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Article

A Field Evaluation of Sodium Silicate and Bacillus subtilis on the Growth and Yield of Bananas following Fusarium Wilt Disease Infection

by
Md Aiman Takrim Zakaria
1,
Siti Zaharah Sakimin
1,2,*,
Mohd Razi Ismail
1,
Khairulmazmi Ahmad
3 and
Susilawati Kasim
4
1
Department of Crop Science, Faculty of Agriculture, Universiti Putra Malaysia, Serdang 43400, Selangor, Malaysia
2
Institute of Tropical Agriculture and Food Security (ITAFoS), Universiti Putra Malaysia, Serdang 43400, Selangor, Malaysia
3
Department of Plant Protection, Faculty of Agriculture, Universiti Putra Malaysia, Serdang 43400, Selangor, Malaysia
4
Department of Land Management, Faculty of Agriculture, Universiti Putra Malaysia, Serdang 43400, Selangor, Malaysia
*
Author to whom correspondence should be addressed.
Sustainability 2023, 15(4), 3141; https://doi.org/10.3390/su15043141
Submission received: 14 June 2022 / Revised: 3 August 2022 / Accepted: 4 August 2022 / Published: 9 February 2023
(This article belongs to the Special Issue Integration of Sustainable Agriculture Approaches for Food Security under Climate Change II)
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Abstract

:
A field investigation was conducted in a Fusarium-infected area to evaluate the effectiveness of silicate compounds with antagonist bacteria on morpho-physiological growth performance in bananas. The roots of banana plants were treated by drenching the soil with four different treatments: control (without any treatment), CBZ (Carbendazim fungicide alone), SS + BS (integration sodium silicate with Bacillus subtilis), and CBZ + SS + BS (integration CBZ, SS, and BS). All treatments were arranged in a randomized complete block design with four replications. The results confirm that plant height, pseudo-stem diameter, and canopy diameter markedly increased from weeks 2 to 10 after transplantation. Amendment with these elements induced a higher total chlorophyll content, which contributed to the increased rate of leaf gas exchange and biochemical changes for controlling Fusarium wilt disease infection. From these findings, the CBZ + SS + BS application in the farm had significantly reduced disease incidence by 16.07% and disease severity by 14.28%. The same treatment achieved the greatest disease reduction by 63.05%. Therefore, the integration between CBZ + SS + BS had good significant effects in controlling Fusarium wilt disease and enhanced the morpho-physiological growth performance with an average yield production of about 24.72 kg per fruit bunch.

1. Introduction

One of the most serious, negative environmental issues is increasing antibiotic resistance, which makes it important to find new biomolecules with a broad range of antibiotic actions [1]. Fusarium wilt disease is one of the major constraints of plant growth. It causes a high post-transplanting mortality rate and seriously affects banana production, which is the staple diet for more than 400 million people globally [2,3]. At present, over 100,000 acres of banana plantations around the world are seriously infected by Fusarium wilt disease, and the total loss to farmers is around USD 2 billion [4,5]. In Malaysia, bananas are grown from the north to the south of the country for both economic and nutritional reasons [6]. According to [7], the causative agent of Fusarium wilt disease is Fusarium oxysporum f. sp. cubense (FOC). Nowadays, tropical Race 4 (FOC-TR4) has spread considerably in the Eastern hemisphere due to climate change and climatic variability [8,9,10].
The use of fungicides in banana plantations can improve plant resistance to FOC, but the long-term overuse of pesticides might have negative consequences for the environment. Thus, in situ biological control approaches are a good, sustainable alternative for controlling Fusarium wilt disease. [11]. According to [12], Bacillus strains work effectively against Fusarium wilt disease and can bind together on a silicon (Si)-rich surface without forming cell clusters, and elements of Si also serve as a food source for antagonists. Etesami and Jeong (2020) [13] suggested that exogenous SS application on plant tissues stimulates plant growth and systemic defense mechanisms against pathogens for controlling various types of plant diseases. Gbongue et al. (2019) [14] reported that applying elemental Si to the cell walls of the host plant prevents FOC’s entry through the epidermal cell wall and provides nutrients and resistance to the host plant where it acts as a mechanical barrier. However, monosilicic acid (H4SiO4) is the only form of Si that can be absorbed by plants, which is important for plant growth and development. Putrie et al. (2021) [15] mentioned that Bacillus spp. is a genus of bacteria with great potential to be plant-growth boosters and fungus antagonists, making them viable as sustainable, eco-friendly alternatives.
Jayanti and Joko (2020) [16] revealed that BS has a good potential to produce more of the indole 3-acetic acid (IAA) hormone to enhance cell elongation, vascular tissue development, and the apical dominance of the host plant. This study aims to point out the effectiveness of SS and BS on growth performance, physio-biochemical properties, and yield of bananas grown in Fusarium-infected areas.

2. Materials and Methods

2.1. Preparation and Treatment of Experminetal Materials

A field trial plot was conducted on a commercial banana farm in Kampung Labohan Dagang, Selangor. This farm was declared a potential FOC transmission hotspot by the Department of Agriculture (DOA). Two-month-old tissue culture-derived Berangan banana seedlings from NNS Permata Holdings Sdn. Bhd. were used in this experiment, and selected based on their uniformity in size and the health of the seedlings. The planting distance between the banana plants was 2 × 2.2 m. All treatments were arranged in a randomized complete block design (RCBD). The roots of the banana plants were treated with four different treatments, control, CBZ, SS + BS, and CBZ + SS + BS, by saturating the soil pit and the soil under the plant canopy. The concentration of 0.1% CBZ application was considered as standard practice for suppressing Fusarium wilt disease, and 0.0901 M of SS, about 300 mL/plant, was integrated together with 108 CFUmL−1 BS inoculation at 15-day intervals throughout the experimental period. Standard banana farm management practices recommended by the DOA were applied in all treatments.

