Defense responses of tomato plants grown in substrate amended with mushrooms for the control of Meloidogyne javanica

ABSTRACT

Root-knot, caused by Meloidogyne javanica, is a serious disease on tomato. This study aimed to investigate the potential of using Lentinula edodes and Pleurotus eryngii to boost the resistance of tomato roots against infection by M. javanica. Tomato plants were grown in different conditions: substrate made of a mixture of soil with sand (SS) and infested with M. javanica; substrate made of a mixture of SS with mushroom (SSM) and colonized by L. edodes; SSM colonized by L. edodes and infested with M. javanica; SSM colonized by P. eryngii; and SSM colonized by P. eryngii and infested with M. javanica. Root samples were examined at 0, 4, 10, and 20 days after growing the tomato plants to determine the fresh weight of roots, activities of phenylalanine ammonia-lyase (PAL), chitinase (CHI), and β-1,3-glucanase (GLU), as well as the concentration of phenolics. There was no significant difference in PAL activity nor in the concentration of phenolics regardless of treatments and sampling time. Activities of CHI and GLU were greater for plants grown on SSM colonized by either L. edodes or P. eryngii regardless of the presence of M. javanica. Mushroom substrates enhance tomato plant defenses against root-knot nematodes by increasing CHI and GLU activities, suggesting potential for both direct antagonistic effects and indirect stimulation of plant resistance mechanisms.

Key words
alternative disease control; defense-related enzymes; host defense reactions; induced resistance

INTRODUCTION

Tomato (Solanum lycopersicum L.) is a common crop in tropical and subtropical regions. In 2022, 4.9 million hectares of tomato were cultivated worldwide and produced 186.1 million tons of fruits (FAO 2024). However, one of the factors that contribute to the reduction in tomato yield is the occurrence of diseases, mainly those caused by nematodes belonging to the genus Meloidogyne, with the species M. javanica, M. incognita, M. hapla, and M. arenaria considered the most important ones (Brito et al. 2020).

Nematode management is important for reducing yield losses in tomato. However, such management is complex, because it depends on the integration of control measures to reduce the population of nematodes in the soil (Shilpa et al. 2022). Among the available measures, biological control using nematophagous fungi has gaining great importance, since they are able to prey and parasitize fungal structures and produce nematicidal metabolites (Castañeda-Ramírez et al. 2020, Rahman et al. 2023). A total of 185 species of nematophagous fungi with potential to affect the infection process of Meloidogyne spp. have been reported (Hahn et al. 2018). Among these species showing nematicidal potential, mushrooms stand out for having several medicinal properties (e.g., antitumor, antimutagenic, antidiabetic, anti-inflammatory, antibacterial, antifungal, antiviral, and antithrombotic) (Castañeda-Ramírez et al. 2020) stimulating, therefore, worldwide research regarding their nematicidal potential.

Mushrooms cultivated in Brazil has the potential for the control of root-knot as demonstrated by Hahn et al. (2019) in in-vitro tests proving nematicidal potential of Lentinula edodes and Pleurotus eryngii to control M. javanica. These results indicated the direct effect of mushrooms against the nematodes due to the production of nematicidal metabolites or predatory activity against M. javanica. Other authors have also observed a direct effect of L. edodes and P. eryngii against M. javanica (Sufiate et al. 2017) and Bursaphelenchus xylophilus (Ishizaki et al. 2015). The efficacy of the mushrooms in controlling the root-knot nematode found in vitro was also confirmed under in planta conditions. The amendment of soil with L. edodes or P. eryngii affects the infection process of M. javanica in tomato plants (Hahn et al. 2025). However, information indicating that this effect originated only from their direct incorporation in the soil or whether there was also an indirect effect through inducing the plants to react against the nematodes through mechanisms of defense need to be determined. Induced resistance can be an effective control measure to reduce the intensity of diseases on different crops. Mushrooms have already been studied to control bacterial (Aguiar et al. 2020) and fungal (Nishimura et al. 2021) diseases by inducing the resistance of plants.

Potential of mushrooms to promote biochemical changes in tomato plants lead this study to investigate the potential of using the L. edodes and P. eryngii to boost the resistance of tomato roots against infection by M. javanica.

