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Article

Serendipita indica as a Plant Growth Promoter and Biocontrol Agent against Black Rot Disease in Cabbage Grown in a Phytotron

by
Sana Saleem
1,*,
Lucia Nedorost Ragasova
1,
Dorota Tekielska
2,
Maciej Fidurski
3,
Agnieszka Sekara
3 and
Robert Pokluda
1
1
Department of Vegetable Sciences and Floriculture, Faculty of Horticulture, Mendel University in Brno, 691 44 Lednice, Czech Republic
2
Mendeleum—Institute of Genetics, Mendel University in Brno, 691 44 Lednice, Czech Republic
3
Department of Horticulture, Faculty of Biotechnology and Horticulture, University of Agriculture, 31-120 Krakow, Poland
*
Author to whom correspondence should be addressed.
Agriculture 2023, 13(11), 2048; https://doi.org/10.3390/agriculture13112048
Submission received: 27 September 2023 / Revised: 21 October 2023 / Accepted: 24 October 2023 / Published: 25 October 2023
(This article belongs to the Section Crop Protection, Diseases, Pests and Weeds)
Browse Figures
Versions Notes

Abstract

:
Serendipita indica, a mutualistic root endophytic fungus, has gained attention for its potential to enhance plant health and resistance to various stresses. This study investigated the impact of S. indica (strain DSM 11827) on plant growth promotion and the management of black rot disease. This is a devastating bacterial ailment caused by Xanthomonas campestris pv. campestris, which affects cruciferous crops worldwide. The experiment was conducted under sterile conditions in a phytotron for 10 weeks. It involved the substrate and seed inoculation of S. indica in a cabbage crop. The findings suggested that S. indica establishes mutualistic relationships with cruciferous plants, positively influencing their growth while simultaneously reducing their susceptibility to black rot disease. Plant morphological and physiological parameters were enhanced by S. indica application. Additionally, bio stress markers were also enhanced in response to black rot disease. Moreover, disease severity was reduced by 27.9% and 18.8% in the substrate and seeds treated with S. indica, respectively. However, our findings did not report any antagonistic effect between S. indica and two pathogens, i.e., Xanthomonas campestris pv. campestris and Alternaria brassicicola under the in vitro test, suggesting that the suppression of black rot disease in cabbage seedlings was induced indirectly by S. indica. This study, therefore, underscores the promising prospect of utilizing S. indica to promote crop productivity and combat the destructive impact of black rot disease in cruciferous plants, contributing to more sustainable and resilient agriculture.

1. Introduction

The root systems of plants host a variety of microorganisms, some of which are beneficial to the growth and development of plants and are known as plant growth promoting microorganisms (PGPM), such as arbuscular mycorrhizal fungi (AMF), Azospirillum, Azotobacter, Bacillus subtilis, Pseudomonas fluorescens, Rhizobium, Trichoderma harzianum. and many more [1]. The use of these advantageous microbes is regarded as a novel biological strategy currently being developed to improve growth and stress regulation in plants [2]. The benefits of these microorganisms include promoting plant development, nutrient absorption, phytohormone synthesis, regulating phytopathogens and environmental stress, improving inorganic compounds, and the bioremediation of metal-contaminated soils to restore soil fertility [3,4]. These microorganisms employ different strategies to induce the aforementioned benefits to plants, such as root symbiosis, biological nitrogen fixation, phosphorus and potassium solubilization, and the synthesis of siderophores, which enhances iron accumulation and content in plants [1]. Moreover, beneficial microorganisms can also secrete various phytohormones or enzymes which modulate the concentration of hormones in plants [1,3]. By producing diverse bioactive substances and developing systemic resistance against many plant diseases, these beneficial microbes can suppress phytopathogens. In addition to their many advantages, these organisms have the potential to serve as an alternative to numerous chemical fertilizers and pesticides. They contribute to sustainable agriculture practices, thereby emphasizing their ecological and economic viability [1].
One of these beneficial microorganisms is Serendipita indica, which belongs to the Sebacinaceae family. S. indica was first isolated from Prosopis juliflora and Ziziphus nummularia in the Thar Desert of Rajasthan, India [5]. It shares similarities with arbuscular mycorrhizal fungi and can develop inter- and intracellularly in host plant rhizospheres, where it produces pear-shaped chlamydospores [5]. S. indica is known to have an extensive host range and can be cultivated without host plants on artificial media, differentiating it from arbuscular mycorrhizal fungi [6].
Serendipita indica has a diverse positive impact on host plants and has been effectively used in plant growth stimulation, stress resistance, and improvement in the fruit quality of many horticultural crops by enhancing nutrient and water uptake [7]. In a variety of vegetable crops, including tomato, lettuce, cabbage, bell pepper, spinach, and sweet potatoes, it improves plant growth, quality, and productivity [8,9,10,11,12,13]. In addition, S. indica has been demonstrated to shield crops from a variety of diseases, including verticillium wilt and early blight in tomatoes [14,15], club root in Chinese cabbage [16], black spot in cabbage [10], and stemphylium leaf blight in onion [17]. Furthermore, S. indica has been shown to mitigate heavy metal concentrations and their absorption in soil, hence alleviating biotic and abiotic stresses [18,19]. Therefore, this fungus is considered a potential source of biofertilizer for sustainable agricultural production that ensures environmental safety and soil detoxification.
Crops are vulnerable to a wide range of pathogenic infections, causing colossal crop loss and, as a result, a fiscal disaster for the farming industry. Among these, black rot is a serious vegetable disease caused by Xanthomonas campestris, a seed-born, Gram-negative pathogen considered the most destructive pathogen of crucifers, with an optimal growing temperature of 25–30 °C. It infects plants through hydathodes found on the leaf margin, stomata, wounds, and roots, eventually infiltrating the vascular tissues [20]. This plant infection is characterized by forming a V-shaped lesion at the leaf margin that progresses towards the center through vascular tissues, followed by leaf darkening, and ultimately, leaf wilting and necrosis of the leaves. Moreover, this pathogen infects soil and seedlings and persists in crop waste [21].
Although many management strategies, such as treating seeds and using copper and copper-based anti-microbial measures, are available to help combat this devastating disease, these approaches are sometimes ineffective, and the latter poses toxicity issues that must be addressed [22]. Therefore, the need for sustainable and ecological crop protection against Xanthomonas campestris persists. To this end, one of the best ways to address this issue is the use of beneficial microorganisms in agriculture.
This study aimed to investigate the effects of S. indica on the growth and development of cabbage plants under protected conditions. The experiment also involved the study of S. indica as a biocontrol agent against Xanthomonas campestris pv. campestris.

