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Bacterial endophyte Pseudomonas mosselii PR5 improves growth, nutrient accumulation, and yield of rice (Oryza sativa L.) through various application methods

BMC Plant Biology volume 24, Article number: 1030 (2024) Cite this article

Abstract

Background

Pseudomonas spp. have drawn considerable attention due to their rhizospheric abundance and exceptional plant growth-promoting attributes. However, more research is needed on the optimal application methods of Pseudomonas mosselii for rice growth, nutrient accumulation, and yield improvement. This research explored the application of the endophytic bacterium P. mosselii PR5 on rice cultivar BRRI dhan29 with four treatments: control, seedling priming, root drenching, and bacterial cell-free culture (CFC) foliar application.

Results

PR5 led to better rice growth, improved nutrient acquisition, and higher yields compared to the control, regardless of the application method used. The highest results in fresh weight of root (146.93 g/pot), shoot (758.98 g/pot), and flag leaf (7.88 g/pot), dry weight of root (42.16 g/pot), shoot (97.32 g/pot), and flag leaf (2.69 g/pot), and grains/panicle (224.67), were obtained from seedling priming treatment, whereas root drenching resulted in maximum plant height (105.67 cm), root length (49.0 cm), tillers/pot (23.7), and panicles/pot (17.67). In all three application methods, rice grain yield per pot was higher in PR5 inoculated treatments, compared to the control. The amount of P, Mg and Zn in the shoot and N, P, Ca, Mg and Si content in the flag leaf was significantly increased along with effective suppression of naturally occurring blast disease in bacterial CFC foliar application, validated by multivariate analysis.

Conclusion

Our results indicated that rice seedlings priming with PR5 improved rice growth, yield and nutrient uptake, whereas CFC foliar application significantly increased the concentration of most nutrients in the rice plant and suppressed the naturally occurring rice blast disease. This research highlights the significant potential of P. mosselii PR5 in enhancing rice growth, yield, and nutrient uptake, particularly through seedling priming and CFC foliar application methods.

Highlights

Pseudomonas mosselii PR5 significantly improved the growth and yield of rice.

Inoculation of PR5 changed the root structure of rice plant.

PR5 boosted the N, P, Mg, S, Fe and Zn content in rice plant.

Seedling priming enhanced plant growth most and bacterial cell free culture (CFC) foliar treatment enriched most nutrients.

Bacterial CFC foliar application suppressed naturally occurred rice blast disease.

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Introduction

Over half of the world’s population relies on rice (Oryza sativa L.) as their primary food source [1, 2]. The Food and Agriculture Organization (FAO) considers rice a key crop for food security [3]. Rice production is often hindered due to adverse environmental conditions, low amounts of nutrients in the soil and their less availability to crops. Farmers have been using chemical fertilizers to increase rice yields. Nevertheless, unbalanced chemical fertilizer application can alter soil pH, increase insect activity, lead to acidification and soil crust, reduce soil organic carbon and beneficial organisms, and ultimately cause substantial soil degradation [4, 5]. Excessive use of agrochemicals further contributes to greenhouse gas (GHG) emissions and climate change [6,7,8,9]. Under these circumstances, a sustainable practice to improve crop yield as well as restore soil health using environmentally friendly technology is the most important. A different and more sustainable method is the use of bioinoculants, particularly plant growth-promoting rhizobacteria (PGPR), which directly and indirectly help plants grow well and give better yields [10].

The rhizospheric zone of plant roots is naturally colonized by free-living soil microorganisms, which regulate a number of illnesses and promote plant growth [11,12,13,14]. Numerous benefits are conferred upon plants by these bacteria, such as enhanced root development, increased plant growth, nutrient uptake, plant hormone stimulation, suppression of pathogenic activity, and restoration of soil health by mineralizing organic pollutants [15, 16]. They accelerate the mineralization and absorption of several nutrients, such as N, P, Fe, Mn, Zn, and K, etc [17, 18]. In agriculture, PGPR is becoming more and more popular as a viable alternative to chemical pesticides, fertilizers, and supplements. PGPR has been applied to a variety of crops to improve growth, seed germination, and crop yield; some PGPRs have even been commercialized [19, 20]. The use and diversity of PGPR, their capacity to colonize new areas, and the mechanisms of action that can be employed to support their application as a dependable component in the management of sustainable agricultural systems are all vital to the recent advancements in the field of sustainable development [21, 22].

