Abstract
The utilization of plant growth-promoting microorganisms (PGPMs) represents a promising and environmentally sustainable approach to enhance global food production. These microorganisms improve nutrient availability by solubilizing minerals such as phosphates and silicates, especially when used in combination with organic fertilizers, thereby stimulating plant development. This study aimed to evaluate the rock powder solubilization capacity of PGPMs in vitro and their agronomic efficiency when combined with organic fertilizers on the growth of Passiflora edulis seedlings. Four bacterial strains Bradyrhizobium viridifuturi, Achromobacter spanius and Bacillus cereus. were characterized based on genetic, biochemical, and physiological traits, including hydrolytic enzyme production and their ability to solubilize rock powder. Parameters influencing solubilization, such as pH and electrical conductivity, were also evaluated. Greenhouse experiments were conducted over 60 and 90 days to assess seedling growth under four substrate conditions, with and without chemical fertilization. Growth parameters, including plant height, stem diameter, leaf number, and nutrient accumulation, were measured. (A) spanius and (B) cereus, effectively solubilized silicate rock in vitro. Notably, B. viridifuturi significantly enhanced seedling growth and nutrient uptake when applied to substrates containing both organic fertilizer and rock powder. These findings underscore the potential of PGPMs particularly B. viridifuturi as sustainable bioinoculants to improve nutrient availability and optimize seedling development in agricultural systems.
Introduction
Yellow passion fruit (Passiflora edulis Sims) plays a key role in Brazil’s agricultural economy, being one of the principal tropical fruits cultivated for both domestic consumption and export. In 2021, national production reached 697,859 tons [24]. However, maintaining high productivity and fruit quality remains a challenge, particularly due to the dependence on seedling vigor and appropriate fertilization practices [46, 53].
To reduce reliance on synthetic fertilizers without compromising crop performance, the use of plant growth-promoting bacteria (PGPB) has emerged as a promising and sustainable alternative [51]. These beneficial bacteria enhance plant growth by increasing nutrient availability, inducing plant defense mechanisms, and promoting tolerance to biotic and abiotic stresses. Their effects are commonly observed in improvements in plant height, stem thickness, leaf number, biomass accumulation, root development, and nitrogen uptake [8, 37, 38, 41, 46, 52].
PGPBs exert these effects through mechanisms such as the production of phytohormones (e.g., auxins), organic acids, siderophores, and extracellular enzymes (e.g., urease, phosphatases, proteases), which contribute to nutrient solubilization and uptake [15, 29, 38, 41, 51].
The use of remineralizing rock powders in agriculture has gained prominence as a sustainable practice for improving soil fertility and enhancing plant nutrition. These materials, derived from ground rocks, are natural sources of essential nutrients such as phosphorus (P), potassium (K), and silicon (Si), which play critical roles in plant growth, development, and responses to adverse environmental conditions. Silicon, in particular, has been widely recognized for its ability to increase plant resistance to both biotic and abiotic stresses. Through bacterial weathering of silicate minerals, soluble silicon is released into the soil, improving nutrient availability and overall plant performance [17]. The ability of silicate-solubilizing bactéria, notably species belonging to the genera Bacillus, Burkholderia, Rhizobium, and Pseudomonas to mobilize Si and K from rock powders represents a sustainable alternative that can reduce dependency on synthetic fertilizers [17, 60].
However, the efficiency of SSB inoculation depends on interactions between microbial traits, plant genotype, and substrate nutrient content. Therefore, this study aimed to assess the in vitro rock powder solubilization potential of selected PGPBs and their agronomic efficiency, in combination with organic fertilizers, on the growth and nutrition of P. edulis seedlings.
Materials and Methods
Identification and Characterization of Bacterial Strains
Bacterial strains from the microorganism collections of the Federal University of Recôncavo da Bahia (UFRB), Cruz das Almas, BA, and the Federal University of Lavras (UFLA), Lavras, MG, Brazil, were reactivated on synthetic nutrient agar (SNA) and incubated at 28 ± 1 °C under a 12-hour photoperiod. Subsequently, the strains were cultured in nutrient broth for the extraction of genomic DNA encoding the 16 S rRNA gene. DNA extraction was performed following the protocol described by Sambrook et al. [48]. Amplification was conducted using a GeneAmp PCR System 9700 (Applied Biosystems), and the purified PCR amplicons were sequenced at Eurofins Genomics India (Bengaluru). The resulting sequences were analyzed using BLAST against reference sequences available in the NCBI GenBank database [4]. The bacterial strains Bradyrhizobium viridifuturi – SEMIA 6461 [16], UFRB FA72A2-1 and UFRB FA34C2-2 were selected based on previous studies, as presented in Table 1.
Table 1.
Origin, characteristics, hosts, and functions of the bacterial strains
| Strains | Origin | Characteristics | Hosts | Functions | |
|---|---|---|---|---|---|
| Bradyrhizobium viridifuturi – UFLA 03–84 (SEMIA 6461) | Isolated from soils of the Brazilian Amazon; obtained from the collection of the Soil Science Department at the Federal University of Lavras, authorized by the Ministry of Agriculture, Livestock, and Food Supply (MAPA) [11] as an inoculant for cowpea. | Slow growth of 4 to 6 days. | Cowpea [Vigna unguiculata (L.) Walp.] [15, 27, 54]. | Biological nitrogen fixation, plant growth promotion, nitrogen accumulation in the aerial parts, and solubilization of CaHPO₄ and Al(H₂PO₄)₃ [10, 34, 35, 56]. | |
| UFRB FA34C2-2 | Isolated from an area with a history of cassava effluent application in the municipality of Vitória da Conquista, Brazil [55] | Rapid growth − 1 to 2 days. | Cowpea [55]. | Plant growth promotion, biological nitrogen fixation [9, 10, 14, 41]. | |
| UFRB FA72A2-1 | Isolated from an area with a history of cassava effluent application in the municipality of Vitória da Conquista [55]. | Rapid growth – 1 to 2 days. | Cowpea [55]. | Solubilization of CaHPO4 [55]; Plant growth promotion [41] | |
After reactivation, the bacterial strains were evaluated for their ability to synthesize auxins, siderophores, and extracellular hydrolytic enzymes, including urease, catalase, cellulase, protease, pectinase, and amylase [3, 12, 22, 28, 30, 40]. Biochemical and physiological analyses were performed in triplicate at the Soil Microbiology Laboratory of Embrapa Cassava and Tropical Fruits
In Vitro Solubilization of Rock Powder
To assess the ability of bacterial strains to solubilize rock powder, an in vitro experiment was conducted using a completely randomized design arranged in a 4 × 2 factorial scheme with three replicates in 150 mL Erlenmeyer flasks. The factors consisted of: (1) bacterial treatments—control (uninoculated), UFRB FA34C2-2, UFRB FA72A2-1 and UFLA 03–84, and (2) rock powder (SRP) doses—absence (0 g) and presence (0.5 g). Evaluations were conducted on days 7, 21, and 35.
The silicate rock powder (Ipirá Fértil) used in the experiment is derived from pyroxenite rock and was sourced from the region of Ipirá, Bahia, Brazil. The physicochemical analysis was provided by SGS GEOSOL LABORATÓRIOS LTDA (Report CA n° GQ2104274, REV.:00, issued on 16 July 2021). According to the laboratory report, the rock powder had the following chemical composition (%): SiO₂: 58.3; Al₂O₃: 13.3; Fe₂O₃: 7.15; CaO: 6.09; MgO: 4.36; TiO₂: 0.47; P₂O₅: 0.73; Na₂O: 1.36; K₂O: 5.44; MnO: 0.24; and Loss on Ignition (LOI): 3.04. The particle size was 0.3 mm, according to the manufacturer.
The bacterial strains were cultured in 50 mL of nutrient broth containing 5 g NaCl, 5 g peptone, 1.5 g meat extract, and 1.5 g yeast extract per 1000 mL of distilled water (Merck, Germany). The nutrient broth without inoculum or rock powder presented initial concentrations of Na⁺ (5.03 mg L⁻¹), Si (1.12 mg L⁻¹), and K⁺ (0.21 mg L⁻¹). The initial pH and electrical conductivity (σ) of the medium with and without rock powder were 6.8 and 8.2 µS cm⁻¹, and 6.0 µS cm⁻¹ and 8.0 µS cm⁻¹, respectively.
For inoculated treatments, 1 mL of bacterial suspension (1 × 10⁸ CFU mL⁻¹) was added to the culture medium. The nine flasks para cada tratamento were incubated at 30 °C with constant shaking at 160 rpm for 35 days. Measurements of pH and electrical conductivity were taken em três flasks on days 7, em três flasks 21, and três flasks 35. On the final day, the culture media were filtered using Whatman No. 01 filter paper under vacuum, and the concentrations of K⁺ and Na⁺ in the filtrate were determined by flame photometry, while Si was measured using atomic absorption spectrophotometry. Element concentrations were expressed in mg L⁻¹.
Effect of Bacterial Inoculation on Seedling Growth and Nutrition
To evaluate the effects of bacterial inoculation on the growth and nutrient status of Passiflora edulis seedlings, two greenhouse experiments were conducted at the experimental farm of the Center for Agricultural, Environmental, and Biological Sciences (CCAAB), Federal University of Recôncavo da Bahia (UFRB), in Cruz das Almas, Bahia, Brazil (12°39’27” S, 39°04’58” W; 215 m altitude).