METHODS

Tomato seeds (cultivar “Santa Clara”) were sown in 128-cell polystyrene trays containing commercial organic compost (Horta 3, Mecplant, Telêmaco Borba, PR, Brazil) and vermiculite (60% of water holding capacity, Brasil Minérios, São Luís de Montes Belos, GO, Brazil) at the ratio of 1:1 (v/v). The trays were kept in a greenhouse (relative humidity higher than 60% and temperature ranging from 14 to 32°C), and sprinkler irrigation was applied as needed. Seedlings in each pot were fertilized (50 mL per pot) with commercial nutrient solution (Plantpar Tomate, Plantpar, Umuarama, PR, Brazil) every five days.

Two commercial isolates of mushrooms belonging to the species L. edodes (LEMID-Led01) and P. eryngii (LEMID-Per01) were previously selected considering their potential to control M. javanica (Hahn et al. 2019). The substrate for growing these mushrooms was composed of coarse sawdust, wheat bran (140 g·kg^-1 of protein, Anaconda, Curitiba, PR, Brazil), agricultural dolomitic limestone (effective calcium carbonate equivalent of 90.1%, Solo Branco, Almirante Tamandaré, PR, Brazil), and gypsum (AM60, AM Gesso, Araripina, PE, Brazil) in the proportion of 88:10:1:1 (v/v). The mushroom was mixed by hands and packed in 30 × 45-cm polypropylene bags that were closed with foam stoppers and tied up with latex rubber bands. The packed mixture of mushroom was autoclaved (121°C for 1 h) and cooled in a laminar flow chamber for 12 h. The infestation of mushroom mixture was performed by adding 7 g of potato-dextrose-agar medium to Petri dishes (90 mm in diameter), and 14-day-old mycelia was placed on the top of each bag. The infested mixture of mushroom was incubated at room temperature for 120 days in the dark. The population of M. javanica was multiplied on tomato plants (cultivar “Santa Clara”) under greenhouse conditions. Nematodes were extracted from the tomato roots, and the suspension of eggs was collected in a 200-mesh sieve over a 500-mesh sieve (Hahn et al. 2019, Hahn et al. 2025).

Polystyrene cups (180 mL) with a hole in their bottoms were prepared 30 days after seedlings emergence for each treatment without the presence of nematode. The polystyrene cups for each treatment were incubated for 15 days in a growth chamber with temperature of 25°C, 12-h photoperiod, and relative humidity greater than 70%. The mixture was irrigated every two days. At 45 days after seedlings emergence, a 4-cm deep cavity was opened in the substrate using a 50-mL Falcon tube, and one tomato seedling was placed in the center of each polystyrene cup. Soon after transplanting the seedlings, a 2-cm deep cavity was opened with the help of a 2-mL conical microtube near to the roots of plants in polystyrene cups that corresponded to the treatments containing the inoculation with M. javanica. A total of 500 μL of eggs suspension (≈1,000 eggs and possible juveniles) was deposited into each cavity. Plants were kept inside of a growth chamber at 25°C, photoperiod of 12 h, and relative humidity of approximately 70%. During the experiment, plants were fertilized with a nutrient solution mentioned above with half concentration of nutrients and watered as needed.

A 5 × 4-factorial experiment was carried out in a completely randomized design with five treatments and three replications for each sampling time. The treatments used were as follows:

• Substrate made of a mixture of soil with sand (SS) and infested with M. javanica;

• Substrate made of a mixture of SS with mushroom (SSM) and colonized by L. edodes;

• SSM colonized by L. edodes and infested with M. javanica;

• SSM colonized by P. eryngii;

• SSM colonized by P. eryngii and infested with M. javanica.

A polystyrene cup containing one tomato plant corresponded to one replication. The experiment was repeated once.

Seedlings were collected at 0 (before infestation of substrate with the nematode), 4, 10, and 20 days after inoculation, and their roots were washed under tap water with the excess removed using paper towel. From each plant, stem was separate from leaves. The height of each plant, from base to top, was obtained. The roots were fragmented into pieces of 2 cm long. The gall index in the roots was classified as follows:

• 0: no galls or egg mass;

• 1: one or two galls or egg masses;

• 2: from three to 10 galls;

• 3: from 11 to 30 galls;

• 4: from 31 to 100 galls;

• 5: more than 100 galls.

Nematodes inside of 0.1 g of roots was quantified according to Gabriel et al. (2024). Roots (0.1 g) were collected after nematodes quantification in the roots, and stem and leaves of each plant were individually placed in aluminum foil using liquid nitrogen and then stored at -20°C until the biochemical analysis.