Pseudomonas is a common PGPR that thrives in the rhizosphere and is found in agricultural soils due to its molecular, environmental, and physiological diversity [23]. It is the most diverse group of bacteria, including over 100 species [24] and the most researched group of bacteria [25]. Pseudomonus chlororaphis, Pseudomonus aeruginosa, Pseudomonus putida, Pseudomonus syringe, and Pseudomonus fluroscencs were found to be significantly effective in promoting crop growth [26,27,28]. A great deal of attention has been paid to Pseudomonas, which is abundant in the rhizosphere [29] and exhibits remarkable growth-promoting traits like improved root colonization, enzyme and metabolite production, nutrient solubilization, indole acetic acid (IAA) and siderophore production, acting as a biocontrol agent, and promoting systemic resistance against diseases [30]. Pseudomonas mosselii is a rod-shaped, aerobic, gram-negative bacterium that belongs to the P. putida group and is well known for its metabolic flexibility. It ubiquitously inhabits diverse soil and water environments [31]. In addition to its phosphate solubilizing and other plant growth-promoting enzymes and hormone-producing abilities [32, 33], strains of Pseudomonas mosselii were also reported to have pseudopyronine as a potent antimicrobial and anticancer agent [34], and it is documented to produce pseudoiodinine that has antimicrobial properties against several fungal and bacterial pathogens of rice [35].

Despite the considerable potential of P. mosselii in promoting crop growth, the existing research predominantly concentrates on its ability to suppress diseases rather than exploring its potential contributions to rice growth, nutrient levels, and yield. While there are several studies available on the application of P. mosselii in rice, little attention has been given to investigating the impact of bacterial inoculation on the nutrient content and translocation of nutrients from the root, shoot, and flag leaf of the rice plant. Additionally, to the best of our knowledge, there is a notable absence of research on the optimal method for applying P. mosselii in rice. Taking into consideration the above facts, we isolated a native P. mosselii from the rice rhizosphere. The isolate showed several PGPR traits in culture media, exhibited multimetal tolerance, and showed excellent plant growth-promoting potential in the growth of rice seedlings in vitro [36]. Therefore, this present research investigated the impact of native P. mosselii PR5 on growth, nutrient contents in root, shoot, and flag leaf, and yield of rice, under different application methods for a sustainable rice production strategy.

Materials and methods

Soil and plant materials

The field soil was collected from 0 to 15 cm deep. It was pulverized and inert materials, visible insect pests, and plant residues were removed, followed by air drying and mixing and used for initial soil analysis. Soil pH and EC were measured using a soil water suspension of 1:2.5, as described by Jackson [37]. The organic carbon of the initial soil was determined by oxidizing the organic matter with an excess of 1 N K2Cr2O7 in the presence of concentrated H2SO4 and concentrated H3PO4 and titrating the excess K2Cr2O7 solution with 1 N FeSO4 [38]. The amount of organic carbon was multiplied by the van bammelen factor 1.73 to obtain organic matter content. Total nitrogen (N) was determined from the soil extract by the semi-micro Kjeldahl method as described by Bremner [39]. Available phosphorus (P) was determined from the initial soil extracted following the method of Olsen et al., 1954 [40]. Exchangeable potassium (K) was determined from the IN NH4OAc (pH 7.0) extract of the soil by using a flame photometer [41]. Exchangeable calcium (Ca) and magnesium (Mg) were also determined from NH4OAc extract by the titrimetric method [38]. Physicochemical characteristics of the initial soil are presented in supplementary Table 1S. Seed of rice variety BRRI dhan29 was collected from Bangladesh Rice Research Institute (BRRI), Gazipur, Bangladesh. This is a popular rice variety which is cultivated in boro season throughout the country. The grain size is thin with a high yield in irrigated conditions.

Bacterial isolate and tests for plant growth-promoting traits

A native Pseudomonas mosselii strain PR5, isolated from rice rhizosphere and molecularly characterized in our previous experiment (NCBI accession MZ540030), was used in this study.

The isolate was characterized for several growth-promoting traits, including atmospheric N fixation, P solubilization, indole acetic acid (IAA)production, HCN test, NH3 test and catalase test in our previous research [36]. The other growth-promoting traits were tested in the present study as follows:

Siderophore production assay

To assess siderophore production, the chrome azurol-S (CAS) method was followed as outlined by Perez-Miranda et al. [42]. The bacterial culture was introduced onto agar medium and allowed to incubate at 28 °C for 24 h. Siderophore production was determined by the detection of an orange halo zone surrounding the bacterial isolate on a blue background [43].

Zinc solubilization assay

The zinc-solubilizing ability was evaluated in mineral salt medium (MSM: NaCl 1 g, CaCl2 0.1 g, MgSO4 0.5 g, KH2PO4 1 g, K2HPO4 1 g, yeast extract 4 g, agar 16–18 g in 1 L, and pH was maintained at 7.2) [44]. As a source of insoluble zinc, 0.1% zinc oxide (ZnO) was added to the medium and autoclaved at 121 °C for 30 min [45]. A loop full of bacterial overnight growth in nutrient broth was spread on MS medium. Plates were incubated at 30 °C for 7 days. Strains showing a clear zone around the colony are considered zinc-solubilizing strains.