In the first experiment, seeds were sown in polyethylene tubes with a capacity of 280 cm³ and cultivated for 60 days after sowing (DAS). In the second experiment, the seeds were sown in polyethylene bags with a capacity of 1.02 dm³, and the cultivation period was extended to 90 DAS.
Preparation of Inoculum and Growing Substrates
For inoculum preparation, the strain UFLA 03–84 was cultivated in semi-solid 79 medium for four days [36], while the strains UFRB FA34C2-2 and UFRB FA72A2-1, were grown in liquid nutrient broth for two days at 25 °C, reaching the logarithmic growth phase (1 × 10⁸ CFU mL⁻¹).
The growing substrates consisted of the following combinations: (1) soil + organic fertilizer (2:1, v/v) + rock powder; (2) soil + organic fertilizer (2:1, v/v); (3) soil + rock powder; and (4) soil alone. The soil used in both experiments—evaluated at 60 and 90 days after sowing (DAS) was a Dystrophic Yellow Latosol collected from the subsurface layer (> 40 cm) on the UFRB campus. Its chemical and physical properties were as follows: pH (H₂O): 5.0; pH (KCl): 4.0; ΔpH: 1.1; organic matter (OM): 1.43 kg kg⁻¹; available P (Mehlich 1): 0.04 mg dm⁻³; K⁺: 39.01 mg dm⁻³; Ca²⁺: 0.7 cmolc dm⁻³; Mg²⁺: 0.6 cmolc dm⁻³; (H + Al): 1.9 cmolc dm⁻³; Na: 0.17 cmolc kg⁻¹; sum of bases (SB): 40.32 cmolc dm⁻³; effective CEC: 1.81 cmolc dm⁻³; potential CEC: 3.21 cmolc dm⁻³; base saturation (V): 40.81%; sand: 514 g kg⁻¹; silt: 104 g kg⁻¹; clay: 382 g kg⁻¹; clay dispersion: 94 g kg⁻¹; flocculation degree: 193 g kg⁻¹. Soil electrical conductivity was 0.13 dS m⁻¹.
The organic fertilizer used in the substrates was produced at UFRB from composted tree prunings and manure from cattle and goats (3:1:1 ratio). Its composition was: pH (CaCl₂ 0.01 M): 7.6; total OM: 13.96%; N: 0.60%; P₂O₅: 1.36%; K₂O: 0.75%; Ca: 0.98%; Mg: 0.21%; S: 0.07%; C/N ratio: 9.0; Cu: 2 mg kg⁻¹; Mn: 200 mg kg⁻¹; Zn: 85 mg kg⁻¹; Fe: 10,089 mg kg⁻¹; B: 5 mg kg⁻¹; Na: 1,274 mg kg⁻¹. The composition of the silicate rock powder was previously described (see Sect. 2.1). Chemical fertilization in the control treatment (soil only) was applied based on the crop’s nutritional requirements during the sowing stage: 150 kg ha⁻¹ of N, 120 kg ha⁻¹ of P, and 20 kg ha⁻¹ of K [7].
Experimental Design
In the first experiment, a completely randomized design was used in a 5 × 4 factorial arrangement (inoculation sources × substrates), with 10 replicates and one plant per polyethylene tube. The treatments included: Factor 1- no inoculation and no chemical fertilization- No Che (SI) (i), no inoculation with chemical fertilization - Whit Che (SF) (ii), and inoculation with one of three bacterial strains UFLA 03–84 (iii), UFRB FA34C2-2 (iv), or UFRB FA72A2-1 (v); and Factor 2- four substrate compositions: soil + organic fertilizer + rock powder (i); soil + organic fertilizer (ii); soil + rock powder (iii); and soil alone (iv).
To validate the results obtained in the first experiment, a second experiment was conducted using a similar design, arranged in a 5 × 4 factorial scheme (five inocula × four substrates), with eight replicates and one plant per 1.02 dm³ polyethylene bag.
Planting, Inoculation, and Fertilization
Two seeds of Passiflora edulis Sims (accession BGP190 from the Embrapa Cassava and Fruits Germplasm Bank) were sown per container at a depth of 1 cm. Inoculation was carried out by applying 1 × 10⁸ CFU mL⁻¹ of bacterial suspension directly to the disinfected seeds. Control treatments received only the sterile culture medium (nutrient broth composed of 5 g NaCl, 5 g peptone, 1.5 g meat extract, and 1.5 g yeast extract per 1000 mL of distilled water; Merck, Germany), without inoculation.
In the chemical fertilization treatment, 41 mg dm⁻³ of N (urea), 18 mg dm⁻³ of P₂O₅ (triple superphosphate), and 4.8 mg dm⁻³ of K₂O (potassium chloride) were applied in the first experiment. In the second experiment, doses were increased to 48 mg dm⁻³ of N, 41 mg dm⁻³ of P₂O₅, and 21 mg dm⁻³ of K₂O. In treatments without chemical fertilization, P₂O₅ and K₂O were omitted to evaluate the isolated effects of inoculation, organic fertilizer, and/or silicate rock powder.
For treatments with rock powder, 0.48 g dm⁻³ (tubes) or 2.08 g dm⁻³ (bags) of the material was incorporated into the substrate [31]. The fertilizer doses in both experiments were adjusted based on container volume. All plants were irrigated daily under greenhouse conditions. Thinning was performed 15 days after sowing.
Morphological and Nutritional Characteristics of Passion Fruit Seedlings
In Experiments 1 and 2, seedlings were evaluated at 60 and 90 days after sowing (DAS), respectively, for the following parameters: plant height, stem diameter, number of leaves, root length, and chlorophyll content (chlorophyll a, chlorophyll b, and total chlorophyll a + b). Chlorophyll content was measured using a portable chlorophyll meter (ClorofiLOG CFL 1030).
Following these measurements, shoots and roots were separated and dried in a forced-air oven at 65 °C for 48 h. The dry mass of shoots, roots, and total biomass was determined, and the Dickson Quality Index (DQI) was calculated as proposed by Dickson et al. [19].
Dried shoot samples from three seedlings per treatment were selected for nutrient analysis. Nitrogen (N), phosphorus (P), and potassium (K) concentrations (%) were determined following the protocols described by Tedesco, Volkweiss, and Bohnen [57]. The accumulations of N, P, and K (mg per plant) were calculated by multiplying the shoot dry mass by the corresponding nutrient concentration.
Reisolation of Bacterial Strains
To validate the causal relationship, the bacterial strains were reisolated from inoculated plants following the observation of beneficial effects on growth and nutritional status. No strains were recovered from non-inoculated controls. These findings confirm that the observed improvements can be attributed to the inoculation with the tested strains.
Statistical Analysis
In the in vitro solubilization experiment, means corresponding to rock powder doses were compared using the F-test at a 5% significance level. All data were subjected to analysis of variance (ANOVA), and treatment means were grouped using the Scott–Knott test at the 5% probability level. For the in vivo experiments (Experiments 1 and 2), treatment means were compared using the Tukey test at a 5% significance level. All statistical analyses were performed using the R statistical software [47].
Results
Identification and Characterization of Bacterial Strains
All bacterial strains were capable of producing auxin and the enzyme amylase. Strain UFRB FA34C2-2 exhibited outstanding activity in producing lytic enzymes, including catalase, amylase, and protease. Strain UFRB FA72A2-1 produced cellulase, amylase, and protease. None of the strains were able to produce siderophores or the enzyme pectinase (Table 2).
Table 2.
Biochemical and physiological of the bacterial strain
| Characteristics | A. spanius | B. cereus | B. viridifuturi |
|---|---|---|---|
| UFRB FA34C2-2 | UFRB FA72A2-1 | UFLA-0384 | |
| Siderophore | - | - | - |
| Auxin | + | + | + |
| Urease | - | - | - |
| Cellulase | - | + | - |
| Catalase | + | - | + |
| Amylase | + | + | + |
| Pectinase | - | - | - |
| Protease | + | + | nd |
+ (produces); - (not produces); nd (not determined)
Sequencing of the DNA region encoding the 16 S rRNA gene indicated that strain UFRB FA34C2-2 (PQ219077.1) belongs to the genus Achromobacter, showing 99.3% similarity to Achromobacter spanius LMG 5911^T (AY_170848.1), its closest type strain. Similarly, strain UFRB FA72A2-1 (PQ219078.1) was identified as a member of the genus Bacillus, with 99.5% similarity to Bacillus cereus ATCC 14,579^T (MH_806388.1). The sequences obtained were analyzed using the BLAST tool against reference sequences available in the NCBI GenBank database. The identification of both strains was based on sequence similarity to their respective type strains and further supported by the comparison of additional housekeeping genes, conducted using PCR-amplified sequences.
In Vitro Solubilization of Rock Powder by Bacterial Strains
A significant three-way interaction was observed among bacterial inoculation, the presence or absence of rock powder, and the evaluation period for electrical conductivity. Additionally, a two-way interaction between the inoculants and the presence or absence of rock powder significantly affected pH, sodium, and silicon concentrations. The pH was influenced by interactions between the bacterial strains and rock powder, as well as between rock powder and the evaluation periods (p < 0.05) (Fig. 1).
Fig. 1.
pH of the culture medium under the effect of bacterial inoculation in the presence and absence of rock powder. Means followed by the same uppercase letter (for bacterial strains) or lowercase letter (for rock powder treatments) did not differ significantly according to the Scott–Knott or F-test at the 5% probability level
Treatments inoculated with B. viridifuturi UFLA 03–84, both in the presence and absence of rock powder, exhibited the highest average pH values. In contrast, the control treatment (without rock powder) showed the lowest pH values compared to the other treatments (Fig. 1).
