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Article

The Use of a New Benzothiadiazole Derivative for the Control of Cercospora Leaf Spot in Sugar Beet and Its Effect on the Yield

by
Agnieszka Kiniec
1,*,
Maciej Spychalski
2,3,
Rafal Kukawka
2,3,
Katarzyna Pieczul
4,
Adrian Zajac
2 and
Marcin Smiglak
2,5,*
1
Regional Experimental Station, Institute of Plant Protection, National Research Institute, ul. Pigwowa 16, 87-100 Torun, Poland
2
Poznan Science and Technology Park, Adam Mickiewicz University Foundation, ul. Rubiez 46, 61-612 Poznan, Poland
3
Innosil Sp. z o.o., Rubież 46, 61-612 Poznan, Poland
4
Department of Mycology, Institute of Plant Protection, National Research Institute, ul. Wł. Węgorka 20, 60-318 Poznan, Poland
5
Department of Plant Protection, The National Institute of Horticultural Research, ul. Konstytucji 3 Maja 1/3, 96-100 Skierniewice, Poland
*
Authors to whom correspondence should be addressed.
Agriculture 2025, 15(6), 605; https://doi.org/10.3390/agriculture15060605
Submission received: 12 November 2024 / Revised: 5 March 2025 / Accepted: 8 March 2025 / Published: 12 March 2025
(This article belongs to the Section Crop Protection, Diseases, Pests and Weeds)
Browse Figure
Versions Notes

Abstract

:
The use of plant protection products (PPPs) is the main method of controlling Cercospora leaf spot (CLS), as it constitutes a cheap and effective approach that is easy for farmers to follow. Unfortunately, it is widely recognized that the use of PPPs poses a risk not only to the environment but also to human health. The urgent need for sustainable development, recommended by the European Union and expressed in the “Farm to Fork Strategy”, includes a serious restriction on the use of PPPs. This strategy assumes a 50% reduction in the use of PPPs by 2030. These efforts have driven the exploration of innovative and effective plant protection strategies utilizing new active compounds. The examined substance, N-methyl-N-methoxyamide-7-carboxybenzo(1.2.3)thiadiazole (BTHWA), is a novel amide derivative of benzothiadiazole with the ability to induce systemic acquired resistance (SAR). This work presents a series of experiments conducted in the process of determining the appropriate technology for BTHWA use and proving its effectiveness in controlling CLS in sugar beet cultivation. It has been demonstrated that the application of treatments using BTHWA or BTHWA combined with a fungicide in a reduced number of treatments had the same effect on the reduction of plant infection with C. beticola and obtained root and technological sugar yields the same as those that resulted from the use of a full fungicidal treatment. The results provide grounds for reducing the use of fungicides by showing that the same effects can be attained by combining or replacing them with BTHWA.

1. Introduction

Growing world population requires an increase in the efficiency of agricultural production to meet the growing demand for food. To achieve this goal, it is crucial to provide effective protection against various pathogens, reducing the quantity and quality of the yields. The application of plant protection products (PPPs) has been the main procedure used for this purpose, as it is cheap, effective, and easy for farmers to follow. Unfortunately, it has been established beyond doubt that large-scale and prolonged use of pesticides poses a serious threat to the environment and humans [1,2]. The need to curb or even eliminate the use of pesticides has been recognized by the European Union, a leader in legislation on sustainable and ecological development. The measures that need to be introduced should reduce the adverse effects on humans and the environment as well as incentivize the development of procedures aimed at integrated plant protection based on the use of other methods. The resolution to undertake such actions is indicated in the “Farm to Fork Strategy”, which recommends a 50% reduction in the use of PPPs by 2030. Considering the acquisition of resistance to active ingredients of pesticides by pathogens, the reduction in their number will cause additional difficulties in providing effective protection. A rational step is to first eliminate the ones that are the most toxic to the environment, which usually is also the most effective against pathogens [3,4,5]. Their removal has driven the pursuit of novel and effective plant protection methods utilizing new active ingredients that comply with legal regulations and meet societal expectations [6].
Plants have developed defense mechanisms to protect themselves against pathogens. One of them is the phenomenon of systemic acquired resistance (SAR), which is activated in the plant after pathogen infection [7]. The signaling molecules that trigger the activation of SAR include salicylic acid (SA) and its derivatives, such as methyl salicylate (MeSA) [8]. Other compounds involved in SAR induction in plants are jasmonic acid (JA) and ethylene (ET) [9,10]. A large body of evidence indicates that SA and JA/ET pathways are involved in a complicated signaling network. Both negative [11] and positive [12,13] regulatory interactions describing the cross-talk between SA and JA/ET pathways have also been reported.
Pathogens can not only induce the SAR phenomenon in plants but can also induce the application of some natural [14,15] and chemical [16,17] compounds that mimic the pathogens that lead to such a response in the plant. A SAR inducer whose activity has been extensively studied is benzo(1.2.3)thiadiazole-7-carboxylic acid, S-methyl ester (BTH, ASM) [18,19]. This active substance was available on the market in Actigard and Bion 50 WG products marketed by Syngenta.
Reliable assessment of the effects of the use of resistance inducers should take into account not only the parameters describing the level of plant infection by the pathogens but also their growth, yield, or quality parameters describing the yield. The reason for such a wide approach is the risk of the growth–immunity trade-off phenomenon [20,21] related to SAR induction and, likewise, SAR regulated by salicylic acid [22]. The change in plant resource allocation related to SAR induction can lead to a reduction in yield [23]. Improper application of the tested SAR inducer, e.g., its use in a too high concentration, in too many treatments over the vegetation season, or in too short intervals between them, may produce this phenomenon. These aspects associated with the application of a particular resistance inducer are the major barrier to the fast introduction of such compounds into agricultural practice.
However, the development of a technology that would allow the appropriate use of a given SAR inducer is of high significance due to the advantages that these substances have over the standard plant protection products. The activity of SAR inducers permits overcoming the problem of pathogens’ resistance to pesticides. At the same time, it may lead to long-term plant resistance against a wide range of pathogens that remain even after the termination of resistance-inducer applications and usually last for weeks after the last application [24]. Another notable advantage is that SAR inducers can be applied at significantly lower doses compared to other plant protection products. As a result, a considerably smaller quantity of active substances is introduced into the environment, thereby greatly minimizing the potential negative impacts of their use in agricultural practice.
In our previous work, we focused on the synthesis of derivatives of benzo(1.2.3)thiadiazole-7-carboxylic acid with the aim of overcoming the main drawback of this substance, which was its low solubility. Novel derivatives, either in neutral or ionic form, maintained resistance-inducing properties and had improved solubility in water [25]. A group of dual-functional salts was also synthesized, with the second function of direct antifungal activity [26]. Another study utilizing the most effective plant resistance inducer identified by our research, N-methoxy-N-methylbenzo(1.2.3)thiadiazole-7-carboxamide (BTHWA), demonstrated strong induction efficacy, as validated by molecular analyses [27]. A higher level of marker genes, which are typical to demonstrate SAR induction in plants, has been observed in plants treated with BTHWA. Moreover, treatment with this substance resulted in a lower viral replication in tobacco plants that were infected with the TMV virus compared to the plants that were not treated with BTHWA before viral inoculation [26].
The general aim of this study undertaken was to check the effect of using a new active substance, namely N-methyl-N-methoxyamide-7-carboxybenzo(1.2.3)thiadiazoles (BTHWA), on the field cultivation of sugar beets. Sugar beets are mostly produced in EU countries. In 2020, Poland produced 14 million tons of sugar beets from an area of 245,900 ha [28]. Sugar extracted from beetroots has been a necessary ingredient in food, fuel, and pharmaceutical industries [29,30]. In the process of sugar production, the by-products are pulp and molasses. The pulp can be further used as animal feed or processed in biogas power plants, whereas molasses is used in the production of alcohol and organic acids or as a medium for yeast production. Sugar beet cultivation is of high importance not only in terms of economic aspects but also in terms of crop rotation, as it is beneficial to soil structure. The development of roots reaching deep into the soil also results in improved water management since the nitrogen from deeper soil layers is fixed, which reduces the amount that enters the groundwater [31].
Cercospora beticola Sacc., the fungus causing Cercospora leaf spot (CLS), is the most economically impactful pathogen of sugar beets, occurring worldwide [32]. Controlling C. beticola is of high importance, as it can even lead to complete leaf dieback. Cercosporin and beticolins are two types of toxins produced by C. beticola that participate in the infection process and the formation of necrosis on the leaves. As for beticolins, they cause loss of solutes from root tissues and inhibit ATP-dependent H+ transport [33]. Cercosporin affects diverse physiological cell functions, including proton transport and ATPase activity. Cell membranes are dissolved by cercosporin, which gives the fungal hyphae access to nutrients [34]. When the plant is not properly protected, it has to use stored sugar to rebuild the leaves, which leads to a reduction of both beetroot yield, up to 40%, and sugar yield, up to 10%. In that case, the plant has to use stored sugar to rebuild the leaves, which leads to a reduction of both beetroot yield, up to 40%, and sugar yield, up to 10% [35,36]. Additionally, increasing the contents of melassigenic elements, in particular sodium and α-amino nitrogen, in the roots leads to a decrease in the technological sugar yield [37]. The severity of the disease can be reduced by non-chemical and chemical methods. Non-chemical methods include elimination of weeds C. beticola, sowing resistant varieties, or appropriate crop rotation [38,39]. However, the use of fungicides still constitutes the main method of controlling C. beticola, even though this pathogen easily develops resistance toward active ingredients of some fungicides. This is mainly due to its short disease cycle, production of numerous spores, and high genetic variability. Repeated infections during the growing season require frequent fungicide treatments, which increases the selection pressure to form resistant strains [40,41]. As of September 2024, around 52 fungicides have been registered in Poland for the protection of beetroot against CLS, comprised of compounds from three various groups: triazoles (including epoxiconazole, tebuconazole, and difenoconazole), morpholines (including fenpropidin), and strobilurins (including azoxystrobin). Moreover, there is one multi-site fungicide that contains sulfur and copper. The entire C. beticola population already shows high resistance to azoxystrobin (unpublished data), making its application unwarranted. Such a small number of active substances approved for the control of C. beticola in sugar beet has stimulated the search for new and effective methods of plant protection based on the use of new active ingredients that should satisfy legal requirements, environmental issues, and societal expectations.
Diverse treatments were tested to determine if the new SAR inducer could substitute some or all of the fungicide treatments without inducing a growth–immunity trade-off.

