Abstract
The study was aimed to evaluate the efficacy of supplying a mixture of four phosphorus (P)-solubilizing purple nonsulfur bacteria strains, Rhodopseudomonas palustris VNW64, VNS89, TLS06, and VNW02 (P-solubilizing purple nonsulfur bacteria (PS-PNSB)) on soil properties, P uptake, growth, and yield of canary melon (Cucumis melo L.). The experiment consisted of eight treatments, including 100% P (150 kg P2O5 ha−1) as recommended, 75% P, 50% P (75 kg P2O5 ha−1), and no fertilizers, and these treatments with adding PS-PNSB mixture. The results showed that supplying the PS-PNSB mixture had improved the soil pH and the available P content. Moreover, fertilizing 100% P with the mixture of the four PS-PNSB strains resulted in the greatest P uptake (7.88 kg P ha−1). However, interestingly, when supplying 75% P with the PS-PNSB mixture, the P uptake was 6.11 kg P ha−1 and was statistically equal to the 100% P treatment (5.87 kg P ha−1). This could be found in other parameters. Therefore, supplying the PS-PNSB mixture can be claimed to reduce 25% P, but still maintain plant height, fruit length, fruit perimeter, and yield of canary. In addition, supplying the PS-PNSB mixture contributed to a 5.26–9.42% increase in the canary melon yield among P fertilizer rates. Based on the aforementioned results, the PS-PNSB mixture in the current study should be further commercialized and transferred for farmers’ use to enhance the yield of canary melons and reduce the rate of chemical fertilizers for the ultimate goal of sustainable agriculture.
Graphical abstract
1 Introduction
Canary melon (Cucumis melo L.) is known to be greatly nutritious with glucose, fructose, vitamins [1], and antioxidants, such as acid ascorbic, β-carotene, and polyphenol [2,3]. Nowadays, canary melon is popularly cultivated in high-tech farms [4] because of difficulties in field cultivation. Therein, fertilizers use efficiency is one of the main factors limiting nutrition uptake and leading to low yield and fruit quality [5,6]. Phosphorus (P) is a vital nutrient for the growth of crops and agricultural production, but most P exists in unavailable forms for plants [7], leading to P deficiency in plants. The P deficiency tremendously affects the growth and development of leaves, and the photosynthesis capacity of plants because of the lack of nutrients for plants to grow [8]. Soils without enough P also result in a decrease in the plant yield, affecting roughly 50% of the total productivity of global agriculture [9,10]. Thus, great volumes of chemical fertilizers have been used to achieve high yields [11]. However, this leads to greater production costs [12], environmental pollution, and greenhouse gas emissions [13,14]. Many approaches have been applied to increase P use efficiency, among which bacterial application is one of the potent methods to ameliorate soil fertility and promote the development of plants [15] due to the long duration of usage and environmentally friendly characteristics [16,17]. Among the P-solubilizing microbes, P-solubilizing purple nonsulfur bacteria (PS-PNSB) are greatly promising for agricultural applications because they can adapt to many adverse conditions, including high salinity, high acidity, and low nutrients [18,19,20,21,22]. Therefore, this is considered to be a sustainable approach to reduce P chemical fertilizers for plants [23]. The roles of these bacteria in increasing available P contents in different soil types have attracted significant interest [19,21,24,25,26]. Recently, some strains of this bacterial group have been defined to be capable of solubilizing P in acid sulfate soils, including Rhodopseudomonas palustris VNW64, VNS89, TLS06, and VNW02 [18,20]. Besides, these bacteria secrete plant growth hormones such as indole-3-acetic acid (IAA) and metabolites such as 5-aminolevulinic acid (ALA) [20,27] and exopolymeric substances (EPS) [28] to elevate plant growth [19,27,29]. Bacterial strains of R. palustris can survive well under both anaerobic and aerobic conditions [18,19,20,21,28], and this characteristic is similar to the condition in upland soils for canary melon cultivation. In the meantime, there is a lack of studies investigating the role of PS-PNSB in providing P nutrients for canary melon. At the same time, recently, on rice and sesame, mixtures of PNSB have shown greater performances than single applications of each PNSB strain [29,30]. Therefore, the current study was proposed to certify the efficiency of mixed P-solubilizing R. palustris in reducing the use of P chemical fertilizer and in improving soil fertility, and P uptake and performance of canary melon. The current study hypothesized that the PS-PNSB strains can improve soil P availability by solubilizing insoluble P in soil, thereby the growth and yield of canary melon can be enhanced.
2 Materials and methods
2.1 Experimental design
The experiment was carried out in the greenhouse from March to May 2021. (Each experimental plot was 5 m2 in width.) There were eight treatments (three replications): (i) fertilized with 100% P (150 kg P2O5 ha−1), (ii) fertilized with 75% P (112.5 kg P2O5 ha−1), (iii) fertilized with 50% P (75 kg P2O5 ha−1), (iv) fertilized with 100% P and supplied with a mixture of four PS-PNSB strains, (v) fertilized with 75% P and supplied with PS-PNSB, (vi) fertilized with 50% P and supplied with PS-PNSB, (vii) supplied with PS-PNSB only, and (viii) fertilized with no fertilizers and no PS-PNSB supplementation in completely randomized blocks. In addition, the characteristics of the alluvial soil used for cultivating canary melon are presented in Table 1.