2.2. Data Collection

2.2.1. Determination of Crop Growth and Physiological Attributes

The height of the banana plants was measured from the soil surface level to the first internode located at the top of the plant shoots using a measuring tape, while the pseudo-stem diameter was measured using a vernier caliper at 3 cm above the soil level. The data were measured on a monthly basis. Meanwhile, the canopy diameter of the plant was obtained using a measuring tape from end to end of the leaf canopy. The data were measured on a monthly basis. Total chlorophyll content (Chla+b) was determined following the method described by [17]. Four discs were obtained from the middle part of the banana leaf using a cork borer and transferred into a plastic vial (rapidly covered with aluminum foil) containing 20 mL of 80% acetone. The samples were kept in the dark for 7 days until all the pigments were extracted. The absorbance values of the solution of each sample were read at 647 and 664 nm using a spectrophotometer (UV-3101PC UV-VIS-NIR, Shimadzu, Japan) to determine Chla, Chlb, and Chla=b. The contents were calculated as follows:
Chla = 13.19 (A664) − 2.57 (A647)
Chlb = 22.1 (A647) − 5.26 (A664)
Chla+b = 3.5 (Chla + Chlb)/4
where Chla, Chlb, and Chla+b denote chlorophyll a, chlorophyll b, and total chlorophyll (a + b), respectively. A647 and A664 denote the absorbance of the solution at 647 and 664 nm, respectively; 13.19, 2.57, 22.1, and 5.26 are the absorption coefficients, 3.5 is the total volume used in the analysis obtained from the original solution (mL), and 4 is the total disc area (cm2).
The electrolyte leakage (EL) of the root membrane was assessed based on the membrane permeability, according to the method of [18] and expressed as a percentage (%). The root (0.3 cm in diameter) was obtained and washed with de-ionized water to remove any contaminants and then placed in individual vials containing 10 mL of de-ionized water. The samples were incubated at 25 °C in a shaker with a running speed of 100 rpm for 24 h. The electrical conductivity (EC) of the bathing solution was read following incubation (EC1). The same samples were autoclaved at 120 °C for 20 min, and again, the second reading (EC2) was determined after cooling at room temperature by using a portable meter HI993310 (Hanna Instrument Company, Woonsocket, RI, USA). The percentage of EL was calculated as follows:
EL = (EC1/EC2) × 100

2.2.2. Measurement of Leaf Gas Exchange

The leaf gas exchange was determined by using a portable photosynthesis system (Model: L1-6400, Li-COR Inc., Lincoln, NE, USA). The third fully expanded leaf was chosen from each treatment for the determination of the rate of photosynthesis (Ps), stomata conductance, transpiration rate, and vapor pressure deficit (VPD). The measurements used optimal conditions set at 400 µmol mol−1 CO2, 30 °C cuvette temperature, and 60% relative humidity with an air-flow rate set at 500 cm3 min−1. The measurement was performed at 6 WAT by clipping the leaf in the chamber at a standard time (from 08:00 to 11:00 a.m.). The reading of Ps, stomata conductance, transpiration rate, and VPD were expressed as µmol CO2 m−2s−1, mmol m−2s−1, mmol H2O m−2s−1, and mol H2O m−2s−1, respectively.

2.2.3. Biochemical Assay and Nutrient Uptake

The quantification of the total phenolic content (TPC) and lignin content from the root samples was measured by following the method described by [19], and the results of the TPC obtained were expressed as μg gallic acid/g FW. For the determination of the lignin content, alkali lignin was used as a standard and the results obtained were expressed as μg LTGA/g FW.
Malonyldialdehyde (MDA) is a product of lipid obtained from peroxidation activity. The quantification of MDA content in the root was performed according to the method described by [20] and expressed as the µmol MDA g−1 of fresh weight. Approximately 0.5 g of fresh banana root was ground in liquid nitrogen (N2) and stored for further analysis. Only one gram of the banana root sample was macerated in 3 mL of 0.1% trichloroacetic acid (TCA), and then the homogenate was centrifuged at 10,000× g for 20 min. About 0.5 mL of the supernatant was mixed with a 1.5 mL solution of 20% TCA containing 0.5% thiobarbituric acid (TBA). Then, the mixture was heated at 95 °C for 30 min and rapidly cooled in an ice bath, and warmed up at room temperature. The extinction was measured at 532 and 600 nm by using a spectrophotometer (Model: Shimadzu UV-160A Visible Recording Spectrophotometer, Kyoto, Japan). Lastly, the MDA content was calculated as follows:
MDA (µmolg−1) = [(A532 − A600)/155] × 103 × dilution factor
where A532 and A600 denote the absorbance of the solution at 532 and 600 nm, respectively. The value of 155 represents the extinction coefficient, while 103 was the conversion unit, and 1 was the dilution factor.
The uptake of nitrogen (N), phosphorus (P), potassium (K), calcium (Ca), and magnesium (Mg) was determined using the method described by [21]. The third fully expanded dried-leaf samples of banana were finely ground to undergo plant nutrient analysis. To conduct the analysis, 0.25 g of dry ground-leaf tissue was homogenized with 5 mL of concentrated sulfuric acid (H2SO4) for a minimum of 2 h before adding 2 mL of 50% hydrogen peroxide (H2O2) and heated up to 285 °C in a digestion chamber for approximately 45 min. However, this step was repeated until the sample became clear in color. Lastly, the solutions were made up to 100 mL with distilled water and filtered; N and P contents were determined by using an Auto Analyzer, AA (LACHART Instruments, Model Quikchem IC + FIA 8000 Series, Milwaukee, WI, USA), whereas the Atomic Absorption Spectrophotometer, AAS (Perkin-Elmer, 5100 PC, Houston, TX, USA), was used for the determination of K, Ca, and Mg.

