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Article

Effects of Plant Growth Regulators and Foliar Nutrients on the Alkaloid Content in Poppy Straw of Opium Poppy (Papaver somniferum L.)

by
Ľuboš Nastišin
1,2,
Jozef Fejér
1,*,
Richard Hercek
3,
Alena Miháliková
3,
Alexander Fehér
4,
Pavol Porvaz
5,
Štefan Tóth
5 and
Peter Hozlár
6
1
Department of Ecology, Faculty of Humanities and Natural Sciences, University of Presov, 17. November 1, SK-081 16 Prešov, Slovakia
2
Research and Breeding Station Malý Šariš, Research Institute of Plant Production, National Agricultural and Food Centre, Malý Šariš 221, SK-080 01 Prešov, Slovakia
3
Saneca Pharmaceuticals a. s., Nitrianska 100, SK-920 27 Hlohovec, Slovakia
4
Institute of Plant Production, Faculty of Agrobiology and Food Resources, Slovak University of Agriculture, Tr. A. Hlinku 2, SK-949 76 Nitra, Slovakia
5
Institute of Agroecology, Research Institute of Plant Production, National Agricultural and Food Centre, Špitálska 1273/12, SK-071 01 Michalovce, Slovakia
6
Research and Breeding Station Vígľaš-Pstruša, Research Institute of Plant Production, National Agricultural and Food Centre, Pstruša 334, SK-962 12 Detva, Slovakia
*
Author to whom correspondence should be addressed.
Int. J. Plant Biol. 2025, 16(2), 66; https://doi.org/10.3390/ijpb16020066
Submission received: 29 April 2025 / Revised: 23 May 2025 / Accepted: 4 June 2025 / Published: 11 June 2025
(This article belongs to the Section Plant Physiology)
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Versions Notes

Abstract

:
Poppy (Papaver somniferum L.) is an important industrial plant worldwide. It is legally cultivated in seven countries around the world for the production of poppy straw or raw opium in India for alkaloid extraction. This work focused on testing different types of growth regulators and foliar nutrients to increase and stabilize basic alkaloids, mainly morphine in dry capsules. Field trials were carried out for three years (2021–2023). Selected preparations and their combinations were applied on the seeds before sowing and on the leaves during vegetation. The content of basic alkaloids in the dry capsules was analyzed by liquid chromatography. The results obtained confirmed the demonstrable effects of pre-sowing seed treatment and foliar treatment during the growing season on alkaloid content. In the experimental treatments in which the seeds were not treated but foliar treatment was applied during vegetation, more alkaloids were accumulated compared to the control (untreated seeds, not foliar treatment), but this difference was not statistically significant. The influence of the weather conditions during the experimental year on the accumulation of alkaloids was confirmed. Environmental conditions during the growing season and plant stress influenced alkaloid accumulation. An additional supply of growth regulators and foliar fertilizers reduced the stress and positively influenced the accumulation of individual alkaloids. The results obtained provide important insights into the technology of cultivating industrial poppy varieties.

1. Introduction

Opium poppy (Papaver somniferum L.) is a globally important crop that is cultivated in many countries around the world [1]. Based on the UN Convention on Narcotic Drugs, three different types of poppies are described [2]. The first is the technical type, grown for the purpose of producing poppy straw from which the basic alkaloids are extracted. India is the only legal producer of opium for pharmaceutical purposes [3,4]. The second type is food crops intended for the production of poppy seeds for consumption purposes (direct consumption, oil production, but also biodiesel production). The third type of poppy variety is a collection of ornamental forms with different flower and capsule shapes and colors.
Slovakia is one of the seven countries in the world where poppy is grown under legal control for the production of alkaloids. In Slovakia, morphine is produced from the concentrate of poppy straw (CPS), similar to Turkey. Australia, France, and Spain produce morphine and thebaine from CPS. Hungary is a producer of morphine, thebaine, and codeine. As already mentioned, legal opium is produced in India for the extraction of morphine. In 2019, the area for industrial poppy cultivation was 93,661 hectares [5].
In addition to its employment in pharmacology, poppy is also used traditionally in various countries and cultures around the world. This involves the use of various pharmacologically active extracts to treat diseases. Anticancer, antioxidant, antimicrobial, and analgesic effects have been reported [6].
The accumulation of secondary metabolites is highly dependent on various environmental factors such as light, temperature, soil water, soil fertility, salinity, etc. In most plants, the change within a single factor can modify the secondary metabolite content even if the other factors are constant [7]. Due to stress factors, plants reduce the synthesis of secondary metabolites compared to their growth in optimal conditions [8]. Drought is one of the most important abiotic stress factors that negatively affects plant growth and development. Drought often leads to oxidative stress and is reflected, for example, in an increase in the amount of morphine [9,10]. Temperature is also an important factor influencing the accumulation of alkaloids. At low temperatures, the accumulation of alkaloids in poppy is reduced [11,12]. In addition, the actual production potential is also influenced by the genetic potential of the plant [13]. There is a significant genotype–environment interaction in poppy [14]. According to Fist [15], the most important factors influencing the alkaloid content are the genotype and the nitrogen supply of the plant. The yield of poppy straw is influenced by the genotype and the nitrogen and phosphorus nutrition. Important factors are the water balance of the soil (precipitation) and the control of weeds, pests, and diseases. This means that agrotechnical measures are important during the growing season.
The aim of the presented research was to increase and stabilize the accumulation of basic alkaloids in dry poppy capsules. For this purpose, different types of foliar preparations (growth regulators—biostimulants and foliar nutrients) were used. Different combinations of the selected preparations were applied to the seed or to the leaves during the vegetation season.