Properties | Unit | Depth | |
---|---|---|---|
0–20 cm | 20–40 cm | ||
pHH2O | — | 4.45 ± 0.057 | 3.40 ± 0.375 |
pHKCl | — | 3.58 ± 0.163 | 2.85 ± 0.163 |
EC | mS cm−1 | 0.515 ± 0.064 | 0.445 ± 0.035 |
OM | % C | 5.44 ± 0.071 | 6.73 ± 0.212 |
Ntotal | % N | 0.158 ± 0.005 | 0.123 ± 0.015 |
|
mg
|
13.6 ± 0.14 | 9.16 ± 0.52 |
|
mg
|
6.59 ± 0.777 | 17.9 ± 0.544 |
Ptotal | % P2O5 | 0.064 ± 0.014 | 0.041 ± 0.000 |
Pavailable | mg P kg−1 | 36.0 ± 2.03 | 45.9 ± 0.860 |
Al–P | mg P kg−1 | 65.0 ± 2.46 | 19.0 ± 2.85 |
Fe–P | mg P kg−1 | 354.1 ± 7.18 | 219.2 ± 3.26 |
Ca–P | mg P kg−1 | 20.6 ± 0.97 | 24.6 ± 1.71 |
CEC | meq 100 g−1 | 12.2 ± 1.02 | 13.4 ± 0.00 |
Na+ | meq Na+ 100 g−1 | 0.341 ± 0.038 | 0.301 ± 0.057 |
K+ | meq K+ 100 g−1 | 0.471 ± 0.123 | 0.554 ± 0.018 |
Mg2+ | meq Mg2+ 100 g−1 | 1.65 ± 0.036 | 1.59 ± 0.379 |
Ca2+ | meq Ca2+ 100 g−1 | 1.47 ± 0.238 | 0.914 ± 0.068 |
The values that appeared were the mean of the four replications. EC – electrical conductivity; OM – organic matter; CEC – cation exchange capacity.
The P-solubilizing R. palustris VNW64, VNS89, TLS06, and VNW02 were isolated by Khuong et al. [18,20,27] with accession numbers of KY624606, KY624607, KY624609, and KY624605 according to the National Center for Biotechnology Information (NCBI). These strains have been studied on acid sulfate soils and have shown significant performance as a plant growth promoter and a bioremediator. The bacterial culture was conducted following the description of Khuong et al. [31]. Each bacterial strain was cultured separately in a basic isolation medium (BIM; pH 4.5) under microaerobic light conditions (a tungsten light bulb at 3,000 lux) for 48 h. The BIM was composed of 1.0 g (NH4)2SO4, 0.5 g K2HPO4, 0.2 g MgSO4, 2.0 g NaCl, 5.0 g NaHCO3, 1.5 g yeast extract, 1.5 g glycerol, and 0.03 g L-cysteine in 1 L of distilled water [32]. Subsequently, the culture solution was centrifuged at 6,000 rpm for 15 min for cells to be collected and rinsed twice with 0.1% peptone. Then, the bacterial suspension was adjusted to 108 cells mL−1. The solution used was the mixture of four equal volumes of the PS-PNSB strains.
The cultivar of canary melon used in the current study was the F1 variety by company. This is a local canary melon variety, which had filled, smooth, and crunchy flesh, with a 15–18% Brix index, a short vegetative stage, roughly 60–65 days, and grew well at 20–32°C.
Seeds of the canary melon after being submerged in warm water (ratio 1: 1) for 1 h were incubated for germination. These seeds (200 seeds) were divided into two portions: the 100 seeds were soaked in 100 mL of the mixture of the four R. palustris VNW64, VNS89, TLS06, and VNW02. Similarly, the other 100 seeds were put into 100 mL of sterilized distilled water, all of them were submerged for 1 h, and then sowed into a seed starter tray. When plants had one true leaf (10 days after sowing), they were treated with pesticides and planted into experimental plots. The mixture of the four PS-PNSB strains was supplied at 0 day after planting (DAP), 5 DAP, 25 DAP, and 40 DAP, with the population of bacteria of 1 × 108 CFU g−1 dry soil weight.
The fertilizer formula for canary melon was, according to the recommendation of the local government, 600 kg of organic fertilizers and 150 N–150 P2O5–150 K2O kg ha−1. In detail, fertilizers used in this study included NPK 16–16–8, KCl, and chicken manure containing 60% organic matter, 3% N, 2% P2O5, 2% K2O, and urea.
2.2 Surveyed parameters
2.2.1 Soil analysis
Chemical properties of soil were analyzed following the method of Sparks et al. [33]. The pHH2O and pHKCl were extracted with water at a ratio of 1 soil:5 water, and KCl 1.0 M at a ratio of 1 soil:5 KCl 1.0 M, respectively, and measured by a pH meter. The pH extract was used to measure the electrical conductivity (EC) by an EC meter. Total nitrogen (N) was calculated by soil being digested by a mixture of saturated H2SO4:CuSO4:Se (100:10:1) and determined by the Kjeldahl distilling method (UDK 129, Velp, Italy).
The soil total population of bacteria was found by a relatively counting method in the basic isolating medium under microaerobic conditions, following the method of Naoki et al. [34], adjusted according to Kantachote et al. [35]. In short, soil samples were diluted to 10−6, spread on a dish, and incubated in an anaerobic jar for 7 days. After incubation, the number of colonies on the dish was counted.
2.2.2 Plant samples analysis
Stem, leaf, and fruit samples were collected at harvest and dried up at 70°C for 72 h. The samples were analyzed following the method of Houba et al. [36]. The samples were ground through a 0.2 mm sieve. Subsequently, 0.3 g of sample (proceeding separately from each part of the plant) was digested by 3.3 mL of a mixture of 18 mL diluted water, 100 mL saturated H2SO4, and 6 g salicylic acid. The mixture was heated for 24 h, and 30% H2O2 (3–4 drops for each) was added until it turned clear. The digested solution was adjusted to a volume of 50 mL to determine the concentrations of P measured at the 880 nm wavelength by a spectrophotometer.
2.2.3 Dry biomass (kg plant−1)
All oven-dried stems, leaves, and fruits in 5 m2 were weighed and converted into t ha−1.
Total P uptake was equal to the sum of individual uptake [(dry biomass in stems, leaves × P content in stems, leaves) + (dry biomass in fruits × P content in fruits)].