2. Materials and Methods

2.1. Active Substance Used in This Study

The substance studied was N-methoxy-N-methylbenzo(1.2.3)thiadiazole-7-carboxamide (BTHWA) [42], which was designed and synthesized in our laboratory as a result of research on derivatization of the first commercially available “plant activator”, which is known under the names benzo(1.2.3)thiadiazole-7-carbothioic acid or S-methyl ester (acibenzolar-S-methyl ester, ASM, BTH, CGA245704) and its derivative in the form of benzo(1.2.3)thiadiazole-7-carboxylic acid. Both compounds, that is, BTHWA and its derivative, were used as a platform for designing the new compounds and performing research aimed at introducing such a modification of a chemical structure that will improve water solubility.
The substance BTHWA (99.9% purity) was used to prepare an SC (suspension concentrate)-type formulation containing 10 g of BTHWA per liter. As an insoluble substance, BTHWA was dispersed in a water medium with the addition of thickeners, stabilizers, and dispersants. That BTHWA formulation was used to obtain working solution with concentrations of 20 mg/L BTHWA. The amount of spray liquid was 400 L per hectare, which gives a dose of 8 g of BTHWA per hectare. The concentration was established on the basis of our earlier greenhouse experiments, the results of which have not yet been published. Moreover, the concentration of BTHWA used in this study corresponds to the concentration of BTH, which was recommended on the manufacturer’s label.

2.2. Locations and Characteristics of the Experimental Fields

A total of 11 field experiments in sugar beet cultivation were conducted between 2019 and 2021. In the first year of this study (year 2019), a preliminary experiment was conducted, the results of which were taken into account when determining treatments in subsequent experiments (years 2020 and 2021). All experimental plots were located in the Kuyavian–Pomeranian Voivodeship in Poland, and the characteristic features of each experimental plot are given in Table 1. A suitable crop rotation was maintained in each plot. Sugar beet was not cultivated more often than every 4 years. The meteorological data for all experimental periods were obtained from the weather station of Falęcin and are shown in Figure 1.

2.3. Plant Material

Field tests were conducted on two differentiated sugar beet varieties, Pacific and Mariza. Pacific (Maribo, Denmark) is a normal-type variety registered in 2018 and is characterized by resistance to rhizomania (caused by BNYVV) and Cercospora leaf spot (caused by Cercospora beticola) and increased resistance to powdery mildew, seedling rot, and beetroot tip rot. Mariza (Maribo, Denmark), on the other hand, is a normal sugar-type variety registered in 2020 and known to show resistance to rhizomania and powdery mildew.

2.4. Experimental Design

Each experiment had 4 replicates in a randomized block design. The five-row experimental plots were 22.5 m2 each (10 m long and 2.25 m wide). In 2019, only the var. Pacific sugar beets were used, whereas, in 2020 and 2021, both sugar beet varieties were sown. The sowing dates of the sugar beets in all experiments were in early April, while the harvest dates were in early October. The sowing was performed with a 6-row drill at a row spacing of 0.45 m. The spacing between plants was 0.18 m. The roots of sugar beets were harvested manually from an area of 10.08 m2.
Detailed schedules of performed treatments with plant protection products and tested substance BTHWA are provided in Table 2 and Table 3. Names of treatments indicated in the tables are used throughout the entire manuscript. The standard fungicide program (henceforth referred to as SFP) and the untreated control (henceforth referred to as UTC) were used as a reference in the field trials. Treatments were performed with a wheelbarrow sprayer intended to spray the experimental plots. The amount of spray liquid was 400 L per hectare.

2.5. Assessment of C. beticola Infection

The assessment of the CLS incidence and severity was made on plants from three middle rows within each block separately, consistent with the EPPO Standard scale [43]. It is a 10-point scale, where 0 means no symptoms of the disease, while 9 indicates completely destroyed foliage and occurrence of new leaves produced by the plant (Table 4). The disease incidence and severity were assessed on the day of harvesting plants. Within each block, 10 consecutive plants from each row were scored for the severity of CLS.

2.6. Determination of Root Yield Quality

A Venema auto-analyzer IIIG (Venema Consulting, Groningen, The Netherlands) was used for evaluation of qualitative parameters of sugar beets. Representative storage root samples of 30 kg from each plot were first washed, then ground to obtain a uniform pulp, and clarified with 0.3% Al2(SO4)3 solution. Potassium and sodium contents were determined by flame photometry, and α-amino nitrogen content (AmN) was analyzed using the fluorometric ortho-phthaldialdehyde (OPA) method. Polarimetry was used for determination of sucrose content (SC) in fresh taproots. White sugar yield (WSY) was calculated based on the Brunswick formula [44].
Sugar processing losses were calculated based on the formula of Buchholz et al. [44]
CT = 0.12 × (K + Na)+ 0.24 × (N-α-amines) + 0.48 [%],
where CT is the sugar processing loss [in %], and K, Na, and N-α-amines are the potassium, sodium, and α-amino nitrogen contents [mmol (100 g−1 fresh roots)].
Refined sugar content was calculated based on the formula of Buchholz et al. [45]:
RSC = Pol − CT − 0.6 [%]
where RSC is the refined sugar content [%]; Pol is the biological sugar content in roots—sugar polarization [in % fresh weight]; and CT is the sugar processing loss [%].
Technological sugar yield was calculated based on the formula of Trzebiński [45]:
TSY = RY × RSC × 100−1 [t ha−1]
where TSY is the technological sugar yield [%], RY is the root yield [t ha−1], and RSC is the refined sugar content [%]