The plant extract was obtained by macerating 0.2 g of plant material in a previously chilled mortar containing 0.1 g of glass microspheres, 0.1 g of Dowex 1-X8 resin, 0.1 g of polyvinylpolypyrrolidone, and 4 mL of sodium borate buffer (0.1 M and pH 8.8) containing ethylenediaminetetraacetic acid (EDTA) (1 mM) bisodic, and ascorbic acid (50 mM). The fine powder was centrifuged at 13,500 g at 4°C for 30 min. A volume of 1,200 μL of the supernatant was collected, stored in a 2-mL microtube, and frozen at -20°C. The concentration of protein in each sample was determined using the Bradford’s method (Adamuchio-Oliveira et al. 2020). Activity of chitinase (CHI) was determined by colorimetric quantification of chitin hydrolysis (Adamuchio-Oliveira et al. 2020). A total of 400 µL of protein extract was diluted in 500 µL of sodium phosphate buffer (0.2 M) and 100 mg of substrate for CHI. The extract was vortexed and incubated at 50°C for 1 h. The enzymatic reaction was stopped by boiling the mixture in water bath for 5 min. The extract was centrifuged at 7,000 g for 10 min. The absorbance was read at 595 nm in a spectrophotometer. Activity of β-1,3-glucanase (GLU) was determined by colorimetric quantification of β-1,3-glucan hydrolysis (Adamuchio-Oliveira et al. 2020). A total of 200 µL of protein extract was diluted in 400 µL of sodium acetate buffer (50 mM and pH 5) and 200 µL of enzyme-substrate (CM-Curdlan-RBB; 4 mg/mL). The extract was vortexed and incubated at 40°C for 2 h. The enzymatic reaction was stopped by adding 200 µL of hydrochloric acid (HCl) (2 N) and cooled in an ice bath for 10 min. The extract was centrifuged at 10,000 g for 5 min. The absorbance was read at 600 nm in a spectrophotometer.

The activity of GLU was determined using a glucose standard curve. Activity of phenylalanine ammonia-lyase (PAL) was performed by the absorbance difference resulting from the conversion of phenylalanine to trans-cinnamic acid (Adamuchio-Oliveira et al. 2020). A total of 0.2 g of plant material was macerated in a previously chilled mortar with 4 mL of Tris-HCl buffer (pH 8). The extraction buffer was prepared with a mixture of 22.2 g of Tris, 0.37 g of EDTA, 85.5 g of sucrose, and 10 g of polyvinylpyrrolidone (PVP) in a final volume of 1 L of distilled water. The pH was adjusted to 8 with HCl 2 N. The fine powder was centrifuged at 6,000 g for 10 min at 4°C. A total of 200 μL from the supernatant was transferred to 15-mL microcentrifuge tube added with 5 mL of the extraction buffer. The extract was vortexed, and a 1.5-mL aliquot of the extract was transferred to a new microcentrifuge tube plus 1 mL of the extraction buffer and 0.5 mL of phenylalanine (49.6 mg·mL^-1) before being vortexed again. The solution was incubated in a water bath for 1 h at 40°C. After incubation, the tubes were transferred to an ice bath to stop the enzymatic reaction. The absorbance was read at 290 nm in a spectrophotometer. The PAL activity was estimated using a standard curve of trans-cinnamic acid.

The Folin-Ciocalteu method was used to determine the concentration of soluble phenolics (Adamuchio-Oliveira et al. 2020). A total of 0.2 g of plant material was macerated in a mortar with 5 mL of extraction solution. The extraction solution was prepared using methanol, chloroform, and water in the ratio of 12:5:3 v/v. The macerated material was centrifuged at 6,000 g at 20°C for 20 min. A 500-μL aliquot of the supernatant was transferred to 15-mL microcentrifuge tubes plus 500 μL of distilled water and 500 μL of Folin-Ciocalteu reagent diluted in distilled water (1:10 v/v). The extract was vortexed and, after 15 min, 5 mL of alkaline reagent A (2% sodium carbonate in 0.1 N sodium hydroxide solution) was added. The solution was vortexed and incubated for 50 min. The absorbance was measured at 760 nm in a spectrophotometer.

