Control of Meloidogyne javanica with Pleurotus djamor spent mushroom substrate

doi:10.21203/rs.3.rs-2114638/v1

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Control of Meloidogyne javanica with Pleurotus djamor spent mushroom substrate

https://doi.org/10.21203/rs.3.rs-2114638/v1

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Background

The interest in the development of ecologically correct products associated with the loss of efficiency of chemical nematicides for the control management of this pest is growing. Thus, the adoption of biological control or the use of biopesticides are excellent options for these products. Spent mushroom substrate (SMS), a product of the mushroom production industry, has great potential for biological control due to its high levels of mycelium, residual enzymes, high humidity and unique microbiota that may contain other nematode antagonists. For this reason, this study aimed to evaluate the potential of spent mushroom substrate (SMS) from Pleurotus djamor cultivation in the control of Meloidogyne javanica in lettuce and assess its effects on plant resistance enzymes and soil biological activity.

Results

SMS reduced nematode reproduction, and a plateau was reached at SMS concentrations above 15%. Higher concentrations of SMS caused phytotoxicity in lettuce, with reduction of vegetative variables, chlorophyll content and nitrogen balance in the leaves; however, SMS increases the anthocyanin content. Guaiacol peroxidase activity was highest in treatments containing 0% and 30% SMS and phenylalanine ammonia-lyase activity was highest in the 60% SMS treatment, suggesting induction of resistance to M. javanica. The maximum soil basal respiration was estimated to be achieved with 25.75% SMS, whereas the maximum soil metabolic quotient was estimated to be achieved with 8.8% SMS. Soil biomass carbon increased with increasing SMS proportion.

Conclusions

Spent substrate from P. djamor cultivation incorporated in soil at proportions of 15, 30, 45 e 60% is efficient in controlling M. javanica in lettuce.

root-knot nematode

nematophagous fungi

biological control

edible mushrooms

agro-industrial waste

The global edible mushroom market is estimated at US$16.7 billion and projected to reach US$20.4 billion by 2025 (Fortune 2020). In Brazil, predictions indicate a growth in mushroom production and consumption as a reflection of globalization and the consequent cultural interconnection, including cultural exchange of cooking habits and a focus on healthier and more functional foods (Martínez-Ibarra 2019). In most Western countries, a large part of mushroom production is still carried out under rustic conditions by small rural producers, who combine fungiculture with other agricultural activities (Machado 2019).

Mushrooms can be grown on different substrates, such as wood, industrial waste, fruit pulp and peel, banana leaves, coffee pulp (Paim et al. 2010; Saad et al. 2017), and grasses (Okorie et al. 2011; Oseni et al. 2012), often combined with nitrogen or protein sources to maintain an adequate carbon/nitrogen (C/N) ratio (Montessi et al. 2016). Examples of nitrogen and protein sources include plant and oilseed meals (such as from soybean, cotton, sunflower, wheat, and maize), rice straw, sugarcane bagasse, juice waste, and wine waste (Baysal et al. 2003; Bernardi et al. 2008). After a given number of cycles, which may vary according to fungal species and growing medium, the substrate used for mushroom production has to be changed, generating a residue commonly known as spent mushroom substrate (SMS). SMS can be used as animal feed (Schmidt et al. 2003) as well as for bioremediation and organic fertilization (Ribas et al. 2009). An interesting characteristic is that some cultivated mushrooms have nematophagous activity, holding potential in the control of soil nematodes (Aslam 2013; Heydari et al. 2006; Okorie et al. 2011).

Several members of the mushroom genus Pleurotus have been reported to interact with nematodes, such as P. cornucopiae (Heydari et al. 2006; Thorn and Barron 1984), P. cystidiosus (Thorn and Barron 1984), P. florida (Heydari et al. 2006), P. ostreatus (Thorn and Barron 1984; Heydari et al. 2006; Okorie et al. 2011), P. sajor-caju (Heydari et al. 2006), P. strigosus, P. subareolatus (Thorn and Barron 1984), and P. tuber-regium (Hibbett and Thorn 1994; Okorie et al. 2011). Some species can act as predators of plant-parasitic nematodes (Thorn and Barron 1984), extending their hyphae and paralyzing these phytoparasites through secretion of toxins, such as ostreatins, or production of toxin-containing structures known as toxocysts (Barron and Thorn 1987; Clémençon et al. 2004; Hibbett and Thorn 1994). Of note, information on interactions between nematodes and Pleurotus djamor is scarce.