2.2.4. Disease Assessment

Fusarium wilt disease symptoms on banana plants were monitored and recorded for yellowing or wilting leaves. To evaluate the disease incidence (DI), the number of banana plants with apparent symptoms, the chlorosis and necrosis of leaves for the total number of plants, was assessed for each treatment [22]. The following formula was adopted to calculate the percentage of DI:
DI (%) = (number of infected seedlings/total number of seedlings assessed) × 100
Symptom appearance delays were expressed in the percentage of disease reduction (DR) derived from the area under AUDPC. The area under the disease progress curve (AUDPC) was assessed using the same plotted data as the disease progress curve. The AUDPC was calculated according to the formula presented by [4]. However, the highest AUDPC value revealed that the DI of the banana plants obtained a high value during the treatment.
The disease severity (DS) was assessed and recorded separately based on the extent of leaf yellowing and wilting for the DI evaluation based on disease symptoms that existed on the plant’s canopy. The DI grading followed the index described by [20]. The leaf symptom index was rated on each plant between scale 0 to 4 as follows:
  • Without disease symptoms on the plant canopy = 0;
  • Yellowing of lower leaves and necrotic symptom less than 25% = 1;
  • Less than 50% of the total number of leaves have a yellowish color or necrosis present = 2;
  • A total of 50 to 75% of the total number of leaves have a yellowish color or necrosis present = 3;
  • All leaves have a yellowish color or necrosis present (severe wilting), or plant death = 4.
Based on the infection counts and the disease-symptom assessments, the DS index was calculated as follows:
DS   ( % ) = Σ   ( Number   of   seedlings   in   the   scale   ×   Severity   scale ) × 100 Total   number   of   seedlings   assessed   ×   Highest   scale

2.2.5. Yield

During the harvest stage, about 10 months after transplantation (MAT), the weight of the banana bunch after each treatment was calculated using a digital weighing balance.

2.3. Statistical Analysis

All the data collected from this experiment were recorded and analyzed using the analysis of variance (ANOVA) by a statistical analysis system (SAS 9.4) to determine the significant difference between the treatment means. The differences between separated means were made using the least significant difference (LSD) at the p < 0.05 level.

3. Results

3.1. Crop Growth and Physiological Attributes

The plant height presented as the pseudo-stem height of bananas significantly affected (p < 0.05) by the treatments. The integration of CBZ + SS + BS by drenching the soil significantly increased the plant height of Berangan bananas from 4 to 10 MAT consistently (Figure 1). The analysis of variance for the plant showed a highly significant difference (p < 0.05) at the 10th MAT. By a comparison of the means, CBZ + SS + BS gained the highest value in terms of plant height with a mean value about 240 cm, followed by CBZ (194 cm), and SS + BS (173 cm), and plants without any treatments had the lowest plant height (90 cm). The treatment of SS + BS significantly increased the plant’s height by 91.71%, compared to the control. However, the treatment with SS + BS and CBZ significantly reduced the plant’s height by 38.47% and 23.52%, respectively, compared to CBZ + SS + BS.
Various growth traits are presented in Table 1. The pseudo-stem diameter size of bananas significantly increased by 18.88% (CBZ), 15.10% (SS + BS), and 26.74% (CBZ + SS + BS), compared to the control (16.02 cm). Following 10 MAT, plants treated with CBZ + SS + BS had the largest canopy diameter size (368.50 cm), followed by SS + BS (291.50 cm) and CBZ (290.25 cm), while the banana plant without any treatments (control) had the smallest canopy diameter with a mean value of about 188.60 cm. Plants treated with CBZ + SS + BS had a significantly increased pseudo-stem diameter of 26.74% and canopy diameter of 48.81% relative to the control. Systemic fungicide application without integration with SS and BS significantly reduced the pseudo-stem diameter by 10.73% and the canopy diameter by 26.95%, in comparison to CBZ + SS + BS.
The inoculation of BS in the soil under the plant’s canopy significantly increased the Chla+b content by 37.96% (SS + BS) and 35.27% (CBZ + SS + BS), respectively, compared to the control treatment. Based on the mean comparison, plants that did not receive any treatment had the lowest Chla+b content with a mean value of about 4.33 mgcm−2, followed by CBZ (5.56 mgcm−2) and CBZ + SS + BS (6.69 mgcm−2), whereas plants treated with SS + BS had the highest Chla+b content with a mean value of 6.98 mgcm−2. Furthermore, EL significantly reduced by 1.16% (SS + BS) and 10% (CBZ + SS + BS), respectively, compared to the control. However, the application of CBZ alone to the banana‘s root significantly reduced the EL by 4.24% relative to the plant without any treatments. However, banana plants treated with CBZ + SS + BS noticeably had the lowest percentage of EL (about 61.27%), whereas the control plant had the highest percentage of EL among the others (71.27%).

