesses. In our study, the same trends were noted for the treatments S. marcescens; P. cichorii, and P. putida at the height of the plants level. Indeed, inoculation of these strains has led to a considerable improvement of the plant height varying from 44.76% to 58.83% in comparison to the winesses plants. These results resemble the 45% achieved by [54] in Argentina on the height of corn plants inoculated with Pseudomonas tolaasii IEXb. Also, all strains tested in this study proved to be very effective on leaf area of plants. Plants inoculated with S. marcescens had the highest leave followed by those treated by P. putida. These values exceed respectively 108.43% and 107.09% the average value obtained at the level of the non-inoculated control. These results are similar to those of [55] who reported the effectiveness of S. marcescens TRS-1 on the increase of the height and aerial biomass of tea plants. Devi et al., [56] reported that the application of S. marcescens AL2-16 induces a better increase in leaf area, roots length, seedlings length, and dry weight of the fresh aerial biomass on Achyranthes aspera plants.

The higher aerial biomass was observed with the plants treated with P. putida and S. marcescens either respective increases of 161.60 and 94.37% compared to the control. On the underground biomass, best results were incurred with the inoculation of S. marcescens (59.16%) followed by B. panthetonicus (52.08%). The results achieved with the effect of the strain S. marcescens on biomass of the plants are in agreement with those [57] to the Brazil. These authors reported that inoculation of S. marcescens UENF-22GI (SMU) on corn has significantly increased the aerial biomass fresh and underground biomass fresh with a percentage of 64% and 80%, respectively, compared to the plants improvement witnesses collected 10 after days of experience in controlled condition. The PGPR performance observed on aerial and underground plant biomass was related to their production capacity of growth, in particular the auxins and gibberellins the hormones. These hormones are known to induce an increase in root hairs and the growth of aerial parts [58] .

As for the rate of the material dry air and underground developed by corn plants, the largest aerial dry matter production were recorded by plants treated with P. putida (78.83%) followed by S. marcescens (78.09%). Their combination has led to the largest underground dry matter (82.64%). This rate would be due to the synergistic effect of combined two strains. Our results are similar to those of [59] who have obtained a significant increase of the dry biomass of plants respectively 99% and 94% compared to the control with the inoculation of Serratia marcescens sp. EB 67 and Pseudomonas sp. CDB 35 on corn. The production of phytohormone and other metabolites by the rhizobacteria is one of the most important factors in the promotion of the growth of plants. Agbodjato et al., [60] have recently highlighted the ability of the majority of the strains tested in our study to solubilize the inorganic phosphate and produce metabolites of agricultural interest such as acid indole acetic (AIA). The positive effects of the inoculation on the parameters evaluated in our study would be so related to the ability of strains of PGPR particulary S. marcescens, P. putida, and P. cichorii to produce the AIA, to solubilize phosphate or a conjunction of the two mechanisms. Mezaache [61] explains that the rhizobacteria producing AIA are known for their ability to increase growth and the length of the roots. This effect results in a greater root surface and accessibility for most nutrients for the plant. Our results are related to these observations because the maize plants inoculated with the rhizobacteria P. putida, S. marcescens (Table 4) having given biomass yields the highest underground are those who have potassium and phosphorus content the significantly higher. Similar increases in absorption of the macronutrients include nitrogen and phosphorus have been reported in the host plant after inoculation of wheat grain by S. marcescens [62] . These observations have also been confirmed by [63] [64] .

In our study, the improvement of nutritional status at the level of the inoculated plants would result from a better accumulation of dry matter in the aerial part of the plant maize. Tarafdar et al., [65] explained the increase absorption of phosphorus, nitrogen, potassium, as well as other micronutrients by significant dry matter production in barley plants inoculated with the PGPR. Results for nutritional status obtained are in favour of a sustainable and environment-friendly agriculture. Indeed, the growth and the yield of plants are determined by the availability of some specific nutrients essential for the completion of their life cycle [66] . That is why the application of these essential nutrients (nitrogen, phosphorus and potassium) plants in the form of chemical fertilizers is part of intensive agriculture. Adjanohoun et al., [67] attributed the improvement of yields of corn achieved at the level of the plants inoculated with P. fluorescens, P. putida and A. lipoferum by increased absorption of nitrogen and potassium.

4.3. Conclusion

The results of the present study showed the beneficial role of PGPR inoculation on maize seed germination and seedling growth under laboratory and greenhouse conditions. For the majority of the evaluated parameters, the rhizobacteria S. marcescens, P. putida, and P. cichorii are most effective among those in the study. Furthermore, treatment of seeds with S. marcescens, and P. putida have led to better improvement in the nutritional status of plants including the content in phosphorous and potassium in aerial biomass of corn with a percentage plants improvement between 11.29% and 80% compared to plants not inoculated. These results are very interesting, and thus leave the possibility to exploit all of the strains selected in future experimental studies in order to produce some biofertilizers.

Acknowledgements

The authors thank the “Centre National de Spécialisation sur le Maïs (CNS-Maïs), the National Fund for scientific research and Innovation Technology (FNRSIT) for theit financial supports.

Conflicts of Interest

The authors declare no conflicts of interest regarding the publication of this paper.

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