In addition to controlling nematodes, SMS can be used to improve soil microbiological quality and increase organic matter and mineral availability, stimulating plant development (Gobbi et al. 2015). Furthermore, studies suggest that SMS amendment may induce plant resistance against pathogens, owing to the presence of secondary metabolites and toxic fungal structures (Askary and Martinelli 2015; Sandoval et al. 2020). It should be noted that large-scale use of SMS in agriculture may be limited by the low availability of this waste material. However, it may be feasible to apply SMS as substrate for vegetable seedling production, as this activity requires low amounts of material. An interesting advantage of such use is that, at the time of planting in the field, seedlings would have been pre-exposed to fungi and their metabolites.

In view of the above, it is hypothesized that spent substrate from P. djamor cultivation may be able to control nematodes and activate natural defense mechanisms in plants. This study aimed to assess the potential of P. djamor SMS in the control of Meloidogyne javanica in lettuce and investigate its effects on plant development, total chlorophyll content, nitrogen balance, flavonoid content, anthocyanin content, defense enzyme activities, and soil microbial activity.

Methods

Installation of the experiment and seedling production

The experiment was carried out in a greenhouse (23°47′34.5″S 53°15′22.1″W, 430 m a.s.l.) between July and September 2021. The design was completely randomized with five treatments and six replications. Treatments consisted of five proportions of SMS (0%, 15%, 30%, 45%, and 60%) added to a commercial substrate (Bioplant^®) for seedling production. SMS, obtained after two cycles of P. djamor cultivation, was kindly donated by a local mushroom grower. The growing substrate was initially composed of 80% Pine spp. sawdust pellets, 18% wheat bran, 1% hydrated lime, and 1% calcitic limestone.

Mixtures of SMS and commercial substrate at the proportions defined in the experimental design were placed in 128-cell polystyrene trays and sown with seeds of lettuce 'Vera'. At 18 days after sowing, seedlings were transplanted to pots containing 950 cm³ of autoclaved (120°C, 2 h) soil and sand at a ratio of 2:1, previously limed (0.7 g pot^− 1) and fertilized with NPK fertilizer (15-09-12, 0.12 g pot^− 1). After a further 10 days, plants were inoculated with a suspension containing 2000 eggs and eventual second-stage juveniles (J2) of M. javanica. Nematodes were extracted from a pure population maintained on soybean M6210 IPRO, according to the method proposed by Hussey and Barker and adapted by Boneti and Ferraz (1981). The suspension was quantified under an optical microscope using a Peters' chamber and calibrated to 2000 eggs + J2 mL^− 1. Nitrogen top dressing (2% urea, 0.1 g pot^− 1) was performed 30 days after transplanting.

Vegetative and physiological parameters

After 50 days of cultivation, plants were evaluated for total chlorophyll index, nitrogen balance index (NBI), flavonoid, content, and anthocyanin content using a portable chlorophyll meter (Force A, Dualex Scientific™). Results are the mean of three readings from the middle third of each plant. Plants were then removed from the pots and divided into shoots and roots. Shoot fresh weight was determined using an analytical balance. Leaf number was determined by counting the number of leaves per plant, starting from the basal region to the last expanded leaf and excluding yellow and/or dry leaves, whenever present (Bezerra Neto et al. 2005). Head height was measured from the stem to the top of the head by using a millimeter ruler. Shoot dry weight was determined by placing samples in paper bags and drying in a forced-air oven at 65°C to constant weight. Root samples were thoroughly washed, placed on paper towels to remove excess water, and weighed to obtain the root fresh weight.

Nematode analysis

After fresh weight determination, roots were subjected to the above-mentioned method for nematode extraction and quantification. The number of nematodes per root system was divided by root fresh weight to obtain the number of nematodes per gram of root (population density). Reproduction factor was calculated as the ratio of final to initial population (Oostenbrink 1966).