2. Materials and Methods

2.1. Plant Growth Condition and Treatments

The trial was carried out at Mendel University in Brno, Faculty of Horticulture, in Lednice. Cultivation was performed in a phytotron (Fytoscope FS-SI 4600 (PSI LTD., Drasov, Czech Republic) under sterile conditions. Plants were grown at a daytime temperature of 21 ± 2 °C, a nighttime temperature of 16 ± 2 °C, and a relative humidity of 75%, with a light intensity of 200 μmol m−2 s−1 and 16 h of daylight. Later, to ensure pathogen growth, the temperature was raised to 25 °C and the relative humidity was increased to 78%. Seeds of cabbage cultivar Avak F1 (Moravoseed, Mikulov, Czech Republic) were sown in square pots with dimensions of 90 × 90 × 80 mm, using a sterile perlite substrate. The cabbage seeds were disinfected with 0.5% sodium hypochlorite for 10 min before planting, washed three times with distilled water, and air dried. During the 10-week experiment, the seedlings were fertigated twice a week with 30 mL/L doses of Solinure GT fertiliser composed of 18% N, 11% P, and 11% K. (ICL Specialty Fertilizers, Brno, Czech Republic). The multifactorial design was adopted, consisting of 8 treatments in three replications and total of 12 plants per treatment were maintained. The experiment included two methods of treatment: substrate treatments and seed treatment comprised of a single inoculation of S. indica (Sp) and co-inoculation of S. indica with Xanthomonas campestris pv. campestris (Xcc). Distilled water was used as the control treatment under normal conditions while phosphate-buffered saline (PBS) served as the control treatment to investigate disease management against Xanthomonas campestris. The treatments used were:
Substrate treatment: Sp—S. indica, Xcc + Sp—Xanthomonas + S. indica, Xcc—Xan-thomonas and C-H2O—distilled water, and C-PBS—Phosphate-buffered saline.
Seed inoculation: Ssp—S. indica, Ssp + Xcc—S. indica + Xanthomonas, SXcc—Xanthomonas and SH2O—distilled water, and C-PBS—Control-phosphate-buffered saline.

2.2. Serendipita indica Inoculation

Serendipita indica strain DSM 11827 was obtained from the Deutsche Sammlung für Mikroorganismen und Zellkulturen, Braunschweig, Germany. The S. indica inoculum was prepared using the same method as described by Saleem et al. [10]. The fungus was grown on potato dextrose agar (PDA) plates and maintained in sterile potato dextrose broth (PDB). Mycelium was retained after filtration, smashed, and rinsed with distilled water. Inoculating solution with a 3% (w/v) concentration was prepared by mixing S. indica with distilled water. To inoculate the substrate, a 10 mL liquid S. indica solution was infused into the root zone of a 26-day-old seedling. For seed treatment, the S. indica suspension was used to treat the seeds by soaking them in the solution for 10 min prior to planting, and the remaining suspension was poured into each pot after sowing. The same amount of distilled water (SH2O) was provided to the control plants.