On the 7th day of fermentation, the highest pH was observed in the culture medium inoculated with B. viridifuturi UFLA 03–84. Media inoculated with B. cereus presented the lowest pH values (7.8), while the control maintained the initial pH level (Fig. 2). From the 7th to the 21 st day, the pH increased across all treatments, with B. viridifuturi UFLA 03–84 reaching the highest value. By the 21 st day, strains (A) spanius UFRB FA34C2-2 and (B) cereus UFRB FA72A2-1, exhibited similar pH values, while the control recorded the lowest (6.8). On the 35th day, pH levels decreased in all treatments, except for (A) spanius UFRB FA34C2-2 and (B) viridifuturi UFLA 03–84, which maintained the highest averages. Interestingly, the control treatment showed an increase in pH, reaching 6.8.
Fig. 2.

pH of the culture medium under the effect of inoculation with bacterial strains at different fermentation times. Means followed by the same uppercase letter (for bacterial strains) or lowercase letter (for evaluation days) did not differ significantly according to the Scott–Knott or F-test at the 5% probability level
Electrical conductivity was influenced by the treatments and their interactions. A continuous increase in conductivity was observed in the treatments inoculated with B. viridifuturi UFLA 03–84, (A) spanius UFRB FA34C2-2 and (B) cereus UFRBFA72A2-1, both in the presence and absence of rock powder. In the control treatment with rock powder, conductivity decreased on the 21 st day and increased again on the 35th day. In the absence of rock powder, conductivity peaked on the 21 st day and remained unchanged between the 7th and 35th days (Fig. 3).
Fig. 3.
Electrical conductivity of the culture medium under the effects of bacterial inoculation and rock powder at different fermentation times. Means followed by the same uppercase letter (for bacterial strains) or lowercase letter (for evaluation times) did not differ significantly according to the Scott–Knott or F-test at the 5% probability level
The highest average concentrations of Na⁺ and Si were recorded in treatments with silicate rock powder, particularly in those inoculated with B. viridifuturi UFLA 03–84, both in the presence and absence of rock powder. This was followed by B. cereus UFRB FA72A2-1 for Na⁺ concentration and A. spanius UFRB FA34C2-2 for Si concentration (Fig. 4).
Fig. 4.
(A) Concentration of sodium (Na⁺) and (B) silicon (Si) available in the liquid culture medium with and without rock powder under the influence of bacterial inoculation on the 35th day. Means followed by the same uppercase letter (for bacterial strains) or lowercase letter (for rock powder treatments) did not differ significantly according to the Scott–Knott or F-test at the 5% probability level
A significant interaction (p < 0.05) was observed between the bacterial inocula and the presence of rock powder, influencing the concentration of K⁺. However, in the absence of rock powder, no significant effect (p > 0.05) on K⁺ concentration was detected, except for the treatment with B. viridifuturi UFLA 03–84, which exhibited the highest K⁺ concentration (Fig. 5).
Fig. 5.
Concentration of available potassium (K⁺) in the liquid culture medium under the influence of bacterial inoculation at 35 days. Means were grouped using the Scott–Knott test at a 5% probability level
Inoculation Experiments with Bacterial Strains in Seedlings Grown in Substrates
In both the first and second experiments, significant interaction (p < 0.05) was observed between cultivation substrates and bacterial inocula for all biometric variables (Tables 3 and 4). Seedlings inoculated with B. viridifuturi UFLA 03–84, followed by A. spanius UFRB FA34C2-2, exhibited the highest averages for plant height, number of leaves, and root length in both experiments. The most significant results were observed when seedlings were grown in soil + organic fertilizer + silicate rock powder and in soil + organic fertilizer, respectively, at 60 and 90 days after sowing (DAS).
Table 3.
Averages of the biometric variables of Passiflora edulis Sims seedlings based on the interaction between the cultivation substrate and inoculum, at 60 days after sowing on polyethylene tubes
| Subtrates | Inoculum | ||||
|---|---|---|---|---|---|
| B. viridifuturi | B. cereus | A. spanius | Whit Che | No Che | |
| Height (cm plant− 1) | |||||
| SFR | 20.16Aa | 17.88Ca | 18.59Ba | 17.80Cc | 17.02Da |
| SF | 18.12Bb | 16.47Bb | 16.98Bb | 16.89Bb | 15.70Cb |
| SR | 14.89Ac | 11.85Bc | 11.68Bc | 11.90Bc | 8.84Cc |
| Pure soil | 14.02Ad | 8.77Bd | 9.01Bd | 9.19Bd | 7.48Cd |
| CV (%) | 3.82 | 3.82 | 3.82 | 3.82 | 3.82 |
| Leaf number (leaves plant⁻¹) | |||||
| SFR | 8.1Aa | 7.0Aa | 6.7Ba | 6.5Ba | 6.8Ba |
| SF | 7.0Ab | 6.5Aa | 6.6Aa | 6.5Aa | 6.8Aa |
| SR | 6.6Ab | 5.3Bb | 5.1Bb | 5.2Bb | 4.8Bb |
| Pure soil | 6.1Ac | 4.8Bb | 5.1Bb | 5.3Bb | 4.5Bb |
| CV (%) | 11.31 | 11.31 | 11.31 | 11.31 | 11.31 |
| Root length (cm plant⁻¹) | |||||
| SFR | 21.15Aa | 19.53Ba | 19.55Ba | 17.81Ca | 16.69Da |
| SF | 20.09Ab | 19.00Ba | 19.88Aa | 17.00Ca | 14.81Db |
| SR | 20.32Ab | 17.87Bb | 20.32Aa | 15.89Cb | 13.06Dc |
| Pure soil | 16.98Bc | 15.58Cc | 17.95Ab | 15.52Cb | 12.26Dc |
| CV (%) | 5.3 | 5.3 | 5.3 | 5.3 | 5.3 |
| Shoot dry mass (g plant⁻¹) | |||||
| SFR | 0.99Aa | 0.50Da | 0.60Ca | 0.91Ba | 0.50Da |
| SF | 0.89Ab | 0.50Db | 0.50Cb | 0.51Bb | 0.40Cb |
| SR | 0.59Ac | 0.26Cc | 0.20Dc | 0.30Bc | 0.18Ec |
| Pure soil | 0.40Ad | 0.16Cd | 0.16Dd | 0.20Bd | 0.13Ed |
| CV (%) | 0.86 | 0.86 | 0.86 | 0.86 | 0.86 |
| Root dry mass (g plant⁻¹) | |||||
| SFR | 0.60Aa | 0.40Ca | 0.40Ca | 0.50Ba | 0.29Db |
| SF | 0.50Ab | 0.39Cb | 0.40Ba | 0.40Bb | 0.25Da |
| SR | 0.39Ac | 0.14Cc | 0.09Db | 0.20Bc | 0.08Ec |
| Pure soil | 0.28Ad | 0.08Cd | 0.07Dc | 0.10Bd | 0.06Ed |
| CV (%) | 0.96 | 0.96 | 0.96 | 0.96 | 0.96 |
| Total dry mass (g plant⁻¹) | |||||
| SFR | 1.59Aa | 0.90Da | 1.00Ca | 1.41Ba | 0.79Ea |
| SF | 1.39Ab | 0.88Db | 0.90Cb | 0.91Bb | 0.66Fb |
| SR | 0.97Ac | 0.39Cc | 0.29Dc | 0.50Bc | 0.26Ec |
| Pure soil | 0.68Ad | 0.24Cd | 0.22Dd | 0.30Bd | 0.19Ed |
| CV (%) | 0.62 | 0.62 | 0.62 | 0.62 | 0.62 |
| Dickson Quality Index | |||||
| SFP | 0.31Aa | 0.17Ca | 0.18Ca | 0.25Ba | 0.12Da |
| SF | 0.26Ab | 0.14Cb | 0.14Cb | 0.17Bb | 0.10Da |
| SR | 0.17Ac | 0.07Cc | 0.06Cc | 0.11Bc | 0.07Cb |
| Pure soil | 0.06Ad | 0.07Ac | 0.05Bc | 0.07Ad | 0.04Bc |
| CV (%) | 15.78 | 15.78 | 15.78 | 15.78 | 15.78 |
SFR = soil + organic fertilizer + rock powder; SF = soil + organic fertilizer; SR = soil + rock powder. Means followed by the same uppercase letter in a row belong to the same group according to the Scott–Knott test at the 5% probability level; means followed by the same lowercase letter in a column do not differ significantly according to the Tukey test at the 5% probability level. With Che: with chemical fertilization; No Che: without chemical fertilization and without inoculation
Table 4.