Enzyme analysis

Fresh shoot and root samples (0.5 g) were collected from the median portion of each organ for enzymatic analysis, with three replications per treatment. Samples were ground in a mortar with liquid nitrogen, polyvinylpyrrolidone, and 50 mM potassium phosphate buffer (pH 7.0) containing 0.1 mM EDTA. After centrifugation, the extract was transferred to 1.5 mL microtubes and stored in a freezer (− 8°C) for subsequent protein quantification (Bradford 1976). Protein concentration (mg mL^− 1) was determined against a standard curve of bovine serum albumin.

Guaiacol peroxidase (POX; EC 1.11.1.7) activity was measured based on the conversion of guaiacol to tetraguaiacol in the presence of hydrogen peroxide, and the results are expressed in ∆abs₄₇₀ min^− 1 mg^− 1 protein (Lusso and Pascholati 1999). Phenylalanine ammonia-lyase (PAL; EC 4.3.1.5) activity was determined according to Umesha (2006). Absorbance readings were taken at 290 nm. Enzymatic activity was calculated from the difference between the absorbance of sample and blank based on a standard curve of trans-cinnamic acid. Results are expressed in mg trans-cinnamic acid h^− 1 mg^− 1 protein (Umesha 2006).

Soil biological analysis

At the end of the experiment, about 400 g of soil was collected from three replicates per treatment for biological analysis. Soil microbial biomass carbon was determined according to the fumigation–extraction method (Silva et al. 2007a). Soil basal respiration and metabolic quotient (qCO₂, representing the ratio of soil basal respiration to microbial biomass carbon) were estimated according to Silva et al. (2007b). All analyses were performed in triplicate.

Statistical analysis

Data were subjected to analysis of variance at the 5% significance level. When necessary, to meet Shapiro-Wilk normality assumptions, data were transformed to $\sqrt{x+1}$ before regression analysis at the 5% significance level, with the exception of enzyme data, whose means were compared by Tukey's test at the 5% significance level. Statistical analyses were performed using Sisvar software (Ferreira 2011). Data for nematode population were subjected to linear-plateau segmented regression analysis using R statistical language (R Core Team 2021). The regression model consisted of two segments, the first describing an increasing or decreasing line up to a given p-value (response plateau) and the second assuming a nearly constant value (Schabenberger and Pierce 2002).

Nematode population density and reproduction factor decreased with increasing SMS proportion, reaching the plateau at about 15% SMS (Fig. 1A and B) with reductions of 99.75% and 98.68%, respectively, compared with the control (0% SMS).

There were no differences in root fresh weight or head height between treatments, whose means ranged from 2.16 to 6.22 g and from 1.43 to 2.42 cm, respectively (data not shown). On the other hand, increasing SMS proportions led to a reduction in shoot fresh weight (Fig. 2A), which decreased by 30.19% in seedlings grown in substrate added with 60% SMS and by 2.69% and 4.67% in seedlings grown with 15% and 30% SMS, respectively, compared with the control. Leaf number followed the same pattern (Fig. 2C), with 60% SMS leading to a 33.33% reduction in this parameter and 15% SMS causing a reduction of only 1.33%. There was a quadratic effect on shoot dry weight, which was estimated to reach the maximum value at 10.83% SMS (Fig. 2B).

Chlorophyll content decreased with SMS addition (Fig. 3A), being lowest in seedlings grown in substrate containing 34.19% SMS, corresponding to a 21.79% reduction. In this study, NBI had a similar behavior to that of chlorophyll content, with lower values observed in the treatment containing 38.22% SMS, which led to a reduction of 35.66% (Fig. 3B). Anthocyanin content increased with SMS treatment, reaching a maximum at 40% SMS (Fig. 3C). For flavonoid content, there were no significant differences between treatments, whose means ranged from 0.62 to 0.79 (data not shown).

PAL and POX activities were measured in plant leaves and roots at the end of the experimental period. Both enzymes were found to be activated only in leaves (Fig. 4A, B). PAL activity increased in seedlings grown in substrate containing 30% SMS (Fig. 4A). POX activity was highest in treatments containing 0% and 30% SMS (Fig. 4B).

Regression models did not provide a good fit to soil basal respiration data. Experimental results indicated a peak of biological activity in substrate added with 25.75% SMS, whose basal respiration was 14% higher than that of the control.

Microbial biomass carbon, that is, the living portion of the soil (Kaschuk et al. 2010), increased proportionally to SMS concentration (Fig. 5B). qCO₂, by contrast, had the opposite behavior, decreasing as a function of increasing SMS concentration (Fig. 5C).

