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Article

Biofumigation Treatment Using Tagetes patula, Sinapis alba and Raphanus sativus Changes the Biological Properties of Replanted Soil in a Fruit Tree Nursery

by
Robert Wieczorek
1,
Zofia Zydlik
1 and
Piotr Zydlik
2,*
1
Department of Ornamental Plant, Dendrology and Pomology, Faculty of Agronomy, Horticulture and Bioengineering, Poznan University of Life Sciences, 60-637 Poznan, Poland
2
Department of Entomology and Environment Protection, Faculty of Agronomy, Horticulture and Bioengineering, Poznan University of Life Sciences, 60-637 Poznan, Poland
*
Author to whom correspondence should be addressed.
Agriculture 2024, 14(7), 1023; https://doi.org/10.3390/agriculture14071023
Submission received: 15 May 2024 / Revised: 20 June 2024 / Accepted: 24 June 2024 / Published: 27 June 2024
(This article belongs to the Section Crop Protection, Diseases, Pests and Weeds)
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Abstract

:
Apple replant disease (ARD) may cause significant losses both in commercial orchards and in fruit tree nurseries. The negative effects of ARD may be limited by using biofumigation. The aim of the study was to assess the influence of this treatment on the biological properties of replanted soil in a tree nursery. In two-year experiment, apple trees of the ‘Golden Delicious’ cultivar were used. The trees were planted into soil from two sites. The soil from one site had not been used in a nursery before (crop rotation soil). The other soil had been used for the production of apple trees (replanted soil). Three species of plants were used in the replanted soil as a forecrop: French marigold (Tagetes patula), white mustard (Sinapis alba), and oilseed radish (Raphanus sativus var. oleifera). The following parameters were assessed in the experiment: the enzyme and respiratory activity of the soil, the total count of bacteria, fungi, oomycetes and actinobacteria in the soil, as well as the count and species composition of soil nematodes. The vegetative growth parameters of the apple trees were also assessed. The biological properties of the replanted soil were worse than those of the crop rotation soil. In the replanted soil, the organic matter content, enzyme and respiratory activity as well as the count of soil microorganisms were lower. The biofumigants, used as a forecrop on the replanted soil, significantly increased its enzyme activity and respiratory activity. Dehydrogenase activity increased more than twofold. Growth parameters of the trees were significantly improved. The height of the trees increased by more than 50%, and the leaf area, weight and total length of side shoots were higher as well. The density of nematodes in the replanted soil after biofumigation was significantly reduced, with a larger reduction in the marigold fumigated soil. Eight of the eleven nematode species were completely reduced in the first year after biofumigation treatment.