Averages of the growth variables of Passiflora edulis Sims based on the cultivation substrate and inoculum, at 90 days after sowing on polyethylene bags
| Substrates | Inoculum | ||||
|---|---|---|---|---|---|
| B. viridifuturi UFLA 0384 | A. spanius UFRB FA34C2-2 | B. cereusUFRB FA72A2-1 | With Che | No Che | |
| Height (cm plant-1) | |||||
| SFR | 29.91Aa | 29.03Ba | 26.18Da | 28.54Da | 17.51Ea |
| SF | 28.96Ab | 27.03Bb | 24.96Cb | 24.64Cb | 16.95Db |
| SR | 23.01Ac | 22.23Bc | 20.29Dc | 14.05Dc | 9.35Ec |
| Pure soil | 21.80Ad | 21.58Ad | 15.01Bd | 11.80Cd | 8.74Dd |
| CV (%) | 2.05 | 2.05 | 2.05 | 2.05 | 2.05 |
| Leaf number (leaves plant⁻¹) | |||||
| SFR | 11.25Aa | 10.50Ba | 9.50Ca | 9.38Ca | 7.38Da |
| SF | 9.50Ab | 9.50Ab | 9.13Aa | 8.63Ba | 7.8Ca |
| SR | 6.63Ac | 5.63Bc | 6.38Ab | 6.38Ab | 5.38Bb |
| Pure soil | 5.25Ad | 4.38Bd | 4.75Bc | 4.38Bc | 4.63Bb |
| CV (%) | 8.02 | 8.02 | 8.02 | 8.02 | 8.02 |
| Root length (cm plant⁻¹) | |||||
| SFR | 26.15Aa | 25.90Aa | 24.00Ca | 25.24Ba | 17.25Da |
| SF | 25.05Ab | 24.98Ab | 23.96Ba | 23.95Bb | 16.35Cb |
| SR | 23.89Ac | 19.90Cc | 18.00Db | 22.00Bc | 13.10Ec |
| Pure soil | 22.43Ad | 15.18Dd | 15.18Cc | 20.06Cd | 12.09Ed |
| CV (%) | 2.0 | 2.0s | 2.0 | 2.0 | 2.0 |
| Shoot dry mass (g plant⁻¹) | |||||
| SFR | 1.91Aa | 1.60Ba | 1.72Ba | 1.82Aa | 0.51Ca |
| SF | 1.91Aa | 1.33Bb | 1.21Cb | 1.41Bb | 0.41Da |
| SR | 0.79Ab | 0.60Bc | 0.50Bc | 0.68Bc | 0.19Cb |
| Pure soil | 0.50Ac | 0.43Ac | 0.29Bd | 0.40Ad | 0.17Bb |
| CV (%) | 16.67 | 16.67 | 16.67 | 16.67 | 16.67 |
| Root dry mass (g plant⁻¹) | |||||
| SFR | 0.90Aa | 0.90Aa | 0.50Ba | 0.90Aa | 0.39Ca |
| SF | 0.83Ab | 0.73Cb | 0.49Da | 0.80Bb | 0.35Eb |
| SR | 0.69Ac | 0.22Cc | 0.24Cb | 0.30Bc | 0.19Dc |
| Pure soil | 0.39Ad | 0.12Cd | 0.91Dc | 0.20Bd | 0.09Dd |
| CV (%) | 3.4 | 3.4 | 3.4 | 3.4 | 3.4 |
| Total dry mass (g plant⁻¹) | |||||
| SFR | 2.81Aa | 2.50Ba | 2.22Ca | 2.72Aa | 0.91Da |
| SF | 2.74Aa | 2.05Cb | 1.69Db | 2.21Bb | 0.76Ea |
| SR | 1.47Ab | 0.82Cc | 0.73Cc | 0.98Bc | 0.38Db |
| Pure soil | 0.88Ac | 0.55Bd | 0.38Cd | 0.59Bd | 0.27Cb |
| CV (%) | 10.93 | 10.93 | 10.93 | 10.93 | 10.93 |
| Dickson Quality Index | |||||
| SFR | 0.34Aa | 0.28Ba | 0.29Ba | 0.32Aa | 0.15Ca |
| SF | 0.29Ab | 0.25Ba | 0.21Cb | 0.21Cb | 0.12Da |
| SR | 0.15Ac | 0.10Bb | 0.06Bc | 0.15Ac | 0.07Bb |
| Pure soil | 0.09Ad | 0.05Bc | 0.04Bc | 0.08Ad | 0.05Bb |
| CV (%) | 29.93 | 29.93 | 29.93 | 29.93 | 29.93 |
SFR = soil + organic fertilizer + rock powder; SF = soil + organic fertilizer; SR = soil + rock powder. Means followed by the same uppercase letter in a row belong to the same group according to the Scott–Knott test at the 5% probability level; means followed by the same lowercase letter in a column do not differ significantly according to the Tukey test at the 5% probability level. With Che: with chemical fertilization; No Che: without chemical fertilization and without inoculation
Seedlings inoculated with (A) spanius UFRB FA34C2-2 also showed significantly higher values for these variables when compared to those inoculated with (B) cereus UFRB FA72A2-1 (Tables 3 and 4).
Seedlings that received no bacterial inoculation or fertilization, as well as those cultivated in soil + rock powder and in pure soil, presented reduced values for number of leaves and root length, regardless of the cultivation substrate used (Table 3).
For shoot dry mass, root dry mass, total dry mass, and the Dickson Quality Index (DQI), seedlings inoculated with B. viridifuturi UFLA 03–84 and cultivated in substrates composed of soil + organic fertilizer + rock powder and soil + organic fertilizer exhibited significantly higher averages than the other treatments, followed by the treatment with chemical fertilization (p < 0.05), at 60 and 90 days after sowing (DAS). Seedlings grown in soil + organic fertilizer + rock powder and inoculated with (A) spanius UFRB FA34C2-2 and (B) cereus UFRB FA72A2-1 also exhibited significantly higher values for these variables when compared to the uninoculated control and the treatment with soil alone (Tables 3 and 4).
In Experiment 2, the highest averages were observed in plants cultivated in the substrate composed of soil + organic fertilizer + rock powder and inoculated with B. viridifuturi UFLA 03–84 and A. spanius UFRB FA34C2-2, as well as in the treatment with chemical fertilization; no significant differences were found among these three treatments (Table 4).
Lower averages of dry mass and Dickson Quality Index (DQI) were observed in seedlings that did not receive bacterial inoculation or chemical fertilization across all evaluated substrates (Tables 3 and 4).
Passion fruit seedlings inoculated with B. viridifuturi UFLA 03–84 and cultivated in a substrate composed of soil, and rock powder exhibited the highest values for chlorophyll a, chlorophyll b, and total chlorophyll content, followed by seedlings subjected to chemical fertilization, at 60 and 90 days after sowing (DAS) (Tables 5 and 6).
Table 5.
Averages of the nutritional variables of Passiflora edulis Sims seedlings based on the interaction between the cultivation substrate and inoculum, at 60 days after sowing on polyethylene tubes
| Substrates | Inoculum | ||||
|---|---|---|---|---|---|
| B. viridifuturiUFLA 0384 | A. spaniusUFRB FA34C2-2 | B. cereusUFRB FA72A2-1 | With Che | No Che | |
| Chlorophyll a | |||||
| SFR | 37.23Aa | 36.13Ba | 32.31Da | 35.17Ca | 29.84Ea |
| SF | 35.83Ab | 33.23Bb | 30.45Cb | 33.68Bb | 28.00Db |
| SR | 32.84Ac | 28.43Bc | 27.85Bc | 32.52Ac | 25.29Cc |
| Pure soil | 27.92Ad | 24.12Cd | 24.22Cd | 25.01Bd | 22.45Dd |
| CV (%) | 2.38 | 2.38 | 2.38 | 2.38 | 2.38 |
| Chlorophyll b | |||||
| SFR | 15.28Aa | 10.95Ca | 11.04Ca | 12.72Ba | 12.72Ba |
| SF | 14.90Aa | 9.29Db | 9.99Cb | 10.50Bb | 10.50Bb |
| SR | 13.86Ab | 9.20Cb | 9.28Cc | 9.94Bc | 9.94Bc |
| Pure soil | 12.78Bc | 8.68Dc | 13.41Ad | 9.23Cd | 9.23Cd |
| CV (%) | 4.74 | 4.74 | 4.74 | 4.74 | 4.74 |
| Total Chlorophyll | |||||
| SFR | 52.51Aa | 47.08CEa | 43.35Da | 47.89Ba | 38.82Ea |
| SF | 50.73Ab | 42.52Cb | 40.44Db | 44.18Bb | 36.59Eb |
| SR | 46.70Ac | 39.20Cc | 37.13Cc | 42.46Bc | 33.42Ec |
| Pure soil | 40.70Ad | 32.80Dd | 37.63Bc | 34.24Cd | 29.45Ed |
| CV (%) | 2.13 | 2.13 | 2.13 | 2.13 | 2.13 |
| N accumulation (mg plant⁻¹) | |||||
| SFR | 43.78Aa | 17.51Da | 21.64Ca | 33.32Ba | 8.64Ea |
| SF | 24.81Bb | 12.99Cb | 14.19Bb | 14.45Bb | 6.10Db |
| SR | 13.84Ac | 4.35Cc | 4.32CBc | 6.62Bc | 2.46Dc |
| Pure soil | 6.92Ad | 2.42Cd | 2.30Cd | 3.12Bd | 1.64Cd |
| CV (%) | 3.47 | 3.47 | 3.47 | 3.47 | 3.47 |
| P accumulation (mg plant⁻¹) | |||||
| SFR | 7.78Aa | 3.31Ba | 3.69Ba | 6.90Ba | 0.91Da |
| SF | 6.23Ab | 3.16Ba | 2.94Ba | 3.18Bb | 0.76Ea |
| SR | 3.26Ac | 1.78Bb | 1.18Bb | 1.46Bc | 0.38Db |
| Pure soil | 1.81Ad | 0.51Bb | 0.51Bb | 0.74Bc | 0.27Cb |
| CV (%) | 10.93 | 10.93 | 10.93 | 10.93 | 10.93 |
| K accumulation (mg plant⁻¹) | |||||
| SFR | 5.00Aa | 2.39Ca | 3.02Ba | 4.90Aa | 1.55Da |
| SF | 2.38Ab | 1.71Bb | 1.66Bb | 1.81Bb | 1.18Ba |
| SR | 1.62Ac | 0.75Bc | 0.54Bc | 0.95Bc | 0.54Bb |
| Pure soil | 1.06Ad | 0.38Bc | 0.33Bc | 0.56Bc | 0.29Bb |
| CV (%) | 19.63 | 19.63 | 19.63 | 19.63 | 19.63 |
SFR = soil + organic fertilizer + rock powder; SF = soil + organic fertilizer; SR = soil + rock powder. Means followed by the same uppercase letter in a row belong to the same group according to the Scott–Knott test at the 5% probability level; means followed by the same lowercase letter in a column do not differ significantly according to the Tukey test at the 5% probability level. With Che: with chemical fertilization; No Che: without chemical fertilization and without inoculation
Table 6.