2. Materials and Methods

2.1. Plant Material

The variety Senmorteco of opium poppy (Papaver somniferum L.) was used for the field trials. The breeder’s certificate (in 2019) is held by Saneca Pharmaceuticals a.s. Hlohovec, Slovak Republic. It is a variety of the universal type for dual use, i.e., it is primarily intended for the production of poppy straw with a morphine content of 1.2% and more (up to 1.5%) in dry capsules and the production of poppy seeds for food purposes.

2.2. Soil and Climatic Characterization of the Experimental Plots

The experimental plot in Vígľaš-Pstruša (Detva district, Slovakia) is located in a moderately warm, moderately humid climate region with a temperature sum of TS ≥ 10 °C 2500–2200 °C, with a period of air temperature above 5 °C for 215 days. The soil type is pseudogley, consisting of loess and polygenetic clays. The soil type is medium loamy, sometimes even heavy, locally very heavy. The land is slightly sloping, with south to east–west orientation, no skeleton in the soil (max. skeleton content vol. up to a depth of 0.6 m below 10%), and deep soil (60 cm and more). The soil-climatic properties are described based on the evaluated soil ecological unit (BPEJ) code 0757202 [16]. and decoded [17]. The soil of the experimental plot has a slightly acidic soil reaction (pH 5.69). The content of available phosphorus is low (48 mg·kg−1), potassium is low (64 mg·kg−1), and magnesium is sufficient (157 mg·kg−1).
The average monthly temperatures and total precipitation during the growing season in the experimental years 2021—2023 are listed in Table 1 and Table 2.

2.3. Method of Sowing

The experiments were carried out using the randomized block design in four repetitions. The size of the experimental area was 5.0 m2 (1.25 m × 4.0 m). A quantity of 1.2 g of seed was used for sowing each experimental variant. Sowing was carried out with an Oyord small-plot seed drill (Wintersteiger, Ried, Austria; Figure 1 and Figure 2). The sowing was provided on dates 23 March 2021, 18 March 2022, and 20 March 2023. Individual variants of the trial were matched in each repetition. The scheme of the trial is shown in Figure 3 [19,20].

2.4. Application of Biostimulants and Foliar Fertilizers

The seeds were treated by hand. A precisely weighed/measured amount of the preparation in g·ml−1 for weighing the seeds was diluted with water in a ratio of 1:3, applied to the seeds in a closed glass cup and mixed thoroughly. Immediately after application of the solution, the seeds were dried.
The preparations were applied during vegetation using a SOLO 430 backpack sprayer with nozzle type 015 F80. The individual preparations were dosed directly onto the test plot. The dosages listed in Table 3 were converted to the area of the test variant. In total, 0.2 L of water was used per test plot—one experimental variant—which corresponds to 400 l·ha−1 of spray liquid. The solution was prepared and mixed directly in the sprayer for all repetitions of the experiment separately for each variant. The spray was applied in the morning after the dew had dried on the plants. The individual application is shown in Figure 4. The application at the individual growth stages is shown in Figure 5.

2.5. List of the Experimental Treatments

The treatments and combinations of the preparations are shown in Table 3.

2.6. Characteristics of the Preparations Used

Enviseed contains 3.0% N, 1.0% K2O, humic acids, and a mixture of microelements, B, Cu, Mn, Fe, and Zn, which support better germination and the formation of the root system. Envistart contains 4.0% N, 6.0% potassium humate, and a mixture of microelements, B, Cu, Mn, Fe, and Zn. This stimulates the plants in the first stages of growth. Proveo Star contains 1.0% N, 2.5% P2O5, 0.5% K2O, 1.0% SO3, and the trace elements B, Fe, Mn, Zn, and Mo. This increases resistance to fungal diseases and environmental stress. PhaNi Stim contains 5.0% N, 18.0% P2O5, 2.0% K2O, 1.5% SO3, and the trace elements B, Fe, Mg, Cu, Zn, and Mo. Its application helps to accelerate and maintain the growth rate, especially in climatically demanding periods. Boris P + K contains 6.0% P2O5, 10.0% K2O, 2.0% SO3, and the trace elements B, Zn, Mn, Fe, Cu, and Mo, recommended for use in stressful conditions—high temperatures and drought. Zina P + K contains 6.2% N, 3.7% P2O5, 6.7% K2O, potassium humate, Ca, B, Cu, Fe, Mn, and Zn. It supports the quality parameters of the harvest and the health of the crop. Lecithin is used in crop protection, as it is approved as a substitute for fungicides.
Trichopron contains chitosan hydrochloride 50 g·kg−1 (5% w/w), i.e., poly[beta-(1,4)-D-glucosamine] hydrochloride and Trichoderma asperellum. It supports the growth of the root system and protects against pathogens. AmazonN contains bacteria Bacillus mojavensis strain KN32, NCAIM 497/2020, a minimum number of bacteria of 5 × 109 CFU·m−3, and perlite. Biomit is a plant extract (extracts from 60 plant species) with a content of 8.0%, containing 7.0% Ca, 5.0% Mg, and the trace elements Cu, Zn, Mn, Fe, and B. Bioka Equisetum horsetail extract (Equisetum arvense). It contains ortho-silicic acid of at least 2.3%. Cupro Tonic foliar fertilizer has a content of 5.3% Cu and 1.0% Zn. PlanTonic consists of an aqueous extract of nettle and an oil extract of willow. Rokohumín contains 4.0% N, 9.0% P2O5, 14.0% K2O, and 13.0% humic acids, as well as Ca, Mg, and the trace elements molybdenum Mo, Cu, B, Mn, and Zn. SoilTonic is a plant extract.
Energen Germin FH contains 2.6% N, 1.5% P, 1.2% K, B, Fe, Mn, Zn, and Cu. It also contains auxins, an auxin precursor, and an extract from the algae Ascophytum nodosum. Energen Fulhum Plus consists of humic substances and their salts in an amount of 8.0% and an extract of the algae Ascophytum nodosum with a content of 12.0%. Energen Algan is an extract from the seaweed Ascophytum nodosum. Its content is 25.0%. Individual components of the extract, such as amino acids, alginates, mannitol, laminarin, and others, have an adaptogenic effect and increase the resistance of plants to drought and cold. Energen Fruktus Plus contains 8.0% humic substances and their salts. It also contains extracts from the seaweed Ascophytum nodosum, adaptogens, and a wetting agent. This helps to increase the yield and content of substances under stressful conditions. Energen Stimul Plus contains humic substances and their salts in an amount of 8.0%, free amino acids at 10.0%, as well as extracts from the seaweed Ascophytum nodosum, adaptogens, and a wetting agent.
YaraVita Seedlift contains 8.6% N, 15.0% P2O5, 13.5% CaO, 15.8% Zn, and 2.7% total organic carbon. YaraVita Brassitrel Pro contains 4.5% N, 9.0% CaO, 7.6% MgO, 3.9% B, 4.6% Mn, and 0.3% Mo. YaraVita Zintrac fertilizer concentrate contains 40.9% zinc oxide content and 1.0% N content. YaraVita Bortrac contains 11.5% B and 4.8% N. It contains a wetting agent, adhesives, and substances that improve plant uptake. YaraVita Thiotrac contains 15.2% N and 62.0% SO3. YaraVita Maris is a plant-based biostimulant with an extract from the algae Ascophyllum nodosum. It contains 8.0% organic carbon and 6.4% K2O. Agrovital contains 96% beta-pinene oligomerization products.