1. Introduction

Intensification is a prerequisite for high profitability of fruit production. It involves growing a large number of low-vigorous trees, which requires a large amount of high-quality nursery material. Due to changing market requirements for the selection of cultivars, nurserymen have to change plantings frequently and search for new areas for nursery plantations. New nurseries may be established in areas used as nurseries before because of the high risks due to replanting disease [1], soil fatigue [2] or, usually, apple replant disease (ARD). The occurrence of ARD is most common in apple plantations. Research on the effects of replant disease is also usually conducted in apple plantations, but rather rarely in fruit tree nurseries. Regardless of the crop type, researchers generally agree on the effects of ARD. When establishing new orchards in the place of old ones, the production properties of the soil may decrease due to its low enzyme activity and respiratory activity [3,4]. As a result, the content of soil nutrients decreases [5,6]. In consequence of decreased productive properties of the soil affected by ARD, the vegetative growth of plants is poorer [7,8,9,10,11], and the yield and quality of fruit are lower [1,12,13].
Owing to the progressive intensification of fruit cultivation, the incidence of ARD is expected to increase, especially in regions where the regular replacement of land is limited due to its intensive use. Thus, it is necessary to find an effective method of mitigating the consequences of the disease. First, it is necessary to clearly identify the causes of ARD, which is not an easy task. As results from numerous studies show, ARD may be caused by abiotic or biotic factors. The former include soil acidification, high salinity, and phenolic compounds formed after the decomposition of root residues [14]. The latter are bacteria of the Bacillius and Pseudomonas genera [15,16], fungi/oomycetes of the Cylindrocarpon, Rhizoctonia Alternaria, Phytophtora, and Pythium genera [17,18], and nematodes [19,20,21]. The fact that the fumigation of replanted soil significantly reduces the consequences of ARD may indicate the decisive role of biological factors in its development. This treatment is particularly effective against nematodes [12,19,21]. It is estimated that there are several hundred to several million species of nematodes in the environment, but only a small group of them are considered to be plant parasites. The largest population of soil nematodes are non-pathogenic species [22], which are bioindicators of soil quality. Parasitic nematodes have been best investigated, especially the Pratylenchidae family [17]. They damage plant roots as they move through the soil in search of food [16]. Kanfra et al. [21] observed that when nematodes extracted from ARD soil were added to the soil in a nursery, they inhibited the growth of the root system of apple rootstocks. Available reference publications on nematodes include some results that do not confirm the relationship between parasitic nematodes and the occurrence of ARD [10,23]. Moreover, the symptoms of nematodes feeding on plants are rather non-specific, which makes it difficult to identify the loss they cause [22].
It may take a dozen years or so to restore the fertility of soil with ARD symptoms. According to Long et al. [24], the structure of soil microorganisms in replanted soil becomes imbalanced. In consequence, pathogenic organisms gain an advantage. Therefore, the primary goal should be to restore the balance of the species composition in the soil microflora, which involves reducing the count of pathogenic organisms in replanted soil. This can be performed by thermal sterilisation or chemical fumigation. Currently, dazomet, sodium methane, or chloropicrin are mainly used in the latter procedure [25,26]. Both methods very effectively reduce the count of biological perpetrators of ARD, including the Fusarium spp. [27] and Phytophtora spp. [28]. However, both thermal sterilisation of the substrate [29] and chemical fumigation [30] may also reduce the soil microbiota completely.
The undesirable effects of ARD can also be reduced through soil biofumigation. This involves using some plant species, mainly as forecrops, to reduce the count of harmful nematodes, pathogenic bacteria or fungi and oomycetes in the soil. The most common of these plants are marigold (Tagetes L.), white mustard (Sinapis alba), oilseed radish (Raphanus sativus var. oleifera), spring rapeseed (Brassica napus), and rye (Secale cereale L.) [31]. Plants used for biofumigation produce specific compounds—secondary metabolites (e.g., glucosinolates) and thiophene compounds, which have fungicidal, nematocidal, insecticidal, and antiviral effects [32]. Such plant properties make it possible to reduce the number of pathogenic organisms in the soil, including oomycetes: Phytophthora cactorum [33], and fungi as Fusarium oxysporum [34]. One of the best-investigated effects of biofumigation is the nematocidal effect [35]. Plants from the Asteraceae family (Asteraceae Dum) are also highly effective in combating nematodes, thanks to thiophene compounds released by their roots [36]. The highest content of these compounds was found in Tagetes patula and Tagetes erecta. Their cultivation causes significantly increase the vegetative growth of apple trees in an orchard on soil with ARD [37].
The aim of the study was to assess the influence of three plant species—French marigold (Tagetes patula), white mustard (Sinapis alba), and oilseed radish (Raphanus sativus var. oleifera) on improving the biological properties of replanted soil measured by its microbial activity in a fruit tree nursery.

2. Materials and Methods

2.1. Experiment Design

Between 2019 and 2021, an experiment was conducted on apple trees growing in a commercial nursery in western Poland (52°25′49.10″ N 17°11′34.08″ E). The trees were planted in containers with soil taken from two sites. The soil from one site had been used for agricultural crops (crop rotation soil—CRS). The other one came from a nursery where apple trees had been produced for two seasons (replanted soil—RS). At the first site, crops had been cultivated in a rotation system for 10 years. No treatments had been applied to improve the productive properties of the soil in the other site. The physicochemical properties of the soil from both sites are shown in Table 1. The soils from the two sites differed significantly in the content of nutrients. The content of P, K, Ca, Mg, and Zn in the replanted soil was lower than in the crop rotation soil. The humus content was also much lower (4.08% and 1.70%, respectively), but the acidity was higher (Table 1).
Three species of plants were used in the experiment: French marigold (Tagetes patula), white mustard (Sinapis alba), and oilseed radish (Raphanus sativus var. oleifera). They were sown in the autumn of 2019 at the site with replanted soil. In the next year, in early spring, the plants were comminuted, mixed with the soil, and put into 8 L plastic containers. Apple trees of the ‘Golden Delicious’ cultivar, grafted on M9 rootstock, were planted in the containers.
Five treatments in the experiment were used: crop rotation soil (control variant—1), replanted soil (variant 2), replanted soil with a French marigold forecrop (Tagetes patula) (variant 3), replanted soil with a white mustard forecrop (Sinapis alba) (variant 4), and replanted soil with an oilseed radish forecrop (Raphanus sativus var. oleiformis) (variant 5). There were twenty containers (replicates) in each variant.
In 2020 and 2021, the containers with the plants were systematically weeded and watered with a drip irrigation system. The plants were protected in accordance with the recommendations for such crops. In each growing season, the plants were fertilised with a multi-component fertiliser (NPK 16+8+12+ micronutrients) at a dose of 3 g dm−3.
The analysis of the climatic conditions at the site of the experiment included the average annual temperature and the amount of rainfall. Both of these parameters were higher (temperature) or lower (rainfall) than the long-term average values (1982–2016) (Appendix A).