Spent substrate from P. djamor cultivation efficiently controlled M. javanica reproduction on lettuce, demonstrating the nematicidal potential of metabolites released during mushroom cultivation. Hyphae remaining from mushroom cultivation might have contributed to this effect by releasing hydrolytic enzymes, including proteases, collagenases, and chitinases, which penetrate and digest the cuticle of nematodes (Affokpon et al. 2011). The results of the current study may also be explained by predation of Pleurotus spp. on nematodes. These fungi form traps to capture and predate or parasitize nematodes (Liu et al. 2009; Siddiqui and Mahmood 1996). Pleurotus ostreatus and other species of the genus contain specialized cells in hyphae that are capable of secreting tiny droplets of toxins, which paralyze nematodes within 30 seconds of contact, without killing the parasites (Truong et al. 2006). Although alive, nematodes remain immobile, and the liquids that extravasate from their tissues stimulate hyphal growth via chemotaxis; hyphae may then penetrate and digest nematode tissues, absorbing the nutrients released during this process (Thorn and Barron 1984; Barron and Thorn 1987; Maccheroni et al. 2004; Truong et al. 2006).

The first nematicidal compound isolated and characterized from mushrooms of the genus Pleurotus (P. ostreatus) was trans-2-decenedioic acid, derived from linoleic acid. The compound was obtained from aqueous extract of P. ostreatus substrate and found to have nematotoxic action. The toxin affects not only nematodes but also insects and fungi, possibly by altering cell membrane permeability (Kwok et al. 1992). These authors observed that, at a concentration of 300 µg mL^-1, the nematicidal compound immobilized Panagrellus redivivus by 95% in 1 h. Other compounds, such as saturated fatty acids (palmitic acid, lauric acid, stearic acid), unsaturated fatty acids (oleic acid, linoleic acid), fatty acid methyl esters (oleic acid methyl esters), carbonyl compounds, and alcohols (p-anisyl alcohol) were found to have high nematicidal activity (Stadler et al. 1994). These findings show the potential of the direct use of mushroom residues for the control of plant-parasitic nematodes (Palizi et al. 2009). There are reports that Pleurotus releases fatty acids, such as linoleic acid, which are converted into highly reactive peroxides, instantly halting nematode activity (Li et al. 2007; Satou et al. 2008).

Previous studies demonstrated the nematicidal potential of toxins found in mushroom medium. The filtrates of liquid Pleurotus spp. medium afforded complete (100%) immobilization of M. javanica juveniles after 24 h of application; however, immobilization efficiency differed according to species (Heydari et al. 2006). Other researchers obtained positive results with the use of Pleurotus spp. for the control of root-knot nematodes (Aslam 2013; Okorie et al. 2011). Aqueous extracts of 10 basidiomycetes were tested for M. incognita control; all extracts, particularly that of Pleurotus, inhibited hatching and increased J2 mortality (Wille et al. 2019). Furthermore, the authors found that treatment of soil with fungal extracts reduced nematode reproduction by about 70%.

In addition to controlling root-knot nematodes, P. djamor spent substrate may efficiently promote plant development compared with commercial substrate and can therefore be used as an ingredient of plant substrates (Machado 2019). The positive effect of SMS on root development was attributed to reduction in soil compaction, clod and surface crust formation, and diurnal temperature changes, as well as an increase in aggregate stability (organic matter) and water infiltration rate (Stewart et al. 1998). Aeration and moisture retention are two of the many benefits provided by SMS application in plant substrate, which may positively influence germination in a variety of plant species (Machado 2019). However, it is worth mentioning that SMS may have phytotoxic effects depending on its concentration, as observed here; thus, care should be taken so as not to compromise plant development.

Plants treated with 60% SMS had a smaller size as seedlings and throughout plant development. Thus, at the time of transplanting, seedlings subjected to high SMS concentrations showed a noticeable difference in size, explaining the lower shoot fresh weight, shoot dry weight, and leaf number of these plants. Phytotoxic effects were also observed in plants treated with 75% SMS. The results of this treatment are not reported because such effects culminated in plant death. Agaricus bisporus substrate had a similar effect on tomato seedlings, causing a 2-day delay in germination (Collela et al. 2019).