2.7. Field Trial Harvest

The collection of trials was carried out each year at the time of full maturity, i.e., when the seed in the capsule is separated from the partitions, and it is at the bottom of the capsule (the seed rustles in the capsule), and when it no longer changes color after being poured out of the capsule. The capsules were collected by hand throughout the plot by breaking them open just below the elbow. The collection dates in each year were 2 August 2021, 25 July 2022, and 3 August 2023. Samples were taken from the empty capsules for the analysis of the alkaloid content.

2.8. Determination of Alkaloid Content by HPLC

Opium poppy dry capsules were analyzed on Waters Alliance 2695 or Waters Acquity equipped with an X-Bridge C18 (0.1 m × 4.6 mm, 3.5 µm). Mobile phase A—1.01 g sodium heptanesulfonate R, diluted to 1000 mL with water R, adjusted to a pH of 2.6 with a 50% v/v solution of phosphoric acid R, and mobile phase B—methanol. The flow rate was 1.5 mL per minute. The detection UV was 230 nm. The injection was 2 µL. The column temperature was 35 °C. The running time was 10 min. The assay and the purity were evaluated with an external standard. The analyses were performed in the laboratory of Saneca Pharmaceuticals a.s. Hlohovec, Slovakia.

2.9. Statistical Analysis

The data obtained were analyzed using analysis of variance (ANOVA) with the statistical program STATISTICA 12 using the LSD method (Least Significant Difference). The analysis of variance provided evidence of differences in alkaloid content between experimental variants, experimental locations, and experimental years. Principal component analysis (PCA) was performed using the program Canoco 4.5.
In addition to the analysis of variance, the program Canoco 4.5 was used, which was developed for use in the field of ecology and environmental sciences and enables researchers to analyze multivariate data sets. In our case, we used it for principal component analysis (PCA). The visualization of results was created in the program CanoDraw 4.0.

3. Results

The experiments focused mainly on the dominant basic alkaloid morphine but also on thebaine and codeine, which can be identified as precursors of morphine in the biosynthetic pathway. The contents of these main monitored alkaloids in the dry capsules and their sum are shown in Table 4, Table 5, Table 6 and Table 7. As the tables show, the amounts of alkaloids varied depending on the treatment variant used. The experimental year had a significant influence on their content or the course of the weather conditions in the individual experimental years.
As far as the differences between the variants are concerned, the lowest alkaloid content was found in variant T1, i.e., the control variant, in which the seeds were not treated, and no preparations were applied to the leaf during the vegetation period. In variants no. 6 and 9, whose seeds were not treated but leaf-treated during the vegetation period, an increased content of alkaloids was found in the dry capsules, but this was not significant compared to the control variant (T1). The remaining variants of the experiment (T2, T3, T4, T5, T7, T8, and T10), whose seeds were treated before sowing and whose preparations were applied to the leaf, achieved, in most cases, a demonstrably higher amounts of alkaloids compared to the control variant (T1) and to the variants whose seeds were not treated but foliar-treated during the vegetation period (T6 and T9). These results apply to the trial years 2021 and 2022. In 2023, no detectable differences were found between the evaluated variants. Even the morphine content was highest in the control variant T1. However, this had no influence on the significant detection of differences in the content of alkaloids in dry capsules, on average, in the three years (2021–2023) examined (Table 4, Table 5, Table 6 and Table 7).
The most significant increase in morphine content compared to the untreated control variant (T1) was observed in 2021 from 77.1% to 107.4% (T10/T4). In the trial years 2022 and especially 2023, the opposite effect was also observed, i.e., a decrease in the morphine content in the dry capsules. In 2022, the decrease or increase in this alkaloid fluctuated between −8.0% and 68.1% (T9/T5) compared to the control. A similar trend was observed for thebaine, codeine, and the sum of the monitored alkaloids. In 2023, only a decrease in the formation of morphine was observed. The decrease in accumulation varied from −19.5% to −1.6% (T3/T9) compared to the control. An increase was also observed for other alkaloids and the sum of the alkaloids in this year (e.g., thebaine, 38.3% T7, codeine, 50.0% T8, and the sum of alkaloids, 8.1% T7).
This confirms that the treatment of the seeds is an important factor that most strongly influences the formation of alkaloids. Subsequent foliar treatments during vegetation had no significant effect on alkaloid formation. Variant T1 was the only one to form a separate cluster, as it was the furthest away from the previous two clusters, which is due to the fact that it is a control variant, i.e., its seeds were not treated, and it was not foliar-treated (Figure 6).
In the environment of the computer program Canoco 4.5, the basic axes and vectors of the relationships between the individual variants of the experiment and the formation of the three monitored alkaloids—morphine, codeine, and thebaine—were created as part of the principal component analysis. This interaction apparatus was visualized with the CanoDraw 4.0 program using the imported eigenvalues (Figure 6).
It can be concluded that the results obtained correspond to the statistical evaluation using the analysis of variance. It turned out that a large proportion of the variants behaved similarly and formed a cluster. These are the variants T2, T3, T4, T5, T7, T8, and T10, whose seeds were treated and in which different types of additional energy and material inputs were applied on leaves during vegetation. These variants had a similar effect on alkaloid formation. Variants T6 and T9 are a separate isolated cluster that is clearly distant from the previous group. These are variants whose seeds were not treated but whose leaves were treated with preparations during the growth period.
The vectors of the alkaloids were almost the same length, suggesting that their interactions are approximately the same or at least of comparable strength in terms of the correlations analyzed. All three vectors of the analyzed alkaloids had almost the same direction, so they are positively correlated. When the amount of one alkaloid increases, the other two also increase. The strongest relationship is between morphine and thebaine, and codeine shows less dependence. As the study was conducted at a single site, the effects of specific environmental factors (soil and climatic conditions, etc.) could not be assessed (Figure 6).