2.2. Soil Analyses

The following soil analyses were conducted in the experiment: the enzyme activity and respiratory activity, the content of available form of macro- and micronutrients, the total counts of bacteria, oomycetes, fungi, and actinobacteria, and the number and species composition of soil nematodes. Soil samples for the analysis of the content of macronutrients (N-NO3, P, K, Mg, Ca) and micronutrients (Zn, Cu, Mn, Fe) were collected in September 2021. A small amount of soil was collected from each container (replicate) with a laboratory spoon. Each soil sample representing one experimental variant was mixed and had a total weight of 900 g. The N-NO3 content was measured by microdistillation, the P content—colorimetrically, the K and Ca content—photometrically, the Mg content—by atomic absorption spectrometry (AAS). Lindsay’s Solution was used to extract micronutrients from the soil and their content was measured by AAS. The potentiometric method was applied to measure the soil acidity, Tiurins method for the determination of humus content, weight method for bulk density, and conductivity method for the determination of salinity.
Soil samples for the analysis of biological properties were collected in 2020 and 2021 in spring, summer, and autumn. In each container, samples were collected from the rhizosphere, and after their mixing, one 0.5 kg sample representative of the treatment was obtained. The protease activity in the soil was measured with the spectrophotometric method developed by Ladd and Butler [38]. The measurements were made after one-hour incubation of the samples at 50 °C and at a wavelength of 578 nm. The dehydrogenase activity was measured with a spectrophotometer and 1% TTC solution, according to the methodology developed by Thalman. The measurements were made after 24 h incubation of the samples at 30 °C at a wavelength of 485 nm (TTC test). The absorption method according by Gołębiowska and Pędziwilk [39] was applied to measure the soil respiratory activity. It was based on the amount of CO2 released (CO2 mg kg−1 48 h−1). All analyses were quadruplicated.
Soil samples for microbial abundance analyses were collected once—in autumn 2021. The microbial analysis was based on serial dilution—the method used in soil microbial ecology research. A selective agar was used to determine the counts of colony-forming units of bacteria, actinobacteria, oomycetes and fungi. The total count of bacteria (CFU 105 g−1 d.m.) was measured on standard Merck agar after five days of incubation at 28 °C; the count of actinobacteria (CFU 105 g−1 d.m.)—on Pochon agar after seven days of incubation at 24 °C (according to Grabińska-Łoniewska [40]); the count of oomycetes and fungi (CFU 104 g−1 d.m.)—on Martin agar after five days of incubation at 24 °C [41]. The cultures were quintuplicated.
The number and species composition of soil nematodes were analysed twice—in 2020 and 2021. Soil samples were collected with a soil sampler (diameter—30 mm) directly from the rhizosphere of the trees. The samples were collected from each container. Then, they were mixed, and a pooled sample was prepared (500 mL) for each variant. The quantitative analysis of nematodes was conducted at the Department of Nematology, Plant Protection Institute, Poznań, Poland. Existing keys were used to initially identify the species of nematodes [42,43]. The identifications based on morphology were confirmed by sequencing of molecular markers (D2-D3 28S rDNA).

2.3. Growth Strength Measurements

In autumn 2021, the strength of vegetative growth of two-year-old trees was measured. The following parameters were measured: the height of trees (cm), the number and total growth of side shoots (cm), the leaf weight (g) and area (cm2). The height of all trees in each variant was measured from the root collar to the top of the main shoot. At the end of the growing season, 40 leaves were randomly collected from each variant and weighed. After weighing, the leaves were scanned and their area was measured with the DigiShape 1.9 software. The measurements were quadruplicated.

2.4. Statistical Analyses

The results were analysed statistically with the analysis of variance and Duncan’s test, using the STATISTICA 12.1 program. The significance of differences was set at α = 0.05.