Silicon solubilization assay

Silicon (Si) solubilization assay was done following the procedure as described by Naureen et al. [46]. A basal medium containing 20 g glucose, 0.1 g magnesium sulphate, 0.2 g potassium chloride, 1 g ammonium sulphate, and 0.1 g potassium dihydrogen phosphate and 5 g of potassium alumina silicate as insoluble Si salt in 1 L used to evaluate the solubilization of Silicon. The medium was autoclaved after adding 1.5% agar in it. After solidification, a 0.01 mL freshly prepared bacterial strain suspension was poured onto a sterile filter paper placed in the centre of the Petri plate. After that, the plates were incubated at 28 °C for 5 days. The plates were then checked to see if there was a clear zone surrounding the filter papers that indicates the solubilization of silicon.

Confirmation of bacterial colonization in root

To confirm the endophytic colonization ability of P. mosselii strain PR5the rice root colonization test was done followed by the procedure developed by Chen et al. [47]. Rice seeds were surface sterilized with 1% sodium hypochloride (NaOCl) and primed with PR5 solution for 12 h. Similarly, a separate set of seeds, after being surface sterilized with sodium hypochloride (NaOCl), was soaked in deionized water. Both bacterial primed and unprimed seeds were then placed into separate Petri dishes for germination. After sprouting, when the roots were elongated approximately 2–3 cm, the roots were used for a colonization confirmation test. The roots of control and bacterial primed seedlings were washed separately with ethanol, followed by autoclaved water. Then the roots were cut into approximately 0.5 cm pieces and set into an agar plate. Each set was done in triplicate. After 24 h, the colonization was confirmed by visual observation of the developed colony on the root surface. It was found that PR5 primed seedlings showed 100% colonization in rice roots while control seedlings showed no colonization. The colonization figures are represented in supplementary Fig. 1S.

Pot experimental procedure

After initial analysis, the soil was mixed with the recommended dose of fertilizers and used for the pot experiment. The pots were laid out as per the experimental design and the details were as follows:

Preparation of pots and raising the seedlings

Pots of 20 cm deep, 15 cm diameter at the top, and 13 cm diameter at the bottom were used in this study. Each pot contained 8 kg of soil. Urea, triple super phosphate (TSP), -muriate of potash (MOP), gypsum, and zinc sulphate were applied at the recommended rate for boro rice at 325, 105, 187, 14 and 4.5 Kg/ha, respectively [48]. All the fertilizers were added to the soil as basal dosages in every pot, except for urea, which was applied in three split applications (Basal dose, at 25 DAT, and at 50 DAT). Seeds of rice cultivar BRRI dhan29, were sundried and soaked in distilled water for approximately 12 h. Then the seeds were placed in petridishes over wet tissue paper and kept for germination. The sprouted seeds were cultured in a pot and watered when necessary to raise seedlings for one month.

Preparation of bacterial inoculum and transplanting of the seedlings

The bacterial isolate PR5 was grown in liquid medium and then used for seedling priming following the procedure of Murundee et al. [49] with some modification. To prepare the seedlings for transplanting, 1 month-old rice seedlings were carefully uprooted and soaked in either distilled water or PR5 solution (108-109 CFU mL− 1) for seedling priming for 12 h. There were four treatments used for this study: control, seedling priming, root drenching, and cell-free culture (CFC) foliar application. The seedlings that were soaked in PR5 solution were used for seedling priming treatment and those were soaked in distilled water used for the three other treatments including control. Three seedlings were transplanted in each pot. The experiment was carried out in a completely randomized design with three replications.

Bacterial inoculation procedure for root drenching and CFC foliar treatment

For root drenching and cell free culture (CFC) filtrate foliar application treatments, the bacterium was applied at the tillering stage of rice seedlings following the procedure described by sultana et al. [50]. The liquid culture of bacteria (approx.108-109 CFU mL− 1) was filtered, and the bacterial cell that was retained on the filter paper was washed with deionized water, mixed with 1% carboxymethyl cellulose (CMC), and used for root drenching. The filtrated solution was centrifuged, and the supernatant was collected, mixed with 1% CMC, and applied as cell-free culture (CFC) by spraying over the canopy of the plant using a small sprayer. In the case of root drenching, the prepared solution was poured onto the soil around the perimeter of the hill in order to penetrate the root. For each treatment, approximately 10 mL solution was used for each plant. Thus, in both the root drenching and CFC foliar application methods and also in the seedling priming, bacterial inoculation was done once per treatment.

Harvesting and data collection

The plants were raised till they reach the maturity stage (130 days after transplanting). Intercultural operations such as weeding, watering and hand hoeing were done when necessary. After the grains became bright golden yellow, harvesting was done. Data were recorded on plant height, total tillers/pot, effective tillers or total panicles/pot, total gains/panicle, chaffy grains/panicle, 1000 grain weight, disease infestation (spot/plant), root length, fresh and dry weight of root, shoot, and flag leaf. The rice plants showed symptom of leaf blast disease at harvest and thus, the blast disease spots were recorded. The number of spots of blast disease in leaves were counted from each plant and averaged from each treatment.