The area under the progress curve (AUPC) was obtained for plant height, fresh weights of stem and leaves, roots, number of galls, number of nematodes, activities of CHI, GLU, and PAL, as well as concentration of soluble phenolics for each treatment during the time course evaluated. For the AUPC data, analysis of variance (ANOVA) was performed for trials 1 and 2. Since the mean square of the residue showed a ratio of less than 7:1 between the repetitions of the trials, a joint analysis was carried out with the repetitions of the two trials (Banzatto and Kronka 2013). Considering that the analysis did not meet the assumptions and there were many zeros, all responses were added a constant of 0.001. The box-cox transformation parameters were checked. Subsequently, ANOVA was performed, and treatment means were compared using the Tukey’s test at 5% of probability. Statistical analyses were performed using the R software.

RESULTS AND DISCUSSION

There was no significant difference for AUPC of plant height, fresh weight of stem, fresh weight of leaves, gall index (Table 1), PAL activity, and soluble phenolics concentration on roots and stem and leaves (Table 2). The number of nematodes in the roots was significantly lower by 54% for plants grown in the SSM mixture amended only with L. edodes compared to plants grown in the SS and infested with M. javanica (Table 1). The AUPC of GLU activity in the roots was not significant among the treatments (Table 2). For stem and leaves, the AUPC of GLU activity was significantly higher by 21% for plants grown in the mixture SSM amended only with L. edodes compared to plants grown in the SS and infested with M. javanica. The AUPC of CHI activity in stem and leaves for plants grown in the SSM mixture amended with L. edodes or P. eryngii in the absence or presence of M. javanica was significantly higher by 22 and 32% compared to plants grown in the SS mixture infested with M. javanica (Table 2). The AUPC for CHI activity in roots was significantly higher by 42 and 41% for plants from treatments SSM mixture containing P. eryngii in the absence or presence of M. javanica, respectively, compared to plants grown in the SS mixture infested with M. javanica (Table 2). There was no significant difference between the treatments SSM amended with L. edodes in the absence or presence of M. javanica for AUPC of CHI activity. The amendment of SSM substrate with either L. edodes or P. eryngii did not result in increased AUPC of PAL activity and AUPC of soluble phenolics concentration in the roots, stem, and leaves. However, the treatments affected the AUPC for CHI and GLU.

Table 1
Area under the progress curve for plant height, fresh weight of stem and leaves, fresh weight of roots, gall index, and number of nematodes in the roots of tomato plants that were submitted to different treatments*.

Treatments | Species	Plant height	Fresh weight		Gall index	Number of nematodes
		Stem and leaves	Roots
Meloidogyne javanica	405.0a	69.7a	14.9a	37.7a	1,001.0a
Lentinula edodes	407.5a	72.1a	13.8ab	-	-
M. javanica + L. edodes	387.3a	70.0a	14.8a	29.7a	463.0b
Pleurotus eryngii	403.1a	69.7a	13.1b	-	-
M. javanica + P. eryngii	414.8a	67.8a	12.8b	38.0a	848.0a

• ^*
  Means for each variable following by the same letter, within each column, are not significantly different (p ≥ 0.05) according to Tukey’s test.w

Table 2
Area under the progress curve for the activities of phenyalanine ammonia-lyase (PAL), β-1,3-glucanase (GLU) and chitinase (CHI), as well as the concentration of soluble phenolics (SP) on the stem and leaves and roots of tomato plants that were submitted to different treatments*.

Treatments | Species	PAL	GLU	CHI	SP
	Steam and leaves
Meloidogyne javanica	0.03a	0.29a	7.71b	20.80a
Lentinula edodes	0.02a	0.35b	9.56a	21.31a
M. javanica + L. edodes	0.03a	0.33ab	9.42a	18.22a
Pleurotus eryngii	0.02a	0.33ab	10.15a	21.27a
M. javanica + P. eryngii	0.02a	0.32ab	9.58a	21.59a
	Roots
M. javanica	0.05a	0.40a	9.16b	5.55a
L. edodes	0.05a	0.43a	12.60ab	6.59a
M. javanica + L. edodes	0.05a	0.50a	12.06ab	5.37a
P. eryngii	0.06a	0.51a	12.99a	6.97a
M. javanica + P. eryngii	0.06a	0.46a	12.95a	6.52a

• ^*
  Means followed by the same letter, within each column, are not significantly different (p ≥ 0.05) according to Tukey’s test.