3. Results and Discussion

3.1. Physicochemical and Biological Properties of Soil

The quality of soil was assessed on the basis of its enzyme activity and respiratory activity, the content of micro- and macronutrients, humidity, pH, and the count of microorganisms. Our experiment revealed significant differences in the physicochemical parameters of the soil, which depended on its earlier use. The replanted soil (RS) was more acidic than the crop rotation soil (CRS) (pH 4.8 and 5.0, respectively) and contained almost three times less organic matter (0.8% and 2.17%) (Table 2). The quality of replanted soil was significantly better in the variants with biofumigation. The soil pH increased from 4.8 to 5.0 (French marigold) and 5.5 (oilseed radish). The humus content also increased significantly and was the highest in the variant with white mustard. It was over 50% higher than in the variant with replanted soil without forecrops (RS), i.e., 0.8% and 1.09% (Table 2).
Humus is a basic source of nutrients available to plants. The rate of its mineralisation depends on the efficiency of the activity of soil microorganisms, which can be measured with the activity of soil enzymes [44]. It is believed that the assessment of quality of soil should be based on the activity of soil enzymes and other properties of soil [45]. Soil microorganisms (mainly bacteria) and root debris are basic sources of soil enzymes. One of the most important soil enzymes are oxidoreductases (dehydrogenases) and hydrolases (protease, urease). Our experiment showed significant differences in the activity of soil enzymes, which depended on the earlier use of the soil. The biggest differences were found in the dehydrogenase activity (0.56 and 1.22 cm−3 H2 24 h−1 kg−1 DM, respectively) (Table 3). These enzymes are considered very sensitive indicators of changes in soil properties [46].
The amount of CO2 released from soil indicates the respiratory activity of soil microorganisms [47]. The earlier method of soil use significantly influenced the values of this parameter. The respiratory activity of the replanted soil (RS)—19.25 CO2 in mg kg−1 48 h−1 was significantly lower than that of the crop rotation soil (CRS)—27.70 CO2 in mg kg−1 48 h−1.
The worse biological properties of the replanted soil, manifested by its enzyme activity and respiratory activity, were also observed in earlier studies [48]. The decrease in the enzyme activity and respiratory activity of replanted soil may result from its higher acidity. Järvan et al. [49] indicated that the count and activity of soil bacteria are reduced in an acidic environment. As a result, the dehydrogenase activity also decreases. An increase in the soil pH increases the activity of this enzyme [50,51].
A significant increase in both the enzyme activity and respiratory activity of the replanted soil in the variants with biofumigation were noted. On average, over the two years of the research, the dehydrogenase activity in the replanted soil in the variants with forecrops of French marigold (Tagetes patula) and oilseed radish (Raphanus sativus var. oleifera) was more than two times greater than in the soil without forecrops (1.3 and 0.56 cm−3 H2 24 h−1 kg−1 DM, respectively) (Table 3). The analysis of the soil respiratory activity led to a similar conclusion (32.6 and 19.25 CO2 mg kg−1 48 h−1). The protease activity in the replanted soil was the highest in the variant with French marigold. It is noteworthy that both the enzyme activity and respiratory activity of the replanted soil in the variants with biofumigation were significantly higher than in the control treatment with the crop rotation soil (CRS).
Plants used for biofumigation provide the soil with a large amount of organic matter. In consequence, there are a sufficient amount of nutrients for microorganisms, which produce more enzymes. These are the reasons for the increased enzyme activity and respiratory activity of the replanted soil in the variants with biofumigation treatment. Other researchers indicate a positive correlation between the content of organic matter in the soil and its enzyme activity [52,53].
The activity of soil enzymes depends on the physicochemical properties of soil (pH, organic matter content, heavy metal contamination), climate, and cultivation system [53,54]. According to Weaver [55], an insufficient amount of water in the soil may significantly limit the enzyme activity. In our experiment, the enzyme activity and respiratory activity of the of soil were analysed in spring, summer, and autumn. There were differences in the results depending on the vegetation period. The activity of soil dehydrogenases and proteases was the highest in autumn but the lowest in spring (Table 4).
The high dehydrogenase activity in the soil in autumn was also observed by Yuan and Yue [52] and Zydlik et al. [6]. There was a different relationship in the soil respiratory activity. On average, in 2020 and 2021, it was the lowest at the end of the growing season. In autumn, the soil humidity is usually high and there is optimal temperature for the development of soil microorganisms. The availability of water considerably influences the activity of soil enzymes because increased moisture facilitates the solution of organic matter in the soil [56]. Sardans et al. [57] observed that a 10% decrease in the soil moisture caused the protease activity to drop by 15–66%. Results from the analysis of the weather conditions at the site of the experiment show that in September 2020 and 2021, the monthly rainfall was higher than the long-term average (Appendix A).
The high enzyme activity and respiratory activity of soil depends on the count and diversity of microbial communities. The analysis of the count of soil microorganisms conducted in our experiment confirmed the positive effect of biofumigation treatment on this parameter. The most effective plant was French marigold (Tagetes patula). The total bacterial count in the French marigold variant was almost two times greater than in the variant without it (Figure 1A).
Hanschen and Winkelmann [31] also observed an increase in the count of plant growth-promoting bacteria in the replanted soil after the application of Brassica juncea and Sinapis alba. The analysis of the count of oomycetes and fungi gave similar results. The total count of oomycetes and fungi in the variants with French marigold and white mustard was more than two times greater than in the replanted soil without forecrops (Figure 1B). There was a slightly different result in the count of actinobacteria. The total count of these microorganisms (17.92 CFU 105 g−1 d.m.) was the highest in the oilseed radish variant (Raphanus sativus var. oleifera) (Figure 1C).
The increase in the soil enzyme activity increased the rate of mineralisation of organic matter, and consequently, the amount of macro- and micronutrients available to plants. In our experiment, significant differences in the content of macro- and micronutrients in the soil, depending on its earlier use, were noted. The content of all macro- and micronutrients (except Mn) in the replanted soil was significantly lower than in the crop rotation soil (Table 5). Other researchers also observed the low content of nutrients in replanted soil [5,6].
The increase in the microbial activity manifested by the higher enzyme activity and respiratory activity of the soil in the variants with forecrops of three species of biofumigants translated into an increase in the content of soil macro- and micronutrients. There was a significant increase in the content of N, P, K, Zn, Cu, and Fe in the replanted soil with the phytosanitary plants, especially in the variant with Tagetes patula. The content of minerals in the oilseed radish variant (Raphanus sativus var. oleifera) was from about 9% (Fe) to about 90% (Zn) greater than in the replanted soil (RS) without forecrops (Table 5).