3.2. Leaf Gas Exchange

Bar chart in Figure 2 demonstrates that plants treated with CBZ + SS + BS presented the highest rate of Ps activity by 23.27 μmol CO2 m−2s−1, followed by SS + BS (22.24 μmol CO2 m−2s−1) and CBZ (19.92 μmol CO2 m−2s−1), while the control-treatment plants presented the lowest rate by 15.67 μmol CO2 m−2s−1. The root of banana plants treated with CBZ + SS + BS significantly increased Ps by 14.39%, compared to plants treated with CBZ alone. However, the Ps of banana plants that were only treated with SS + BS significantly increased by 29.54% compared to the control. The variance analysis results of the studied physiological traits presented in Table 2 show that CBZ + SS + BS applied to the root of the banana plant did not affect stomata conductance, but the transpiration rate and VPD from the shoot of the plants were affected. Plants treated with integration treatment of CBZ + SS + BS enhanced the transpiration rate by 8.19 mmol H2O m−2s−1, followed by SS + BS (7.91 mmol H2O m−2s−1), and CBZ (7.85 mmol H2O m−2s−1), while the control treatment presented the lowest rate of 2.95 mmol H2O m−2s−1. Somehow, the consistent application at 15DI with SS + BS presented the highest VPD by 1.925 mol H2O m−2s−1, followed by CBZ (1.887 mol H2O m−2s−1), and CBZ + SS + BS (1.879 mol H2O m−2s−1), and the control treatment presented the lowest VPD by 0.704 mol H2O m−2s−1. The application of SS + BS significantly increased the VPD by 63.42% when stomata conductance decreased by 1.71%, but the transpiration rate of the plant treated with SS + BS significantly increased by 62.32% compared to the control treatment. The results suggest that stomata closure leads to a decrease in stomata conductance, but VPD increases when the transfer of water vapor driven from the banana’s leaf increases due to limited stomata closure. Thus, the response of increasing VPD directly decreases stomata conductance.

3.3. Biochemical Content and Nutrient Uptake

The results in Table 3 show that the biochemical accumulation of TPC, lignin, and MDA content from the sampled root of the banana is significantly affected (p < 0.05) by the treatments. The TPC of the sampled root of the banana significantly decreased by 21.29% (CBZ), 9.39% (SS + BS), and 49.15% (CBZ + SS + BS) compared to the control. However, the lignin content in the root significantly increased by 43.16% (CBZ), 58.63% (SS + BS), and 57.75% (CBZ + SS + BS) compared to the control treatment. The MDA content from the infected root significantly decreased by 39.21% (CBZ), 47.91% (SS + BS), and 82.05% (CBZ + SS + BS) compared to the control, which had the highest accumulation of MDA content of about 0.71 µmolg−1 FW. In this experiment, the macronutrient uptake of N, P, K, and Ca presented in Table 4 shows that these elements are highly significantly affected by the integration of BS with SS and CBZ.
There was no significant different in the element of Mg content in the banana leaf tissues between these treatments. The accumulation of N uptake increased by 0.03% (CBZ), followed by 0.19% (SS + BS) and 0.78% (CBZ + SS + BS), compared to plants without any treatment, which served as the control (0.49%). The element of P uptake significantly increased by 0.01% (CBZ), but the accumulation of P markedly decreased by 0.05% (SS + BS) and 0.03% (CBZ + SS + BS) in comparison to the control (0.68%). The uptake of the K nutrient significantly increased when the plant was treated with SS + BS (46.81%), followed by CBZ + SS + BS (46.3%) and the control (46.2%), but plants treated with CBZ alone presented the lowest K concentration of about 40.38%. When compared to the control plant (0.32%), the accumulation of Ca in bananas significantly increased by 0.09% (CBZ), 0.13% (SS + BS), and 0.12% (CBZ + SS + BS).

3.4. Disease Assessment

Figure 3 shows that the DI of the plant received CBZ treatment that was significantly less than the banana plant treated with only with SS + BS. At the early planting stage, at about 2nd MAT, no DI was observed in the plant treated with CBZ and CBZ + SS + BS. This indicated that the seedlings treated with CBZ had partially suppressed the disease. The appearance of Fusarium wilt disease symptoms in the plant treated with CBZ treatment was observed at 4th MAT. The disease progression in the banana was gradually increased thereafter with DI of 32.14% at 10th WAT of observation. The plant without any treatments gained the highest DI of 66.07% at the 10th MAT of assessment. These results suggest that the soil application with CBZ alone significantly increases DI by 1.78%, but integration treatments of CBZ + SS + BS reduce the DI by 16.07% compared to plants treated with SS + BS.
The extent of severity from foliar external symptoms was demonstrated as a percentage of DS where the banana plant was assessed. Figure 4 shows that DS is significantly reduced (p < 0.05) when the plant receives CBZ treatment to suppress Fusarium wilt disease; however, disease progression in the plant gradually increases thereafter, with a DS of 27.23% at 10th MAT. The control plant presented the highest DS of 66.07%, whereas the plant treated with CBZ+ SS + BS presented the lowest DS of 14.28% throughout the 10th MAT of observation. The application of SS + BS to the root of the banana plant significantly reduced the DS by 35.72%, whereas the plant treated with CBZ + SS + BS significantly reduced the DS by 51.79% compared to the control with a mean value of 66.07%. Thus, these results suggest that a lower percentage of DS indicates a successful suppression of Fusarium wilt disease infection development in banana plants.
The investigation results presented in Table 5 show that the disease development reduced. The application of SS + BS (45.36%) was more effective than CBZ (43.64%) treatment alone, based on the (DR%), while the plant treated by a combination of CBZ and SS + BS presented the highest DR rate of 63.05% among the others. However, the control plant without any treatments displayed 0% of DR, which indicated a greater susceptibility of the banana plants to Fusarium wilt disease. Moreover, the treatment that presented the lowest AUDPC values indicated the effectiveness of treatments in controlling Fusarium wilt disease, where 166.07, 160.71, and 108.92 square units were recorded for CBZ, followed by SS + BS and CBZ + SS + BS, respectively, relative to the control treatment (294.64 square units). Therefore, it was clear that treatment with CBZ + SS + BS was the most effective in slowing down Fusarium wilt disease.