2.3. Detection of S. indica Colonisation in Cabbage Roots

The roots were randomly selected from each treatment at 6 weeks post inoculation with S. indica; washed in distilled water; fixed in a solution of 10% formaldehyde, 50% ethanol, and 5% acetic acid (FAA); and stored at 4 °C before being stained for microscopy. After fixation of each sample in 50 mL solution of FAA, the roots were rinsed in distilled water, cleared in 2% KOH solution, and washed in distilled water. The roots were stained with Alexa Fluor (AF) conjugates of wheat germ agglutinin (WGA), concanavalin A (Con A), and acid fuchsine. All the root preparation for colonization evaluation was performed with an automated tissue processor (Leica EM TP, Wetzlar, Germany) by placing the roots in the tissue processor for 24 h. For microscopic analysis, five randomly selected stained root segments, 10 mm in size, were placed on the slide. A few droplets of Hoechst stain were added to these slides with the roots before mounting on the slide.
Confocal microscopy was conducted using the LSM 800 microscope (Carl Zeiss, Jena, Germany) at 590/617 nm excitation/emission for WGA AF 594, 650/668 nm for Con A AF 647, and 350/461 nm for Hoechst stain, using a 20 × 0.8 NA lens. The pictures were processed in Zen Blue 3.0 (Carl Zeiss, Jena, Germany) [23].

2.4. Pathogen Preparation and Inoculation

2.4.1. Preparation of Xcc Inoculum

The disease management was studied using the black rot disease caused by bacterial pathogen Xanthomonas campestris pv. campestris. The isolate was obtained from the Collection of Microorganisms of Mendeleum—Institute of Genetics, Mendel University in Brno, and stored in cryotubes at −80 °C. The strain MEND-00007 was grown on Luria agar (HiMedia, Mumbai, India) for 24 h to prepare the bacterial inoculum. Subsequently, the bacterial colonies were collected using a sterile loop and then suspended in sterile phosphate-buffered saline (PBS). The concentration of the bacterial suspension was adjusted to 0.1 OD, measured at 600 nm, using a spectrophotometer (SPECTRO star Nano, BMG Labtech, Ortenberg, Germany), which reflected approx. 0.44 × 108 CFU mL−1. Sterile PBS was used as a negative control.

2.4.2. Colony Forming Unit (CFU) Enumeration

In order to enumerate CFU in Xcc suspension adjusted to 0.1 OD600, 100 µL of the suspension was serially 10-fold diluted. Subsequently, four dilutions (10−3, 10−4, 10−5 and 10−6) were plated on plate count agar (PCA, HiMedia, Mumbai, India) using the pour plate method. Briefly, 100 µL of each dilution was pipetted to the center of the sterile Petri dish (90 mm diameter) in duplicates, and approximately 15 mL of molten PCA was poured into the Petri dish and mixed with the sample by swirling. The samples were incubated at 28 °C until bacterial colonies formed in and on the medium were visible. Colonies were formed after approximately 36 h of incubation and were subsequently enumerated.

2.4.3. Pathogen Inoculation

The plants were inoculated with a pathogen 37 days after planting for both the seedling and seed treatment. Using the pricking method of pathogen inoculation, the pathogen was introduced to two leaves per plants. Six pricks of a pathogen suspension were used to contaminate each leaf by puncturing it along the midrib and veins with a sterile wooden needle. The control seedlings were treated with phosphate-buffered saline (PBS) using the same method.

2.5. In Vitro Test of S. indica with Alternaria brassicicola and Xanthomonas campestris

The in vitro test was carried out with two distinct pathogens, Alternaria brassicicola and Xanthomonas campestris pv. campestris, in independent experiments, with 10 replications each. Experiment with Alternaria included aseptic growth of S. indica and Alternaria on Petri dishes (90 mm diameter) using PDA media. Dual inoculation was carried out, using small uniform discs (4 mm diameter) of S. indica at one end of the Petri dish and Alternaria discs (4 mm) on the other end. As a control, S. indica and the pathogen were inoculated separately on Petri dishes. Readings were taken using a standard scale for assessing growth by measuring the radius in millimeters 3, 6, and 9 days after inoculation (DAI).
In vitro inhibition of Xanthomonas by S. indica was examined by growing S. indica on Luria Bertani (LB) agar media for 5 days in Petri dishes. The Xanthomonas was then gently sprayed over the Petri dish, using one push of the spray flask, at a concentration of 106 CFU/mL. Before application, the spray flask was thoroughly cleaned with ethanol and hypochlorite and then rinsed three times with LB broth media to ensure that the hypochlorite or ethanol would not influence the culture. Inoculation was performed under sterile conditions, and visual readings were recorded after 1, 2, and 3 days of inoculation.
The Petri dishes were incubated at 25 °C and 75% relative humidity under dark conditions for both tests, and visuals were captured at each reading.