Preparation of plant samples for analysis

During harvesting, the plants were separated into root and shoot parts. The fresh weight of the shoots was taken after removing mud and dust from the lower part. The roots of the rice plants were carefully uprooted by removing the soil around the roots. Then the roots were washed with copious tap water to remove all the soil and mud. Finally, the roots were washed with distilled water and wiped with tissue paper. Immediately after fresh weight collection, the root, shoot, and flag leaf samples were placed in an oven and dried at 65 °C for 48 h. The dried samples were cooled, and dry weights were taken. The dry samples were then crushed in a grinder. After preparation, the plant samples were placed in paper bags and stored until use.

Extraction of plant samples for nutrient determination

From plant samples (root, shoot, and flag leaf), extracts were prepared using the wet digestion method as described by Jackson [37]. For total N analysis, the plant sample was extracted following the method of Bremner [39]. Exactly 1.0 g plant sample was extracted in a block digester at 450 °C using concentrated sulphuric acid (H₂SO4) and hydrogen peroxide (H2O2) in the presence of a catalyst mixture of potassium sulphate (K₂SO4), copper sulphate (CuSO4.5H2O), and selenium powder. The plant extract for silicon (Si) determination was prepared following Estefan et al. [51]. In each case, reagent blanks were prepared in similar manners.

Determination of nutrients

The amount of N was determined by the semi-microkjeldhal method, as already mentioned in the analysis of the initial soil. The phosphorus content in the root, shoot, and flag leaf of rice was determined by developing a blue color with stannous chloride (SnC12.2H20) reduction of phosphomolybdate complex and measuring the color intensity with the help of a spectrophotometer at 660 nm wavelength [38]. The K content was determined by measuring the intensity of light emitted by potassium at 768 nm wavelength in a flame emission spectrophotometer [52]. Ca and Mg concentrations of plant samples were determined by the complexometric titration method using Na2EDTA as a complexing agent [38]. The turbidimetric analysis of sulfur in plant samples was performed using a spectrophotometer at 425 nm wavelength [53]. The concentrations of iron (Fe) and zinc (Zn) ions were determined using an atomic absorption spectrophotometer (AAS) (model: Shimadzu AA700), with a detection limit of 0.2 ppb. The relative standard deviation (RSD) was set to 2% prior to analysis. A reagent blank was used during the determination. The recovery percentage was maintained 95–105% using external standard at every 10 sample intervals. Standard inorganic iron (Fe), and zinc (Zn) of 1,000 mg L− 1 were used for the determination of the respective elements in the sample. All the standards of AAS grade were obtained from Inorganic Ventures, VA, USA. Silicon in flag leaf samples was determined by the spectrophotometric method following Estefan et al. [51].

Statistical analysis

The data were statistically analyzed using the Microsoft® Excel program and the analysis of variance (ANOVA) was done with the help of the Minitab17 program. The results have been interpreted based on the P test and the level of significance was evaluated by the Least Significance Difference (LSD) test at 5% level of significance. The mean values from various plant parameters of BRRI dhan29 were normalized and clustered for hierarchical analysis using the ‘pheatmap’ package in ‘R’. A color scale represents the intensity of these normalized mean values for each parameter. Principal component analysis (PCA) for the first two components (PC1 and PC2) was performed using the ‘‘Factoextra’ package in ‘R’ to reveal the relationships between treatments and variables.

Results

Plant growth-promoting characteristics of PR5

The Supplementary Table 2S summarized the plant growth-promoting traits of PR5 revealed in the present study and in our earlier study. In the current study, PR5 showed very good siderophore production ability with a very clear orange zone around the colony in CAS-agar media (Fig. 1A). Additionally, PR5 solubilized Zn from insoluble zinc oxide (ZnO) in MS medium (Fig. 1B). The isolate also showed Si solubilization potentiality and produced a clear zone around the colony in the basal medium containing insoluble aluminum silicate (Fig. 1C).

Fig. 1
figure 1

Characterization of PR5 for (A) Siderophore production indicated by the orange zone, (B) Zinc solubilization (inside the red circle) indicated by the clear zone, and (C) Silicon solubilization (shown by the arrow) indicated by the clear zone around the colony of PR5

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PR5 upregulated the growth and biomass of rice

Figure 2A and B showed that the inoculation of P. mosselii strain PR5 improved the rice plant height and number of tillers irrespective of bacterial inoculation methods, compared to the uninoculated control. The tallest plant was found in soil drenching treatment. Similarly, the application of PR5 increased the fresh and dry biomass of rice plants. The maximum shoot fresh weight (758.98 g/pot) was recorded in the seedling priming treatment (Fig. 2C). In contrast, plants without any bacterial strain (control) had the lowest shoot fresh weight (508.27 g/pot). The dry weight of bacterial treated plants was statistically similar in all the methods of application and was higher than the control. Similar to the shoot, the fresh weight of the flag leaf was higher in all the bacterial-treated plants compared to the control (Fig. 2D). However, the dry weight of flag leaf was statistically similar in all the treatments.