2.7. Statistical Analysis

The data collected from the plants from the 4 blocks for each treatment were subjected to analysis of variance (ANOVA). The mean differences were subjected to comparison by post hoc test at a p < 0.05 level, according to Tukey’s HSD. Statistical analyses were performed with the OriginLab 2022 software for Windows (OriginLab Corp., Northampton, MA, USA)

3. Results

3.1. Meteorological Data

Weather conditions are given in Figure 1. As follows, the warmest month of 2019 was June, with an average daily temperature of 21.4 °C, which was 5.0 °C higher than the 2000–2017 average. In 2020, August was the month with the highest average daily temperature of 19.8 °C, which was 1.2 °C higher than the August average daily temperature observed in the multi-year period. In 2021, the warmest month was July, with an average daily temperature of 21.3 °C.
The highest total precipitation during the experimental period was recorded in 2021. It was equal to 410 mm and was 7 mm higher than the average precipitation recorded during the same period of the years 2000–2017. In both 2019 and 2020, precipitation totals during the sugar beet growing season were lower than the many-year average for the same period of the year. The driest year was 2019, with an April–September rainfall total of 300 mm, 104 mm lower than the average many-year total recorded in 2000–2017.
Although the precipitation over the growing season in 2021 was the highest of those in the 3 years studied and higher than the average long-term precipitation, a significant anomaly was observed in the month of June. In 2021, the average precipitation was lower than in 2019 and 2020 and lower than the long-term average, while at the same time, the daily temperature was higher than in 2019 and the long-term average. The occurrence of reduced precipitation in June, when beet water demand is high, reduced root yields at all three locations (see Section 2.4).

3.2. Experiment 2019

In our preliminary experiment, we decided to apply a SAR inducer every 10 to 14 days based on the results of our previous studies on plant–pathogen models. The same assumptions were applied to this field experiment to provide effective induction of SAR in a more complex system than in the greenhouse experiments. However, the application of a total of seven treatments with BTHWA resulted in overstimulation of the plant, which was in line with the growth–immunity trade-off postulate (Table 5).
The same applies to the technological sugar yield. The percentage of sugar polarization was the highest in the SFP treatment and the lowest in the BTHWA + FUNGICIDE treatment.
The most effective protection was observed in plants subjected to SFP and BTHWA + FUNGICIDE treatments. The second-best protection against CLS was observed in plants subjected to BTHWA (seven times) treatment.

3.3. Experiment 2020

An analysis of the results from 2019 led us to the conclusion that proper adjustment of treatment schedules is of key importance. It was expected that we would observe a significant reduction in disease severity at a level comparable to that of plants protected with fungicides. Thus, the total number of treatments with BTHWA was reduced to either three or four treatments.

3.3.1. Location A

The highest root yield in the experiment with var. Pacific sugar beets was obtained using the SFP treatment (Table 6). However, apart from the results for UTC, the yields attained in all other treatments belonged to the same statistical group, with those for the plants in the BTHWA + FUNGICIDE 1 treatment being the lowest among them. As for the technological sugar yield, the yields obtained for the treatments SFP, BTHWA (four times), and BTHWA + FUNGICIDE 2 were significantly higher relative to those in the other treatments.
The most effective protection was observed in plants subjected to the SFP and BTHWA + FUNGICIDE 1. The second-best protection against CLS was observed in plants treated with BTHWA (four times) and BTHWA + FUNGICIDE 2.
The overall pattern of results remains similar in the experiment conducted on var. Mariza sugar beets (Table 7). The highest root yield was obtained for the plants treated in the SFP treatment. However, apart from UTC and the plants treated with BTHWA + FUNGICIDE 1, the root yields for the plants treated with all other treatments were not significantly different from those of SFP. Values of technological sugar yield follow a similar pattern as those of root yield.
The most effective protection against the disease was achieved for the plants subjected to the SFP, BTHWA + FUNGICIDE 1, and BTHWA + FUNGICIDE 2 treatments. Treatment using BTHWA (four times) provided the second-best protection against CLS. The value of infection on the EPPO scale obtained for BTHWA (four times) was significantly lower compared to the value observed for BTHWA (three times) treatment.

3.3.2. Location B

Regardless of the treatment, no differences were found in the root yield in location B in the experiment conducted on var. Pacific sugar beets (Table 8). However, there was a trend toward increasing technological sugar yield observed in the plants subjected to all tested treatments relative to that of UTC.
As for the level of infection with CLS, the lowest value on the EPPO scale was observed for the plants subjected to BTHWA + FUNGICIDE 2 treatment. The second lowest value on the EPPO scale was observed for the plants subjected to SFP treatment.
Results of the study carried out on var. Mariza sugar beets showed significant differences in root yield, with the highest value observed in SFP treatment (Table 9). The second highest value was observed in BTHWA (four times) treatment, which was not significantly different from that for the plants in SFP.
Significant differences were observed in the nitrogen content. The highest values were obtained for the plants treated with BTHWA (three times), while the lowest ones were for UTC.
The highest value of technological sugar yield was obtained for the plants treated with SFP, while the second highest one was observed for those treated with BTHWA (four times) (not significantly different from those in the SFP variant). A significant difference in technological sugar yield obtained after BTHWA (four times) was significantly higher than this obtained after BTHWA (four times).
The most effective protection against the disease was achieved for the plants subjected to the BTHWA + FUNGICIDE 1 treatment. Treatment according to BTHWA (three times) and BTHWA + FUNGICIDE 2 provided the second-best protection against CLS.

3.3.3. Location C

The treatment of var. Pacific plants with the variant SFP resulted in a significant increase in the root yield (Table 10). However, the values obtained for the plants treated with variants BTHWA (four times) and BTHWA + FUNGICIDE 2 were not statistically different from those obtained for the sugar beets subjected to SFP treatment. The overall pattern of results obtained for technological sugar yield remains similar to that of root yield; however, the value obtained for the plants treated with BTHWA (four times) was not statistically different than that obtained after SFP treatment.
Statistical differences were also found in the sodium content in the pulp. The lowest values were observed for the plants treated with variants UTC and BTHWA + FUNGICIDE 2, while the other values were higher; although, only for the plants after BTHWA (four times) and BTHWA (three times) treatment was the difference was statistically significant.
The lowest value of infection on the EPPO scale was found in the plants treated with SFP. The second lowest value was observed for the sugar beets subjected to the BTHWA + FUNGICIDE 2 treatment.
All treatments performed on var. Mariza sugar beets resulted in increased yield and increased technological sugar compared to the UTC (Table 11).
The lowest values of infection on the EPPO scale were observed for the plants treated with SFP, BTHWA + FUNGICIDE 1, and BTHWA + FUNGICIDE 2. The values of this parameter observed for plants subjected to BTHWA (three times) and BTHWA (four times) treatments were significantly lower compared to UTC plants.

3.4. Experiment 2021

3.4.1. Location B

The treatment of plants using the UTC variant resulted in the lowest root yield in this location for the experiment conducted on var. Pacific sugar beets. Except for the plants subjected to the BTHWA + FUNGICIDE 1 variants, the root yield of the plants in all other treatments was statistically higher than that determined for UTC (Table 12). The results of technological sugar yield followed the same pattern.
The most effective protection was observed for the plants subjected to BTHWA + FUNGICIDE 1 treatment. The second-best protection was found in the plants subjected to BTHWA + FUNGICIDE 2.
As for the experiment conducted on var. Mariza sugar beets (Table 13), all experimental variants either consisting of treatment only with BTHWA or combined use of BTHWA and fungicide resulted in obtaining higher root yields compared to those for UTC and SFP treatments, even though the results for the plants after SFP treatment were not statistically different from the results for plants of UTC (Table 13).
Statistical differences were also found in the nitrogen content in the pulp, which was the highest in the plants treated with BTHWA (three times) treatment.
The lowest value of infection on the EPPO scale was observed for the plants subjected to SFP, BTHWA (four times), BTHWA + FUNGICIDE 1, and BTHWA + FUNGICIDE 2 treatments.