2.2.4 Agronomic characteristics
Six plants in each plot were selected to determine their agronomic parameters at 38 DAP as described below. The average height of plants (cm): Measurement was conducted from the stem (on the two cotyledons) to the shoot apical meristem. Number of leaves on the main body (leaves plant−1): Counting was conducted from the first true leaf (the rough leaf) to the peak one (the leaf with a size bigger than 2 cm). Stem diameter (mm): Measurement was conducted at the position 2 cm to the ground by a caliper. Fruit leaf position (leaf): Counting was conducted from the first true leaf to the fruit-bearing leaf. Canary melon was harvested at 64 DAP and six fruits in each plot were randomly collected (the first and the last fruit in each plot were not selected) to be analyzed and recorded for parameters of yield components, yield, fruit quality factors, and nutrition components.
2.2.5 Yield components
Fruit length (cm): The length from both ends of a fruit was measured by a ruler. Fruit perimeter (cm): The measurement began at the fruit’s middle with a tape measure. Average fruit weight−1 (kg fruit−1): All of the fruits in a plot were weighed and the weight was converted to a mean of a fruit.
2.2.6 Actual yield (t ha−1)
The weight of all of the fruits in each plot was used to calculate yield t ha−1.
Fruit quality: Stiffness: a knife was used to cut out a 1 cm thick flesh at both ends and the middle of a fruit. The flesh was then measured for its stiffness by the Fruit Penetrometer FT327 (QA Supplies LLC, USA). Color: Indexes of L*, a*, and b* were determined at both ends and the middle of a fruit by a colorimeter (Colorimeter CR-200, Colorimetry Research, Inc., USA). Thickness of fruit peel: A canary melon was cut vertically, and its peel thickness was averagely measured at both ends and the fruit’s middle by a caliper. To be more specific, at both ends of a fruit, measurement took place at 2 cm from the top and the bottom of it. Thickness of fruit flesh: The measurement was similar to that for the peel thickness.
2.3 Statistical analysis
The data demonstrated in this study were means of the three replications. They were subjected to variance analysis by SPSS, version 13.0, and compared by Duncan’s post hoc test at a 5% significance level. The correlation between the population of bacteria of PS-PNSB and available P content, Al–P, Fe–P, Ca–P, total P uptake, and yield was conducted. Correlations between available P content and concentrations of insoluble P compounds, P uptake, and yield were analyzed by Pearson correlation coefficient (R 2). The correlation coefficient r in a range between −1 and +1 showed the linearity between the two variants and 0 showed no correlation between them. The correlation coefficients +0.8, +0.5, and +0.1 represented highly, moderately, and lowly positive correlation, while those at −0.8, −0.5, and −0.1 indicated negative correlation at high, moderate, and low, respectively [39]. The calibration and standard curves built in the current study were based on measurements of a suitable substrate and calculated by the Excel 2016 software.
3 Results
3.1 Supplying the PS-PNSB R. palustris changed alluvial soil properties and characteristics of canary melon
3.1.1 Properties of alluvial soil for canary melon cultivation
pHH2O values differed at 5% significance between treatments, i.e., the treatments with the bacteria had greater pHH2O than ones without bacteria, at the same P fertilizer level. In detail, in the cases with P fertilizer plus the supplementation of the four PS-PNSB strains, the pHH2O value was 4.94 on average and greater than in the case fertilized with only P fertilizer. In the treatments supplied with the mixture of the four PS-PNSB strains, pHH2O reached 4.97, greater than the treatments without bacteria supplied, in the case without chemical fertilizers. In addition, EC among treatments fluctuated roughly 0.533–1.68 ms cm−1, i.e., the treatments supplied with or without bacteria at the same P fertilizer level had identical values of EC at the depth of 0–20 cm (Table 2).
Treatments | pHH2O | pHKCl | EC | Ntotal |
|
|
Ptotal | Pavailable | Al–P | Fe–P | Ca–P | CEC | K+ | Na+ | Ca2+ | Mg2+ | Log PNSB |
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
mS cm−1 | % | mg kg−1 | % | mg kg−1 | meq 100 g−1 | MPN g−1 DSW | |||||||||||
100% P | 4.40 cd | 4.06 | 1.68a | 0.182 | 19.9c | 165.9a | 0.088 | 108.2b | 81.7a | 552.2a | 106.6a | 13.7 | 0.493bc | 0.287a | 8.13b | 2.77 | 1.52b |
75% P | 4.20d | 4.28 | 1.56ab | 0.163 | 19.8c | 167.0a | 0.087 | 104.2b | 78.9a | 445.5b | 81.2b | 13.7 | 0.408c | 0.277a | 7.94bc | 2.96 | 1.42b |
50% P | 4.55c | 4.18 | 1.33bc | 0.163 | 20.5c | 158.1a | 0.078 | 80.6c | 75.7a | 349.3c | 65.1c | 13.9 | 0.499bc | 0.182b | 8.06b | 2.55 | 1.50b |
100% P + PS-PNSB | 5.11a | 4.28 | 1.55ab | 0.165 | 22.9b | 163.2a | 0.084 | 150.1a | 62.1b | 328.3 cd | 62.5c | 13.4 | 0.670a | 0.080c | 7.01d | 2.63 | 4.83a |
75% P + PS-PNSB | 4.86ab | 4.20 | 1.43ab | 0.168 | 23.6b | 165.3a | 0.087 | 135.1a | 60.5b | 324.3 cd | 54.0d | 13.8 | 0.585ab | 0.082c | 7.11d | 2.82 | 4.78a |
50% P + PS-PNSB | 4.86ab | 4.25 | 1.10c | 0.166 | 25.8a | 158.9a | 0.080 | 109.4b | 61.4b | 322.0 cd | 49.4de | 13.6 | 0.522b | 0.087c | 6.97d | 2.38 | 4.76a |
0% P + PS-PNSB | 4.97a | 4.58 | 0.53d | 0.165 | 16.8d | 25.6b | 0.079 | 79.6c | 41.5c | 283.3e | 37.9 f | 13.5 | 0.257d | 0.093c | 7.59c | 2.78 | 4.72a |
0% P | 4.67bc | 4.44 | 0.68d | 0.161 | 10.7e | 22.9b | 0.074 | 60.7d | 55.7b | 315.0d | 47.1e | 13.8 | 0.166d | 0.172b | 8.78a | 2.89 | 1.44b |
P | * | ns | * | ns | * | * | ns | * | * | * | * | ns | * | * | * | ns | * |
CV (%) | 3.15 | 4.48 | 13.8 | 6.74 | 5.66 | 9.82 | 7.51 | 8.49 | 5.27 | 4.11 | 5.76 | 5.11 | 12.2 | 8.64 | 3.02 | 17.8 | 3.04 |
In the same column, data followed by the same letter were not different at 5% significance, according to Duncan’s test. * different at 5% significance; ns – no significance; PS-PNSB – the mixture of the four P-solubilizing R. palustris VNW64, VNS89, TLS06, and VNW02; N – Nitrogen; P – phosphorus; EC – electrical conductivity; CEC – cation exchange capacity.