Because SMS contains lignocellulosic compounds (e.g., wheat or rice straw, sugarcane bagasse, sawdust), which act as a source of carbon, and additional protein nutrients (organic bran or mineral elements) (Figueiredo and Dias 2014), it is possible that seedling development and plant growth were affected by nitrogen imbalance. It is also possible that the salinity of the culture medium increased after the production cycle (Paula et al. 2017), resulting from addition of inputs, such as limestone, gypsum, and chemical fertilizers. Furthermore, the substrate used here was not subjected to composting, a practice that tends to promote stability and reduce salinity (Colella et al. 2019). It should be noted that the negative effects of SMS on vegetative development were negligible at low concentrations, thus not precluding the use of the material. Application of SMS in legume production can contribute to integrating production chains. Producers may optimize space, minimize costs, and maximize product diversity (Machado 2019).

There was a decrease in chlorophyll content, which might be due to nitrogen imbalance. Nitrogen is indispensable for the synthesis of chlorophyll, a compound that is essential for plant growth and adaptation to the most varied environments. Chlorophyll index is an indicator of the physiological status of plants (Rêgo and Possamai 2004), and the quality of the molecule is related to photosynthetic activity (Zotarelli et al. 2003). Some saprophytic fungi, such as basidiomycetes, can only survive on substrates with high C/N ratios and, therefore, depend on nitrogen supplementation. These fungi, to meet their nitrogen needs, developed nematode predation strategies (Luo et al. 2004; Thorn and Barron 1984). Thus, the higher demand for nitrogen in the growth medium might have compromised nitrogen absorption by plants, but remaining fungal populations might have been favored.

NBI had a similar behavior to chlorophyll. The index is an estimate of nitrogen in plants, obtained from the relationship between chlorophyll index and flavonoid content (Rabier et al. 2014). About 70% of nitrogen contained in the leaves is found in chloroplasts, participating in the synthesis and structure of chlorophyll molecules (Wood et al. 1993). These findings further support the interaction between nematodes and microorganisms from SMS.

Anthocyanins act as photoprotectors and antioxidants (Carletti et al. 2013). Higher anthocyanin levels in plant tissues tend to confer greater resistance to abiotic stresses, particularly drought stress (Ramakrishna and Ravishankar 2011). However, there are few reports in the literature on anthocyanin accumulation in plants exposed to biotic stress, such as that caused by phytonematodes.

Peak PAL activity was observed in the treatment with the highest SMS concentration (60%). It is possible that microorganisms from SMS or their byproducts served as elicitors of plant resistance. In general, when plants are exposed to nematodes, resistance induction occurs within 8 days of inoculation (Owen et al. 2002; Sahebani et al. 2011; Puerari et al. 2019). In the current study, enzyme activity was evaluated only at the end of the experiment, which may explain the non-activation of POX and PAL routes in the root system and the reduction in POX activity as a function of increasing SMS levels.

PAL contributes to plant resistance to pathogens, as it is involved in the first step of phenylpropanoid synthesis, whereby phenylalanine is converted into trans-cinnamic acid, resulting in compounds such as phytoalexins and, mainly, lignin (Chaves et al. 2016; Puerari et al. 2019). Lignin, in turn, confers resistance to plant cell walls, restricting nematode activity at feeding sites (Puerari et al. 2019). PAL also acts as a precursor of several compounds, such as benzoic acid derivatives, coumarins, lignin precursors, flavones, isoflavones, flavonols, anthocyanins, condensed tannins, caffeic acid, ammonia, and other simple phenylpropanoids, all of which are important for plant defense against pathogens (Schwan-Estrada et al. 2008).

Research on resistance induction stimulated by Pleurotus is still scarce. A previous study showed that these fungi induce resistance to M. incognita in tomato when used alone or in combination with rabbit manure and wheat straw (Sandoval et al. 2020). Wille et al. (2019) observed resistance induction in lettuce with the use of aqueous extracts of fruiting bodies of five Pleurotus species. The extracts showed nematostatic activity in vitro, reduced nematode reproduction factor, and increased nematode control. Hahn et al. (2019) obtained good results with the use of Pleurotus extracts, including P. djamor extract, for M. javanica immobilization and mortality.