3.2. Growth Strength of Apple Trees

The worse biological properties of the replanted soil, manifested by its enzyme activity and respiratory activity, resulted in a weaker vegetative growth of the apple trees. The plants in the RS variant were significantly shorter than those in the CRS treatment (117.3 and 138.7 cm, respectively). They had a smaller number of side shoots, and their total length was shorter (Table 6).
The values of the other parameters of apple tree leaves under analysis, i.e., the weight and, especially, the surface area, were also several dozen per cent lower (Figure 2). Weiß et al. [9] also observed poor vegetative growth of apple rootstocks growing under ARD conditions in their experiment. Sobiczewski et al. [10] found that the leaf area of apple trees growing under ARD conditions was smaller. One of the reasons for the poor growth of plants growing under ARD conditions is the limited growth of their root system. According to Grunewaldt-Stöcker et al. [58], ARD causes the necrosis of root cells and inhibits the growth of hairy roots. In consequence, the uptake of water and nutrients by plants was significantly reduced.
Three species of biofumigants used in our experiment improved the growth parameters of the apple trees cultivated on the replanted soil. The best effect was observed in the white mustard variant (Sinapis alba), where the weight of apple tree leaves was over 50% greater than in the replanted soil without forecrops—RS (15.1 and 10.1 g, respectively) (Figure 2). There were smaller differences between the French marigold and oilseed radish variants and the replanted soil without forecrops. The leaf area in the variants with the phytosanitary plants was about 50% greater than in the RS variant. The apple trees in the variants with the forecrops of phytosanitary plants were significantly taller than in the variant without forecrops (RS). The biggest differences were observed in the variants with Sinapis alba and Raphanus sativus var. oleifera (125, 126 and 177 cm, respectively) (Table 6).
In comparison with the RS variant, the total length of side shoots in the other variants increased significantly, regardless of the used plant species. The measured values were similar to those recorded in the control variant (CRS). There were no significant variant-dependent differences in the number of side shoots of the apple trees. As results from earlier studies show, biofumigation has a positive effect on the vegetative growth of plants growing under ARD conditions. This effect was observed in fruit trees growing on soil with French marigold [12,34] and in trees growing in a nursery [59]. The positive effect of phytosanitary plants on vegetative growth of fruit trees may result from the fact that they reduce pathogenic soil microorganisms responsible for the development of ARD, e.g., Fusarium oxysporum [34].

3.3. Species Composition and Number of Nematodes in Soil

Nematodes are among the biological causative agents responsible for the development of ARD [21]. In our experiment, eleven species of nematodes were identified in the soil (Table 7). In the control variant (CRS), there were four species of nematodes, mostly Ecumenicus monohystera (about 34 individuals in 100 cm3 of soil). The population of Mesorhabditis spiculigera was much smaller. The replanted soil (RS) had the most nematodes of the Mesorhabditis spiculigera and Tylenchorhynchus dubius species (79 and 60 individuals in 100 cm3 of soil, respectively) (Table 7).
According to Dutta et al. [35], the nematocidal properties of plants used for biofumigation have been well investigated. In our experiment, all the three species of biofumigants effectively reduced the number of nematodes, especially in the replanted soil. The French marigold (Tagetes patula) was highly effective, because in the variant with it, the number of nematodes of the Pratylenhus penetrans species was reduced from about 33 individuals in 100 cm3 of soil to zero. This species belongs to the Pratylenchidae family, which is considered one of the most important pests in orchards as well as plantations of vegetables and ornamental plants. The Pratylenhus penetrans feed on roots, where they cause necrotic spots, which significantly reduce the active surface of the roots. The experiments conducted by Weerakoon et al. [60], Mazolla et al. [61], and Wang et al. [62] showed that the use of plants from the Brassicaceae family (Brassica juncea, Sinapis alba) or radish (Raphanus sativus) [16] reduced the number of phytopathogenic nematodes of the Pratylenhus penetrans species in replanted soil. In comparison with the variant without forecrops (RS), the forecrop of French marigold reduced the population of Tylenchorhynchus dubius several dozen times, the populations of Prismatolaimus sp. and Geocenamus nothus—about a dozen times, and the population of Mononhoides sp.—several times (Table 7). It is noteworthy that the population of Tylenchorhynchus dubius (another internal plant parasite after Pratylenhus penetrans that feeds on roots) in the replanted soil was significantly reduced. Tylenchorhynchus dubius is able to survive and develop in various environmental conditions. It occurs in the root zone of over one hundred plant species. The populations of species such as Ecumenicus monohystera and Mononhoides sp. in the soil with the white mustard forecrop (Sinapis alba) were completely reduced. The populations of Cephalobus persegnis and Geocenamus nothus were also reduced several times. There were no significant variant-dependent differences in the population of Cuticularia oxycerca. Oilseed radish was relatively the least effective in reducing the number of nematodes in the replanted soil. In the variant with the forecrop of this plant, the number of nematodes of the Geocenamus nothus and Terrtocephalus terrestris species in the soil was reduced to zero. However, the populations of Ecumenicus monohystera and Mononhoides sp. did not change.
The analysis of the populations of soil nematodes in individual years of the research showed that the nematocidal effect of the plants used for biofumigation was noticeable as early as one year after their application. The populations of eight of the eleven species of nematodes identified in 2020 decreased significantly in the following year of the research (Figure 3). These were mostly Geocenamus nothus, Mesorhabditis spiculigera, Mononhoides sp., Pratylenhus penetrans, and Prismatolaimus sp. In the second year of the experiment, no nematodes of these species were found in the soil.