4. Discussion

The treatment of poppy seeds is a common measure in the cultivation of this plant. Primarily, fungicidal seed treatments are used against seed-borne diseases. Thangavel et al. [21,22] reported on the positive effects of the chemical–physical treatment of the seeds before sowing for the health of the seedlings. Washes in acidified electrolytic water (400 ppm of hypochlorous acid for 5 min) and hypochlorite solution (2% NaOCI for 5 min) proved to be effective methods. These two treatments reduced the disease transmission of Peronospora somniferi by 88.8% and 74.61% and of Peronospora meconopsidis by 93.3% and 100%, respectively [22]. Not only seed-borne diseases but also soil-borne fungal pathogens pose a threat to germinating and emerging plants. In vitro tests against the four pathogens, Alternaria spp., Dendryphion penicillatum, Fusarium spp., and Penicillium spp., showed a reduced infection rate and a 9–10% higher plant emergence. Temperature also had a significant effect on germination. Increasing the temperature to 12 °C also increased emergence by 8–16% [23]. The elimination of pathogens and the increase in germination capacity through pre-sowing seed treatment subsequently have an effect on poppy yield. A positive effect was found on plant emergence, yield parameters such as the number of pods per plant, seed weight per pod, the weight of a thousand seeds, and thus on the final yield [24]. In addition to protection against pathogens, the stimulating effect of many preparations on production parameters is also of great importance. When using the biostimulants TS Osivo and Enviseed, similar results were obtained in field emergence and seed yield as in the treatment with the chemical preparation Cruiser OSR. All evaluated parameters were strongly influenced by the year, i.e., the weather conditions of the year [24].
The accumulation of the alkaloid sanguinarine has been demonstrated in poppy root [25]. It was found that salt stress (presence of NaCl) has a negative effect on the production of sanguinarine. Its content was found in key plants. In the case of the reduced biosynthesis of sanguinarine due to stress, the reduced biosynthesis of morphine can also be assumed [26]. The amount of sanguinarine can be increased by the use of various elicitors. The application of an extract of Trichoderma harzianum to the suspension culture of the Sujata poppy (latex-less variety) led to an increase in the content [27]. While sanguinarine only accumulates in the roots, morphine accumulates both in the roots and in the above-ground organs. The first steps in the biosynthesis of a large group of tetrahydroisoquinoline alkaloids begin with the catalysis of tyramine and dopamine formation by tyrosine/dopa decarboxylase (TYDC). TYDC transcripts are present in the vascular bundles of mature roots and stems but are also expressed in cortical tissues at earlier developmental stages [25]. We can therefore assume that the treatments affected this part of the morphine biosynthetic pathway, which was positively reflected in the increased accumulation of morphine.
Morariu and Caulet [28] stated that in the earlier growth phase, i.e., in the leaf rosette, morphine was only detected in the roots at a concentration of 0.001% dry weight. No content was found in the letters. Williams and Ellis [29] determined the morphine content in the roots of poppy grown 20 days after emergence in the field. The highest content was found 30 days after emergence. Codeine was detected in the roots on the 15th day. In contrast, Shukla and Singh [30] found the morphine content, even in germinating plants (3–4 days after germination), in all three parts, namely, the upper part, the root part, and the entire cotyledon. In a study on somatic embryogenesis and rhizogenesis [31], no morphine was detected in the root, in contrast to experiments carried out under field conditions where morphine was detected [29]. However, the alkaloids codeine, thebaine, and papaverine were detected. The results of this study indicate that root organogenesis is causally related to alkaloid biosynthesis. These results indicate the complexity of alkaloid biosynthesis, transport, and accumulation in poppy plants. They also indicate that the basis of the anatomical structures in which alkaloid biosynthesis takes place is already formed in the early stages of poppy growth. This statement is also supported by the studies of Bajpai et al. [32], who investigated the relationship between morphine and codeine in different poppy genotypes. He found that morphine is first produced in the root, then in the cotyledons and true leaves, and finally, in the stem and capsule.
Our experiments confirmed the positive effect of the pre-sowing treatment of poppy seeds on the amount of the alkaloids morphine, thebaine, and codeine accumulated in the dry capsules. A double effect of the preparations used can be assumed. Firstly, the seed treatment protected the germinating and emerging plants from biotic and abiotic stress factors. The contained nutrients promoted germination, emergence, and initial growth. Secondly, the stimulating effect of the preparations (especially the content of humic substances) probably contributed to the development of the root system and thus also to the better formation of anatomical structures as a basic prerequisite for the successful start of alkaloid biosynthesis. Nitrogen and carbon, mainly in organic form (humic acids), seem to be key elements in the process of germination and in the first stages of growth, as well as in the subsequent biosynthesis of alkaloids. In a study conducted by Hope et al. [33], it was reported that flower formation in opium poppy starts 3 weeks after sowing in controlled cultivation. The study also showed that the development of capsules and seeds, as well as the production of alkaloids, is significantly influenced by the availability of carbon. The latter is of crucial importance in the early stages of development. It can therefore be concluded that the content of humic substances and organic carbon in the seed treatments used has a positive influence on the formation of alkaloids. Our results also agree with the finding of Hope et al. [33] that carbon can no longer be compensated for in later growth phases. The foliar application of preparations that also contain organic carbon could no longer significantly increase alkaloid synthesis compared to variants in which the carbon was supplied in the early phase in the form of a seed treatment. Kuchtová et al. [34] reported on the positive effect of the biological preparations based on mycoparasitic fungi used on poppy seed yield. They found that seed treatment has a more significant effect on seed yield than foliar application during vegetation, which is also consistent with our results on the effect of treatment on alkaloid content compared to foliar application. Cihlář et al. [35] showed the positive effect of foliar application (phase 6–8, true leaves) of foliar fertilizers containing sulfur, boron, and humic substances on poppy yield in field trials. In their study on poppy nutrition, Losák and Páleníček [36] found that an increased dose of nitrogen increases the morphine concentration in the poppy straw. The positive effect of potassium and magnesium fertilization on seed yield was demonstrated in pot experiments [37]. Khaldari et al. [38] investigated the effects of green and chemical copper oxide nanoparticles (CuO NPs) elicitors of oxidative stress and the benzylisoquinoline alkaloids (BIA) biosynthetic pathway in the cell suspension culture of Papaver orientale. He found that the concentration of CuO NPs and the duration of cell treatment had a more significant effect on the induction of oxidative stress and the stimulation of the gene expression of the BIA synthesis pathway than the type of CuO NPs. The size and morphology of the capsule may also play an important role in the accumulation of poppy alkaloids. Májer and Németh [39] confirmed the role of capsule size and genotype on seed ratio and alkaloid accumulation. In large capsules, the alkaloid content and the ratio of morphinans (morphine, codeine, and thebaine) may differ from those in smaller capsules. However, the actual concentrations depend on the genotype. In our research, we have tested the preparations on one variety, but it can be assumed that the treatments have a positive effect on the capsule size and its health status, and thus on the alkaloid content, especially on the stabilization of the content during maturation. Recent studies [40] indicate the possibility that phospholipid signaling pathways are disrupted, which in turn leads to changes in the secondary metabolism of BIAs in opium poppy. Poppy plants may simultaneously activate one signaling pathway and suppress another branch of BIA production. However, this is beyond the scope of our present study.
The literature reports an increased accumulation of secondary metabolites under stress conditions. The strong influence of various environmental factors and management practices on the accumulation of alkaloids is reported by [7]. Due to the decrease in primary metabolism, secondary metabolism increases [8]. The content of morphine and other alkaloids in poppy seeds is mainly affected by drought [9,10] and water stress [41]. The results of our study showed a negative effect of stress on the content of alkaloids in the dry capsules. Each of the experimental years showed a different pattern of weather conditions—temperatures and precipitation (Table 1 and Table 2). In 2021, the average air temperature during the poppy growing season was +0.48 °C higher, in 2022, it was −0.45 °C lower, and in the third year, 2023, the average temperature was at the level of the long-term normal value. The total precipitation in 2021 was 47.7% below normal, while in 2022, the total precipitation was close to normal at 97.4%. In terms of precipitation, 2023 was at the level of the long-term normal value. From the point of view of the influence of weather conditions on the biosynthesis of alkaloids, we can consider the phase of germination, emergence, and the beginning of rosette formation as a critical period. This falls within a period of several weeks after sowing, which was carried out in the month of March. In 2021 and 2022, the average temperatures in March were 0.91 °C and 0.97 °C lower than normal, and the total amounts of precipitation were 30.0% and 68.7% of the long-term normal, respectively. On the other hand, the temperature in March 2023 was 1.03 °C above normal, and the amount of precipitation was 99.4% of the normal. The month of April was characterized by relatively low air temperatures compared to the long-term normal value (2.81 °C, 2.11 °C, and 2.23 °C lower, respectively). The first decade of this month, in 2021 and 2022, were also characterized by frequent frost. The critical periods in terms of temperature and precipitation are also the growth phase, flowering, and ripening. The months of June and July in 2021 and 2022 were characterized by a higher average air temperature (by 1.89 to 2.61 °C). A significant precipitation deficit was also observed in 2022 (June, 36.9% and July, 34.5% compared to the long-term normal value). These stresses of low temperatures and moisture deficits in the early stages of growth and high temperatures and moisture deficits, especially in 2022, at the time of flowering and maturity, are probably the cause of the lower accumulation of alkaloids in the first two years of the experiment compared to 2023. Our results are consistent with those of Gümüşçü and Gümüşçü [42], who found that alkaloid formation in poppy cultivation is strongly influenced by extreme weather conditions. Battisti and Naylor [43] reported that high temperatures during the growing season can have a negative impact on agricultural production, which is also consistent with our results. Due to the changing climatic conditions, which are stressful for the spring poppy (especially at the beginning of the growing season), winter poppy varieties sown in the autumn are an alternative in the Pannonian climate in Central Europe. This ensures an increase in poppy seed yield and an increase in the alkaloid content of the poppy straw [44]. However, since the supply of winter poppy varieties is limited, and it is assumed that the spring varieties of poppy will prevail in cultivation practice in the near future, the knowledge gained through this research will be useful for the technology of their cultivation.