Averages of the nutritional variables of Passiflora edulis Sims seedlings based on the interaction between the cultivation substrate and inoculum, at 90 days after sowing on polyethylene bags
| Substrates | Inoculum | ||||
|---|---|---|---|---|---|
| B. viridifuturiUFLA 0384 | A. spaniusUFRB FA34C2-2 | B. cereusUFRB FA72A2-1 | With Che | No Che | |
| Chlorophyll a | |||||
| SFR | 45.66Aa | 40.69Ca | 40.40Ca | 44.15Ba | 29.90Da |
| SF | 39.73Ab | 35.55Bb | 34.12Bb | 39.90Ab | 28.60Db |
| SR | 35.26Ac | 30.76Cc | 29.61Dc | 34.06Bc | 27.57Ec |
| Pure soil | 29.99Ad | 28.44Bd | 26.18Cd | 26.03Cd | 23.95Dd |
| CV (%) | 2.25 | 2.25 | 2.25 | 2.25 | 2.25 |
| Chlorophyll b | |||||
| SFP | 20.31Aa | 19.14Ba | 16.15Db | 17.73Ca | 11.08Ea |
| SF | 19.74Ab | 13.98Db | 18.06Ba | 16.43Cb | 9.05Eb |
| SR | 12.19Ac | 12.21Ac | 11.95Ac | 11.01Bc | 9.08cb |
| Pure soil | 10.99Ad | 10.06Ad | 10.66Ad | 9.93Bd | 9.19Cb |
| CV (%) | 3.19 | 3.19 | 3.19 | 3.19 | 3.19 |
| Total Chlorophyll | |||||
| SFR | 65.92Aa | 59.83Ca | 56.15Da | 61.86Ba | 40.96Ea |
| SF | 59.46Ab | 49.53Db | 52.23Cb | 56.33Bb | 37.65Eb |
| SR | 47.45Ac | 42.98Cc | 41.54Dc | 45.08Bc | 36.65Ec |
| Pure soil | 40.98Ad | 38.50Bd | 36.84Cd | 35.95Cd | 33.14Dd |
| CV (%) | 1.96 | 1.96 | 1.96 | 1.96 | 1.96 |
| N accumulation (mg plant⁻¹) | |||||
| SFR | 92.49Aa | 85.40Aa | 80.79Ba | 76.84Ba | 21.22Da |
| SF | 84.07Ab | 57.11Cb | 52.32Cb | 63.01Bb | 15.19Da |
| SR | 34.78Ac | 26.03Bc | 20.90Bc | 28.95Ac | 5.34Cb |
| Pure soil | 20.00Ad | 16.18Ad | 9.25Bd | 15.18Bd | 4.36Bb |
| CV (%) | 10.54 | 10.54 | 10.54 | 10.54 | 10.54 |
| P accumulation (mg plant⁻¹) | |||||
| SFR | 28.05Aa | 19.84Ca | 21.17Ca | 23.44Ba | 4.65Da |
| SF | 23.80Ab | 12.97Cb | 11.10Cb | 15.56Bb | 3.33Dab |
| SR | 7.91Ac | 5.47Ac | 4.16Bc | 6.77Ac | 1.41Cab |
| Pure soil | 4.98Ac | 4.26Ac | 2.29Bc | 3.99Ac | 4.65Db |
| CV (%) | 15.28 | 15.28 | 15.28 | 15.28 | 15.28 |
| P accumulation (mg plant⁻¹) | |||||
| SFR | 13.75Aa | 9.92Ba | 12.29Aa | 12.88Aa | 3.03Ca |
| SF | 11.09Bb | 7.72Bb | 6.14Cb | 8.62Bb | 2.23Dab |
| SR | 4.01Ac | 2.99Bc | 2.13Cc | 4.01Ac | 0.83Dbc |
| Pure soil | 2.57Ad | 2.32Ac | 1.16Bc | 2.15Ad | 0.56Bc |
| CV (%) | 13.07 | 13.07 | 13.07 | 13.07 | 13.07 |
SFR = soil + organic fertilizer + rock powder; SF = soil + organic fertilizer; SR = soil + rock powder. Means followed by the same uppercase letter in a row belong to the same group according to the Scott–Knott test at the 5% probability level; means followed by the same lowercase letter in a column do not differ significantly according to the Tukey test at the 5% probability level. With Che: with chemical fertilization; No Che: without chemical fertilization and without inoculation
In Experiment 1, seedlings inoculated with A. spanius UFRB FA34C2-2 and B. cereus UFRB FA72A2-1 and cultivated in soil + organic fertilizer + rock powder also showed significantly higher chlorophyll levels compared to control (Table 5).
Seedlings grown in the substrate composed only of soil, without bacterial inoculation or chemical fertilization, exhibited the lowest chlorophyll values in both experiments (Tables 5 and 6).
Substrates composed of soil + organic fertilizer + silicate rock powder and soil + organic fertilizer, when combined with bacterial inoculation particularly with strain B. viridifuturi UFLA 03–84 enhanced the nutritional status of the seedlings, resulting in significantly higher accumulations of nitrogen (N), phosphorus (P), and potassium (K) (p < 0.05) (Tables 5 and 6).
In Experiment 1, seedlings grown in these substrates and inoculated with B. viridifuturi UFLA 03–84, (A) spanius UFRB FA34C2-2, (B) cereus UFRB FA72A2-1, or supplemented with mineral nitrogen exhibited the highest K accumulation (Table 5).
In Experiment 2, seedlings cultivated in soil + organic fertilizer + silicate rock powder, inoculated with B. viridifuturi UFLA 03–84, and supplemented with chemical fertilization showed no significant difference in K accumulation when compared to each other (Table 6).
Seedlings inoculated with (A) spanius UFRB FA34C2-1 and (B) cereus UFRB FA72A2-1 exhibited significantly higher nutrient accumulation compared to the treatment without inoculation and chemical fertilization in both experiments (Tables 5 and 6). Lower accumulations of N, P, and K were observed in seedlings grown in pure soil, regardless of inoculation.
In Experiment 1, no significant difference in phosphorus accumulation was observed between the substrates composed of soil + silicate rock powder and pure soil (Table 5). The lowest averages for these variables were recorded in the treatment without inoculation and chemical fertilization.
Discussion
All bacterial strains demonstrated the ability to convert insoluble minerals, including silicon (Si), potassium (K), and sodium (Na), into soluble forms, with varying degrees of efficiency. Bradyrhizobium viridifuturi UFLA 03–84 showed outstanding performance in increasing Si and K availability in the culture medium (Figs. 4 and 5). These results suggest that strain B. viridifuturi UFLA 03–84 acts as a silicate-solubilizing bacterium capable of enhancing the benefits of rock powder application. Given that the rock powder used in this study originated from pyroxenite, a mafic–ultramafic silicate rock rich in ferromagnesian minerals such as pyroxenes, its mineralogical composition is particularly relevant.
Additionally, strain B. viridifuturi UFLA 03–84 solubilized Si and K in alkaline media with high electrical conductivity (Figs. 3 and 4, and 5). In other studies, this strain was also shown to solubilize Ca3(PO4)2 [36] and tolerate up to 30 g L⁻¹ of NaCl in culture media [39]. Nutrient solubilization by rhizobacteria is a promising strategy for improving nutrient availability to plants [2, 23, 29]. However, further research is necessary to validate the effectiveness of these bacteria in enhancing nutrient availability under controlled conditions over time and in various cultivation and substrate contexts for seedling production using silicate rock powder and other microbial agents.
Several studies have suggested that the decrease in pH during fermentation, resulting from organic acid production and proton release, is a key mechanism for phosphate solubilization [20, 36, 49]. However, strains B. viridifuturi UFLA 03–84, Achromobacter spanius UFRB FA34C2-2, and Bacillus cereus UFRB FA72A2-1 did not reduce the initial pH of 6.8 after 35 days of fermentation (Fig. 2), indicating that acidification was not the mechanism responsible for solubilization at this pH. It is possible that the acids were present in anionic forms, contributing instead to Si chelation [25]. Only strain UFLA 03–84 demonstrated effective solubilization of Si (16 mg L⁻¹) and K (16.5 mg L⁻¹), along with an increase in pH (Figs. 3 and 4, and 5), suggesting the involvement of alternative solubilization mechanisms such as siderophore production, exopolysaccharide (EPS) secretion, or silicase enzyme activity [5, 17, 20, 36, 44]. Therefore, the bacterial capacity to solubilize minerals reinforces the agronomic value of both the inoculant and the rock powder.