4. Conclusions

The results of our experiment confirmed the fact that the replanted soil was characterised by a lesser production value. It contained fewer minerals than the crop rotation soil and had worse biological parameters manifested by the enzyme activity and respiratory activity. The apple trees grew worse in such conditions. It was possible to improve the biological properties of the replanted soil by using three species of plants as forecrops. A more than double increase in the content of humus, as well as significant higher enzyme activity and respiratory activity in the replanted soil, in the variants with French marigold, white mustard, and oilseed radish was noted. Compared to the treatments without biofumigation, there was also a significant increase in the number of bacteria in the soil, especially in the variant with the use of Tagetes patula. This significantly improved the growth strength of the apple trees. The leaves of the trees in the variants with the biofumigation treatment had a larger surface area and weight (increase by 50%) than those from the trees growing on the replanted soil without forecrops. Also, the trees were taller and had a greater total growth of side shoots. The experiment also confirmed the nematocidal effect of the three species of the biofumigants, especially French marigold. The biofumigation treatment with its use made it possible to reduce the population of nematode Pratylenhus penetrans species from 33 to 0 individuals in 100 cm−3 of soil.
Biofumigation treatments using Tagetes patula, Sinapis alba and Raphanus sativus on replanted soil should be considered a safer and futuristic alternative to thermal disinfection and chemical fumigation, because it improves the biological properties of replanted soil and reduces the number of parasitic nematodes feeding on plants. It restores the balance of soil microorganisms and improves the growth strength of fruit trees in nurseries.

Author Contributions

Conceptualization, R.W., Z.Z. and P.Z.; methodology R.W. and Z.Z.; formal analysis, P.Z.; investigation, Z.Z., P.Z. and R.W.; supervision, Z.Z.; project administration, P.Z.; resources, R.W.; validation, Z.Z.; data curation, R.W.; funding acquisition, R.W.; writing—original draft preparation, R.W. and Z.Z.; writing—review and editing, P.Z. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The original contributions presented in the study are included in the article, further inquiries can be directed to the corresponding author.

Conflicts of Interest

The authors declare no conflicts of interest.

Appendix A

Table A1. The course of temperatures and precipitation in the 2019–2021 growing seasons.
Table A1. The course of temperatures and precipitation in the 2019–2021 growing seasons.
MonthsTotal Precipitation (mm)Average Temperature (°C)
1982–20162019202020211982–2016201920202021
I30.943.81.243.8−0.8−0.13.2−0.6
II24.413.036.624.40.12.84.6−0.7
III34.341.430.416.23.56.14.74.9
IV29.86.64.635.29.310.38.97.1
V49.574.449.494.614.512.111.611.9
VI62.56.048.624.21.222.518.219.9
VII78.234.878.229.819.519.418.520.7
VIII60.035.457.460.618.920.620.318.9
IX40.945.041.624.214.114.115.115.6
X34.229.053.218.39.010.010.59.8
XI37.534.711.421.23.98.95.97.7
XII37.02.925.819.10.63.12.32.4
Total/Average516.3367.2438.4411.69.110.810.39.9