3.5. Yield

The bar chart presented in Figure 5 shows that the integration of CBZ + SS + BS significantly increases the yield performance of bananas by 25.97%, compared to plants treated with CBZ alone. Plants treated with SS + BS without CBZ treatment significantly increased the yield of bananas by 47.11% compared to the control treatment. As a means comparison, the integration of CBZ + SS + BS produced the largest harvest yield in terms of the weight of fruit bunch by 24.72 kg, followed by CBZ (18.3 kg) and SS + BS (17.87 kg), while the plant in the control treatment greatly affected Fusarium stress and presented the lowest weight of 9.45 kg.

4. Discussion

Fusarium wilt disease is a devastating fungal vascular wilt disease occurring from the emergence of FOC-TR4 fungus in banana plantations, which reduces growth performance and yield production [23,24]. Banana plants with mild to moderate infection levels are always associated with leaf yellowing and wilting because FOC-TR4 invades the xylem vessels causing water scarcity and nutrient transfer [25,26]. Based on the in vitro evaluation of fungicides, [27,28] reported that CBZ totally inhibited the mycelial growth of FOC and proposed that CBZ was acceptable for application in commercial banana plantations for managing soil-borne diseases. Mbasa et al. (2021) [29] also reported that after 120 days of application, CBZ significantly reduced the severity of cashew Fusarium wilt disease and improved plant recovery. Zhou et al. (2018) [30] revealed that SS applied to cucumber plants improved cucumber-seedling plant growth performance and suppressed FOC for controlling Fusarium wilt disease. Surprisingly, the integration between treatments of CBZ and SS with BS to the soil under the plant canopy significantly improved banana-growth performance and provided superior protection against Fusarium wilt disease, which were described in the current field investigation. Results similar to those presented in [31] reported that the integrated control of potato late-blight disease using effective microorganisms and fungicides can improve pathogen-control effectiveness and plant-growth performance with minimal amounts of fungicide application.
Integrated treatments between BSand, an Si-based compound, improved the growth and Ps rates of Solanum melongena, which had a synergistic effect on plant physiological growth and disease resistance [32,33]. Interestingly, BS was able to produce IAA, which has a good plant probiotic impact on the host plant, improving growth and survival capabilities under stressful conditions [34,35,36].
However, the authors discovered that the amount of Chla+b content in the banana leaves was dramatically reduced when the roots of bananas infected with Fusarium wilt disease. Treatment of CBZ + SS + BS induced a higher chlorophyll content, which contributed to the increased rate of Ps. This result is consistent with [37], who observed that when the host plant of bananas is infected with Fusarium wilt disease, the leaf Chla+b decreases as a result of biotic stress. Raiesi and Golmohammadi (2020) [38] also observed that phytoplasma infection reduced Chla+b concentration in lime leaves and boosted chlorophyllase activity in the infected plants.
Furthermore, Awan and Shoaib (2019) [39] observed that integrated bacteria-based biological fungicides were gaining traction in agriculture to boost plant performance through stomatal regulation, increased Ps rate, and subsequent glucose translocation and metabolism activities. In plant physiology, reduced Chla+b content is also regulated by plant or leaf age. Ahmad et al. (2018) [40] observed that the amount of Chla+b in wheat plants decreased as the leaf age increased due to the activation of chlorophyllase activity, but the amount of Chla+b in younger leaves increased due to enzyme activation in the light reaction for chlorophyll production. Changes in plant physiology parameters, particularly the Ps rate, were tightly linked to leaf Chla+b content, which was controlled by how plants responded to their environment [41,42,43,44]. Increased stomata conductance improved CO2 diffusion into the leaf and subsequently increased the Ps rate, thus improving banana plant development and yield productivity [45]. Moreover, when plants are triggered by pathogen infection, lignin deposition, the accumulation of TPC, and MDA concentration are typically related to defense mechanisms [46,47]. According to the findings, the root EL of non-treated banana plants significantly increased with a higher accumulation of TPC, MDA, and lignin content. According to [48], the authors mentioned that a biostimulant combined with Bacillus spp. that creates antimicrobial metabolites on infected plants significantly reduced MDA accumulation, hence enhancing the production compound of TPC in bean plants to protect them from mosaic virus infection.
Pearson’s correlation coefficients between the selected parameters of physiological and biochemical changes were established, and the positive or negative significant correlations are presented in Table 6. The strongest positive correlation was observed between DI and MDA (r2 = 0.94), whereas the strongest negative correlation was observed between Ps and MDA (r2 = 0.85). Interestingly, Pearson’s correlation coefficients matrix analysis showed that Chla+b was highly correlated with the Ps rate, which is associated with each other for the improved physiological growth and yield performance of bananas. However, these results suggest that a decrease in the DI regulates the biochemical composition in banana tissues and physiological attributes as well.
According to our results, plants treated with combination treatments of CBZ + SS + BS have a considerable reduction in plant deaths, yet a considerable increase in banana yield production can be observed. As expected, integrated treatments of CBZ + SS + BS achieved the highest DR values, as well as delaying DI and lowering the AUDPC value of DI and DS, since the best results were achieved by combining CBZ + SS + BS treatments. Bouzoumita et al. (2019) [49] observed that combining the CBZ fungicide with Bacillus spp. as a biocontrol agent resulted in a much higher percentage of DR. Maulidah et al. (2021) [50] observed that treating the roots of banana plants with a rhizo-bacterial isolate reduced the percentage of EL and MDA accumulation from membrane peroxidation activity. Furthermore, Si deposition on plant tissues enhanced the modifications in the membrane function, in addition to lowering EL in the plants under biotic and abiotic stress conditions [51]. Ultimately, CBZ + SS + BS was the best combination to promote banana-growth performance and banan-plant resistance to Fusarium wilt disease in the farm.