An increase in soluble Na⁺ concentration was observed in the nutrient broth (Fig. 4), a result also reported by Setiawati and Mutmainnah [49] when evaluating mineral-solubilizing bacteria on Alexandrov agar medium. During the solubilization of silicate rock powder, protons and organic acids such as ferulic, citric, and coumaric acids are released, acidifying the medium, destabilizing mineral structures [20, 49], and increasing the availability of elements present in the rock (Figs. 4 and 5). Under saline stress conditions, strain B. viridifuturi UFLA 03–84 has demonstrated tolerance to a wide range of pH values (4 to 10), temperatures (15 to 37 °C), and NaCl concentrations (up to 0.75%) [16, 39], highlighting its adaptability to diverse soil and climate conditions in Brazil [16, 33, 55, 56].
Inoculation with strain B. viridifuturi UFLA 03–84 in combination with soil, organic fertilizer, and rock powder improved all morphophysiological traits and nutrient status of Passiflora edulis Sims seedlings. These treatments outperformed the combination of soil, organic fertilizer, rock powder, and chemical fertilizer (Tables 3, 4 and 5, and 6), regardless of substrate volume or cultivation period. The benefits of inoculation may be attributed to the strain’s ability to produce auxins, amylase, and catalase (Table 2), making these compounds available to the plant. These findings indicate that inoculation with this strain, along with organic fertilizer and rock powder, met the nutritional requirements at this developmental stage and may reduce the duration of nursery cultivation.
The observed improvements in morphophysiological traits and nutrient content in P. edulis seedlings (Tables 3, 4, 5 and 6) can also be explained by changes in the chemical and physical properties of the substrates, including pH, cation exchange capacity, organic matter content, moisture, and water retention [8, 37]. Even in substrates with a low organic matter-to-soil ratio (e.g., 20:80), fertility tended to increase, reaching high levels of P and K. In general, substrates containing 10% to 30% organic matter provide the best results [8, 37]. In this study, improvements were observed in the 2:1 (soil: organic compost) substrate, regardless of the bacterial strain used.
The benefits of plant growth-promoting bacteria (PGPB) largely depend on the affinity between microorganisms and plant species. In this study, plant growth promotion was closely linked to root colonization, particularly in seedlings inoculated with B. viridifuturi UFLA 03–84 followed by (A) spanius UFRB FA34C2-2. The increase in root length resulting from inoculation with (B) viridifuturi UFLA 03–84 and cultivation in soil enriched with organic fertilizer and rock powder (Tables 3 and 4) likely provided structural support and greater seedling vigor under field conditions, balancing shoot growth and increasing resistance to mechanical stress. These morphological changes may also result from enhanced P availability via microbial solubilization in the substrate [21].
Inoculation with PGPB improved nutrient availability in cultivation substrates, especially those containing organic fertilizer and silicate rock powder, as well as organic fertilizer alone (Tables 5 and 6). This improvement in plant nutritional status resulted from organic matter mineralization [1] and the gradual nutrient release from rock powder, a process accelerated by the presence of solubilizing bacteria [50].
It is also important to consider that the organic fertilizer used in this study may have introduced a diverse community of native microorganisms capable of influencing nutrient solubilization and plant development. Organic fertilizers are known to harbor beneficial microbial consortia, including bacteria and fungi with functional traits such as phosphate and silicate solubilization, nitrogen fixation, and the production of phytohormones and exopolysaccharides [58]. Therefore, the improved morphophysiological and nutritional parameters observed in treatments containing organic fertilizer, either alone or combined with rock powder, may result not only from the nutrient content of the organic material but also from the synergistic activity between the native microbiota and the inoculated strains. This potential interaction could have enhanced mineral solubilization and nutrient uptake by the plants, reinforcing the importance of further studies to distinguish the individual and combined effects of native and inoculated microorganisms under controlled conditions.
The positive effects of B. viridifuturi UFLA 03–84 on N, P, and K accumulation (Tables 5 and 6) can be attributed to biological nitrogen fixation [13], nutrient solubilization [2, 20], and extracellular enzyme production (Table 2). Other unquantified microbial processes, such as exopolysaccharide secretion, may also have contributed to these effects [23, 45].
Root architecture influences water and nutrient absorption capacity [6]. Root elongation, often triggered by nutrient deficiency, directs energy toward nutrient acquisition, resulting in longer roots and reduced shoot growth. This pattern was observed in seedlings cultivated on soil + rock powder and pure soil (Tables 3 and 4).
The Dickson Quality Index (DQI) [19], which considers plant robustness and biomass distribution, showed significantly higher values in seedlings inoculated with B. viridifuturi UFLA 03–84 and cultivated in soil + organic fertilizer + rock powder. These improvements may be due to enhanced nutrient availability (Figs. 3 and 5; Tables 3 and 5), hormone secretion, and improved water and nutrient uptake, resulting in greater plant growth and biomass accumulation [42, 43]. Combined bacterial inoculation and organomineral fertilization has been reported to reduce nitrogen fertilizer requirements, improve nutrient availability in Vicia faba L., and increase soil nitrogen content (Hannon et al., 2020). These findings corroborate the present study, suggesting that nitrogen fertilization can be reduced or replaced in P. edulis seedling production using organomineral substrates.
Seedlings grown in soil-only substrates showed lower nutrient uptake, reduced growth and biomass, and lower DQI values compared to those cultivated with organic fertilizer and silicate rock powder, with a 75% improvement (Tables 3 and 4). The Dystrophic Yellow Latosol used in this study is acidic and nutrient-poor, emphasizing the importance of substrate fertilization to ensure seedling quality through adequate nutrition, root development, and microbial activity [32].
Nitrogen, phosphorus, and potassium fertilization improved seedling growth and nutrition at 60 and 90 DAS compared to treatments without mineral N and inoculation (Tables 3, 4, 5 and 6). In other studies, applying 600 mg dm⁻³ of mineral K increased seedling height and total dry biomass (Myake et al., 2016). However, inoculation with B. viridifuturi UFLA 03–84 combined with organic fertilization and rock powder may provide comparable gains while reducing chemical fertilizer inputs.
This study clearly demonstrated increased nutrient content in seedlings grown in substrates enriched with rock powder and organic fertilizer. In the context of sustainable agriculture, these results are timely and highlight the potential to improve soil health through alternative substrate formulations that promote the sustainable production of high-quality seedlings.
Bioinputs play a critical role in sustainable development by transforming agriculture through low-impact practices aligned with the Sustainable Development Goals (SDGs). By integrating living organisms, organic fertilization, and biological processes, bioinputs enhance plant nutrition, suppress pests and diseases, and reduce dependence on synthetic inputs, major contributors to soil degradation and water contamination. This approach aligns directly with SDG 2 (Zero Hunger and Sustainable Agriculture), SDG 6 (Clean Water and Sanitation), and SDG 15 (Life on Land), promoting environmental conservation and efficient food production. The application of silicates demonstrates how innovative practices can improve plant nutrition. Silicates are solubilized in soil through root exudates and microbial action, particularly from silicate-solubilizing microorganisms [26, 59], increasing Si availability for plant uptake and enhancing stress resilience [18, 31, 43]. In P. edulis cultivation, the combined use of biological inoculants and rock powder supported vigorous plant development and improved sustainability in production systems. This biotechnology thus represents an innovative solution aligned with the SDGs, fostering food security, soil conservation, and sustainable agricultural practices.
Conclusions
The bacterial strains Bradyrhizobium viridifuturi UFLA 03–84, Achromobacter spanius UFRB FA34C2-2, and Bacillus cereus UFRB FA72A2-1 demonstrated the ability to solubilize nutrients from silicate rock powder, revealing their potential as bioinputs for sustainable agriculture. Among them, B. viridifuturi UFLA 03–84 exhibited superior efficiency in solubilizing silicon and potassium and promoted significant improvements in the morphophysiological and nutritional quality of Passiflora edulis seedlings. Seedlings cultivated in a substrate composed of soil + organic fertilizer + rock powder (2.08 g dm⁻³) and inoculated with this strain showed higher nutrient accumulation and better growth performance at both 60 and 90 days of cultivation, making this combination a promising biotechnological alternative for passion fruit seedling production.
This study advances the understanding of how microbial inoculation can enhance the agronomic efficiency of rock powder and organic fertilizers, reducing dependence on chemical fertilizers. The results also highlight the need for further investigations to elucidate the synergistic interactions between inoculated strains and native microorganisms introduced through organic fertilizers, as well as to evaluate the persistence, colonization dynamics, and efficiency of these bacteria under field conditions. Such studies will strengthen the application of microbial–mineral–organic integrations in sustainable and low-input agricultural systems.
Acknowledgements
The authors would like to thank the Coordination for the Improvement of Higher Education Personnel (CAPES) for financial and logistical support provided for this research.
Author Contributions
Conceptualization, R.S.A.N., F.M.S.M. and C.S.B.; methodology, C.S.B., R.S.A.N. and F.M.M.; validation, C.S.B. and A.J.C.; formal analysis, C.S.B.; investigation, C.S.B.; data curation, C.S.B., R.S.A.N, F.M.S.M., F.M.M. and F.H.;
Funding
The Article Processing Charge (APC) for the publication of this research was funded by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) (ROR identifier: 00x0ma614). This research received external funding from the Brazilian Federal Agency for Support and Evaluation of Graduate Education. To the Federal University of Recôncavo da Bahia (UFRB) and the Brazilian Agricultural Research Corporation (Embrapa Cassava and Fruits) for the institutional support and infrastructure provided, essential for the execution of this study.