Values of pHKCl, total N content, total P content, CEC, and Mg2+ content were insignificantly different between treatments at the depth of 0–20 cm (Table 2).
Concentrations of
Results presented in Table 2 indicated that concentrations of available P, Al–P, Fe–P, and Ca–P were different at 5% significance between treatments. The treatments supplied with the four PS-PNSB strains possessed an available P concentration of 79.6 mg P kg−1, greater than in the treatment without either chemical fertilizers or bacteria. In the cases with P fertilizers, available P amounts were lower than those in the treatments additionally supplied with the four PS-PNSB strains at the same P fertilizers level (Table 2). For insoluble P forms content, in the treatment supplied with the four PS-PNSB strains, concentrations of Al–P, Fe–P, and Ca–P were lower than those in the treatment without bacteria when no chemical fertilizers were applied. Along with an order of 100, 75, and 50% P, Al–P concentration in the cases with only P fertilizer were 81.7, 78.9, and 75.7 mg P kg−1 and greater than 62.1, 60.5, and 61.4 mg P kg−1, respectively, in the treatments added with the four PS-PNSB strains. Fe–P and Ca–P concentrations also shared the same trend (Table 2).
Table 2 shows that concentrations of K+, Na+, and Ca2+ between treatments differed at 5% significance. To be more specific, K+ concentration in the cases with only P fertilizer was an average of 0.467 meq K+ 100 g−1, while in the cases with both P fertilizer and the four PS-PNSB strains, its mean was 0.592 meq K+ 100 g−1. Na+ and Ca2+ concentrations in the cases with 100, 75, and 50% P were 0.249 meq Na+ 100 g−1 and 8.04 meq Ca2+ 100 g−1 on average and greater than those in the cases with both factors (0.083 meq Na+ 100 g−1 and 7.03 meq Ca2+ 100 g−1), respectively. Similarly, in the case with no P fertilizer applied, the treatment supplied with the four PS-PNSB strains had lower concentrations of Na+ and Ca2+ than those in the treatment without bacteria (Table 2). In addition, at the depth of 20–40 cm, the chemical properties of soil were also investigated (see Table S1 in the Supplementary Material).
The total population of bacteria was different between treatments (P < 0.05). Particularly, at 100%, 75% and 50% P, the treatments with the four PS-PNSB strains resulted in bacterial densities at 4.83, 4.78 and 4.76 MPN g−1 dry soil weight (DSW), which were greater than 1.52, 1.42 and 1.50 MPN g−1 DSW, respectively. Simultaneously, the population of bacteria in the case with the four PS-PNSB strains was greater than in the cases without either bacteria or P fertilizer levels (Table 2).
3.1.2 P uptake in canary melon in alluvial soil
P concentration in stems, leaves, and fruits was different at 5% significance between treatments. P concentration in the case with 100 and 75% was an average of 0.239 in stems and leaves, and 0.218in fruits, greater than in the case with 50% P, whose results were 0.197 and 0.160%, respectively. In the cases with P fertilizers combined with supplying the four PS-PNSB strains, P concentrations in stems, leaves, and fruits were correspondingly 0.310 > 0.261 > 0.230% and 0.258 > 0.223 > 0.186% according to 100% > 75% > 50% P. In addition, P concentrations in stems, leaves, and fruits in the treatment supplied with only the four PS-PNSB strains were greater than those in the treatment without either bacteria or chemical fertilizers, and identical to those in the case with 50% P (Table 3).
Treatments | P concentration (%) | Dry biomass (kg ha−1) | P uptake (kg ha−1) | Total P uptake (kg ha−1) | |||
---|---|---|---|---|---|---|---|
Stems, leaves | Fruits | Stems, leaves | Fruits | Stems, leaves | Fruits | ||
100% P | 0.246bc | 0.221b | 795.9b | 1771.5b | 1.96c | 3.91b | 5.87b |
75% P | 0.232c | 0.214b | 723.8c | 1582.8c | 1.68d | 3.39c | 5.06c |
50% P | 0.197d | 0.160d | 621.7d | 1425.9d | 1.23e | 2.28e | 3.51e |
100% P + PS-PNSB | 0.310a | 0.258a | 941.4a | 1923.8a | 2.92a | 4.96a | 7.88a |
75% P + PS-PNSB | 0.261b | 0.223b | 834.1b | 1760.6b | 2.18b | 3.93b | 6.11b |
50% P + PS-PNSB | 0.230c | 0.186c | 739.1c | 1535.4c | 1.70d | 2.86d | 4.55d |
0% P + PS-PNSB | 0.196d | 0.162d | 580.7d | 1421.3d | 1.14e | 2.30e | 3.44e |
0% P | 0.164e | 0.127e | 479.8e | 1235.0e | 0.78 f | 1.57 f | 2.36 f |
P | * | * | * | * | * | * | * |
CV (%) | 5.78 | 3.68 | 3.42 | 3.15 | 4.93 | 4.81 | 3.13 |
In the same column, data followed by the same letter were not different at 5% significance, according to Duncan’s test. * different at 5% significance; PS-PNSB – the mixture of the four P-solubilizing R. palustris VNW64, VNS89, TLS06, and VNW02; P – phosphorus.