3.4.2. Location C

The general conditions for beet growth were less favorable in this location, which is manifested by the lower values of root yield for the sugar beets subjected to all tested treatments in the experiment conducted on var. Pacific sugar beets (Table 14). The highest value was found for the sugar beets treated with the variant BTHWA (three times). The second highest value was found for the plants treated with SFP, and it was not significantly different than that for the plants treated with BTHWA (three times). The root yield found for the plants treated with the other variants was higher than that for UTC, although the difference was not statistically significant. The results of technological sugar yield followed a similar pattern.
The lowest value of infection on the EPPO scale was observed for the plants subjected to BTHWA (four times), BTHWA + FUNGICIDE 1, and BTHWA + FUNGICIDE 2 treatments. Values obtained for the mentioned treatments were significantly lower compared to those obtained for SFP treatment.
The differences in the root yield among the plants subjected to all experimental treatments on var. Mariza sugar beets (Table 15) in this location are not statistically significant. However, the highest root yield was obtained for the plants treated using the variants SFP, BTHWA (three times), BTHWA + FUNGICIDE 1, and BTHWA + FUNGICIDE 2. The results of technological yield followed the same pattern; however, the treatment with the variant BTHWA (three times) resulted in a higher technological sugar yield.
The most effective protection was observed for the plants subjected to BTHWA (four times), BTHWA (three times), and BTHWA + FUNGICIDE 1 treatments.

4. Discussion

As the necessity for sustainable development aimed at the reduction of the use, risk, and dependence on pesticides has been well recognized, the development of new active substances that can be used in agriculture is of key importance. Novel substances have to be designed with the aim of not only providing effective protection but also improving plant health and crop quality and meeting legal requirements related to the safety of their use. Such an approach is in line with green chemistry principles, indicating the need to design safer chemicals whose use brings the same biological results yet reduces the impact on the environment.
Results of the previous study indicate that the use of pesticides can be reduced or even replaced by the use of BTHWA, a synthetic plant elicitor developed in our laboratories, which is capable of inducing SAR. The effectiveness of SAR induction in field trials could be affected by a number of environmental factors or crop nutrition; however, the extent to which these factors influence the overall plant response is still inadequately described [46]. Thus, it was decided to analyze each experiment separately rather than perform a combined analysis. In each of them, attention was paid to analyzing whether the results for the tested variants, assuming the use of either BTHWA or BTHWA combined with fungicide, belong to the same statistical group as those obtained for the standard fungicide treatment.
Analysis of the results obtained in 2019 indicated that overstimulation of plants that were treated with BTHWA seven times was related to the occurrence of the growth–immunity trade-off phenomenon. It was expected that such a large number of treatments would ensure effective protection of plants and thus also allow a higher yield of roots or technological sugar. However, the results obtained for the plants treated with BTHWA substance, although higher than the control, were not statistically different from it. Therefore, we decided to reduce the number of treatments in the following years to lower the energetic expenditure of plants needed to develop resistance. As the literature suggests, too high doses or too frequent applications of resistance inducers may hinder the pace of plant growth, leaf deformation, or decreased yield [27,47,48].
As a general conclusion, it should be noted that when applying only BTHWA, better effects in the context of providing effective protection of plants and obtaining higher yields are achieved after four, not three, treatments. The question arises, however, whether the total number of treatments performed was of importance here or whether the fourth term of treatment was of key importance in achieving such a plant response. Further research on optimal terms and a number of treatments is to be conducted.
A decrease in root yield or sugar technological yield relative to those observed for UTC was not observed for any of the performed experiments. Even in the preliminary experiment conducted in 2019, an increase in the values of both parameters was observed in relation to those noted for UTC. Therefore, it should be concluded that the tested treatments do not cause excessive overstimulation of metabolism, which is understood as a growth–immunity trade-off and could lead to a reduction in beet yield. Similar results were observed when BTHWA was applied to tomato plants cultivated in field conditions [49]. The aim of this work was originally to check the extent to which the growth–immunity trade-off will occur. Therefore, a total of nine treatments were performed with BTHWA at the same concentration as that applied to sugar beet plants, i.e., 20 mg/L, and at a concentration twice as high, i.e., 40 mg/L. As a result, even for the treatment assuming nine applications of BTHWA at a concentration of 40 mg/L, no yield reduction compared to that of UTC was observed. Surprisingly, a slight increase in the values of some parameters describing the tomato yield was noted, although this increase was not always significant. For the treatments assuming a smaller number of treatments, i.e., six ones, a significant increase in the quantitative and qualitative parameters of the yield compared to those for UTC was observed [50]. The appropriate selection of treatment terms is very important, as in the case of the previously discussed difference in response of sugar beet plants treated with variants BTHWA (three times) and BTHWA (four times). This issue could be of high importance in the context of proposing a final technology for using SAR inducers such as BTHWA, which is more difficult to develop than that of PPPs.
Dependence on PPPs and their extensive use in agriculture negatively affects the environment in a variety of ways. One of them is the risk associated with pathogens acquiring resistance to the active substance of pesticides. Resistance acquisition in the form of cross-resistance takes place when a pathogen develops resistance to a particular substance, which leads to the acquisition of resistance to more compounds that can be made resistant by similar mechanisms [50]. Another scenario of resistance acquisition is co-selection, which occurs when the selection of one gene providing resistance is coupled with a selection of another resistance gene [51]. Although the process of acquiring resistance via microbes is natural, its acceleration propelled the emergence of negative consequences [52]. Counteracting this risk assumes the use of various active substances during the vegetative season. However, with a decreasing number of active ingredients authorized for use, effective protection becomes a challenge [3]. Another risk is related to non-target organisms, e.g., pollinators, that are also affected when treatments with PPPs are performed with the aim of controlling target organisms [53]. All the above-mentioned issues justify the need to search for new active substances that can be an alternative to PPPs, providing sufficient protection as well as satisfying legal and societal expectations.
Numerous advantages of SAR inducers should be pointed out when comparing them to PPPs. Firstly, SAR inducers provide protection against a wide range of pathogens. The possibility of controlling pathogens of viral origin constitutes a great advantage compared to PPPs which can only be used to control, e.g., aphids, which are vectors of viral diseases [54]. Secondly, the state of induction of the plant resistance effect lasts over time, even up to weeks after the last application of SAR inducer, while the effectiveness of treatments with PPPs is strictly dependent on the time of application [55]. Thirdly, neither a direct impact on the development of microorganisms, including pathogens, nor the development of pathogens resistance is expected [5]. This is because the action of resistance inducers is directed toward plants and not a pathogen. Thus, research on the use of SAR inducers should be widely conducted. Research in this area may contribute to the implementation of assumptions related to ensuring sustainable food production recommended in the “Farm to Fork Strategy”. It indicates the need to take action to reduce the number of PPPs used because they contribute to soil, water, and air pollution; biodiversity loss; and can harm non-target organisms. The goal set by the European Union is to lower the use of PPPs by 50%. One of the methods to achieve this might be the replacement of PPPs with SAR inducers. However, the condition for this to be possible is that SAR inducers will both provide an appropriate level of protection against diseases and be free from the threats posed by PPPs.
Of the SAR inducers tested, many reports indicate the use of ASM, which is the active substance of product BION or Actigard and is chemically related to the structure of the investigated BTHWA. Bargabus et al. have shown that the use of acibenzolar-S-methyl (ASM) activated the resistance mechanisms in sugar beetroot [56]. Felipini and di Piero have reported a reduction of symptoms of C. beticola infestation in red beet as a result of ASM application in a dose of 25 mg/L 24 or 72 h before inoculation with this pathogen [57]. Other studies indicate the combined use of SAR inducers and fungicides. Romero et al. [48], who tested the effectiveness of ASM for the protection of pepper against Xanthomonas axonopodis pv. vesicatoria in a four-year study, tested nine combinations of treatments with a resistance inducer, copper hydroxide, and maneb fungicide in different proportions and configurations. Each year, a selected plot of plants was subjected to standard protection procedures with copper hydroxide and maneb. The variant with application of ASM in a dose of 17 g ha–1, which permitted a limitation of the use of copper hydroxide and maneb, was found effective in protection against C. beticola relative to controls and, in general, was statistically not less effective than the standard protection procedure. Combined application of ASM in a dose of 25 mg/L and reduced by half dose of copper hydroxide (from 800 mg/L to 400 mg/L) was more effective against X. campestris pv. vesicatoria in pepper than a full dose of copper hydroxide [58]. Induction of SAR at a sufficient level caused an increase in the yield of sugar beetroot. The strategy of sugar beet protection against CLS has also brought an increase in the sugar beetroot yield relative to controls when using biological products (containing Trichoderma viride) combined with fungicide treatment [59]. The results presented in these articles are in line with the findings of our studies.
In our previous work, we have shown that the application of both resistance inducer and fungicide (in a lower number of treatments than when used alone) resulted in similar levels of protection against CLS disease and achieved technological sugar yield comparable to that after the application of fungicides [60]. In this study, we investigated the effects of the application of another SAR inducer we developed, which is an ionic derivative of salicylic acid named choline 3,5-dichlorosalicylate (3,5diClSal). As for the treatment assuming four applications of 3,5diClSal, the obtained root yield and technological sugar yield were at the same level as for the plants treated with a reduced fungicide program (assuming one application of fungicide instead of two applications). As expected, the values of the above-mentioned parameters obtained for both treatment variants were significantly lower than those obtained for the variant with full fungicide protection (assuming two applications of fungicide) and significantly higher than those for the variant of untreated control. As for the treatments assuming the combined use of 3,5diClSal and fungicide, better effects on plants were observed when the treatment consisted of four applications of 3,5diClSal with reduced fungicide treatment (assuming one fungicide application instead of two) and not three applications of 3,5diClSal with reduced fungicide treatment [60].
SAR inducers’ mode of action is directed toward the stimulation of plants’ natural defense mechanisms and not toward pathogens directly. BTH, the parent compound of BTHWA, was classified as not antimicrobial, as it did not show any direct effect on the number of plant pathogens in in vitro studies [61]. The direct influence of BTH on C. beticola development in plate tests indicated that a reduction in conidia germination was not found with BTH treatment [62]. Contrasting results were found for chitosan, which is a substance with both SAR induction and antimicrobial activity [62]. In conclusion, it was indicated that in the case of BTH, only SAR induction activity was responsible for the reduction of C. beticola infestation on sugar beets [62]. As indicated in our different studies considering BTHWA, no direct effect on Fusarium spp. fungi was observed. Our preliminary unpublished data from in vitro tests conducted on Alternaria alternata, Trichoderma viride, and Erwinia amylovora led to the same conclusion.
As for the implications of the results obtained, they provide an insight into the number of treatments with SAR inducers that should be performed during the growing season. Secondly, it can be concluded that even when seven applications of BTHWA were performed, the occurrence of growth–immunity trade-off was not observed. Most of the research on growth–immunity trade-offs has been conducted in controlled conditions when the influence of other factors on plants is limited. However, it is difficult to transfer the results and observations of such studies to experiments performed in field conditions. Therefore, it is necessary to make certain assumptions regarding the schedule of treatment tested. It seems scientifically and economically reasonable to first perform field studies on the selection of best-performing treatments and only then to conduct more detailed analyses, including those related to SAR-related parameters.
Due to the fact that work on the technology of BTHWA use in agriculture is in the initial phase, the introduction of this substance into agricultural practice will face some challenges. It should be highlighted that the schedule of treatment presented in this work should not be treated as a target but rather as a starting point for establishing the right treatment schedule for subsequent experiments. Further agronomical research on the terms and number of treatments needs to be performed. The long-term goal is to develop a technology for the use of BTHWA that will result in the best efficiency in terms of ensuring effective protection against the disease and a positive impact on the yield. Other challenges concern environmental issues related to BTHWA. It should be noted that the parent compound BTH passed all tests required for its market authorization. Thus, it is expected that the environmental impact of BTHWA will be at a similar level as that of BTH, so the substance will also be authorized for use. However, reaching such a conclusion will only be possible after conducting appropriate research in the relevant area. Among tasks not directly related to the area of agriculture, an important challenge will be to develop an appropriate synthesis method on a scale sufficient to obtain BTHWA at appropriate cost and quantity.