Data Availability
All data are provided in the manuscript.
Code Availability
Not applicable.
Declarations
Competing interests
The authors declare no competing interests.
Consent to Participate
The author has agreed to participate.
Consent to Publish
The author has agreed to the publication.
Ethical Approval
This article does not involve research with humanparticipants and/or animals, and the author has informed consent.
Footnotes
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
References
- 1.Abreu AHM, Leles PSS, Alonso JM, Abel ELS, Oliveira RR (2017v) Characterization of sewage sludge generated in Rio de Janeiro, Brazil, and perspectives for agricultural recycling. Semin Cienc Agrar 38(4):2433–2448. 10.5433/1679-0359.2017vv38n4Supl1p2433 [Google Scholar]
- 2.A Adhikari A, Lee K-E, Khan M, Kang S-M, Adhikari B, Imran M, Jan R, Kim K, Lee IJ (2019) Effect of silicate and phosphate solubilizing rhizobacterium Enterobacter ludwigii GAK2 on Oryza sativa L. under cadmium stress. J Microbiol Biotechn 29(1):118–126. 10.4014/jmb.1906.06010 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3.Alves AJCP (2006) Espécies de Botryosphaeria em Quercus spp. e outros hospedeiros lenhosos: taxonomia e filogenia [PhD thesis]. Universidade de Aveiro, Aveiro, Portugal
- 4.Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programmes. Nucleic Acids Res 25(17):3389–3402. 10.1093/nar/25.17.3389 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Angeli A, De Luca V, Capasso C, Di Costanzo LF, Supuran CT (2024) Comparative CO2 and SiO2 hydratase activity of an enzyme from the siliceous demosponge Suberites domuncula. Arch Biochem Biophys 758:110074. 10.1016/j.abb.2024.110074 [DOI] [PubMed] [Google Scholar]
- 6.Binotto AF, Lúcio DA, Lopes SJ (2010) Correlations between growth variables and the dickson quality index in forest seedlings. Cerne 16(4):457–464. 10.1590/S0104-77602010000400005 [Google Scholar]
- 7.Borges AL, Rosa RCC (2009) Calagem e adubação para o maracujazeiro. Recomendações
- 8.Braulio CS, Nóbrega RSA, Moreira FM, Anjos SJC, Silva JJ, Rocabado JMA (2019) Growth response of Bauhinia variegata L. to inoculation and organic fertilization. Rev Arvore 43(1):e430104. 10.1590/1806-90882019000100004 [Google Scholar]
- 9.Braulio CS, Silva LFL, Silva CS, Correia AJ, Rocabado JMA, Nóbrega RSA (2021) Can inoculation with diazotrophic bacteria decrease the productivity loss of defoliated Vigna unguiculata (L.) Walp? Revista Brasileira de Engenharia Agrícola e Ambiental 25(3):189–196. 10.1590/1807-1929/agriambi.v25n3p189-196 [Google Scholar]
- 10.Braulio CS, Nóbrega RSA, Silva LCV, Correia AJ, Sousa CBC, Pereira EG (2020) Inoculation of diazotrophic bacteria in chicory. Ornam Hortic 38(2):185–191. 10.1590/S0102-053620200211 [Google Scholar]
- 11.BRASIL (2011) Instrução normativa nº 13, de 24 de março de 2011. Protocolo oficial para avaliação da viabilidade e eficiência agronômica de cepas, inoculantes e tecnologias relacionados ao processo de fixação biológica de nitrogênio em leguminosas. Diário Oficial da União, nº 58, 25
- 12.Cattelan AJ (1999) Métodos quantitativos para determinação de características bioquímicas e fisiológicas associadas com bactérias promotoras do crescimento vegetal. Embrapa Soja, Londrina, p 36 [Google Scholar]
- 13.Correia AJ, Nóbrega RSA, Oliveira AS, Santana WS, Silva Braulio C, Oliveira MS, Sousa CBC, Santos AR (2021) Productivity and growth in cowpea inoculated with rhizobia under different light environments. Rev Cienc Agron 37:e37057. 10.14393/BJ-v37n0a2021-51542 [Google Scholar]
- 14.Correia AJ (2017) Eficiência simbiótica de bactérias diazotróficas isoladas de solos com histórico de deposição de manipueira em feijão-caupi cultivar EPACE 10. Undergraduate thesis, Universidade Federal do Recôncavo da Bahia, Cruz das Almas, BA, Brazil
- 15.Costa EM, Carvalho F, Nóbrega RSA, Silva JS, Moreira FMS (2016) Bacterial strains from floodplain soils perform different plant growth promoting processes and enhance cowpea growth. Sci Agrar 73(4):301–310. 10.1590/0103-9016-2015-0294 [Google Scholar]
- 16.Costa EM, Carvalho TS, Guimarães AA, Leão ACR, Cruz LM, Baura VA, Lebbe L, Willems A, Moreira FMS (2019) Classification of the inoculant strain of cowpea UFLA03-84 and of other strains from soils of the Amazon region as Bradyrhizobium viridifuturi (symbiovar tropici). Braz J Microbiol 50(2):335–345. 10.1007/s42770-019-00045-x [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17.Chandrakala C, Voleti SR, Bandeppa S, Kumar NS, Latha PC (2019) Silicate solubilization and plant growth promoting potential of Rhizobium sp. isolated from rice rhizosphere. Silicon. 10.1007/s12633-019-0079-2 [Google Scholar]
- 18.Cheraghi M, Motesharezadeh B, Mousavi SM, Ma Q, Ahmadabadi Z (2023) Silicon (Si): a regulator nutrient for optimum growth of wheat under salinity and drought stresses—a review. J Plant Growth Regul 42:5354–5378. 10.1007/s00344-023-10959-47 [Google Scholar]
- 19.Dickson A, Leaf AL, Hosner JF (1960) Quality appraisal of white spruce and white pine seedling stock in nurseries. Chron 36:10–13 [Google Scholar]
- 20.Etesami H, Emami S, Alikhani HA (2017) Potassium solubilizing bacteria (KSB): mechanisms, promotion of plant growth, and future prospects—a review. J Soil Sci Plant Nutr 17(4):897–911. 10.4067/S0718-95162017000400005 [Google Scholar]
- 21.Ham BK, Chen J, Yan Y, Lucas WJ (2018) Insights into plant phosphate sensing and signaling. Curr Opin Biotechnol 49:1–9. 10.1016/j.copbio.2017.07.005 [DOI] [PubMed] [Google Scholar]
- 22.Hankin L, Anagnostakis SL (1975) The use of solid media for detection of enzyme production by fungi. Mycologia 67(3):597–605. 10.2307/3758395 [Google Scholar]
- 23.He Y, Pantigoso HA, Wu Z, Vivanco JM (2019) Co-inoculation of Bacillus sp. and Pseudomonas putida at different development stages acts as a biostimulant to promote growth, yield and nutrient uptake of tomato. J Appl Microbiol 127(1):196–207. 10.1111/jam.14273 [DOI] [PubMed] [Google Scholar]
- 24.IBGE – Instituto Brasileiro de Geografia e Estatística. Produção Agrícola Municipal (2022) https://www.cnpmf.embrapa.br/Base_de_Dados/index_pdf/dados/brasil/maracuja/b1_maracuja.pdf. Accessed 04 Jan 2024
- 25.Kästele X, Klüfers P, Koppn F, Schuhmacher J, Vogt M (2005) Silicon chelation in aqueous and nonaqueous media: the furanoidic diol approach. Chem Eur J 11(21):6326–6346. 10.1002/chem.200500147 [DOI] [PubMed] [Google Scholar]
- 26.Khan AL (2024) Silicon: a valuable soil element for improving plant growth and CO₂ sequestration. J Adv Res. 10.1016/j.jare.2024.05.027 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 27.Lacerda AM, Moreira FMS, Andrade MJB, Soares ALL (2004) Efeito de estirpes de rizóbio sobre a nodulação e produtividade do feijão caupi. Rev Ceres 51(293):67–82 [Google Scholar]
- 28.Lamichhane JR, Varvaro L (2013) A new medium for the detection of fluorescent pigment production by pseudomonads. Plant Pathol 62(3):624–632. 10.1111/j.1365-3059.2012.02670.x [Google Scholar]
- 29.Lee K-E, Adhikari A, Kang S-M, You Y-H, Joo G-J, Kim J-H, Kim S-J, Lee I-J (2019) Isolation and characterization of the high silicate and phosphate solubilizing novel strain Enterobacter ludwigii GAK2 that promotes growth in rice plants. Agron 9(3):144. 10.3390/agronomy9030144 [Google Scholar]
- 30.Leger RS, Joshi LE, Roberts DW (1992) Adaptation of proteases and carbohydrases of saprophytic, phytopathogenic and entomopathogenic fungi to the requirements of their ecological niches. Microbiology 143(6):1983–1992. 10.1099/00221287-143-6-1983 [DOI] [PubMed] [Google Scholar]
- 31.Linhares GAN (2019) Fontes de silício em mamoeiro e maracujazeiro: crescimento, fisiologia e indução de resistência. Tese Doutorado em Produção Vegetal. Universidade Estadual do Norte Fluminense Darcy Ribeiro. Campos dos Goytacazes – RJ