2.6. Morphological and Physiological Evaluation

The morphological and physiological parameters that were considered in this research included plant height, leaf count, steady-state fluorescence level (Ft), and the normalized difference vegetation index (NDVI).
Using a digital measure with mm units, the height of the plants was determined from their base to their longest leaf. The true leaves were counted to determine the total number of leaves for each plant. The data were recorded for 12 replicates, and an average value was computed.
PlantPen and FluorPen FP 110 (PSI LTD., Drasov, Czech Republic) were used to quantify NDVI and Ft values, respectively. Ft was measured without a dark adaptation from 10 am to 12 noon, with the photon flux density of 3000 mol/m2/s. Data were gathered from two leaves per replicate, and an average value was calculated.

2.7. Biochemical and Stress Biomarker Analyses

After evaluating the morphological and physiological parameters, leaves from each replicate were harvested and used to analyze the biochemical and stress biomarker parameters, including nitrogen content, total antioxidant capacity (TAC), total phenolics, guaiacol peroxidase (GPX), and ascorbate peroxidase (APX) activity.
For nitrogen and TAC analysis, leaves from each treatment were collected, dried, crushed, and analyzed.
The nitrogen concentration of the vegetation was analyzed using the distillation method, according to the Kjeldahl H2SO4 mineralization technique. The nitrogen content of a sample was determined using the measured quantity of ammonia ions in the receiving solution.
The TAC was determined using a modified 2,2-diphenyl-1-picrylhydrazyl (DPPH) assay. A 3.0 g leaf sample was extracted in 75% methanol for 24 h, followed by filtration and analyses. Absorbance was measured after 30 min at a 515 nm wavelength using a Specord 50 plus spectrophotometer (Analytik Jena, Thuringia, Germany). The obtained data were expressed as mM/L and used to calculate the TAC.
To determine the APX, GPX activity and total phenolics, leaves were harvested from each treatment and stored immediately after harvest in a −80 °C deep freezer until analyses.
The activity of APX was measured using the method of Nakano and Asada [24]. Fresh leaf samples weighing 1 g were homogenized in 10 mL of 0.05 M phosphate buffer (1 mM EDTA, 1 mM PMSF 1% PVPP, pH 7.0) and centrifuged at 12,000× g for 10 min at 4 °C. The supernatants collected were used to determine the ascorbate peroxidase (APX). The reduction in absorbance at 290 nm was recorded for 5 min. APX activity was expressed in 1 μmol of ascorbate min−1 g−1 of FW.
GPX activity was evaluated by grinding 1 g of the leaves in an ice bath with 10 cm3 of a 0.05 M potassium phosphate buffer (1 mM EDTA, 1 mM PMSF, 1% PVPP, pH 7.0) and centrifuging at 10,000× g for 10 min. According to the methods of Lin and Kao [25], GPX was next tested, with guaiacol as a substrate and peroxide as an oxidant. A UV-VIS spectrophotometer was used to measure the absorbance at 470 nm at 60 s intervals for 3 min. One unit of peroxidase was defined as the amount of enzyme that caused the formation of 1 μmol of tetraguaiacol per minute.
The modified Folin–Ciocalteu colorimetric technique [26] was used to calculate the total phenolics. A 2.0 g leaf sample was combined with 10 cm3 of 80% methanol and centrifuged (3492× g, 15 min, 4 °C). About 0.1 cm3 of supernatant and 2 cm3 of sodium carbonate were added to the glass tubes, followed by 0.1 cm3 of Folin–Ciocalteu’s reagent mixed with deionized water (1:1 v/v). The phenols were analyzed after 45 min using a UV-VIS spectrophotometer at 750 nm against a reference solution using the colorimetric technique. The total phenol value was calculated as milligrams of gallic acid equivalents (mg GAE) per gram of FW.

2.8. Disease Analyses

Infected leaves were visually assessed for disease severity at 10, 13, 16, 19, and 23 days after inoculation (DAI), for substrate treatment, and at 10, 13, and 19 DAI, for seed treatment. The disease severity was then scored using a 1–5-degree scale [27], as shown in Table 1, and the average degree of infection per plant was determined by averaging the scales.

2.9. Statistical Analysis

The data were analyzed using STATISTICA 12 CZ software (StatSoft CR Ltd., Prague, Czech Republic). ANOVA analysis and the Fisher LSD test at probability level p = 0.05 were performed.

3. Results

3.1. Morphological and Physiological Parameters

Plant height and leaf number were evaluated as morphological characteristics, as shown in Table 2. Serendipita indica treatment enhanced plant height compared to that of the control in the substrate treatment (Figure 1). Additionally, S. indica improved the height in seed treatment, but not significantly. Under disease conditions, S. indica also increased the plant height relative to that of the control, which was significant in the substrate treatment, but insignificant in the seed treatment. In regard to leaf number, S. indica treatment showed an improvement leaf number, but not significantly.
Physiological parameters evaluated during the experiment included NDVI and Ft. As indicated in Table 2, NDVI was significantly higher in S. indica treated plants in both the substrate and seed treatment when compared to the control. Under stress, significantly higher NDVI values were observed in the substrate treatment compared to those of the control. However, in seed treatment, S. indica also reported positive results, but with no significant difference. Ft did not report significant differences among treatments, except for stress conditions in the substrate treatment, where S. indica improved Ft over that of the control. Moreover, as indicated in Table 2, S. indica also improved the nitrogen content in the substrate and seed treatment over that of the control H2O. Moreover, nitrogen content did not display any significant differences between treatments under disease conditions.