5. Conclusions

In this study, we have shown that the use of BTHWA provides efficient protection against C. beticola. What is more, obtaining SAR induction at such an appropriate level was not associated with the occurrence of a growth–immunity trade-off, which would be manifested by a reduction in the obtained yield. It has been demonstrated that for some of the tested treatments assuming the use of BTHWA or BTHWA combined with a fungicide, the effect on the reduction of plant infection caused by C. beticola and obtained yield was statistically the same as that resulted from the use of fungicides alone. The application of combined protection involving the use of SAR inducer and fungicide (in a reduced dose) resulted in a similar level of protection against C. beticola as the full fungicidal treatment. However, the number of applications of protective means to ensure a similar final yield is higher when applying a resistance inducer or a resistance inducer and a fungicide than when applying a fungicide only. The plant protective measures based on the use of resistance inducers are more expensive, but their use is effective and very attractive in view of the EU strategy “Farm to Fork”, which aims to reduce the use of plant protection products by 50% by 2030.

Author Contributions

Conceptualization, A.K., M.S. (Maciej Spychalski), R.K. and M.S. (Marcin Smiglak); methodology, A.K., M.S. (Maciej Spychalski), R.K. and K.P.; formal analysis, A.K. and M.S. (Maciej Spychalski); investigation, A.K., M.S. (Maciej Spychalski), R.K., M.S. (Marcin Smiglak) and A.Z.; resources, A.K., M.S. (Maciej Spychalski), R.K. and M.S. (Marcin Smiglak); writing—original draft preparation, A.K., M.S. (Maciej Spychalski), R.K. and M.S. (Marcin Smiglak); writing—review and editing, A.K., M.S. (Maciej Spychalski), R.K., M.S. (Marcin Smiglak), A.Z. and K.P.; supervision, M.S. (Marcin Smiglak); project administration, M.S. (Marcin Smiglak); funding acquisition, M.S. (Marcin Smiglak). All authors have read and agreed to the published version of the manuscript.

Funding

The “New plant resistance inducers and their application as innovative approach to plant protection against pathogens” project is carried out within the TEAMTECH (POIR.04/04.00-00-5BD9/17-00) program of the Foundation for Polish Science co-financed by the European Union under the European Regional Development Fund. Statutory Topic SIT-02 is carried out at the Field Experimental Station in Toruń of the Plant Protection Institute, National Research Institute, in Poznań.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data presented in this study are available upon request from the corresponding author.

Conflicts of Interest

The authors declare no conflicts of interest.