- 32.Ma R, Zhao W, Zhao Y, Wang Z, Zhu-Barker X, Wright AL, Jiang X (2020) Land use pattern effects after 30 years of shifting cropland to fallow land on soil ammonia-oxidizer community. Appl Soil Ecol 156:103707. 10.1016/j.apsoil.2020.103707 [Google Scholar]
- 33.Marinho RCN, Ferreira LVM, Silva AF, Martins LMV, Nóbrega RSA, Fernandes-Júnior PI (2017) Symbiotic and agronomic efficiency of new cowpea rhizobia from Brazilian semi-arid. Bragantia 76(2):273–281. 10.1590/1678-4499.003 [Google Scholar]
- 34.Marra LM, Oliveira SM, Soares CRFS, Moreira FMS (2011) Solubilisation of inorganic phosphates by inoculant strains from tropical legumes. Sci Agric 68(5):603–609. 10.1590/S0103-90162011000500015 [Google Scholar]
- 35.Marra ML, Soares CRFS, Oliveira SMO, Ferreira PAAF, Soares BL, Carvalho RF, Lima JM, Moreira FMS (2012) Biological nitrogen fixation and phosphate solubilization by bacteria isolated from tropical soils. Plant Soil 357:289–307 [Google Scholar]
- 36.Marra LM, Oliveira-Longatti SMD, Soares CRFS, Lima ML, Olivares FL, Moreira FMS (2015) Initial pH of medium affects organic acids production but does not affect phosphate solubilization. Braz J Microbiol 46(2):367–375. 10.1590/S1517-838246246220131102 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 37.Moreira FM, Cairo PA, Borges AL, Silva LD, Haddad F (2021) Investigating the ideal mixture of soil and organic compound with Bacillus sp. and Trichoderma asperellum inoculations for optimal growth and nutrient content of banana seedlings. S Afr J Bot 137:249–256. 10.1016/j.sajb.2020.10.021 [Google Scholar]
- 38.Moreira FM, Cairo PAR, Nascimento LR, Rosa RCCC, Rocha LS, Haddad F (2023) Optimal growth and N use efficiency enhancements by growth promoting rhizobacteria in seedlings banana under N2 deficiency. Biocatal Agric Biotechnol 50:102143. 10.1016/j.sajb.2020.10.021 [Google Scholar]
- 39.Nóbrega RSA, Moreira FMS, Siqueira JO, Lima AS (2004) Caracterização fenotípica e diversidade de bactérias promotoras de crescimento de plantas associativas isoladas de solos em reabilitação após a mineração de bauxita. Rev Bras Cienc Solo 28(2):269–279. 10.1590/S0100-06832004000200005 [Google Scholar]
- 40.Okura MH, Rende JC (2008) Microbiologia: roteiros de aulas práticas. 1st ed. Tecmedd
- 41.Oliveira EP, Soares PPS, Correia AJ, França RS, Miguel DL, Nóbrega RSA, Leal PL (2024) Humic substances and plant growth-promoting bacteria enhance corn (Zea mays L.) development. S Afr J Bot 166:539–549. 10.1016/j.sajb.2024.01.031 [Google Scholar]
- 42.Omer AM, Emara HM, Zaghloul RA, Monem MO, Dawwam GE (2016) Potential of Azotobacter salinestris as plant growth promoting rhizobacteria under saline stress conditions. Res J Pharm Biol Chem Sci 7:2572–2583 [Google Scholar]
- 43.Raturi G, Sharma Y, Rana V, Thakral V, Myaka B, Salvi P, Singh M, Dhar H, Deshmukh R (2021) Exploration of silicate solubilizing bacteria for sustainable agriculture and silicon biogeochemical cycle. Plant Physiol Biochem 166:827–838. 10.1016/j.plaphy.2021.06.039 [DOI] [PubMed] [Google Scholar]
- 44.Ribeiro LDS, Santos ARD, Souza LFDS, Souza JS (2010) Rochas silicáticas portadoras de potássio como fontes do nutriente para as plantas. Rev Bras Cienc Solo 34(3):891–897. 10.1590/S0100-06832010000300030 [Google Scholar]
- 45.Rocha LB, Costa EM, Ribeiro ACMS, Santos JFS, Miranda RS, Santos AS, Paula-Marinho SO, Fonseca BSF, Moreira FMS (2023) Brazilian semiarid Bradyrhizobium strains increase nitrogen accumulation and modulate physiological parameters to enable superior grain production in soybea genotypes. J Soil Sci Plant Nutr 23:2354–2359. 10.1007/s42729-023-01186-7 [Google Scholar]
- 46.Rodrigues GL, Matteoli FP, Gazara RK, Rodrigues PSL, Santos ST, Alves AF, Pedrosa-Silva F, Oliveira-Pinheiro I, Canedo-Alvarenga D, Olivares FL, Venancio TM (2022) Characterization of cellular, biochemical and genomic features of the diazotrophic plant growth-promoting bacterium Azospirillum sp. UENF-412522, a novel member of the Azospirillum genus. Microbiol Res 254:126896. 10.1016/j.micres.2021.126896 [DOI] [PubMed] [Google Scholar]
- 47.R Core Team (2023) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria [Google Scholar]
- 48.Sambrook J, Fritsch EF, Maniatis T (1989) Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor Laboratory Press
- 49.Setiawati TC, Mutmainnah L (2016) Solubilization of potassium containing mineral by microorganisms from sugarcane rhizosphere. Agric Sci Procedia 9:108–117. 10.1016/j.aaspro.2016.02.134 [Google Scholar]
- 50.Sethi D, Subudhi S, Rajput VD, Kusumavathi K, Sahoo TR, Dash S, Mangaraj S, Nayak DK, Pattanayak SK, Minkina T, Glinuschkin AP, Kalinitcenko VP (2021) Exploring the role of mycorrhizal and Rhizobium inoculation with organic and inorganic fertilizers on the nutrient uptake and growth of Acacia mangium saplings in acidic soil. Forests 12(12):2–15. 10.3390/f12121657 [Google Scholar]
- 51.Silva CFB, Brito TL, Taniguchi CAK, Lopes LA, Pinto GAS, Carvalho ACPP (2018) Growth-promoting potential of bacterial biomass in the banana micropropagated plants. Rev Bras Eng Agric Ambient 22(11):782–787. 10.1590/1807-1929/agriambi.v22n11p782-787 [Google Scholar]
- 52.Silva CS, Santos JMC, Silva JM, Tenório FA, Guedes-Celestino ELF, Cristo CCN, Nascimento MS, Montaldo YC, Oliveira JUL, Santos TMC (2019) Bioprospecting of endophytic bacteria (Bacillus spp.) from passionfruit (Passiflora edulis Sims f. flavicarpa) for plant growth promotion. Aust J Crop Sci 13(08):1369–1374. 10.21475/ajcs.19.13.08.p1837 [Google Scholar]
- 53.Silva JV, Longue LL, Jardim AS, Pinheiro APB, Rosa R, Pagoto ALR, Azeredo ALR, Dousseau S, Fernandes AA (2021) Eficiência nutricional na produção de mudas de maracujazeiro azedo em função das concentrações de fósforo em solução nutritiva. Rev Soc Desenvolv 10(4):1–14. 10.33448/rsd-v10i4.13988 [Google Scholar]
- 54.Soares ALL, Pereira JPAR, Ferreira PAA, Vale HMM, Lima AS, Andrade MJB, Moreira FMS (2006) Eficiência agronômica de rizóbios selecionados e diversidade de populações nativas nodulíferas em Perdões, MG: I caupi. Rev Bras Cienc Solo 30(5):795–802. 10.1590/S0100-06832006000500005 [Google Scholar]
- 55.Sousa JX (2017) Promoção do crescimento vegetal por bactérias diazotróficas no feijão-caupi. MSc dissertation, Universidade Federal do Recôncavo da Bahia, Cruz das Almas, BA, Brazil. Available at: https://sucupira.capes.gov.br/sucupira/public/consultas/coleta/trabalhoConclusao/viewTrabalhoConclusao.jsf?popup=true&id_trabalho=6134874. Accessed 15 Jun 2023
- 56.Sousa JX, Correia AJ, Dias AJC, Silva CC, Leal PL, Rocabado JMA, Morreira FMS, Nóbrega RSA (2022) The Bradyrhizobium uaiense strain UFLA 03-164T enhanced yield performance of cowpea in soils with low or high phosphorus content. Bioscience 38:1981–3163. 10.14393/BJ-v38n0a2022-54182 [Google Scholar]
- 57.Tedesco MJ, Volkweiss SJ, Bohnen H (1995) Análise de solo, plantas e outros materiais. 2nd ed. Universidade Federal do Rio Grande do Sul, Departamento de Solos, Porto Alegre, Brazil. (Boletim Técnico, 5)
- 58.Timofeeva AM, Galyamova MR, Sedykh SE (2024) Plant growth-promoting soil bacteria: nitrogen fixation, phosphate solubilization, siderophore production, and other biological activities. Plants 12(24):4074. 10.3390/plants12244074 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 59.Tombeur F, Cornelis JT, Lambers H (2021) Silicon mobilisation by root-released carboxylates. Trends Plant Sci 26(11):1116–1125. 10.1016/j.tplants.2021.07.003 [DOI] [PubMed] [Google Scholar]
- 60.Vasanthi N, Saleena LM, Raj SA (2016) Silica solubilization potential of certain bacterial species in the presence of different silicate minerals. Silicon 10:267–275. 10.1007/s12633-016-9438-4 [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
All data are provided in the manuscript.
Not applicable.