5. Conclusions

A complex interplay of environmental conditions in conjunction with plant stress and additional energy-substance inputs in various combinations influenced the accumulation of the individual alkaloids observed. Above all, seed treatment proved to be an important factor in the agrotechnics of growing industrial poppy varieties. The foliar application of additional energy substances without seed treatment no longer had as significant an effect on alkaloid accumulation as the combination with seed treatment. The effect of these measures in the poppy cultivation technique was significant in the stress years (2021 and 2022) when demonstrably higher amounts of alkaloids were found in the dry capsules in the variants with seed treatment plus foliar application. Foliar application without seed treatment increased the alkaloid content in these trial years, but this increase was not statistically significant. In the experimental year with optimal weather conditions (2023), no difference was found in the amounts of accumulated alkaloids between the control variant and the variants with seeds and foliar treatment. We can conclude that seed treatment and foliar application seem to be effective agrotechnical measures to accumulate and stabilize the amounts of alkaloids in the dry capsules of industrial poppy cultivars in the long term.

Author Contributions

Investigation and methodology: J.F. and Ľ.N. Design of experiment: J.F., P.H. and Ľ.N. Experimental procedure: J.F., P.H. and Ľ.N. Data analysis: J.F., A.F., P.P., Š.T., A.M. and Ľ.N. Statistics: J.F. and A.F. Manuscript writing—original draft: Ľ.N. and J.F. Conceptualization, supervision, and validation: R.H., J.F. and P.H. Writing—review and editing: P.P., Š.T., A.F. and P.H. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Data Availability Statement

Data are contained within the article.