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Agriculture 15 00605 g001
Figure 1. Weather conditions at experimental location Falecin in the years 2019–2021.
Figure 1. Weather conditions at experimental location Falecin in the years 2019–2021.
Agriculture 15 00605 g001
Table 1. Description of experimental sites.
Table 1. Description of experimental sites.
Year of ExperimentName and Symbol of Location Geographical CoordinatesSoil CharacteristicspH
2019Falęcin (A)53°13′54″ N 18°32′51″ Esandy loam6.5
2020Falęcin (A)53°13′54″ N 18°32′51″ Esandy loam5.8
2020Skąpe (B)53°13′06″ N 18°36′33″ Esandy loam7.4
2020Stolno (C)53°19′20″ N 18°30′17″ Esandy loam6.5
2021Skąpe (B)53°13′06″ N 18°36′33″ Esandy loam6.3
2021Stolno (C) 53°19′20″ N 18°30′17″ Esandy loam6.9
Table 2. The timetable of treatments in the experiment in 2019.
Table 2. The timetable of treatments in the experiment in 2019.
Treatment Dates of Application
03.0713.0723.0702.0812.0814.0822.0803.09
UTC
SFP Safir 125SC Spyrale
475EC
BTHWABTHWABTHWABTHWABTHWABTHWA BTHWABTHWA
BTHWA + FUNGICIDEBTHWABTHWABTHWABTHWABTHWASpyrale
475 EC		BTHWABTHWA
UTC (untreated control)—sugar beets that were treated with neither BTHWA nor with fungicides; SFP (standard fungicide program)—sugar beets treated with fungicide 2 times; BTHWA—plants that were treated only with BTHWA; BTHWA + FUNGICIDE plants that were treated both with fungicides and BTHWA. Safir 125 SC (ADAMA, Warsaw, Poland) active substance: epoxiconazole (125 g L–1); Spyrale 475 EC (ADAMA, Warsaw, Poland) active substance: fenpropidin (375 g L–1), difenoconazole (100 g L–1).
Table 3. The timetable of treatments in the experiment in 2020 and 2021.
Table 3. The timetable of treatments in the experiment in 2020 and 2021.
Treatment Dates of Application
24.0630.0607.0715.0705.08
UTC
SFP Skymaster
280SC		 Spyrale
475EC
BTHWA (4 times)BTHWABTHWA BTHWABTHWA
BTHWA (3 times)BTHWABTHWA BTHWA
BTHWA + FUNGICIDE 1BTHWABTHWA BTHWASpyrale
475EC
BTHWA + FUNGICIDE 2BTHWABTHWA Spyrale
475EC		BTHWA
UTC (untreated control)—sugar beets that were treated with neither BTHWA nor with fungicides; SFP (standard fungicide program)—sugar beets treated with fungicide 2 times; BTHWA—plants that were treated only with BTHWA; BTHWA + FUNGICIDE plants that were treated both with fungicides and BTHWA. Skymaster 280 SC (ADAMA, Warsaw, Poland) active substance: azoxystrobin (200 g L–1), cyproconazole (80 g L–1); Spyrale 475 EC (ADAMA, Warsaw, Poland) active substance: fenpropidin (375 g L–1), difenoconazole (100 g L–1).
Table 4. EPPO scale for assessment of the level of infection with C. beticola.
Table 4. EPPO scale for assessment of the level of infection with C. beticola.
Degree of Infection on the EPPO ScaleDescriptionInfected Leaf Area [%]
0no symptoms0
1single spots on the leaf0.1–1
2single spots on the leaf1–2
3moderately numerous spots on the leaf that begin to merge2–4
4numerous spots on the leaf that are merged together 5–9
5numerous spots on the leaves10–24
6numerous spots on the leaves25–49
7numerous spots on the leaves50–74
8numerous spots on the leaves75–94
9numerous spots on the leaves, new leaves begin to develop95–100
Table 5. Summary of the results of the field experiment conducted in 2019 on var. Pacific sugar beet in location A.
Table 5. Summary of the results of the field experiment conducted in 2019 on var. Pacific sugar beet in location A.
TreatmentRoot Yield [t/ha]Sugar Polarization [%]Potassium Content [mmol 1000 g–1 of Pulp]Sodium Content [mmol 1000 g–1 of Pulp]Nitrogen Content [mmol 1000 g–1 of Pulp]Technological Sugar Yield [t/ha]Mean Value of Infection on the EPPO Scale [0–9]
UTC70.50 a17.63 ab33.23 4.3314.0311.11 a4.5 c
SFP78.64 b18.02 b34.28 3.9513.7512.69 b2.25 a
BTHWA (7 times)74.84 a17.37 ab33.18 5.3515.4311.55 a3.5 b
BTHWA (7 times) + FUNGICIDE71.95 a17.18 a33.48 5.1316.0510.97 a2.75 a
Mean values marked with common letters do not differ significantly at p = 0.05, according to Tukey’s HSD. UTC—sugar beets that were treated neither with BTHWA nor with fungicides; SFP—sugar beets treated with fungicides; BTHWA—sugar beets treated with tested substance BTHWA; BTHWA + FUNGICIDE—sugar beets treated both with BTHWA and fungicide. The timetable of applications performed is provided in Table 2.
Table 6. Summary of the results of the field experiment conducted in 2020 on var. Pacific sugar beet in location A.
Table 6. Summary of the results of the field experiment conducted in 2020 on var. Pacific sugar beet in location A.
TreatmentRoot Yield [t/ha]Sugar Polarization [%]Potassium Content [mmol 1000 g–1 of Pulp]Sodium Content [mmol 1000 g–1 of Pulp]Nitrogen Content [mmol 1000 g–1 of Pulp]Technological Sugar Yield [t/ha]Mean Value of Infection on the EPPO Scale [0–9]
UTC70.31 a15.4634.456.7011.939.56 a6.96 d
SFP79.37 c16.2432.855.6310.4311.47 b4.25 a
BTHWA (4 times)77.11 bc16.0534.735.0811.3010.96 b5.25 b
BTHWA (3 times)76.04 bc15.6532.856.3311.9810.51 ab5.75 c
BTHWA + FUNGICIDE 173.43 abc16.0435.255.4511.1510.43 ab4.5 a
BTHWA + FUNGICIDE 2 76.86 bc16.1134.605.5810.8810.99 b5.25 b
Mean values marked with common letters do not differ significantly at p = 0.05, according to Tukey’s HSD. UTC—sugar beets that were treated neither with BTHWA nor with fungicides; SFP—sugar beets treated with fungicide 2 times; BTHWA (4 times)—sugar beets treated with tested substance BTHWA 4 times; BTHWA (3 times)—sugar beets treated with tested substance BTHWA 3 times; BTHWA + FUNGICIDE 1—sugar beets treated both with BTHWA and fungicide on the third treatment date; BTHWA + FUNGICIDE 2—sugar beets treated both with BTHWA and fungicide on the fourth treatment date. The timetable of applications performed is provided in Table 3.
Table 7. Summary of the results of the field experiment conducted in 2020 on var. Mariza sugar beet in location A.
Table 7. Summary of the results of the field experiment conducted in 2020 on var. Mariza sugar beet in location A.
Treatment Root Yield [t/ha]Sugar Polarization [%]Potassium Content [mmol 1000 g–1 of Pulp]Sodium Content [mmol 1000 g–1 of Pulp]Nitrogen Content [mmol 1000 g–1 of Pulp]Technological Sugar Yield [t/ha]Mean Value of Infection on the EPPO Scale [0–9]
UTC68.69 a14.9937.005.80 bc11.339.02 a7 d
SFP78.01 c16.0634.134.45 a10.3311.14 c5 a
BTHWA (4 times)77.09 bc15.4037.584.73 ab11.6510.43 bc5.5 b
BTHWA (3 times)75.58 bc15.4335.986.15 b12.9010.22 bc6 c
BTHWA + FUNGICIDE 173.02 a15.5436.205.20 abc10.0810.02 abc4.75 a
BTHWA + FUNGICIDE 2 73.88 bc15.9735.734.50 a10.4510.46 bc5 a