Dry stems, leaves, and fruits biomass in canary melon between treatments changed at 5% significance. The case with 100% P plus supplied with the four PS-PNSB strains achieved the greatest dry biomass in stems, leaves, and fruits, which were 941.4 and 1923.8 kg ha−1, while the lowest results were 479.8 and 1235.0 kg ha−1, respectively, in the treatment without either bacteria or chemical fertilizers. Dry biomass in stems, leaves, and fruits in the treatment supplied with the four PS-PNSB strains were greater than in the case with no fertilization from both factors. Between the treatments fertilized with P fertilizer with and without supplying bacteria, dry biomass in stems, leaves, and fruits was different at 5% significance. To be more specific, dry biomass valued at 795.9 > 723.8 > 621.7 > 479.8 kg ha−1 in stems and leaves, and 1771.5 > 1582.8 > 1425.9 > 1235.0 kg ha−1 in fruits, corresponding to 100–75–50–0% P. Likewise, when combined with the four PS-PNSB strains, dry biomass in stems, leaves and fruits were 941.4 > 834.1 > 739.1 > 580.7 kg ha−1, respectively, and those in fruits were 1923.8 > 1760.6 > 1535.4 > 1421.3 kg ha−1, respectively, according to a decreasing levels of P fertilizer (Table 3).
P uptake in stems, leaves, and fruits, and their total uptake between treatments varied at 5% significance. For P uptake in stems and leaves, in the cases with P fertilizer combined with the four PS-PNSB strains, the result was greater than in the cases with only P fertilizer at the same fertilizer level. For P uptake in fruits, in the cases with only P fertilizer, they were between 2.28 and 3.91 kg P ha−1, while in the cases with the combination of P fertilizer and the four PS-PNSB strains, where they fluctuated between 2.86 and 4.96 kg P ha−1. When supplied with only the four PS-PNSB strains, P uptake in stems, leaves, and fruits, and their total were greater than those in the case without both factors. On the other hand, the treatments fertilized with 100, 75, and 50% P and supplied with the four PS-PNSB resulted in greater total P uptake, versus the treatments fertilized with only P fertilizer at the same fertilizer level. In particular, total P uptake in the treatment supplied with the four PS-PNSB was identical to that in the case with 50% P. The treatment with 75% P combined with the four PS-PNSB was statistically equal to the one with 100% P in the P uptake in fruit and in the total P uptake (Table 3).
3.1.3 Growth and yield of canary melon in alluvial soil
3.1.3.1 Canary melon growth
Canary melon plant height between treatments changed significantly at 5%. When no chemical fertilizers were applied, the treatment supplied with the four PS-PNSB strains had plants that were taller than those in the treatment without bacteria. However, between the treatments fertilized with 100, 75, and 50% P plus supplied with either no bacteria or the four PS-PNSB strains, the plant height was identical to each other and was 256.5 cm on average (Table 4).
Treatments | Plant height (cm) | Stem diameter (mm) | Leaves number (leaves plant−1) | Fruit leaf position (leaves) |
---|---|---|---|---|
100% P | 262.3ab | 9.26a | 33.4a | 13.9 |
75% P | 252.6ab | 8.87b | 32.9a | 14.2 |
50% P | 243.7ab | 8.62b | 31.5b | 13.3 |
100% P + PS-PNSB | 268.9a | 9.35a | 33.8a | 13.4 |
75% P + PS-PNSB | 258.4ab | 9.29a | 33.2a | 13.8 |
50% P + PS-PNSB | 253.1ab | 9.25a | 32.7ab | 13.5 |
0% P + PS-PNSB | 240.0b | 8.63b | 30.2c | 13.9 |
0% P | 205.6c | 7.26c | 27.5d | 13.6 |
P | * | * | * | ns |
CV (%) | 5.42 | 2.30 | 2.27 | 13.8 |
In the same column, data followed by the same letter were not different at 5% significance, according to Duncan’s test. * different at 5% significance; ns – no significance; PS-PNSB – the mixture of the four P-solubilizing R. palustris VNW64, VNS89, TLS06, and VNW02; P – Phosphorus.
Stem diameter between the treatments was different significantly at 5%. In detail, stem diameter values in the cases with 100, 75, and 50% P were 9.26 > 8.87 ∼ 8.62 mm, respectively. The treatments fertilized with 100, 75, and 50% P plus supplied with the four PS-PNSB strains had a stem diameter of 9.30 mm on average, which was wider than those in the treatments without bacteria, except for in the case of 100% P. In addition, when supplied with the four PS-PNSB strains, the stem became wider than that in the treatment without bacteria, when there were no chemical fertilizers (Table 4).
The number of leaves between treatments varied at 5% significance. To be more specific, the number of leaves in the treatment supplied with the four PS-PNSB strains was greater than in the case without bacteria when chemical fertilizers were not applied. The number of leaves in the cases with 100, 75, and 50% P with the supplementation of the four PS-PNSB strains reached 33.2 leaves plant−1 on average, and were identical to the treatments at the same P fertilizer level but no bacteria applied (Table 4).
Fruit leaf positions were not significantly different between the treatments fertilized with P fertilizer level plus supplied with either the four PS-PNSB stains or no bacteria, and it was 13.7 on average (Table 4).
3.1.3.2 Yield components of canary melon
Fruit length was different at 5% significance between treatments. In detail, the fruit length was identical to each other between the treatments fertilized with P fertilizer level plus supplied with the four PS-PNSB strains and the treatments fertilized with only P fertilizer (Table 5). However, fruits in the treatment with 100% P with PS-PNSB strains were longer than those in the treatment with only 100% P at 5% significance.