5. Conclusions

Based on the field observations, the banana plants without receiving any treatment presented a significant reduction in morphological growth parameters and physiological traits, but there was an increase in the accumulation of MDA content in the infected root tissues. The percentages of DS and DI determined that soil treated with systemic fungicides of CBZ alone were inadequate for preventing 100 percent root infection by FOC. In comparison to the other treatments, the integrated application of CBZ + SS + BS considerably improved plant-growth performance, Chla+b content, and Ps rate, but reduced the EL, TPC, and TFC in banana plant tissues. From these findings, plants treated with CBZ + SS + BS had significantly reduced DIs (by 16.07%) and presented the lowest DS values (14.28%). Furthermore, the same treatment also presented the highest DR value of 63.05%. Based on the AUDPC result, CBZ + SS + BS showed the most effective combination treatments for controlling Fusarium wilt disease in the farm. Therefore, the integration between CBZ + SS + BS had good, significant effects on controlling Fusarium wilt disease and a better morpho-physiological growth performance, with an average yield production of about 24.72 kg per fruit bunch. Therefore, integrated treatments of CBZ + SS + BS are recommended for use by farmers in the field to enhance the growth of bananas and their resistance to FOC. In the future, experiments should focus on a multigenic method by including more than one gene in transgenic banana plants to boost biotic stress resistance.

Author Contributions

M.A.T.Z. implemented all the research; S.Z.S., M.R.I., K.A., and S.K. supervised the research; S.Z.S. and K.A. offered advice during the planning of the research and M.R.I. provided the technical support; S.K. was also engaged in the supervision and selection of the methodology for this research. This manuscript was written by M.A.T.Z. with the assistance of S.Z.S. and K.A. All authors have read and agreed to the published version of the manuscript.

Funding

This research was conducted with financial support and in-kind contributions from a collaboration between the University of Putra Malaysia and the Malaysian Ministry of Higher Education (MOHE).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

The authors are grateful to the NNS Permata Holdings Sdn. Bhd. for supplying the banana seedlings and Alfian Mohajir Enterprise for assisting in preparing the experimental materials and encouragement to complete the research. We would also like to express our the greatest appreciation to the Department of Crop Science, Department of Plant Protection, and Department of Soil Science Management, UPM for all the facilities provided and all the staff who were directly or indirectly involved in this project.

Conflicts of Interest

The authors declare no potential conflict of interest.