Conflicts of Interest

Author Richard Hercek and Alena Miháliková were employed by the company Saneca Pharmaceuticals a. s. The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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Ijpb 16 00066 g001
Figure 1. Sowing the experiment (author).
Figure 1. Sowing the experiment (author).
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Figure 2. Experiment in the leaf rosette (author).
Figure 2. Experiment in the leaf rosette (author).
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Figure 3. Scheme of the experiment (author).
Figure 3. Scheme of the experiment (author).
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Figure 4. Treatment—green maturity (author). 1–10 = treatments T1–T10; 0 = zero variant.
Figure 4. Treatment—green maturity (author). 1–10 = treatments T1–T10; 0 = zero variant.
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Figure 5. BBCH growth stages of the application. 0 = seed treatment; 1 = leaf rosette with 5–7 leaves, stage BBCH 16–18; 2 = formation of buds, stage BBCH 51–52; 3 = green maturity, stage BBCH 79 (author).
Figure 5. BBCH growth stages of the application. 0 = seed treatment; 1 = leaf rosette with 5–7 leaves, stage BBCH 16–18; 2 = formation of buds, stage BBCH 51–52; 3 = green maturity, stage BBCH 79 (author).
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Figure 6. Clusters of variants (Cluster A = control variant T1, in which the seed was not treated before sowing and was not treated on the leaf during vegetation, Cluster B = T6 and T9, i.e. variants whose seed was not treated before sowing but was treated on the leaf during vegetation, Cluster C = the remaining variants in which the seed was treated before sowing and was also treated on the leaf during vegetation) according to alkaloid formation created using principal component analysis (PCA, expressed variance: 87.9% + 10.0%). Numbers 1–10 = T1–T10 treatments; MOR = morphine; TEB = thebaine; KOD = codeine.
Figure 6. Clusters of variants (Cluster A = control variant T1, in which the seed was not treated before sowing and was not treated on the leaf during vegetation, Cluster B = T6 and T9, i.e. variants whose seed was not treated before sowing but was treated on the leaf during vegetation, Cluster C = the remaining variants in which the seed was treated before sowing and was also treated on the leaf during vegetation) according to alkaloid formation created using principal component analysis (PCA, expressed variance: 87.9% + 10.0%). Numbers 1–10 = T1–T10 treatments; MOR = morphine; TEB = thebaine; KOD = codeine.
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Table 1. Average monthly temperatures (°C) during the growing season.
Table 1. Average monthly temperatures (°C) during the growing season.
YearMonth [°C]Average T [°C]
3 *4567
20212.896.4911.4819.6020.9912.29
20222.837.1914.4820.1121.4913.22
20234.837.2213.7117.8619.7512.67
Long-term average3.809.3014.0017.5019.1012.74
Long-term average of 1991–2020 [18]; * number of months are adequate to the order of months in the calendar—3 = March, 4 = April, 5 = May, 6 = June, and 7 = July.
Table 2. Monthly precipitation (mm) during the growing season.
Table 2. Monthly precipitation (mm) during the growing season.
YearMonth [mm]Sum [mm]
34567
20219.736.3119.165.274.9305.2
202222.239.429.227.930.9149.6
202332.132.9148.060.941.7315.6
Long-term average32.342.373.575.789.7313.5
Long-term average of 1991–2020 [18]; number of months are adequate to the order of months in the calendar—3 = March, 4 = April, 5 = May, 6 = June, and 7 = July.
Table 3. The treatments, list of preparations used, and their combinations.
Table 3. The treatments, list of preparations used, and their combinations.
TreatmentApplication Phase
0123
Seed TreatmentLeaf Rosette (5–7 Leaf)Formation of BudsGreen Maturity
T1Without seed treatmentNo applicationNo applicationNo application
T2Enveseed 30 l·t−1Envistart 1.0 l·ha−1Proveo Star 0.5 l·ha−1Boris PK 3.0 l·ha−1 + Lecitin 3.0 l·ha−1
T3Enveseed 30 l·t−1Envistart 1.0 l·ha−1PhaNi stim 3.0 l·ha−1Zina PK 3.0 l·ha−1 + Lecitin 3.0 l·ha−1
T4Chitopron 1.0 kg·t−1AmazonN 1.0 kg·ha−1 + Biomit 2.0 l·ha−1 + Bioka Equisetum 0.5 l·ha−1PlanTonic 4.0 l·ha−1 + Cuprotonic 2.0 l·ha−1 + Biomit 2.0 l·ha−1Plantonic 4.0 l·ha−1 + Bioka Equisetum 0.5 l·ha−1 + SoilTonic E 4.0 l·ha−1
T5Chitopron 1.0 kg·t−1AmazonN 1.0 kg·ha−1 + Biomit 4.0 l·ha−1 + Rokohumín 5.0 l·ha−1PlanTonic 4.0 l·ha−1 + Biomit 2.0 l·ha−1 + SoilTonic E 4.0 l·ha−1Cuprotonic 2.0 l·ha−1 + Bioka Equisetum 0.5 l·ha−1 + Rokohumín 5.0 l·ha−1
T6Without seed treatmentAmazonN 1.0 kg·ha−1 + Biomit 3.0 l·ha−1 + Rokohumín 10.0 l·ha−1PlanTonic 2.0 l·ha−1 + Cuprotonic 1.0 l·ha−1 + Biomit 2.0 l·ha−1 + Bioka Equisetum 0.5 l·ha−1PlanTonic 2.0 l·ha−1 + Cuprotonic 1.0 l·ha−1 + Biomit 1.0 l·ha−1 + Bioka Equisetum 0.5 l·ha−1
T7Energen Germin FH 25 l·t−1 + Energen Fulhumin Plus 25 l·t−1Energen Algan 1.0 l·ha−1Energen Fruktus Plus 0.5 l·ha−1Energen Fruktus Plus 0.5 l·ha−1
T8Energen Germin FH 25 l·t−1 + Energen Fulhum Plus 25 l·t−1Energen Fulhum Plus 0.5 l·ha−1Energen Stimul Plus 0.5 l·ha−1Energen Stimul Plus 0.5 l·ha−1
T9Without seed treatmentYaraVita Brassitrel PRO 3.0 l·ha−1YaraVita Zintrac 1.0 l·ha−1 + YaraVita Bortrac 0.5 l·ha−1YaraVita Thiotrac 3.0 l·ha−1 + Agrovital 0.7 l·ha−1