Treatments | Fruit length (cm) | Fruit perimeter (cm) | Fruit weight (G) |
---|---|---|---|
100% P | 12.7bc | 42.5bc | 1120.0b |
75% P | 13.0abc | 41.7cd | 1064.0c |
50% P | 12.8abc | 40.6de | 1004.3d |
100% P + PS-PNSB | 13.9a | 43.8a | 1208.3a |
75% P + PS-PNSB | 13.7ab | 42.9ab | 1125.0b |
50% P + PS-PNSB | 13.8a | 41.6cd | 1062.7c |
0% P + PS-PNSB | 13.2abc | 40.4e | 1058.0c |
0% P | 12.2c | 38.2f | 912.0e |
P | * | * | * |
CV (%) | 4.21 | 1.53 | 2.96 |
In the same column, data followed by the same letter were not different at 5% significance, according to Duncan’s test. * different at 5% significance; PS-PNSB – the mixture of the four P-solubilizing R. palustris VNW64, VNS89, TLS06, and VNW02; P – Phosphorus.
Table 5 shows that the fruit perimeter between treatments changed at 5% significance. In the cases with 100 and 75% P added with the four PS-PNSB strains, fruit perimeters were bigger than those in the cases with only P fertilizer at the same P fertilizer level. Furthermore, the treatment supplied with the four PS-PNSB had a fruit perimeter that was bigger than in the case with no bacteria and no chemical fertilizer, and equal to that in the case with 50% P.
Average fruit weight was, as the greatest result, 1208.3 g in the case with 100% P supplied with the four PS-PNSB, and the lowest one was 912.0 g in the treatment without bacteria and chemical fertilizers. A decreasing amount of P fertilizer used led to a reduction in the fruit weight. In particular, in the treatments fertilized with 100, 75, and 50% P, fruit weight was 1120.0 > 1064.0 > 1004.3 g, respectively, lighter than those in the cases with the same chemical fertilizer rate combined with the four PS-PNSB strains, which were valued at 1208.3 > 1125.0 > 1062.7 g, respectively. In the treatment supplied with the four PS-PNSB strains, the fruit weight was identical to that in the case with 50% P and heavier than that in the treatment without neither bacteria nor chemical fertilizers (1058.0 g–1062.7 g > 912.0 g, respectively; Table 5).
3.1.3.3 Canary melon yield
Canary melon fruit yield between treatments differed by 5% significance. When fertilizing with 100, 75, and 50% P, the fruit yield was 17.10 > 16.10 > 15.17 t ha−1, respectively, while that in the cases with 100, 75, and 50% P plus supplied with the four PS-PNSB stains reached 18.00 > 17.27 > 16.33 t ha−1, respectively. Moreover, in the case with 75% P plus supplied with the four PS-PNSB strains, the fruit yield was identical to that in the case with 100% P. Especially in the treatment supplied with the four PS-PNSB strains, the result was 15.10 t ha−1, identical to the yield of the case with 50% P, 15.17 t ha−1 and greater than 3.80 t ha−1 in the treatment without neither bacteria nor chemical fertilizers (Figure 1).
3.2 The P-solubilizing Rhodopseudomonas palustris interacted with available P content and concentrations of Al–P, Fe–P, and Ca–P, total P uptake, yield, and stiffness of canary melon
There was a low correlation between the population of bacteria and the available P content, with a correlation coefficient (r) of 0.3370 (Figure 2a), and a high correlation between the population of bacteria and the concentrations of Al–P, Fe–P, and Ca–P, with correlation coefficients of 0.6345, 0.5886, and 0.5669, respectively (Figure 2b–d). Simultaneously, correlations between the population of bacteria and the total P uptake, yield, and hardness of canary melon flesh were also found with correlation coefficients at 0.4041 (Figure 3a), 0.4373 (Figure 3b), and 0.6444, respectively (Figure 4).
There were correlations between available P content and the concentrations of Al–P, Fe–P, and Ca–P, with correlation coefficients at 0.1480, 0.1175, and 0.2347, respectively (Figure 5a–c). Moreover, a correlation coefficient was 0.9353 between the available P content and the total P uptake (Figure 6a) and 0.8951 between the available P content and the canary melon fruit yield (Figure 6b).
The population of bacteria and the available P density, the total P uptake, and the canary melon fruit yield were proportionally correlated. In detail, supplying the four PS-PNSB strains took part in increasing the population of bacteria in soil, leading to greater available P content, total P uptake, and yield (Figures 2a and 3a and and 6b).