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Figure 1. Changes in plant height affected by different treatments of the roots of banana plants over durations of 10 MAT in the field. Data are the mean ± SEM (standard error of differences between means) of 16 replicates. Bars represent means followed by the different small letters significant at p < 0.05. Control = without any application, CBZ = carbendazim fungicide, SS + BS = sodium silicate applied together with Bacillus subtilis, and CBZ + SS + BS = integrated treatments of CBZ and sodium applied together with Bacillus subtilis.
Figure 1. Changes in plant height affected by different treatments of the roots of banana plants over durations of 10 MAT in the field. Data are the mean ± SEM (standard error of differences between means) of 16 replicates. Bars represent means followed by the different small letters significant at p < 0.05. Control = without any application, CBZ = carbendazim fungicide, SS + BS = sodium silicate applied together with Bacillus subtilis, and CBZ + SS + BS = integrated treatments of CBZ and sodium applied together with Bacillus subtilis.
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Figure 2. Changes in photosynthesis rate (Ps) at 6th MAT as affected by different treatments applied to the roots of bananas. Data are the mean ± SEM (standard error of differences between means) of 16 replicates. Bars represent means followed by the different, small letters significant at p < 0.05. Control = without any application, CBZ = carbendazim fungicide, SS + BS = sodium silicate applied together with Bacillus subtilis, and CBZ + SS + BS = integrated treatments of CBZ and sodium silicate applied together with Bacillus subtilis.
Figure 2. Changes in photosynthesis rate (Ps) at 6th MAT as affected by different treatments applied to the roots of bananas. Data are the mean ± SEM (standard error of differences between means) of 16 replicates. Bars represent means followed by the different, small letters significant at p < 0.05. Control = without any application, CBZ = carbendazim fungicide, SS + BS = sodium silicate applied together with Bacillus subtilis, and CBZ + SS + BS = integrated treatments of CBZ and sodium silicate applied together with Bacillus subtilis.
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Figure 3. Disease incidence (DI) as affected by different treatments applied to the roots of banana plants throughout 10th MAT. Data are the mean ± SEM (standard error of differences between means) by using the least significant difference (p < 0.05). Control = without any application, CBZ = carbendazim fungicide, SS + BS = sodium silicate applied together with Bacillus subtilis, and CBZ + SS + BS = integrated treatments of CBZ and sodium silicate applied together with Bacillus subtilis.
Figure 3. Disease incidence (DI) as affected by different treatments applied to the roots of banana plants throughout 10th MAT. Data are the mean ± SEM (standard error of differences between means) by using the least significant difference (p < 0.05). Control = without any application, CBZ = carbendazim fungicide, SS + BS = sodium silicate applied together with Bacillus subtilis, and CBZ + SS + BS = integrated treatments of CBZ and sodium silicate applied together with Bacillus subtilis.
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Figure 4. Disease severity (DS) as affected by different treatments applied to the roots of banana plants throughout 10th MAT. Data are the mean ± SEM (standard error of differences between means) by using the least significant difference (p < 0.05). Control = without any application, CBZ = carbendazim fungicide, SS + BS = sodium silicate applied together with Bacillus subtilis, and CBZ + SS + BS = integrated treatments of CBZ and sodium silicate applied together with Bacillus subtilis.
Figure 4. Disease severity (DS) as affected by different treatments applied to the roots of banana plants throughout 10th MAT. Data are the mean ± SEM (standard error of differences between means) by using the least significant difference (p < 0.05). Control = without any application, CBZ = carbendazim fungicide, SS + BS = sodium silicate applied together with Bacillus subtilis, and CBZ + SS + BS = integrated treatments of CBZ and sodium silicate applied together with Bacillus subtilis.
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Figure 5. Yield of bananas at harvest stage at about 10th MAT. Data are the mean ± SEM (standard error of differences between means) of 16 replicates. Bars represent means followed by the different small letters significant at p < 0.05. Control = without any application, CBZ = carbendazim fungicide, SS + BS = sodium silicate applied together with Bacillus subtilis, and CBZ + SS + BS = integrated treatments of CBZ and sodium silicate applied together with Bacillus subtilis.
Figure 5. Yield of bananas at harvest stage at about 10th MAT. Data are the mean ± SEM (standard error of differences between means) of 16 replicates. Bars represent means followed by the different small letters significant at p < 0.05. Control = without any application, CBZ = carbendazim fungicide, SS + BS = sodium silicate applied together with Bacillus subtilis, and CBZ + SS + BS = integrated treatments of CBZ and sodium silicate applied together with Bacillus subtilis.
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Table
Table 1. The pseudo-stem, canopy diameter, total chlorophyll content (Chla+b), and root electrolyte leakage (EL) as influenced by different treatments applied to the roots of banana plants.
Table 1. The pseudo-stem, canopy diameter, total chlorophyll content (Chla+b), and root electrolyte leakage (EL) as influenced by different treatments applied to the roots of banana plants.
TreatmentsPseudo-Stem DiameterCanopy
Diameter		Total Chlorophyll ContentRoot Electrolyte Leakage
(cm)(cm)(mgcm−2)(%)
Control16.02 c188.60 c4.33 c71.27 a
CBZ19.75 b290.25 b5.56 b67.03 ab
SS + BS18.87 b291.50 b6.98 a61.41 b
CBZ + SS + BS21.87 a368.5 a6.69 a61.27 b
LSD p < 0.052.08 **36.18 ***1.03 **7.10 *