Fig. 2
figure 2

Effect of Pseudomonas mosselii PR5 on growth and biomass of BRRI dhan29. (A) plant height, (B) Number of tillers/pot, (C) fresh and dry weight of shoot, and (D) fresh and dry weight of flag leaf. Bars (mean ± standard error) with similar letter are not differed significantly according to LSD test (p < 0.05)

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PR5 improved the root characteristics of rice

Bacterial treatment significantly influenced the root length and root biomass especially the formation of lateral roots of the rice plant. The effect is prominent in seedling priming and in root drenching (Fig. 3). Figure 3A and B showed that the root length was highest in seedling priming, followed by root drenching. Maximum root fresh weight (146.93 g/pot) was recorded from the seedling priming treatment, and minimum fresh weight (110.07 g/pot) was recorded from the control (Fig. 3C). In the case of root dry weight, all the treatments were statistically similar except seedling priming. The root growth in the seedling primed rice plant was remarkably different from all the other treatments, with numerous fibrous and lateral roots that formed a mat that ultimately resulted in an increase of 33.5% in the fresh weight of the root compared to control. The dry weight of the root was also found to be highest in the seedling priming treatment. Visible observation showed a clear difference in root formation in the seedling primed and bacterial root drenched plants compared to the control (Fig. 3A).

Fig. 3
figure 3

Effect of Pseudomonas mosselii PR5 on root growth in BRRI dhan29. (A) photograph showing the root growth, (B) Root length, and (C) fresh and dry weight of root. Bars (mean ± standard error) with similar letter are not differed significantly according to LSD test (p < 0.05)

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PR5 improved the yield attributes and yield of rice cultivar BRRI dhan29

The application of PR5 increased the yield attributing parameters including number of panicles/pot, number of grains/panicle and number of filled grains/panicle, in rice in all the methods of application. Figure 4A shows that BRRI dhan29 yielded the maximum panicles/pot in root drenching, which was followed by seed priming and CFC foliar application. However, the number of grains per panicle was highest in seedling primed plants; next to it was root drenching, followed by CFC foliar application (Fig. 4B). Bacterial treatment increased the percentage of filled grain in all the methods of application compared to control (Fig. 4C). The grain weight per pot was also significantly increased by the bacterial inoculation by 53.52%, 52.99% and 42.24% in root drenching, seedling priming and CFC foliar application respectively. Although, the maximum grain weight was found in root drenching, the value was statistically similar to the seedling priming treatment (Fig. 4D). The lowest number of grains per pot and the lowest grain weight per pot were recorded in control plants which resulted the lowest gain yield per pot. Therefore, PR5 improved the yield attributing parameters and ultimately increased the yield of rice cultivar BRRI dhan29 in all the methods of application compared to the control.

Fig. 4
figure 4

Effect of Pseudomonas mosselii PR5 on yield of BRRI dhan29. (A) Numbers of Panicles/pot (B) Numbers of grains/ panicle, (C) Percent filled grain, (D) Grain yield (g/pot). Bars (mean ± standard error) with similar letter(s) are not differed significantly according to LSD test (p < 0.05)

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PR5 increased the major nutrients content in root, shoot and flag leaf of rice

The rice plants were analyzed for primary nutrients N, P and K; secondary nutrients Ca, Mg and S; and micronutrients Fe and Zn separately in the root, shoot and flag leaf. The results revealed that N content was significantly increased due to bacterial treatment in root, shoot and flag leaf, in all method of application. In both root and shoot, seedling priming and root drenching resulted in maximum N content, while in flag leaf, the highest N content was found in CFC foliar application (Fig. 5A). Likewise, the P content was also significantly increased in shoots and flag leaves due to bacterial application. As shown in Fig. 5B, seedling priming and CFC foliar application resulted in maximum P content both in the shoot and in the fag leaf. However, root P content was not affected by the bacterial application. No significant increase was found in K content in shoot and flag leaf, with a little increase in K content in seedling primed roots (Fig. 5C). Among the secondary nutrients, Ca content was not that much affected by bacterial treatment in shoot (Fig. 5D). However, the amount of Ca in root was highest in seedling primed plant whereas, CFC foliar application resulted highest Ca in flag leaf. Unlike the Ca content, the Mg content was significantly increased by bacterial application as compared to the control in all the plant parts (Fig. 5E). The maximum amount of Mg was found in the case of CFC foliar treatment in shoot and flag leaf, while root drenching yielded the maximum Mg content in root. Similarly, S content was significantly increased in bacterial treated plants compared to untreated plants (Fig. 5F). Maximum accumulation of S was found in shoot of rice plant in root drenching treatment. Bacterial CFC foliar application resulted in maximum S content in root and flag leaf and were statistically similar to the S content in seedling primed flag leaf.