3.3 Supplying the PS-PNSB Rhodopseudomonas palustris changed the fruit quality of canary melon in alluvial soil
Fruit hardness, indexes of L*, a*, and b*, Brix, and storage duration of canary melon between treatments were different significantly at 5%. In particular, when there were no chemical fertilizers, the treatment supplied with the four PS-PNSB had a fruit stiffness that was greater than that in the treatment without bacteria. L* index in the cases with only P fertilizer was 69.63 on average, lower than those in the cases with both P fertilizer and the four PS-PNSB strains at the same P fertilizer level (averagely 73.0). The treatment supplied with the four PS-PNSB strains had a greater L* index than that in the treatment without bacteria under no chemical fertilizer. In addition, the a* index peaked at 24.9 in the case with 100% P plus supplied with the four PS-PNSB strains and bottomed at 21.1 in the treatment without bacteria in the condition of no chemical fertilizers. The average b* index in the cases with only P fertilizer was 73.5, greater than 72.1 in the cases with both P fertilizer and the four PS-PNSB strains (Table 6). Furthermore, the Brix index of canary melon in the treatments combined with the supplementation of the four PS-PNSB was 15.9% on average, greater than that in the cases without bacteria (14.6%; Table 6). The storage duration of canary melon in the treatment supplied with the four PS-PNSB strains was 20.2 days, longer than 12.0 days in the treatment without either bacteria or P fertilizer. The treatments fertilized with P fertilizer and the four PS-PNSB strains had a storage time of approximately 23.8 days, longer than those in the cases with only P fertilizer at the same P fertilizer level (17.4 days; Table 6). The thickness of peel and flesh, and concentrations of nitrate, vitamin C, and total acid did not differ significantly between treatments and resulted at 0.254 cm, 2.46 cm, 5.34 mg
Treatments | Stiffness (kg cm−2) | Peel color | Peel thickness (cm) | Flesh thickness (cm) |
|
Vitamin C (mg 100 g−1) | Brix (%) | Total acid (%) | Storage duration (days) | ||
---|---|---|---|---|---|---|---|---|---|---|---|
L* | a* | b* | |||||||||
100% P | 1465.8c | 69.3b | 23.3c | 73.2b | 0.233 | 2.55 | 5.59 | 20.6 | 14.6b | 0.233 | 17.5d |
75% P | 1588.3bc | 69.5b | 23.2c | 73.3b | 0.278 | 2.34 | 5.23 | 20.3 | 14.5b | 0.287 | 17.3d |
50% P | 1724.6a | 70.1b | 20.6d | 73.9b | 0.289 | 2.53 | 5.41 | 20.4 | 14.8b | 0.253 | 17.3d |
100% P + PS-PNSB | 1748.3a | 72.8a | 24.9a | 72.2c | 0.267 | 2.27 | 5.23 | 21.0 | 16.0a | 0.280 | 24.7a |
75% P + PS-PNSB | 1757.1a | 73.4a | 23.8bc | 72.2c | 0.233 | 2.45 | 5.05 | 20.3 | 16.2a | 0.235 | 24.0ab |
50% P + PS-PNSB | 1705.8ab | 72.8a | 24.4ab | 72.0c | 0.222 | 2.63 | 5.59 | 20.8 | 15.6a | 0.240 | 22.7b |
0% P + PS-PNSB | 1694.2ab | 72.7a | 24.5ab | 73.4b | 0.244 | 2.48 | 5.04 | 20.4 | 15.9a | 0.290 | 20.2c |
0% P | 1493.3c | 69.2b | 21.1d | 75.2a | 0.267 | 2.41 | 5.59 | 20.4 | 14.4b | 0.230 | 12.0e |
P | * | * | * | * | ns | ns | ns | ns | * | ns | * |
CV (%) | 4.10 | 0.92 | 2.39 | 0.74 | 21.5 | 7.39 | 12.5 | 3.92 | 2.44 | 12.4 | 4.71 |
In the same column, data followed by the same letter were not different at 5% significance, according to Duncan’s test. * different at 5% significance; ns – no significance; PS-PNSB – the mixture of the four P-solubilizing R. palustris VNW64, VNS89, TLS06, and VNW02; P – Phosphorus.
4 Discussion
pHH2O value in the cases with both P fertilizer levels and the four PS-PNSB strains were greater than those in the treatments without bacteria supplied (Table 2). With neither bacteria nor chemical fertilizers, the pHH2O value was 4.67 (Table 2). This result was in accordance with previous studies where PNSB has been claimed to be able to improve soil pH [20,27]. R. palustris has contributed to the increasing pH in salt-affected acid sulfate soil and saline soil, and concentrations of
Supplying the four PS-PNSB did solubilize insoluble forms of P to available forms to provide them for plants (Table 2). According to the study by Rezakhani et al. [47], P-solubilizing bacteria can solubilize P compounds, leading to enhancements in available P and P uptake. The result also revealed that reducing the amount of P fertilizer led to a decline in P concentration and P uptake in canary melon (Table 3). P concentration in stems and leaves in the treatments supplied with the four PS-PNSB strains were greater than those in the treatments without bacteria (Table 3). Therefore, supplying the four PS-PNSB strains participated in improving biomass in dry stems, leaves, and fruits of canary melon. This proved that the PS-PNSB strains were efficient in increasing P uptake via the dominance of results in the cases with both P fertilizer and the four PS-PNSB to those in the cases with P fertilizer at the same level but no bacteria applied (Table 3). The population of bacteria in the treatments supplied with the four PS-PNSB strains helped to increase P uptake in canary melon, leading to greater total P uptake than that in the treatments without bacteria applied, and there was a correlation between the population of bacteria and the total P uptake, with a correlation coefficient at 0.4041 (Figure 3a). As reported by Wu et al. [7], supplying Bacillus aryabhattai JX285 and Pseudomonas auricularis HN038 has ameliorated concentrations of N and P in leaves, and positively affected the availability of N, P, and K in soil for Camellia oleifera Abel. According to Song et al. [48], supplying Azotobacter chroococcum bacteria has promoted nutrient uptake in plants, leading to an increase in P concentration and grain yield of maize, versus those in the control treatment. Khuong et al. [15] have also indicated that supplying R. palustris bacteria enhances P accumulated in rice plants. Therefore, supplying R. palustris boosted P content in stems and leaves of canary melon (Table 3). Simultaneously, supplying the P-solubilizing R. palustris resulted in greater P uptake in canary melon (Table 3).
Reducing the amount of P fertilizer from 100 to 75% P had not affected plant height and the number of leaves of canary melons yet, but fertilizing 50% P noted lower leaf numbers than fertilizing with 100% P (Table 4). This result was in accordance with the study by Dimkpa et al. [49], in which greater P concentration did not improve plant growth. However, stem diameter at fertilizer levels of 75 and 50% P was smaller than that in the case with 100% P (Table 4). In the cases with only P fertilizer, plant height did not change (Table 4). This was consistent with the study by Zhao et al. [50], in which biofertilizers containing R. palustris and B. subtilis did not affect rice growth significantly, but noticeably ameliorated rice yield by 9.84–17.7%.