T10YaraVita Seedlift 30 l·t−1YaraVita Brassitrel PRO 3.0 l·ha−1 + YaraVita Maris 1.0 l·ha−1YaraVita Zintrac 1.0 l·ha−1 + YaraVita Bortrac 0.5 l·ha−1Thiotrac 3.0 l·ha−1 + YaraVita Maris 1.0 l·ha−1 + Agrovital 0.7 l·ha−1
Table 4. Morphine content in the dry capsules (% by dry weight).
Table 4. Morphine content in the dry capsules (% by dry weight).
VariantYearAverage [%]
2021 b2022 a2023 c
T10.528 a ± 0.0950.565 ab ± 0.0781.280 a ± 0.0000.791 a ± 0.383
T21.003 b ± 0.0180.855 cd ± 0.0211.050 a ± 0.0850.970 bc ± 0.099
T30.970 b ± 0.0280.865 cd ± 0.1201.030 a ± 0.1700.955 abc ± 0.120
T41.092 b ± 0.0530.865 cd ± 0.0351.110 a ± 0.0421.023 c ± 0.127
T51.060 b ± 0.0140.950 d ± 0.1411.160 a ± 0.0711.057 c ± 0.118
T60.660 a ± 0.0640.615 ab ± 0.0351.150 a ± 0.1410.810 ab ± 0.275
T71.040 b ± 0.0210.920 d ± 0.0001.180 a ± 0.0851.048 c ± 0.123
T81.020 b ± 0.0570.905 d ± 0.0921.105 a ± 0.0351.010 c ± 0.103
T90.640 a ± 0.1630.520 a ± 0.0571.255 a ± 0.1340.807 ab ± 0.366
T100.933 b ± 0.0880.715 bc ± 0.0211.160 a ± 0.1840.937 abc ± 0.219
p<0.001=0.002=0.556=0.008
Data represent the mean ± SD (standard deviation); significant differences of p < 0.05 according to the Multiple Range Test LSD (Least Significant Difference, ANOVA); p-value for differences between years, p < 0.001; a–d values for numbers express the evidence of differences between variants; a–c values for years express differences between years.
Table 5. Thebaine content in the dry capsules (% by dry weight).
Table 5. Thebaine content in the dry capsules (% by dry weight).
VariantYearAverage [%]
2021 b2022 a2023 c
T10.153 a ± 0.0180.185 abc ± 0.0640.465 abc ± 0.0920.268 ab ± 0.162
T20.303 bc ± 0.0250.270 cde ± 0.0420.480 abc ± 0.0280.355 bcd ± 0.087
T30.360 c ± 0.0710.305 de ± 0.0640.415 a ± 0.1060.360 bcd ± 0.080
T40.323 c ± 0.0950.205 bc ± 0.0210.410 a ± 0.0000.313 abc ± 0.102
T50.333 c ± 0.0180.265 cde ± 0.0850.530 abc ± 0.0850.377 cd ± 0.129
T60.270 bc ± 0.0850.100 a ± 0.0000.340 a ± 0.0850.237 a ± 0.123
T70.273 bc ± 0.0320.235 bcd ± 0.0210.645 c ± 0.0350.385 cd ± 0.204
T80.298 bc ± 0.0530.330 e ± 0.0140.610 bc ± 0.0280.413 d ± 0.156
T90.205 ab ± 0.0420.165 bc ± 0.0490.395 a ± 0.0780.257 a ± 0.119
T100.300 bc ± 0.0420.230 bcd ± 0.0140.445 ab ± 0.0640.325 abcd ± 0.104
p=0.032=0.007=0.094=0.004
Data represent the mean ± SD (standard deviation); significant differences of p < 0.05 according to the Multiple Range Test LSD (Least Significant Difference, ANOVA); p-value for differences between years, p < 0.001; a–e values for numbers express the evidence of differences between variants; a–d values for years express differences between years.
Table 6. Codeine content in dry capsules (% by dry weight).
Table 6. Codeine content in dry capsules (% by dry weight).
VariantYearAverage [%]
2021 b2022 a2023 b
T10.263 a ± 0.0250.280 bc ± 0.0280.360 ab ± 0.0140.302 ab ± 0.050
T20.457 c ± 0.0140.400 de ± 0.0000.375 ab ± 0.0210.418 ef ± 0.048
T30.405 b ± 0.0210.385 de ± 0.0120.335 ab ± 0.0070.375 cde ± 0.053
T40.395 b ± 0.0000.330 bcd ± 0.0000.335 ab ± 0.0350.355 bcd ± 0.036
T50.430 bc ± 0.0350.385 de ± 0.0070.450 bc ± 0.0140.423 ef ± 0.034
T60.243 a ± 0.0250.180 a ± 0.0280.300 a ± 0.0570.242 a ± 0.062
T70.373 b ± 0.0530.360 cde ± 0.0850.455 bc ± 0.0210.397 de ± 0.065
T80.420 bc ± 0.0140.430 e ± 0.0280.535 c ± 0.0210.462 f ± 0.059
T90.278 a ± 0.0250.245 ab ± 0.0070.420 abc ± 0.1700.315 bc ± 0.113
T100.390 b ± 0.0280.330 bcd ± 0.0280.415 abc ± 0.0780.378 de ± 0.055
p<0.001=0.003=0.090=0.002
Data represent the mean ± SD (standard deviation); significant differences of p < 0.05 according to the Multiple Range Test LSD (Least Significant Difference, ANOVA); p-value for differences between years, p = 0.002; a–e values for numbers express the evidence of differences between variants; a–f values for years express differences between years.
Table 7. Morphine, thebaine, and codeine content in dry capsules (% by dry weight).
Table 7. Morphine, thebaine, and codeine content in dry capsules (% by dry weight).
VariantYearAverage [%]
2021 b2022 a2023 c
T10.943 a ± 0.0881.030 ab ± 0.1702.105 a ± 0.1061.360 a ± 0.587
T21.790 b ± 0.0571.525 cd ± 0.0641.905 a ± 0.1911.740 c ± 0.198
T31.735 b ± 0.1201.555 cd ± 0.2761.780 a ± 0.2691.690 c ± 0.209
T41.810 b ± 0.0421.400 cd ± 0.0141.855 a ± 0.0781.688 c ± 0.228
T51.823 b ± 0.0041.600 d ± 0.1702.140 a ± 0.1411.855 c ± 0.262
T61.173 a ± 0.0460.895 a ± 0.0071.790 a ± 0.4241.287 a ± 0.452
T71.685 b ± 0.0641.515 cd ± 0.1062.280 a ± 0.0711.827 c ± 0.365
T81.738 b ± 0.0111.665 d ± 0.1342.250 a ± 0.0851.885 c ± 0.294
T91.123 a ± 0.0950.930 a ± 0.1132.070 a ± 0.5801.375 ab ± 0.608
T101.623 b ± 0.1571.275 bc ± 0.0072.020 a ± 0.5231.640 bc ± 0.414
p<0.001<0.001=0.377<0.001
Data represent the mean ± SD (standard deviation); significant differences of p < 0.05 according to the Multiple Range Test LSD (Least Significant Difference, ANOVA); p-value for differences between years, p < 0.001; a–d values for numbers express the evidence of differences between variants; a–c values for years express differences between years.
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Nastišin, Ľ.; Fejér, J.; Hercek, R.; Miháliková, A.; Fehér, A.; Porvaz, P.; Tóth, Š.; Hozlár, P. Effects of Plant Growth Regulators and Foliar Nutrients on the Alkaloid Content in Poppy Straw of Opium Poppy (Papaver somniferum L.). Int. J. Plant Biol. 2025, 16, 66. https://doi.org/10.3390/ijpb16020066