3.2. Effects of S. indica on Bio-Stress Parameters of Cabbage

To investigate the impact of S. indica on plants under biotic stress circumstances, biomarkers such as APX, GPX, TAC, and phenolics were examined. As indicated in Table 3, S. indica did not show any substantial differences in APX under regular or stressed substrate treatment. In the case of seed treatment, APX was significantly increased in S. indica-treated seedlings (SXcc + Sp), which were inoculated with the pathogen, as compared to control pathogen treatment (SXcc). Under normal conditions, however, there was no significant difference between the S. indica treated and the control seedlings.
As indicated in Table 3, GPX was significantly increased in both the substrate and seed treatments in response to inoculation with the pathogen over that noted in the control. However, in both treatments, the GPX was lower in S. indica treated seedlings under normal conditions over that of the control.
Regarding TAC, S. indica reported an improvement in TAC over that of the control in response to disease in the seed treatment (Ssp + Xcc). However, no significant difference was reported in either the substrate or seed treatments, as indicated in Table 3. Moreover, S. indica exhibited an increase in phenolics content in both the substrate and seed treatment over the control under stress conditions. However, S. indica did not improve the content of the phenolics over that in the control in either the substrate or the seed treatment under normal conditions, but the control substrate treatment showed a greater phenolics content under normal circumstances, as shown in Table 3. Therefore, this experiment confirmed an overall increase in biomarkers under stress conditions with S. indica inoculation in seed treatment, whereas only GPX and phenols were increased in the substrate treatment.

4. Disease Analyses

Disease analyses were performed ten days after inoculating the pathogen at different intervals, based on the degree of infection on the infected leave surface (Figure 1). Serendipita indica treatment reported significant control of black rot disease in the cabbage seedlings, in both the substrate and seed treatments, as the degree of infection was lower at the last evaluation. On a 5-point scale, the degree of contamination in the last investigation in the substrate (23 DAI) and seed treatment (16 DAI) for the S. indica treated plants was 2.95 and 3.41, while in the control, it was 3.91 and 4.12, respectively (Figure 2).

5. Root Colonization

Successful root colonization was confirmed by confocal microscopic observations in the S. indica treated seedlings, in both seed and substrate treatments. Spores and mycelium were observed in the roots of the cabbage seedlings, confirming the colonization of S. indica to the cabbage roots (Figure 3).

6. In Vitro Test

The results from in vitro testing revealed that S. indica did not limit the growth of Alternaria (Figure 4A) and Xanthomonas (Figure 4B), as no inhibition zones were formed between the pathogens and S. indica. Furthermore, Alternaria and Xanthomonas started to grow after three days and one day, respectively, and no antagonistic effect was observed after any readings.