Mean values marked with common letters do not differ significantly at p = 0.05, according to Tukey’s HSD. UTC—sugar beets that were treated neither with BTHWA nor with fungicides; SFP—sugar beets treated with fungicide 2 times; BTHWA (4 times)—sugar beets treated with tested substance BTHWA 4 times; BTHWA (3 times)—sugar beets treated with tested substance BTHWA 3 times; BTHWA + FUNGICIDE 1—sugar beets treated both with BTHWA and fungicide on the third treatment date; BTHWA + FUNGICIDE 2—sugar beets treated both with BTHWA and fungicide on the fourth treatment date. The timetable of applications performed is provided in Table 3.
Table 8. Summary of the results of the field experiment conducted in 2020 on var. Pacific sugar beet in location B.
Table 8. Summary of the results of the field experiment conducted in 2020 on var. Pacific sugar beet in location B.
TreatmentRoot Yield [t/ha]Sugar Polarization [%]Potassium Content [mmol 1000 g–1 of Pulp]Sodium Content [mmol 1000 g–1 of Pulp]Nitrogen Content [mmol 1000 g–1 of Pulp]Technological Sugar Yield [t/ha]Mean Value of Infection on the EPPO Scale [0–9]
UTC69.1316.1034.684.7022.789.67 a7 c
SFP70.7316.4531.834.2319.3010.24 ab6.25 b
BTHWA (4 times)72.3416.1335.854.5521.2510.16 ab6 ab
BTHWA (3 times)71.3315.9933.354.9322.289.93 ab6 ab
BTHWA + FUNGICIDE 171.4116.1735.054.4821.6310.07 ab5.75 ab
BTHWA + FUNGICIDE 2 72.0416.2033.384.1821.3010.20 ab5.5 a
Mean values marked with common letters do not differ significantly at p = 0.05, according to Tukey’s HSD. UTC—sugar beets that were treated neither with BTHWA nor with fungicides; SFP—sugar beets treated with fungicide 2 times; BTHWA (4 times)—sugar beets treated with tested substance BTHWA 4 times; BTHWA (3 times)—sugar beets treated with tested substance BTHWA 3 times; BTHWA + FUNGICIDE 1—sugar beets treated both with BTHWA and fungicide on the third treatment date; BTHWA + FUNGICIDE 2—sugar beets treated both with BTHWA and fungicide on the fourth treatment date. The timetable of applications performed is provided in Table 3.
Table 9. Summary of the results of the field experiment conducted in 2020 on var. Mariza sugar beet in location B.
Table 9. Summary of the results of the field experiment conducted in 2020 on var. Mariza sugar beet in location B.
TreatmentRoot Yield [t/ha]Sugar Polarization [%]Potassium Content [mmol 1000 g–1 of Pulp]Sodium Content [mmol 1000 g–1 of Pulp]Nitrogen Content [mmol 1000 g–1 of Pulp]Technological Sugar Yield [t/ha]Mean Value of Infection on the EPPO Scale [0–9]
UTC65.86 a16.0134.683.2014.00 a9.22 a7.25 c
SFP76.25 d16.3433.703.2018.08 bc10.97 e6.5 b
BTHWA (4 times)75.62 cd16.0233.333.0819.05 bc10.61 de6.5 b
BTHWA (3 times)69.54 b15.9335.633.6520.85 c9.65 ab6 ab
BTHWA + FUNGICIDE 172.37 bc16.2135.682.4318.85 bc10.29 cd5.75 a
BTHWA + FUNGICIDE 2 69.41 b16.4134.402.4816.90 ab10.05 bc6.25 ab
Mean values marked with common letters do not differ significantly at p = 0.05, according to Tukey’s HSD. UTC—sugar beets that were treated neither with BTHWA nor with fungicides; SFP—sugar beets treated with fungicide 2 times; BTHWA (4 times)—sugar beets treated with tested substance BTHWA 4 times; BTHWA (3 times)—sugar beets treated with tested substance BTHWA 3 times; BTHWA + FUNGICIDE 1—sugar beets treated both with BTHWA and fungicide on the third treatment date; BTHWA + FUNGICIDE 2—sugar beets treated both with BTHWA and fungicide on the fourth treatment date. The timetable of applications performed is provided in Table 3.
Table 10. Summary of the results of the field experiment conducted in 2020 on var. Pacific sugar beet in location C.
Table 10. Summary of the results of the field experiment conducted in 2020 on var. Pacific sugar beet in location C.
TreatmentRoot Yield [t/ha]Sugar Polarization [%]Potassium Content [mmol 1000 g–1 of Pulp]Sodium Content [mmol 1000 g–1 of Pulp]Nitrogen Content [mmol 1000 g–1 of Pulp]Technological Sugar Yield [t/ha]Mean Value of Infection on the EPPO Scale [0–9]
UTC73.71 a17.2134.833.30 a12.3011.34 a7 e
SFP85.44 c17.6834.233.83 ab12.3313.54 c4 a
BTHWA (4 times)82.91 bc17.0334.034.63 b13.8812.57 bc5.5 cd
BTHWA (3 times)77.13 ab16.8633.954.48 b12.2311.59 ab6 d
BTHWA + FUNGICIDE 178.69 ab17.4635.404.18 ab14.9012.23 b5 bc
BTHWA + FUNGICIDE 2 80.32 bc17.0736.753.33 a15.2512.17 b4.5 ab
Mean values marked with common letters do not differ significantly at p = 0.05, according to Tukey’s HSD. UTC—sugar beets that were treated neither with BTHWA nor with fungicides; SFP—sugar beets treated with fungicide 2 times; BTHWA (4 times)—sugar beets treated with tested substance BTHWA 4 times; BTHWA (3 times)—sugar beets treated with tested substance BTHWA 3 times; BTHWA + FUNGICIDE 1—sugar beets treated both with BTHWA and fungicide on the third treatment date; BTHWA + FUNGICIDE 2—sugar beets treated both with BTHWA and fungicide on the fourth treatment date. The timetable of applications performed is provided in Table 3.
Table 11. Summary of the results of the field experiment conducted in 2020 on var. Mariza sugar beet in location C.
Table 11. Summary of the results of the field experiment conducted in 2020 on var. Mariza sugar beet in location C.
TreatmentRoot Yield [t/ha]Sugar Polarization [%]Potassium Content [mmol 1000 g–1 of Pulp]Sodium Content [mmol 1000 g–1 of Pulp]Nitrogen Content [mmol 1000 g–1 of Pulp]Technological Sugar Yield [t/ha]Mean Value of Infection on the EPPO Scale [0–9]
UTC75.60 a17.3031.652.237.6811.82 a7 c
SFP81.42 b17.9730.852.056.6313.31 b4.25 a
BTHWA (4 times)82.60 b17.7633.152.007.9813.27 b5.5 b
BTHWA (3 times)84.58 b17.3531.302.377.2713.27 b5.5 b
BTHWA + FUNGICIDE 183.45 b17.7233.252.386.5813.40 b4 a
BTHWA + FUNGICIDE 2 85.62 b17.6533.702.177.7713.66 b4.25 a
Mean values marked with common letters do not differ significantly at p = 0.05, according to Tukey’s HSD. UTC—sugar beets that were treated neither with BTHWA nor with fungicides; SFP—sugar beets treated with fungicide 2 times; BTHWA (4 times)—sugar beets treated with tested substance BTHWA 4 times; BTHWA (3 times)—sugar beets treated with tested substance BTHWA 3 times; BTHWA + FUNGICIDE 1—sugar beets treated both with BTHWA and fungicide on the third treatment date; BTHWA + FUNGICIDE 2—sugar beets treated both with BTHWA and fungicide on the fourth treatment date. The timetable of applications performed is provided in Table 3.
Table 12. Summary of the results of the field experiment conducted in 2021 on var. Pacific sugar beet in location B.
Table 12. Summary of the results of the field experiment conducted in 2021 on var. Pacific sugar beet in location B.
TreatmentRoot Yield [t/ha]Sugar Polarization [%]Potassium Content [mmol 1000 g–1 of Pulp]Sodium Content [mmol 1000 g–1 of Pulp]Nitrogen Content [mmol 1000 g–1 of Pulp]Technological Sugar Yield [t/ha]Mean Value of Infection on the EPPO Scale [0–9]