AMA Style

Nastišin Ľ, Fejér J, Hercek R, Miháliková A, Fehér A, Porvaz P, Tóth Š, Hozlár P. Effects of Plant Growth Regulators and Foliar Nutrients on the Alkaloid Content in Poppy Straw of Opium Poppy (Papaver somniferum L.). International Journal of Plant Biology. 2025; 16(2):66. https://doi.org/10.3390/ijpb16020066

Chicago/Turabian Style

Nastišin, Ľuboš, Jozef Fejér, Richard Hercek, Alena Miháliková, Alexander Fehér, Pavol Porvaz, Štefan Tóth, and Peter Hozlár. 2025. "Effects of Plant Growth Regulators and Foliar Nutrients on the Alkaloid Content in Poppy Straw of Opium Poppy (Papaver somniferum L.)" International Journal of Plant Biology 16, no. 2: 66. https://doi.org/10.3390/ijpb16020066

APA Style

Nastišin, Ľ., Fejér, J., Hercek, R., Miháliková, A., Fehér, A., Porvaz, P., Tóth, Š., & Hozlár, P. (2025). Effects of Plant Growth Regulators and Foliar Nutrients on the Alkaloid Content in Poppy Straw of Opium Poppy (Papaver somniferum L.). International Journal of Plant Biology, 16(2), 66. https://doi.org/10.3390/ijpb16020066

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