Fig. 5
figure 5

Effect of Pseudomonas mosselii PR5 on nutrient contents of BRRI dhan29. (A) nitrogen, (B) phosphorus, (C) Potassium, (D) Calcium, (E) Magnesium, (F) Sulphur. Bars (mean ± standard error) with similar letter(s) are not differed significantly according to LSD test (p < 0.05)

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PR5 influenced the micronutrients Fe and Zn, and Si content in rice

Among the micronutrients, the Fe content in the root was not significantly increased by bacterial treatment. However, the Fe content in flag leaf and shoot was increased due to bacterial treatment in all methods of application (Fig. 6A). Seedling priming and CFC foliar application resulted in maximum Fe content in the shoot, whereas in the flag leaf, seedling priming, and root drenching resulted in maximum Fe content, followed by CFC foliar application. Similar to Fe, the Zn content in the root was also not affected by the bacterial treatment. Nevertheless, the Zn content in shoots and flag leaves increased in bacterial treated plants compared to control, and the amount of Zn was statistically similar in all the methods of application (Fig. 6B).

Fig. 6
figure 6

Effect of Pseudomonas mosselii PR5 on micronutrients Fe (A) and Zn content (B) of BRRI dhan29. Bars (mean ± standard error) with similar letter are not differed significantly according to LSD test (p < 0.05)

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Figure 7 shows that the Si content increased significantly due to the application of PR5. In the flag leaf of rice, the Si content differed among the treatments. Maximum Si was found in CFC foliar application, which is statistically identical to root drenching followed by seedling priming and control.

Fig. 7
figure 7

Effect of Pseudomonas mosselii PR5 on disease suppression of BRRI dhan29. (A) Photograph showing the leaves of rice plant of different treatments with blast symptoms (B) Number of spots/plant. Bars (mean ± standard error) with similar letter are not differed significantly according to LSD test (p < 0.05)

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PR5 reduced the symptom of the naturally occurred rice blast disease

The application of PR5 suppressed the naturally occurring blast disease. Bacterial CFC foliar application gave the best result against naturally occurring rice blast with no leaf blast symptoms (Fig. 8A). In contrast to the control, which had the highest blast spot per plant, the spot per plant was reduced in the two other bacterial application methods (Fig. 8B).

Fig. 8
figure 8

Effect of Pseudomonas mosselii PR5 on silicon content in flag leaf of BRRI dhan29. Bars (mean ± standard error) with similar letter are not differed significantly according to LSD test (p < 0.05)

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Principal component analysis (PCA) and visualization of data with clustered heatmap

Using colour intensity, a heatmap was created to show how various plant characteristics performed under various treatment scenarios. The parameters were then further sorted into two major clusters (Fig. 9A). Cluster- I, includes disease infestation is positively associated “Control’ treatment and Cluster- II, comprising most plant growth characteristics, is more associated bacterial treatments.

Fig. 9
figure 9

(A) Heatmap showing the hierarchical clusters of the parameters among the treatments using data normalization, (B) Scree plot showing prevalence variance explained by different principal components (dimension), and (C) PCA biplot showing direction of variables toward treatments

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Scree plot showed that the first three components describe 100% explained variance, whereas first two (PC1 and PC2) contribute the major portions (85.2%) (Fig. 9B). PCA biplot showed that most of the growth and yield contributing characters and the nutrient contents are directed to the bacterial treatment (Fig. 9C). Among the methods of PGPR application, seedling priming is related to most of the growth parameters, such as root and shoot fresh and dry biomass and nutrient parameters such as N, P, K, Fe, and Zn in the root, while the root drenching method is related to the plant height, tiller number, K in the shoot and root, and Mg in shoot. Bacterial CFC foliar application is related to most of the nutrient’s parameters especially in the flag leaves. Additionally, the disease infestation showed strong positive association with ‘Control’.