POX activity in lettuce leaves was highest in plants treated with 0% and 30% SMS (Fig. 4B). POX is an antioxidant enzyme that accumulates in tissues subjected to some type of oxidative stress, in this case, nematodes. The enzyme is involved in the release of reactive oxygen species to inhibit parasitic activity at feeding sites (Nguyen et al. 2011). The high POX activity in the untreated sample can be explained by the high nematode population density, which likely promoted oxidative stress in plant tissues.

Application of SMS at a concentration of 25.75% increased soil basal respiration by 14% compared with the control. This parameter represents the amount of carbon in the form of CO₂ resulting from the respiration of decomposing organisms present in the soil (Medeiros et al. 2009). Species of the genus Pleurotus decompose wood and plant residues (Grabarczyk et al. 2019) and are known for their ability to produce ligninolytic enzymes, such as laccase and manganese peroxidase (Kamitsuji et al. 2004). Laccase is an oxidoreductase capable of catalyzing the oxidation of various aromatic compounds (especially phenol) while concomitantly reducing oxygen to water (Valeriano et al. 2009). This information explains the high basal respiration in the 25.75% SMS treatment.

Although high respiration values generally indicate favorable soil conditions, it should be considered that, in the short term, high respiration rates imply the release of nutrients to plants, but, in the long term, they may imply loss of organic carbon from the soil to the atmosphere (Parkin et al. 1996). Treatments with low SMS concentrations were likely influenced by abiotic factors, such as substrate porosity and, consequently, aeration. SMS has high water retention capacity, allowing the creation of a high-humidity microclimate, which might have compromised microbial respiration (Silva et al. 2007b). In the experimental units, microbial populations were composed of nematodes and any remaining fungi in SMS, given that the soil used was previously autoclaved, eliminating other organisms (Hu et al. 2019). Therefore, the results agree with the hypothesis that treatments with a higher concentration of P. djamor spent substrate promoted an increase in soil microbial biomass.

Anderson and Domsch (1993) argued that qCO₂ is a relevant factor for assessing environmental and anthropogenic effects on soil microbial activity. In this study, the highest qCO₂ was observed in treatments containing 8.8% SMS (Fig. 4C). qCO₂ is related to the efficiency of microorganisms in using available carbon for growth (Batista et al. 2018). High values of qCO₂ indicate a correlation with low biomass indices and low C and N contents (Mondino et al. 2009). A similar correlation was found in this study: the lowest qCO₂ values occurred in treatments with the highest microbial biomass carbon.

Overall, our results demonstrate the potential of P. djamor spent substrate in the control of M. javanica. Further studies are needed to assess SMS efficiency and possible interactions of remaining hyphae with nematodes. SMS concentrations of 15–30% are effective for nematode control and do not exert phytotoxic effects on plant development.

Spent substrate from P. djamor cultivation is efficient in controlling M. javanica in lettuce. However, high SMS concentrations may negatively influence shoot development, with no negative effects on roots.

The interaction of SMS microorganisms with nematodes may, on the one hand, affect chlorophyll, NBI, and anthocyanin contents but, on the other hand, protect the photosynthetic apparatus. The presence of fungal residues in SMS may activate enzymes involved in resistance induction (POX and PAL) and reduce the efficiency of microorganisms in utilizing available carbon for growth.

SMS: Spent mushroom substrate; C/N: Carbon/nitrogen ratio; NPK: Nitrogen:phosphorus:potassium; NBI: nitrogen balance index; EDTA: ethylenediaminetetraacetic acid ; POX: Guaiacol peroxidase; PAL: Phenylalanine ammonia-lyase; qCO₂:metabolic quotient; MBC: microbial biomass.

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Availability of data and material

All datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

Competing interests

The authors have no conficts of interest to declare.

Funding

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Authors' contributions

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Acknowledgements

To the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for awarding a postdoctoral fellowship to S.M. Santana-Gomes (grant no. 88887.335098/2019-00) and the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for providing a productivity research grant to C.R. Dias-Arieira (grant no. 303269/2020-0).

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Control of Meloidogyne javanica with Pleurotus djamor spent mushroom substrate

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Installation of the experiment and seedling production

Vegetative and physiological parameters

Nematode analysis

Enzyme analysis

Soil biological analysis

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