7. Discussion

Serendipita indica, a novel endophytic fungus, is the subject of extensive research because of its advantageous traits, simple growing techniques, and broad host range [28]. According to the current study, S. indica has the potential to boost cabbage seedling growth and development, while also protecting them from the Xanthomonas campestris pv. campestris-caused black rot disease. The morphological, physiological, and nitrogen uptake indices were all improved by S. indica, which increased plant growth. In both healthy and diseased situations, treated seedlings showed an increase in plant height of 10.85% and 11.45% under substrate treatment. Even though seed treatments increased plant height, the effects were not statistically significant. These findings are in agreement with those found in Refs. [10,29,30,31], stating that plants treated with S. indica grew better and reduced the detrimental effect of pathogen on plant growth [14]. Additionally, the increase in plant height could be due to enhanced cell division and elongation, attributed to S. indica-induced auxin activity [29]. Other developmental traits of cabbage seedlings, such as NDVI and Ft, were similarly elicited by S. indica. These results were in agreement with those of Saleem et al. [10]. The enhancements in the growth and development of cabbage seedlings can be linked to several elements, including improved nutrient absorption, higher water intake, and the generation of phytohormones [32,33]. Furthermore, S. indica increases the number of additional growth factors, such as metabolite production, fatty acid, and TAC cycle activity, which leads to increased glucose generation, enhancing plant development [34]. In addition, administering S. indica to the seed treatment and the substrate under normal circumstances increased the nitrogen content. Similar results were reported by Refs. [2,30,35,36]. This increase in the nitrogen content by S. indica could be due to the improved activity of nitrate reductase and the expression of gene encoding nitrate reductase in colonized seedlings [2,37]. The application of S. indica therefore showcases the fungus’s ability to foster plant growth and development under controlled conditions, reducing the dependance on chemical fertilizers and addressing pressing environmental challenges.
The outcomes of our study also suggested that S. indica can be employed as a biocontrol agent for the cabbage disease, black rot. The endophytic fungus considerably lessened the pathogen Xanthomonas campestris-induced disease symptoms. These encouraging findings were consistent with other recent research that found that S. indica can promote resistance against various plant diseases [10,17,32,36]. As a result of the comprehensive data on S. indica’s effectiveness as a biocontrol agent against various diseases that have been generated over the years, it has been established that S. indica can exert direct and indirect approaches to induce inhibitory effects against root and leaf pathogens, respectively. In the case of root pathogen, S. indica employs antagonistic effect through its antioxidant activity, while inducing systemic resistance against leaf pathogens [33].
In the case of in vitro experiments, the lack of an inhibitory impact of S. indica against pathogens suggests that S. indica does not directly hinder the pathogen activity itself. Instead, these findings indicate that when applied to infected plants, this fungus regulates the plants’ defense mechanisms to improve their resilience against disease. Similar findings were presented by Cheng et al. and Li et al. [38,39]. Our findings, therefore, manifest the S. indica’s indirect defensive mechanism, whereby the fungus thrives in a host plant’s root system, while offering protection against the leaf pathogen. This impact could be attributed to S. indica’s ability to enhanced systemic resistance in plants under in vivo conditions [39].
In our research, we assessed the activity of several biochemical markers, such as APX, GPX, antioxidants, and phenolic content, to investigate their activity in cabbage seedlings under biotic stress, given that plants under stress are known to generate reactive oxygen species (ROS), resulting in the protection of plants against stress using hypersensitive response and programmed cell death [17]. Plants have a set of enzymatic and non-enzymatic antioxidants that, when altered under stressful circumstances, serve as indicators of excessive ROS generation, and they scavenge different ROS [40]. Beneficial fungi like S. indica may also trigger this process [17]. Our experiment found that the S. indica application as a seed treatment showed improved APX under disease conditions, whereas other treatments showed no significant change. Improvement in APX under disease conditions in S. indica-treated plants has been reported in several studies [17,38,41]. Similar patterns were also observed for GPX and TAC; GPX was improved in S. indica-colonized seedlings after substrate and seed treatment in response to disease. These findings were in accordance with those of Ref. [17]. However, GPX was lower under normal conditions in all S. indica treated compared to that of the control, which might be related to S. indica’s better plant growth and health. Under stress conditions, TAC was also improved when S. indica was applied to the seed, whereas TAC was not significantly different when applied to the substrate. Similar results were reported by Ref. [10]. Additionally, the phenolic concentration of S. indica seed and substrates treated under disease conditions was increased. Under normal substrate treatment, higher phenolic content was discovered in uninoculated seedlings, which might be due to the lower nitrogen content in the control. As explained by Ibrahim et al. and Rozy et al. [42,43], plants with lower amounts of nitrogen can enhance secondary metabolite biosynthesis and allocate more resources towards the production of phenolics in response to nutritional stress.
As a result of the comprehensive study, our findings revealed that S. indica colonization improved antioxidant enzyme activity, thereby strengthening the plant’s defense system against black rot disease. These results may be explained by the role of phenolic compounds and antioxidant enzymes, which are involved in scavenging excessive ROS production in stressed plants [38]. The elimination of free radicals and their function as antipathogen defense enzymes are reportedly accomplished by APX and GPX [17,38]. Additionally, GPX is involved in improving plant metabolites required for producing lignin and other structural barriers, ceasing pathogen spread in plants [17]. In addition, by decreasing oxidative stress, phenolics are recognized as essential elements that help to combat plant diseases and strengthen plant defense [44]. Their structure confers substantial antioxidant activity and the ability to neutralize ROS, mitigating biotic stress [45]. Besides observing bio stress markers, our study also evaluated the degree of black rot infection in cabbage seedlings. The application of S. indica to cabbage seedlings suppressed the onset of black rot symptoms. It reduced the infection, which was 27.9% lower in substrate treatment and 18.8% lower in seed treatment than in non-treated seedlings. As our study shows, this result might be due to elevated antioxidant and phenolic content in the treated seedlings. By squelching the production of reactive oxygen species and offering defense against microbial attack, these enzymes and phenolics tend to reduce infection. These results were in agreement with those of Refs. [17,46], supporting the ability of S. indica to scavenge free radicles by modulating the activities of different antioxidative enzymes. Therefore, this research has explored the potential application of S. indica in cabbage to help plants thrive under stress conditions and further broaden its spectrum of disease management, i.e., resistance against black rot in cabbage.
Additionally, the molecular basis of resistance by S. indica has been reported in different studies, including the upregulation of defense-related genes, such as senescence-associated genes, genes encoding cytochrome P450, Delta (12) oleic acid desaturase FAD2, and calcium-dependent protein kinases (CDPKs), and several Lipoxygenase (LOX) genes coding for AcLOX1 and AcLOX2 lipoxygenases, critical for regulating salicylic acid (SA)/jasmonic acid (JA) signaling pathways, and subsequently, for induced systemic resistance [17,46,47]. Furthermore, the upregulation of WRKY genes on S. indica colonization, involved in the regulation of pathogenesis-related (PR) gene expression, favoring the defense response against various pathogens has been reported by Refs. [17,39].
Consequently, the findings of our research lend credence to earlier accounts that the endophytic fungus S. indica functions as a promising biocontrol agent and an efficient plant growth regulator, when examined under a sterile and controlled environment. Nevertheless, S. indica’s impact on host crops under open conditions requires further investigation to provide valuable insights supporting our promising findings.