UTC59.48 a18.6839.776.9310.8010.01 a6.25 d
SFP65.59 b19.3437.804.878.1711.51 b3.75 bc
BTHWA (4 times)67.44 b19.0540.676.077.9711.62 b4 c
BTHWA (3 times)64.73 b19.2940.676.608.4711.30 b4.25 c
BTHWA + FUNGICIDE 161.90 ab18.9739.404.979.0010.60 ab2.25 a
BTHWA + FUNGICIDE 2 64.19 b19.2239.305.678.2011.17 b3.25 b
Mean values marked with common letters do not differ significantly at p = 0.05, according to Tukey’s HSD. UTC—sugar beets that were treated neither with BTHWA nor with fungicides; SFP—sugar beets treated with fungicide 2 times; BTHWA (4 times)—sugar beets treated with tested substance BTHWA 4 times; BTHWA (3 times)—sugar beets treated with tested substance BTHWA 3 times; BTHWA + FUNGICIDE 1—sugar beets treated both with BTHWA and fungicide on the third treatment date; BTHWA + FUNGICIDE 2—sugar beets treated both with BTHWA and fungicide on the fourth treatment date. The timetable of applications performed is provided in Table 3.
Table 13. Summary of the results of the field experiment conducted in 2021 on var. Mariza sugar beet in location B.
Table 13. Summary of the results of the field experiment conducted in 2021 on var. Mariza sugar beet in location B.
TreatmentRoot Yield [t/ha]Sugar Polarization [%]Potassium Content [mmol 1000 g–1 of Pulp]Sodium Content [mmol 1000 g–1 of Pulp]Nitrogen Content [mmol 1000 g–1 of Pulp]Technological Sugar Yield [t/ha]Mean Value of Infection on the EPPO Scale [0–9]
UTC64.04 a19.9246.004.439.70 a11.53 a4.75 b
SFP66.68 ab19.7345.204.109.80 a11.89 ab3.75 a
BTHWA (4 times)70.61 b20.1348.834.3315.07 b12.75 b3.75 a
BTHWA (3 times)68.49 b20.2445.504.779.50 a12.56 b4.5 b
BTHWA + FUNGICIDE 169.25 b19.8145.904.739.53 a12.40 b3.25 a
BTHWA + FUNGICIDE 2 70.79 b20.0246.734.939.90 a12.80 b3.25 a
Mean values marked with common letters do not differ significantly at p = 0.05, according to Tukey’s HSD. UTC—sugar beets that were treated neither with BTHWA nor with fungicides; SFP—sugar beets treated with fungicide 2 times; BTHWA (4 times)—sugar beets treated with tested substance BTHWA 4 times; BTHWA (3 times)—sugar beets treated with tested substance BTHWA 3 times; BTHWA + FUNGICIDE 1—sugar beets treated both with BTHWA and fungicide on the third treatment date; BTHWA + FUNGICIDE 2—sugar beets treated both with BTHWA and fungicide on the fourth treatment date. The timetable of applications performed is provided in Table 3.
Table 14. Summary of the results of the field experiment conducted in 2021 on var. Pacific sugar beet in location C.
Table 14. Summary of the results of the field experiment conducted in 2021 on var. Pacific sugar beet in location C.
Treatment Root Yield [t/ha]Sugar Polarization [%]Potassium Content [mmol 1000 g–1 of Pulp]Sodium Content [mmol 1000 g–1 of Pulp]Nitrogen Content [mmol 1000 g–1 of Pulp]Technological Sugar Yield [t/ha]Mean Value of Infection on the EPPO Scale [0–9]
UTC42.81 a17.1234.274.9311.106.55 a6 c
SFP46.64 ab17.6433.234.4710.137.40 ab3.75 b
BTHWA (4 times)44.95 a17.2235.475.2012.076.91 a3 a
BTHWA (3 times)49.07 b17.3032.204.4310.607.61 b3.33 ab
BTHWA + FUNGICIDE 145.61 a17.4532.804.8710.177.15 ab3.25 a
BTHWA + FUNGICIDE 243.36 a17.4034.374.3310.576.77 a3 a
Mean values marked with common letters do not differ significantly at p = 0.05, according to Tukey’s HSD. UTC—sugar beets that were treated neither with BTHWA nor with fungicides; SFP—sugar beets treated with fungicide 2 times; BTHWA (4 times)—sugar beets treated with tested substance BTHWA 4 times; BTHWA (3 times)—sugar beets treated with tested substance BTHWA 3 times; BTHWA + FUNGICIDE 1—sugar beets treated both with BTHWA and fungicide on the third treatment date; BTHWA + FUNGICIDE 2—sugar beets treated both with BTHWA and fungicide on the fourth treatment date. The timetable of applications performed is provided in Table 3.
Table 15. Summary of the results of the field experiment conducted in 2021 on var. Mariza sugar beet in location C.
Table 15. Summary of the results of the field experiment conducted in 2021 on var. Mariza sugar beet in location C.
TreatmentRoot Yield [t/ha]Sugar Polarization [%]Potassium Content [mmol 1000 g–1 of Pulp]Sodium Content [mmol 1000 g–1 of Pulp]Nitrogen Content [mmol 1000 g–1 of Pulp]Technological Sugar Yield [t/ha]Mean Value of Infection on the EPPO Scale [0–9]
UTC50.31 a 18.0035.5 a3.7011.638.14 a 4.67 c
SFP55.47 ab17.7434.034.009.608.86 ab4 bc
BTHWA (4 times)52.16 a17.5039.603.4710.908.16 a3 a
BTHWA (3 times)55.78 ab18.0836.374.1712.509.05 b2.67 a
BTHWA + FUNGICIDE 155.20 ab 17.5536.534.7011.878.65 ab3.2 a
BTHWA + FUNGICIDE 2 55.72 ab17.9437.333.6012.138.95 ab3.29 ab
Mean values marked with common letters do not differ significantly at p = 0.05, according to Tukey’s HSD. UTC—sugar beets that were treated neither with BTHWA nor with fungicides; SFP—sugar beets treated with fungicide 2 times; BTHWA (4 times)—sugar beets treated with tested substance BTHWA 4 times; BTHWA (3 times)—sugar beets treated with tested substance BTHWA 3 times; BTHWA + FUNGICIDE 1—sugar beets treated both with BTHWA and fungicide on the third treatment date; BTHWA + FUNGICIDE 2—sugar beets treated both with BTHWA and fungicide on the fourth treatment date. The timetable of applications performed is provided in Table 3.
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Kiniec, A.; Spychalski, M.; Kukawka, R.; Pieczul, K.; Zajac, A.; Smiglak, M. The Use of a New Benzothiadiazole Derivative for the Control of Cercospora Leaf Spot in Sugar Beet and Its Effect on the Yield. Agriculture 2025, 15, 605. https://doi.org/10.3390/agriculture15060605

AMA Style

Kiniec A, Spychalski M, Kukawka R, Pieczul K, Zajac A, Smiglak M. The Use of a New Benzothiadiazole Derivative for the Control of Cercospora Leaf Spot in Sugar Beet and Its Effect on the Yield. Agriculture. 2025; 15(6):605. https://doi.org/10.3390/agriculture15060605

Chicago/Turabian Style

Kiniec, Agnieszka, Maciej Spychalski, Rafal Kukawka, Katarzyna Pieczul, Adrian Zajac, and Marcin Smiglak. 2025. "The Use of a New Benzothiadiazole Derivative for the Control of Cercospora Leaf Spot in Sugar Beet and Its Effect on the Yield" Agriculture 15, no. 6: 605. https://doi.org/10.3390/agriculture15060605

APA Style

Kiniec, A., Spychalski, M., Kukawka, R., Pieczul, K., Zajac, A., & Smiglak, M. (2025). The Use of a New Benzothiadiazole Derivative for the Control of Cercospora Leaf Spot in Sugar Beet and Its Effect on the Yield. Agriculture, 15(6), 605. https://doi.org/10.3390/agriculture15060605

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