Means followed by the same letter within a column are not significantly different at (p > 0.05) by the least significant difference (LSD) with n = 16. *, **, and *** are significantly different at p < 0.05, 0.01, and 0.001, respectively. Control = without any application, CBZ = carbendazim fungicide, SS + BS = sodium silicate applied together with Bacillus subtilis, and CBZ + SS + BS = integrated treatments of CBZ and sodium silicate applied together with Bacillus subtilis.
Table
Table 2. The stomata conductance, transpiration rate, and vapor pressure deficit (VPD) as influenced by different treatments applied to the root of the banana.
Table 2. The stomata conductance, transpiration rate, and vapor pressure deficit (VPD) as influenced by different treatments applied to the root of the banana.
TreatmentsStomata ConductanceTranspiration RateVapour Pressure Deficit
(mmol m−2s−1)(mmol H2O m−2s−1)(mol H2O m−2s−1)
Control0.475 a2.98 b0.704 b
CBZ0.476 a7.85 a1.887 a
SS + BS 0.467 a7.91 a1.925 a
CBZ + SS + BS0.501 a8.19 a1.879 a
LSD p < 0.05NS1.43 ***0.17 ***
Means followed by the same letter within a column are not significantly different at (p > 0.05) by a least significant difference (LSD) with n = 16. *** is significantly different at p < 0.001 and NS = not significant. Control = without any application, CBZ = carbendazim fungicide, SS + BS = sodium silicate applied together with Bacillus subtilis, and CBZ + SS + BS = integrated treatments of CBZ and sodium silicate applied together with Bacillus subtilis.
Table
Table 3. The total phenolic content (TPC), lignin content, and malondialdehyde content (MDA) as influenced by different treatments applied to the roots of bananas.
Table 3. The total phenolic content (TPC), lignin content, and malondialdehyde content (MDA) as influenced by different treatments applied to the roots of bananas.
TreatmentsTotal Phenolic
Content		Lignin
Content		Malondialdehyde Content
(µg/g FW)(LTGAg−1 Tissue)(µmol g−1 FW)
Control142.59 a0.79 b0.71 a
CBZ117.56 b1.39 ab0.51 b
SS + BS 130.35 ab1.91 a0.48 b
CBZ + SS + BS95.60 c1.87 a0.39 c
LSD p < 0.0516.23 ***0.85 *0.05 ***
Means followed by the same letter within a column are not significantly different at (p > 0.05) by least significant difference (LSD) with n = 16. * and *** are significantly different at p < 0.05 and 0.001, respectively. Control = without any application, CBZ = carbendazim fungicide, SS + BS = sodium silicate applied together with Bacillus subtilis, and CBZ + SS + BS = integrated treatments of CBZ and sodium silicate applied together with Bacillus subtilis.
Table
Table 4. The effect of different treatments applied to the foliar nutrient content.
Table 4. The effect of different treatments applied to the foliar nutrient content.
TreatmentsNPKCaMg
(%)(%)(%)(%)(%)
Control0.49 c0.68 ab46.2 ab0.32 c0.56 a
CBZ0.52 c0.69 a40.38 b0.41 b0.44 a
SS + BS0.68 b0.63 c46.81 a0.45 a0.51 a
CBZ + SS + BS1.27 a0.65 bc46.3 a0.44 a0.56 a
LSD p < 0.050.03 ***0.04 *5.86 **0.02 ***NS
Means followed by the same letter within a column are not significantly different at p > 0.05 by least significant difference (LSD) with n = 32. *, **, and *** are significant different at p < 0.05, 0.01, and 0.001, respectively, and NS = not significant. Control = without any application, CBZ = carbendazim fungicide, SS + BS = sodium silicate applied together with Bacillus subtilis, and CBZ + SS + BS = integrated treatments of CBZ and sodium silicate applied together with Bacillus subtilis.
Table
Table 5. Effect of different treatments applied to the roots of banana plants on disease reduction (DR) and area under the disease progress curve (AUDPC).
Table 5. Effect of different treatments applied to the roots of banana plants on disease reduction (DR) and area under the disease progress curve (AUDPC).
TreatmentsDRAUDPC
(%)(Unit2)
Control0 c294.64 a
CBZ43.64 b166.07 b
SS + BS 45.36 b160.71 b
CBZ + SS + BS63.05 a108.92 c
LSD p < 0.055.76 ***17.88 ***
Means followed by the same letter within a column are not significantly different at (p > 0.05) by least significant difference (LSD) with n = 16. *** is significantly different at p < 0.001. Control = without any application, CBZ = carbendazim fungicide, SS + BS = sodium silicate applied together with Bacillus subtilis, and CBZ + SS + BS = integrated treatments of CBZ and sodium silicate applied together with Bacillus subtilis.
Table
Table 6. Pearson’s correlation between total chlorophyll content (Chla+b), photosynthesis rate (Ps), electrolyte leakage (EL), malondialdehyde (MDA) content, total phenolic content (TPC), lignin content, and disease incidence (DI) at 6MAT.
Table 6. Pearson’s correlation between total chlorophyll content (Chla+b), photosynthesis rate (Ps), electrolyte leakage (EL), malondialdehyde (MDA) content, total phenolic content (TPC), lignin content, and disease incidence (DI) at 6MAT.
Chla+bPsELMDATPCLigninDI
Chla+b1.0
Ps0.79 ***1.0
EL−0.51 *−0.72 **1.0
MDA−0.70 **−0.85 ***0.66 **1.0
TPC−0.57 *−0.67 **0.410.69 **1.0
Lignin0.59 *0.61 *−0.42−0.67 **−0.42 *1.0
DI−0.75 ***−0.84 ***0.65 **0.94 ***0.77 ***−0.70 **1.0
Coefficient of variations greater than 0.5 are significant at p < 0.05. *, **, and *** are significant differences at p < 0.01, 0.001, and 0.0001, respectively.
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Zakaria, M.A.T.; Sakimin, S.Z.; Ismail, M.R.; Ahmad, K.; Kasim, S. A Field Evaluation of Sodium Silicate and Bacillus subtilis on the Growth and Yield of Bananas following Fusarium Wilt Disease Infection. Sustainability 2023, 15, 3141. https://doi.org/10.3390/su15043141

AMA Style

Zakaria MAT, Sakimin SZ, Ismail MR, Ahmad K, Kasim S. A Field Evaluation of Sodium Silicate and Bacillus subtilis on the Growth and Yield of Bananas following Fusarium Wilt Disease Infection. Sustainability. 2023; 15(4):3141. https://doi.org/10.3390/su15043141

Chicago/Turabian Style

Zakaria, Md Aiman Takrim, Siti Zaharah Sakimin, Mohd Razi Ismail, Khairulmazmi Ahmad, and Susilawati Kasim. 2023. "A Field Evaluation of Sodium Silicate and Bacillus subtilis on the Growth and Yield of Bananas following Fusarium Wilt Disease Infection" Sustainability 15, no. 4: 3141. https://doi.org/10.3390/su15043141

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