Based on the results from the present study, it is plausible to postulate that the effectiveness of mushrooms in controlling the root-knot nematode can be linked to their direct effect against them through the production of nematicidal toxins or predatory activity of the mushroom hyphae, as reported by Hahn et al. (2019), and possibly to an indirect effect by boosting the activities of CHI and GLU. Tomato plants grown in SSM substrate did not show an increase in PAL activity in their roots, stems, or leaves. The PAL is important for an effective activation of the phenylpropanoid pathway that produces phenolics, flavonoids, and lignin being some of these secondary metabolites acting both indirectly or directly in plant defense mechanisms against pathogens (Zaynab et al. 2018). Consequently, the lack of an increase in PAL activity did not result in greater concentration of phenolics among the treatments. Phenolics play an important role in the resistance of banana plants against Radopholus similis (Dhakshinamoorthy et al. 2014). The use of the nematophagous fungus Pochonia chlamydosporia in tomato plants infested with M. javanica (Medeiros et al. 2015) and the yeast Lachancea thermotolerans to soybean plants infested with M. incognita (Mioranza et al. 2021) did not result in a significant increase in PAL activity.

The increase in GLU activity in tomato plants grown on MS colonized with P. eryngii or L. edodes can be the result of the presence of glucan, a polysaccharide commonly produced by these mushrooms (Avni et al. 2017, Bak et al. 2014). The GLU hydrolyze the β-1,3-D-glycosidic bonds that is the main component of fungal cell walls (Hong et al. 2002). Consequently, GLU hydrolyzes the β-1,3-glucan in the cell wall of fungi helping to reduce the colonization of plant tissues by fungi (Singh and Singh 2018). The increase in CHI activity may be favored by the presence of chitin in the mushroom considering that it can represent between 7 and 36% of the total dietary fiber of edible mushrooms (Boureghda et al. 2021) and is also a major component of nematodes (Chen et al. 2015). However, the presence of the nematode was not important to boost tomato defense reactions considering that chitin from mushroom is able to be recognized by the plant. The CHI can help to reduce the population of nematodes by degrading the chitin present in their cuticle (Lee et al. 2014). In this regard, transgenic plants accumulate chitinases that can inhibit the development of nematodes (Chan et al. 2015). The highest CHI activity was observed in tomato plants treated with Pseudomonas fluorescens Pf 128, which reduced the penetration by the nematodes in the roots of tomato plants (Sankari et al. 2010).

In the present study, the different substrates were incorporated into the soil and closer contact with the nematode. However, the increased CHI and GLU activities in the stem and leaves of tomato plants, away from a direct contact with the substrates, indicated a possible increase in host resistance. Similar results were observed with the amendment of soil with mushroom substrate colonized by Lyophyllum decastes for the control of anthracnose (Colletotrichum orbiculare) in the stem and leaves of cucumber plants (Parada et al. 2011).

CONCLUSION

The results of the present study highlighted the potential of using the mushroom substrates to enhance the defenses of tomato roots against infection by M. javanica due to an increase in CHI and GLU activities, besides displaying a direct antagonistic effect against this nematode. On top of that, the performance of mushroom substrate at different agricultural systems deserves further investigation considering that the decomposition of this substrate may favor the development of antagonistics in the soil, in addition to the mushroom itself that may reduce the nematode population. The economic efficiency of nematode control using substrate of mushroom is also an interesting topic to be checked in the next studies.

ACKNOWLEDGMENTS

The authors would like to thank the Academic Publishing Advisory Center (Centro de Assessoria de Publicação Acadêmica) of the Universidade Federal do Paraná (UFPR) for assistance with English language translation and developmental editing.

• How to cite: Hahn, M. H., Silva, M. C. C., Rocha, M. G. C., Quadros, L. P., Rodrigues, F. A., May De Mio, L. L., Russiano, M. C. S., Mazaro, S. M. and Duarte, H. S. S. (2025). Defense responses of tomato plants grown in substrate amended with mushrooms for the control of Meloidogyne javanica. Bragantia, 84, e20240287. https://doi.org/10.1590/1678-4499.20240287
• FUNDING
  Coordenação de Aperfeiçoamento de Pessoal de Nível Superior
  Finance Code 001
  Conselho Nacional de Desenvolvimento Científico e Tecnológico
  Grant No.: 306647/2021-4

DATA AVAILABILITY STATEMENT

The data that support the findings of this study are available from the corresponding author upon reasonable request.

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Edited by

• Section Editor:
  Gabriel Constantino Blain https://orcid.org/0000-0001-8832-7734

Publication Dates

• Publication in this collection
  03 Mar 2025
• Date of issue
  2025

History

• Received
  09 Dec 2024
• Accepted
  09 Jan 2025