The treatments fertilized with P fertilizer levels plus supplied with the four PS-PNSB strains took part in increasing fruit perimeter (Table 5). Therefore, the fruit weight in the treatments additionally supplied with the four PS-PNSB strains was greater than those in the cases with only P fertilizers (Table 5). According to Wang et al. [23], supplying R. palutris and B. cepacia ISOP5 enhance the grain yield of peanuts by 8.1–19.5% after a 5-year application. The result also proved that reducing 25% P plus supplied with the four PS-PNSB still ensured the growth and the yield of canary melon identical to in the case with 100% P, because PS-PNSB were able to solubilize P and produce growth-stimulating substances supporting canary melon development (Table 4). A fruit weight in the treatments supplied with the four PS-PNSB strains was heavier, because a greater population of bacteria led to greater P uptake in fruit, so the fruit yield was also greater. As can be seen, between the fruit yield and the population of bacteria, there was a correlation with a coefficient of 0.4373 (Figure 2b). Khuong et al. [15] have also pointed out that supplying R. palustris has contributed to the increasing growth and grain yield of rice by up to 10% in salt-affected acid sulfate soil and by 18% in saline soil.
Supplying the four PS-PNSB strains increased fruit flesh hardness, versus that in the cases without bacteria, and there was a strong correlation between the population of bacteria and fruit flesh hardness (Figure 4). The treatments fertilized with P fertilizer levels plus supplied with the four PS-PNSB possessed greater values of L* and a*, but lower b* value, versus those in the cases with only P fertilizer. From the lowest values to the greatest ones, the L* indices show the brightness of the current, while the a* and b* values represent for the variation between green to red and blue to yellow, respectively [51]. In other words, great L* means brighter color, and great a* means redder color. This showed that supplying the four PS-PNSB made fruit brighter and redder. The Brix index of a canary melon fruit tremendously increased in the cases with P fertilizers plus supplied with the four PS-PNSB strains compared with the treatments without bacteria (Table 6). This result was in accordance with a study by Seymen et al. [52], in which applying plant growth-promoting rhizosphere bacteria enhanced the fruit quality. Moreover, concentrations of nitrate, vitamin C, and total acid in the treatments additionally supplied with the four PS-PNSB strains remained unchanged and identical to those in the treatments without bacteria supplied (Table 6). Although storage duration was not in the objectives of this study, in the treatments supplied with the four PS-PNSB strains, storage duration was longer than in the case with only P fertilizer (Table 6). According to Su et al. [53] and Zhai et al. [54], R. palustris GJ-22 secrete two plant growth-promoting hormones, IAA and ALA, which stimulate growth and create pathogenic resistance in plants. This result showed that supplying the purple nonsulfur bacteria improved fruit stiffness, color indexes of fruit, and Brix in canary melon fruit.
Such bacteria that can tolerate various environmental stresses, promote plant growth, and improve soil fertility have great potential for commercial application as a biofertilizer to replace the use of chemical fertilizers [55]. Recently, a study by Khuong et al. [56] used a liquid biofertilizer of PNSB to increase N and P availability and decrease Al3+ and Fe2+ toxicity in soil, which led to an improvement in rice growth and yield. Because of the mentioned traits of the current strains, their biofertilizer can be further commercialized and transferred for farmers’ use. However, a suitable carrier should be found for these bacteria along with checking quality, environmental, and procedure standards before commercialization [57]. Therefore, further research should be done to commercialize these PNSB strains in the current study.
5 Conclusions
Supplying the four P-solubilizing Rhodopseudomonas palustris VNW64, VNS89, TLS06, and VNW02 has remediated the soil fertility, including pH by 0.30–0.71, and available P content by 18.9–41.9 mg P kg−1 at the same P fertilizer rate. Moreover, it also improved the total P uptake and fruit yield of canary melon by 1.04–2.01 kg P ha−1 and 5.26–9.42%, respectively, as well. This result has proven that the PS-PNSB strain ameliorated the available P nutrient level in soils, which led to increases in the P uptake and the canary melon yield. Referring to the combination with chemical P fertilizers, the PS-PNSB strains have reduced the required amount of the P fertilizer. Supplying 75% P with the four PS-PNSB strains achieved an identical fruit yield to that in the case with 100% P. Moreover, supplying the four PS-PNSB strains was also beneficial in improving the storage duration of canary melon. The R. palustris VNW64, VNS89, TLS06, and VNW02 strains have shown their capability of providing P nutrients for plants, as well as improving the growth, yield, and fruit quality of the canary melon. These strains are promising in reducing the amount of chemical P fertilizer used, addressing the P deficiency in different soils around the world and applying it to crops that vitally demand P nutrients. Therefore, they should be investigated under field conditions and further transferred to the farmers to improve their income and to conserve the environment from the overuse of chemical fertilization.
Acknowledgments
The authors sincerely appreciate the Purple Nonsulfur Bacteria Laboratory and Cultivation Practices Laboratory (Faculty of Crop Science, College of Agriculture, Can Tho University), which provided equipment, chemicals, and materials for this study to be completed.
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Funding information: This research is funded by Vietnam National University Ho Chi Minh City (VNU-HCM) [C2023-16-08].
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Author contributions: L.N.T.X: conceptualization and writing – original draft; N.P.T.H: formal analysis, investigation, and writing – original draft; L.T.M.T: formal analysis, methodology, and validation; V.T.B.T.: investigation, supervision, and validation; L.M.T.: formal analysis, investigation, and writing – review & editing; L.T.Q.: investigation and writing – review & editing; N.T.X.D.: formal analysis, methodology, and validation; L.V.T: formal analysis, methodology, and validation; N.Q.K.: conceptualization and writing – review & editing.
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Conflict of interest: The authors state no conflict of interest.
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Supporting information: We added the data of soil characteristics at 20–40 cm depth. The data are presented in the supplementary file to this article.
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Data availability statement: The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
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