References

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Agriculture 14 01023 g001aAgriculture 14 01023 g001b
Figure 1. Microbial abundance in the soil (CRS = crop rotation soil; RS = replanted soil). Means marked with the same letters do not differ significantly at = 0.05. (A) The total count of bacteria; (B) The total count of fungi; (C) The total count of actinobacteria.
Figure 1. Microbial abundance in the soil (CRS = crop rotation soil; RS = replanted soil). Means marked with the same letters do not differ significantly at = 0.05. (A) The total count of bacteria; (B) The total count of fungi; (C) The total count of actinobacteria.
Agriculture 14 01023 g001aAgriculture 14 01023 g001b
Agriculture 14 01023 g002
Figure 2. Biometric parameters of apple tree leaves (CRS = crop rotation soil; RS = replanted soil). Means marked with the same letters do not differ significantly at α = 0.05.
Figure 2. Biometric parameters of apple tree leaves (CRS = crop rotation soil; RS = replanted soil). Means marked with the same letters do not differ significantly at α = 0.05.
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Agriculture 14 01023 g003
Figure 3. Nematode abundance in the replanted soil after biofumigation treatment (in 100 cm−3 of soil) in 2020 and 2021.
Figure 3. Nematode abundance in the replanted soil after biofumigation treatment (in 100 cm−3 of soil) in 2020 and 2021.
Agriculture 14 01023 g003
Table 1. Physicochemical and biological properties of the soil (CRS = crop rotation soil; RS = replanted soil).
Table 1. Physicochemical and biological properties of the soil (CRS = crop rotation soil; RS = replanted soil).
Properties of the SoilCRSRS
pH (H2O)7.25.8
Bulk density (kg m–3)16001830
Salinity (g NaCl dm–3)0.230.23
Humus content (%)4.881.70
Content of macro- and microelements (mg dm–3)
N-NO3119
P12730
K22989
Ca1333240
Mg18838
Zn6.203.03
Cu2.101.27
Mn34.38111.63
Fe170.60380.85
Table 2. Physicochemical and biological properties of the soil in 2021 (CRS = crop rotation soil; RS = replanted soil).
Table 2. Physicochemical and biological properties of the soil in 2021 (CRS = crop rotation soil; RS = replanted soil).
TreatmentspH (H2O)Bulk Density (kg m−3)Salinity (g NaCl dm−3)Humus Content (%)
CRS5.0 ± 0.34 b1660 ± 37 c0.13 ± 0.04 c2.17 ± 0.09 e
RS4.8 ± 0.71 a1790 ± 45 e0.97 ± 0.06 a0.80 ± 0.11 a
French marigold forecrop5.0 ± 0.27 b1610 ± 26 a0.12 ± 0.04 b1.19 ± 0.06 c
White mustard forecrop5.3 ± 0.32 c1640 ± 41 b0.18 ± 0.03 e1.24 ± 0.07 d
Oilseed radish forecrop5.5 ± 0.28 d1740 ± 35 d0.14 ± 0.03 d1.09 ± 0.06 b
Means marked with the same letters do not differ significantly at α = 0.05.
Table 3. Enzymatic and respiratory activity of the soil (average for years 2020–2021) (CRS = crop rotation soil; RS = replanted soil).
Table 3. Enzymatic and respiratory activity of the soil (average for years 2020–2021) (CRS = crop rotation soil; RS = replanted soil).
TreatmentsDehydrogenase Activity (in cm−3 H2 24 h−1 kg−1 DM)Protease Activity (in mg Tyrosine h−1 kg−1 DM)Respiratory Activity (CO2 in mg kg−1 48 h−1)
CRS1.22 ± 0.13 bc2.96 ± 0.28 b27.70 ± 1.03 b
RS0.56 ± 0.08 a1.97 ± 0.13 a19.25 ± 4.97 a
French marigold forecrop1.30 ± 0.17 c3.88 ± 0.36 c32.22 ± 1.94 d
White mustard forecrop1.03 ± 0.03 b3.04 ± 0.39 b29.62 ± 3.63 c
Oilseed radish forecrop1.31 ± 0.05 c3.36 ± 0.25 b32.61 ± 1.22 d
Means marked with the same letters do not differ significantly at α = 0.05.
Table 4. The enzymatic and respiratory activity of the of soil during the vegetation period (average for years 2020–2021).
Table 4. The enzymatic and respiratory activity of the of soil during the vegetation period (average for years 2020–2021).
Vegetation PeriodDehydrogenase Activity (in cm−3 H2 24 h−1 kg−1 DM)Protease ACTIVITY (in mg tyrosine h−1 kg−1 DM)Respiratory Activity (CO2 in mg kg−1 48 h−1)
Spring0.89 ± 0.08 a2.31 ± 0.72 a31.53 ± 2.01 b
Summer1.00 ± 0.07 a3.17 ± 0.25 b32.24 ± 2.12 b
Autumn1.36 ± 0.09 b3.66 ± 0.29 c21.07 ± 1.94 a
Means marked with the same letters do not differ significantly at α = 0.05.