8. Conclusions

This study demonstrated that S. indica could colonize cabbage roots and generate beneficial interactions when applied to both seeds and the root zone under sterile conditions. This endophytic fungus aided in the growth and development of plants both under typical circumstances and during biotic stress. Additionally, this fungus promoted the growth of cabbage seedlings, in addition to controlling black rot disease, one of the most damaging diseases of crucifers. This work thus supports the potential use of S. indica as a growth stimulant and a biocontrol agent under controlled conditions.

Author Contributions

Conceptualization, R.P. and S.S.; methodology, R.P., S.S., L.N.R., M.F. and D.T.; software, R.P. and S.S.; validation, R.P.; formal analysis, R.P.; investigation, S.S. and R.P.; resources, S.S. and R.P.; data curation, S.S. and L.N.R.; writing—original draft preparation, S.S.; writing—review and editing, S.S. and R.P.; visualization, R.P., S.S., L.N.R., A.S. and D.T.; supervision, R.P. and A.S.; project administration, R.P.; funding acquisition, R.P. All authors have read and agreed to the published version of the manuscript.

Funding

This study was supported by the project of the Internal Grant Agency of Mendel University in Brno, IGA-ZF/2023-SI1-005. Microscopic analyses were carried out on infrastructure supported by project OP VVV CZ.02.1.01/0.0/0.0/16_017/0002334, and research infrastructure for young scientists, financed from structural funds of EU and Ministry of Education of the Czech Republic.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

All relevant data are contained within the manuscript.

Acknowledgments

The authors are thankful to Sarka Frankova and Marcela Horinkova for providing help with sample preparation and microscopy.

Conflicts of Interest

The authors declare no conflict of interest.