Discussion

Our research demonstrated three key findings upon inoculating native bacterium P. mosselii PR5 in rice, including increased agronomic characteristics, improved nutrient contents, and increased rice yield, with an additional suppression of naturally occurring rice blast disease. Among the agronomic characteristics, plant height and number of tillers, shoot and fresh and dry biomass, root length, and root biomass are the parameters where PR5 showed significant potential and thereby improved the rice growth. The growth-promoting effects of Pseudomonas sp. have been reported earlier in several research findings on diverse crops [54,55,56,57]. In rice, different Pseudomonas sp. and other PGPRs are reported to have efficacy in improving growth, agronomic performance, and grain yield [58,59,60,61]. Our findings align with the previous research regarding all the growth and yield attributes. The mechanism of improving growth by PR5 is the direct effect of nutrient absorption through atmospheric nitrogen fixation, solubilization of mineral nutrients such as P and Zn, and siderophore production by the bacterium as revealed in the current research and in our previous research [36]. The atmospheric nitrogen fixation by PR5 contributed to protein synthesis, which might ultimately increase the initiation of the number of panicles per hill, as described by Levedev et al. [62]. Additionally, phytohormone IAA production is another direct mechanism that triggers fibrous and lateral root formation and thereby increases the growth and yield of plants, as reported earlier in several studies [28, 63, 64]. Indirectly, the growth improvements might be enhanced by the siderophore production by PR5, which helps to protect the plant from pathogenic organisms, induces systemic resistance in plants, and provides a healthy environment for plant growth [65, 66]. Thus, the plant growth-promoting attributes of the bacterium PR5 found in the laboratory tests were also reflected in the pot experiment in actual field conditions.

In addition to the increase in growth and yield, PR5 showed significant improvement in several mineral nutrients in the rice plant. PCA analysis confirmed a positive association of most of the nutrient contents in the root, shoot, and flag leaf with PR5 inoculated treatments. The increase in N in the root, shoot, and flag leaf of rice can be explained by the direct effect of the atmospheric nitrogen fixing ability of PR5. The increased nitrogen content in rice plants might also be attributed to changes in bacterial-mediated soil enzyme activities, as reported by Zhang et al. [67]. The phosphate solubilization ability of PR5 may be another mechanism for increasing the P and other nutrient contents in rice, as described by Richardson [68]. The higher level of magnesium (Mg) and the micronutrients, particularly iron (Fe) and zinc (Zn), in the shoot and flag leaf can be attributed to the improved root structure facilitated by PR5, enabling better nutrient absorption from the soil. Additionally, PR5 solubilized insoluble Zn and produced siderophore under laboratory conditions, which could potentially increase Zn and Fe content in the shoot and flag leaf of rice. Though several studies have reported species of Pseudomonas as K-solubilizers [69], our results did not show any remarkable increase in K content in rice, suggesting that PR5 might not solubilize insoluble K.

In the current study, PR5 inoculation assisted rice plants in suppressing blast disease that occurred naturally, with the CFC foliar application treatment resulting in the most noticeable effect. Hierarchical clusters evidently demonstrate the strong negative association of CFC foliar application with disease suppression. Previous studies have widely explored the capability of P. mosselii to suppress disease in rice and other crops. Natural pyrazolotraizine pseudoiodinine in P. mosselii 923 is reported to suppress the rice blast pathogen Magnoprthe oryzae and the bacterial leaf blight (BLB) pathogen Xanthomonas oryzae [35], while pseudopyronine is reported as a potent antimicrobial agent in P. mosselii strain TR [34]. The c-xtl gene cluster in P. mosselii BS011 is proven to play an important role in antagonism against M. oryzae in rice [70] whereas ripAA gene is reported for the same function in another study [71]. Pseudomonas mediated induced systemic resistance (ISR) of plants and chitinase secretion were reported in several studies [72, 73]. In light of all these reports, we assumed that PR5 could potentially be able to produce one or more specific natural antifungal metabolites with the potential to prevent rice blast pathogen, which is our future research endeavor on PR5. The best result in blast disease control by bacterial CFC might be because the culture filtrate of bacteria contained different enzymes that might work directly to prevent the pathogen from invading and infecting plant tissue as described by Wu et al. [70]. Additionally, PR5 showed a positive result in the siderophore production test. Bacterial siderophore is well reported to help plants grow better by suppressing pathogenic fungi [74]. Furthermore, we previously reported that PR5 is a bacterium that produces HCN [36], which may help rice plants grow better by suppressing the pathogenic fungus and other microbes that grow around the inoculated root [75]. Moreover, the enhanced Si content in the flag leaf of PR5 inoculated rice plants indicated the possible interaction of Si with blast disease suppression. The importance of plant Si content in regulating bacterial and fungal diseases in rice has been recognized earlier in several studies [76, 77]. Previous research reports have shown that the severity of both leaf and panicle blasts in irrigated rice can be suppressed by applying Si-containing fertilizer to paddy fields [78,79,80]. Hayasaka et al. [76] reported that silicon content in rice seedlings significantly affected rice blast, with a reduced number of lesions when Si content increased in the rice seedlings, reinforcing the relevance of Si in controlling naturally occurring rice blast in our research.