Table 5. Content of macro- and microelements (mg dm–3) in the soil in 2021 (CRS = crop rotation soil; RS = replanted soil).
Table 5. Content of macro- and microelements (mg dm–3) in the soil in 2021 (CRS = crop rotation soil; RS = replanted soil).
Mineral ElementsCRSRSFrench Marigold ForecropWhite Mustard ForecropOilseed Radish Forecrop
N-NO398.1 ± 8.62 c83.2 ± 10.4 a91.3 ± 9.77 b132.6 ± 11.2 e124.5 ± 10.7 d
P310.3 ± 16.4 c249.2 ± 21.7 a275.0 ± 26.6 b 318.5 ± 30.9 d440.0 ± 36.5 e
K247.0 ± 20.6 b190.2 ± 19.8 a256.4 ± 22.3 d251.4 ± 19.6 c290.8 ± 21.9 e
Ca117.5 ± 10.3 c101.1 ± 9.4 a105.0 ± 9.90 b128.6 ± 11.2 d127.4 ± 13.6 d
Mg15.0 ± 1.34 a16.0 ± 1.72 a19.0 ± 1.63 b16.0 ± 1.45 a19.0 ± 1.9 b
Zn7.7 ± 0.67 d4.37 ± 0.74 a6.17 ± 0.56 b7.3 ± 0.60 c8.3 ± 0.49 e
Cu2.2 ± 0,11 c1.56 ± 0.09 a1.9 ± 0.08 b2.3 ± 0.10 d2.3 ± 0.94 d
Mn50.8 ± 2.34 e28.2 ± 1.96 b20.4 ± 1.36 a41.1 ± 0.45 d40.1 ± 2.17 c
Fe106.1 ± 10.3 d96.9 ± 9.75 b79.7 ± 8.32 a111.6 ± 9.69 e107.3 ± 9.73 d
Means marked with the same letters do not differ significantly at α = 0.05.
Table 6. Vegetative growth of the apple trees (CRS = crop rotation soil; RS = replanted soil).
Table 6. Vegetative growth of the apple trees (CRS = crop rotation soil; RS = replanted soil).
TreatmentsHeight (cm)Number of Side ShootsTotal Length of Shoots (cm)
CRS138.75 ± 15.22 c4.0 ± 1.26 b25.24 ± 13.74 b
RS117.30 ± 19.25 a2.0 ± 0.87 a6.87 ± 4.27 a
French marigold forecrop123.22 ± 12.46 ab3.0 ± 1.20 ab24.26 ± 4.20 b
Whight mustard forecrop125.02 ± 16.77 b3.0 ± 1.41 ab20.36 ± 7.37 b
Oilseed radish forecrop121.05 ± 20.22 ab3.0 ± 1.19 ab24.11 ± 11.75 b
Means marked with the same letters do not differ significantly at α = 0.05.
Table 7. Average for years 2020–2021 nematode abundance in the soil (in 100 cm−3 of soil) (CRS = crop rotation soil; RS = replanted soil).
Table 7. Average for years 2020–2021 nematode abundance in the soil (in 100 cm−3 of soil) (CRS = crop rotation soil; RS = replanted soil).
SpeciesCRSRSFrench Marigold ForecropWhight Mustard ForecropOilseed Radish Forecrop
Cephalobus persegnis4.1 ± 0.9 a44.9 ± 9.2 b0.0 ± 0.0 a2.9 ± 1.0 a1.0 ± 0.0 a
Cuticularia oxycerca0.0 ± 0.0 a3.3 ± 1.1 a12.8 ± 3.4 b3.3 ± 1.6 a13.2 ± 3.1 a
Ecumenicus monohystera33.9 ± 8.0 c49.6 ± 5.6 c44.2 ± 6.0 c0.0 ± 0.0 a42.7 ± 1.6 c
Geocenamus nothus0.0 ± 0.0 a16.5 ± 5.4 b0.0 ± 0.0 a0.0 ± 0.0 a0.0 ± 0.0 a
Mesorhabditis spiculigera19.2 ± 5.2 b79.2 ± 8.3 c39.5 ± 4.9 b9.9 ± 2.2 a75.9 ± 14.8 c
Mononhoides sp.6.6 ± 2.0 a 13.2 ± 6.7 c6.6 ± 1.1 b0.0 ± 0.0 a9.9 ± 3.3 b
Panagralaimus rigidus0.0 ± 0.0 a56.2 ± 9.2 a249.2 ± 24.5 b240.9 ± 27.3 b211.2 ± 28.1 b
Pratylenhus penetrans0.0 ± 0.0 a33.5 ± 5.8 c0.2 ± 0.0 a7.3 ± 2.0 b7.2 ± 2.2 b
Prismatolaimus sp.0.0 ± 0.0 a49.5 ± 7.7 c6.6 ± 1.0 a19.5 ± 5.8 b13.2 ± 3.5 a
Terrtocephalus terrestris0.0 ± 0.0 a21.3 ± 4.3 b16.1 ± 3.7 b36.0 ± 9.7 b0.0 ± 0.0 b
Tylenchorhynchus dubius0.0 ± 0.0 a60.1 ± 8.8 c3.7 ± 1.2 a25.3 ± 4.4 b25.1 ± 5.3 b
Means marked with the same letters do not differ significantly at α = 0.05.
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Wieczorek, R.; Zydlik, Z.; Zydlik, P. Biofumigation Treatment Using Tagetes patula, Sinapis alba and Raphanus sativus Changes the Biological Properties of Replanted Soil in a Fruit Tree Nursery. Agriculture 2024, 14, 1023. https://doi.org/10.3390/agriculture14071023

AMA Style

Wieczorek R, Zydlik Z, Zydlik P. Biofumigation Treatment Using Tagetes patula, Sinapis alba and Raphanus sativus Changes the Biological Properties of Replanted Soil in a Fruit Tree Nursery. Agriculture. 2024; 14(7):1023. https://doi.org/10.3390/agriculture14071023

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Wieczorek, Robert, Zofia Zydlik, and Piotr Zydlik. 2024. "Biofumigation Treatment Using Tagetes patula, Sinapis alba and Raphanus sativus Changes the Biological Properties of Replanted Soil in a Fruit Tree Nursery" Agriculture 14, no. 7: 1023. https://doi.org/10.3390/agriculture14071023

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