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Agriculture 13 02048 g001
Figure 1. (a) Effect of S. indica colonization on growth of cabbage seedling. (b) Xanthomonas campestris pv. campestris infected leaf of cabbage seedling without S. indica inoculation; (c) with S. indica inoculation.
Figure 1. (a) Effect of S. indica colonization on growth of cabbage seedling. (b) Xanthomonas campestris pv. campestris infected leaf of cabbage seedling without S. indica inoculation; (c) with S. indica inoculation.
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Agriculture 13 02048 g002
Figure 2. Effects of S. indica on black rot of cabbage leaves, as measured on a 5-degree scale at different intervals. (A) substrate treatment; (B) seed treatment. * Indicates a significant difference.
Figure 2. Effects of S. indica on black rot of cabbage leaves, as measured on a 5-degree scale at different intervals. (A) substrate treatment; (B) seed treatment. * Indicates a significant difference.
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Agriculture 13 02048 g003
Figure 3. Cabbage roots with S. indica colonization under confocal microscope. (a) Typical chlamydospores of S. indica. (b) Mycelium of S. indica covering cabbage roots. White and blue arrows represent spores and mycelium of S. indica, with a scale bar of 20 μm and 50 μm, respectively.
Figure 3. Cabbage roots with S. indica colonization under confocal microscope. (a) Typical chlamydospores of S. indica. (b) Mycelium of S. indica covering cabbage roots. White and blue arrows represent spores and mycelium of S. indica, with a scale bar of 20 μm and 50 μm, respectively.
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Agriculture 13 02048 g004
Figure 4. (A) Effect of S. indica on growth of Alternaria brassicicola. (a) Control culture of S. indica. (b) Control culture of A. brassicicola. (c–e) Dual culture of S. indica and A. brassicicola 3, 6, and 9 DAI. (B) Effect of S. indica on growth of X. campestris. (a) Dual culture of S. indica and X. campestris 1, 2, and 3 DAI.
Figure 4. (A) Effect of S. indica on growth of Alternaria brassicicola. (a) Control culture of S. indica. (b) Control culture of A. brassicicola. (c–e) Dual culture of S. indica and A. brassicicola 3, 6, and 9 DAI. (B) Effect of S. indica on growth of X. campestris. (a) Dual culture of S. indica and X. campestris 1, 2, and 3 DAI.
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Table 1. Table of 5-degree scale.
Table 1. Table of 5-degree scale.
Degree of infection12345
Affected surface0%10–24%25–50%51–75%>75%
Table 2. Effects if S. indica on the morphological and physiological parameters of cabbage.
Table 2. Effects if S. indica on the morphological and physiological parameters of cabbage.
TreatmentPlant Height (mm)Leaf NumberNDVIFtNitrogen %
Substrate treatment
Sp193.91 (±4.35) a8.91 (±0.24) a0.64 (±0.003) a0.83 (±0.003) a4.71 (±0.15) a
C-H2O174.92 (±3.47) b8.37 (±0.26) ab0.61 (±0.005) b0.83 (±0.001) a4.08 (±0.10) c
Sp + Xcc202.76 (±1.83) a7.79 ( ±0.24) bc0.63 (±0.003) a0.82 (±0.002) b4.33 (±0.07) bc
Xcc181.92 (±2.67) b7.62 (±0.18) c0.59 (±0.007) c0.80 (±0.006) c4.57 (±0.11) ab
Seed treatment
Ssp200.00 (±3.85) bc7.25 (±0.14) a0.63 (±0.004) a0.82 (±0.001) a6.17 (±0.08) a
SH2O191.72 (±3.08) c7.08 (±0.19) a0.60 (±0.004) c0.81 (±0.001) a5.66 (±0.09) b
Ssp + Xcc213.81 (±4.43) a6.41 (±0.18) b0.63 (±0.002) ab0.82 (±0.003) a5.03 (±0.09) c
SXcc203.48 (±5.11) ab6.33 (±0.34) b0.62 (±0.002) b0.81 (±0.002) a5.03 (±0.09) c
Sp—Serendipita indica; C-H2O—control water; Xcc—Xanthomonas campestris; Ssp—seed application of Serendipita indica; SH2O—seed application of water; SXcc—seed application of Xanthomonas campestris. The mean values denoted by different letters show significantly significant differences. The standard error values are presented after the means.
Table 3. Effects if S. indica on the bio-stress parameters of cabbage.
Table 3. Effects if S. indica on the bio-stress parameters of cabbage.
TreatmentAPX (μmol min−1 g−1 FM)GPX (μmol/tetraguaiacol min−1 g−1)TAC (mML−1)Phenols (mg GAE g−1 FM)
Substrate treatment
Sp0.49 (±0.01) a9.66 (±0.47) b2.12 (± 0.06) a29.79 (±0.17) d
C-H2O0.50 (±0.04) a10.98 (±0.03) a1.70 (±0.15) a40.96 (±0.55) a
Sp + Xcc0.44 (±0.01) a9.68 (±0.09) b2.53 (± 0.26) a36.49 (±0.23) b
Xcc0.52 (±0.03) a8.32 (±0.25) c2.17 (± 0.17) a31.57 (±0.11) c
Seed treatment
Ssp0.39 (±0.01) b4.86 (±0.01) c2.11 (± 0.13) a29.00 (±1.01) a
SH2O0.41 (±0.03) ab9.28 (±0.09) a2.34 (± 0.15) a29.21 (±0.08) a
Ssp + Xcc0.49 (±0.03) a9.51 (±0.05) a2.65 ( ±0.13) a29.41 (±0.34) a
SXcc0.29 (±0.03) c7.33 (±0.09) b2.07 (±0.10) b27.20 (±0.52) b
Sp—Serendipita indica; C-H2O—control water; Xcc—Xanthomonas campestris; Ssp—seed application of Serendipita indica; SH2O—seed application of water; SXcc—seed application of Xanthomonas campestris; TAC—total antioxidant capacity; GPX—guaiacol peroxidase; APX—ascorbate peroxidase. The mean values denoted by different letters show significantly significant differences. The standard error values are presented after the means.
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Saleem, S.; Ragasova, L.N.; Tekielska, D.; Fidurski, M.; Sekara, A.; Pokluda, R. Serendipita indica as a Plant Growth Promoter and Biocontrol Agent against Black Rot Disease in Cabbage Grown in a Phytotron. Agriculture 2023, 13, 2048. https://doi.org/10.3390/agriculture13112048

AMA Style

Saleem S, Ragasova LN, Tekielska D, Fidurski M, Sekara A, Pokluda R. Serendipita indica as a Plant Growth Promoter and Biocontrol Agent against Black Rot Disease in Cabbage Grown in a Phytotron. Agriculture. 2023; 13(11):2048. https://doi.org/10.3390/agriculture13112048

Chicago/Turabian Style

Saleem, Sana, Lucia Nedorost Ragasova, Dorota Tekielska, Maciej Fidurski, Agnieszka Sekara, and Robert Pokluda. 2023. "Serendipita indica as a Plant Growth Promoter and Biocontrol Agent against Black Rot Disease in Cabbage Grown in a Phytotron" Agriculture 13, no. 11: 2048. https://doi.org/10.3390/agriculture13112048

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