Overall, it is evident that PR5 regulates plant growth through varied mechanisms. Firstly, through solubilizing insoluble nutrients P, Zn, and Si and by fixing atmospheric nitrogen, it enabled the rice plant to grow better and absorb more nutrients. Secondly, by secreting phytohormones that enhanced plant growth, especially changed the root characteristics that helped plants forage more water and nutrients, thereby increasing growth and yield. Finally, by protecting the plants from disease, especially from rice blast, through several ways, such as by producing siderophore, increasing the amount of silicon, producing HCN, or secreting any other potential antifungal metabolites in the root zone that might induce the resistance of plants against blast disease and thereby increase the growth and yield of rice.

Among the three bacterial inoculation methods evaluated, seedling priming demonstrated the most significant impact on plant growth parameters, particularly plant biomass, and greatly influenced yield attributes, resulting in the highest overall yield. This method notably altered root architecture, leading to an increase in lateral and fibrous roots, likely due to IAA production at a high level by the PR5 strain, as stated by Zhao [81]. Additionally, seedling priming facilitated maximum nutrient accumulation in the roots and enhanced nutrient mobilization to the shoots. In comparison, root drenching treatment produced the tallest plants, the highest number of panicles, and yields comparable to those achieved with seedling priming. The CFC foliar application was characterized by high nutrient accumulation, especially in the shoot and flag leaf, and protection against naturally occurring blast disease. Research has shown that applying PGPR and/or biochemicals to plant leaves can enhance nutrient uptake through several mechanisms, including boosting plant growth, improving nutrient use efficiency, promoting nutrient remobilization, and activating defence-related genes in rice and other crops [82,83,84,85,86,87], which might also happen in the present study. In terms of yield, seedling priming and root drenching methods were equally effective. However, for optimal nutrient uptake and practical field application, seedling priming could be the best choice of application. Combining seedling priming with CFC foliar application could provide additional benefits by further enriching plant nutrients and offering protection against blast disease.

Conclusion

The findings of the present research provide an insight into the exclusive role of P. mosselii PR5 in enhancing rice growth, nutrient uptake and yield in three different application methods. In comparison to the uninoculated control, PR5 inoculated rice plants exhibited a significant improvement in growth characteristics, yield attributes, and nutrient contents. Our result suggested that the application of P. mosselii PR5 could contribute to increasing rice production in a sustainable manner. The suppression of naturally occurring blast disease in bacterial inoculated plants, especially by the application of bacterial CFC is a sign that this bacterium might have an antagonistic effect against rice blast disease. Bacterial seedling priming produced the best root development and highest yield out of the three application methods examined; root drenching came in second. Conversely, the foliar application of bacterial CFC protected rice plant against pathogens and helped in nutrient absorption. Although both seedling priming and root drenching with the bacterium resulted in similar rice yields, seedling priming is easier to apply. Farmers can use this method before transplanting without incurring extra application costs. Therefore, rice seedling priming with PR5 could be an effective strategy for sustainable rice production. An additional benefit of disease control could be obtained by foliar application of the bacterium. Further study is necessary to reveal the efficacy of PR5 through seedling priming in combination with the foliar application of bacterial CFC that might boost the efficacy of the bacterium in rice.

Data availability

The bacterial isolate used in this study is collected from our previous experiment with the NCBI accession MZ540030.

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Acknowledgements

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Funding

The work was funded by Grant for Advance research in Education (GARE), Ministry of education (MoE), Bangladesh, with the grant number LS20211677.

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Authors and Affiliations

  1. Department of Agricultural Chemistry, Bangladesh Agricultural University, Mymensingh, Bangladesh

    Razia Sultana, Asif Iqbal Ibne Jashim & Md. Habibur Rahman

  2. Institute of Biotechnology and Genetic Engineering, Bangabandhu Sheikh Mujibur Rahman Agricultural University, Gazipur, Bangladesh

    Shah Mohammad Naimul Islam

  3. Division of Plant Pathology, Bangladesh Institute of Nuclear Agriculture (BINA), Mymensingh, Bangladesh

    Mohammad Mahbubul Haque

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  1. Razia Sultana
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  2. Asif Iqbal Ibne Jashim
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  3. Shah Mohammad Naimul Islam
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  4. Md. Habibur Rahman
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  5. Mohammad Mahbubul Haque
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Contributions

RS and SMNI: Conceived and designed the experiment; RS and MMH Conducted laboratory experiments; RS did the investigation, resources management, fund acquisition and supervision. AIIJ and HR performed the pot experiment, cured the data and performed chemical analysis. SMNI and AIIJ Performed the statistical analysis, RS wrote the manuscript; RS and SMNI revised the manuscript. All authors read and approved the manuscript.

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Correspondence to Razia Sultana.

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Sultana, R., Jashim, A.I.I., Islam, S.M.N. et al. Bacterial endophyte Pseudomonas mosselii PR5 improves growth, nutrient accumulation, and yield of rice (Oryza sativa L.) through various application methods. BMC Plant Biol 24, 1030 (2024). https://doi.org/10.1186/s12870-024-05649-6

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Keywords

BMC Plant Biology

ISSN: 1471-2229

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