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Chemical and Biological Technologies in Agriculture
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Impact of essential oils on seed quality and seed-borne pathogens of Althea officinalis seeds of different ages

Chemical and Biological Technologies in Agriculture volume 10, Article number: 33 (2023) Cite this article

Abstract

Background

The cultivation of medicinal plants is a promising alternative to overcoming problems in the overharvesting of wild plants and ecosystem degradation. Cultivation depends upon two major factors: seed quality and the presence of seed-borne pathogens. Organic production of marshmallow plants (Althea officinalis L.) does not allow for the use of conventional pesticides. This study aimed to find an environmentally safe solution and the equilibrium between seed germination and the presence of fungal pathogens. The study was performed on a population of marshmallows which were cultivated for a period of 3 years (2018–2020) in Pančevo, The Republic of Serbia. The following six essential oils: Origanum vulgare L., Cinnamomum cassia Presl., Ocimum basilicum L., Carum carvi L., Mentha piperita L., Lavandula angustifolia Mill. at five concentrations (1%, 0.5%, 0.2%, 0.02%, 0.002%) were used for seed treatment along with water and PEG-40 (emulsifier) as controls. Germination, dormant seeds, dead seeds, abnormal seedlings and the presence of seed-borne pathogens were determined under laboratory conditions.

Results

Among the aforementioned treatments using oregano, cinnamon, basil, caraway, mint, and lavender essential oils, the most effective treatment resulted with lavender essential oil at a concentration of 0.02% in 3-year-old seeds. The highest values for seed germination and dead seeds were 46% and 20% in 3-year-old seeds, respectively. This treatment increased seed germination by 13%, and seedling growth i.e., the growth of seedling stems and radicles by 24–35%, respectively. It also reduced the presence of seed-borne fungal pathogens from 53 to 100%.

Conclusions

The results revealed that an increase in seed germination rate and simultaneous reduction in seed-borne fungal infection was achieved with the lavender essential oil seed treatments. This is the first discovery of the stimulating effect of lavender essential oil on seed quality parameters. Furthermore, the study demonstrates its potential application in seed processing in the organic production of marshmallow plants.

Graphical Abstract

Introduction

Marshmallow (Althea officinalis L.) is a medicinal plant that is widely used for human and animal healing treatments [1,2,3]. In nature, the cultivation of medicinal plants gradually decreased over time, especially as national lows became stricter. The solution to this problem appears to be the direct cultivation of seeds necessary to conserve the natural eco-balance of the environment and to promote biodiversity. From an economic point of view, the cultivation of marshmallows remains the most uncertain [4]. The main reasons for the high-risk production of marshmallows are due to low seed quality (primarily low seed germination) and seed health due to the presence of seed-borne pathogens [5, 6].

In the most general sense, seed germination is a process by which plants elongate. This process is strongly influenced by air temperature, soil moisture, air humidity, and light [7], but mostly by seed dormancy [8]. However, seed germination can be improved by applying various seed treatments [9, 10]. Previous studies, performed on marshmallow seeds from Serbian-grown populations, indicated a seed germination rate varying from 9.5% to 37.7% [11,12,13].

Essential oils (Eos) as ecological alternatives to conventional pesticides, show high potential for controlling seed-borne pathogens, but Eos seed germination reports are contradictory. Thyme Eo at a concentration of 400 µL/L showed the highest effect (100%) on Alternaria spp., seed-borne pathogens of carrots, tomatoes and onions [14], while the same oil, at a concentration of 1000 ppm, prevented fruit decay on Valencia oranges induced by Penicillium italicum [15]. Laurel Eo reduced the incidence of Stagonosporopsis cucurbitacearum to 67%, while seed germination was not affected by the treatment with 0.5 mg/mL Eo [16]. Oregano and cinnamon Eos inhibited the growth of tomato pathogens and did not inhibit seed germination [17]. Oregano and rosemary Eos inhibited the seed germination of wheat cultivars up to 87% [18]. In Myosotis arvensis seeds Juniperus excelsa Eo stimulated seed germination (43.3%), while J. sabina Eo inhibited germination (11.7%), compared to the control treatment of 31.7% [19].

In an attempt to establish an optimal method for improving seed quality, primarily the ability for germination, i.e., improving early seedling growth while reducing or eliminating pathogens, the objectives of this study were: to test the effect of oregano, cinnamon, basil, caraway, mint, and lavender Eos on marshmallow seeds at concentrations from 0.002% to 1%, to determine the impact of Eos on seed quality (percentages of germination, dormancy, dead seeds, and abnormal seedlings), to determine the effect of Eos on seedling growth (stem and root seedling growth), as well as to determine the presence of seed-borne pathogens, namely Mucor, Alternaria, Fusarium, and Penicillium spp.

Materials and methods

Plant materials

In 2018, 2019 and 2020, marshmallow seeds were collected in the South Banat region near the city of Pančevo (44°50′01′′N; 20°44′46′′E). Seeds were stored in three-layer paper bags under environmental conditions [20]. 1-, 2- and 3-year old seeds (2020-Y1, 2019-Y2 and 2018-Y3, respectively) were used as factor Y in the experiment.

Treatments with essential oils

Treatments with essential oils (factor A) include: oregano (Origanum vulgare L.) essential oil—Eo O, cinnamon (Cinnamomum cassia Presl.)—Eo C, basil (Ocimum basilicum L.)—Eo B, caraway (Carum carvi L.)—Eo K, mint (Mentha piperita L.)—Eo M, lavender (Lavandula angustifolia Mill.)—Eo L. The essential oils used were commercial products, purchased at a retail market. The aforementioned Eos were dissolved in distilled water at the following concentrations: 0.002, 0.02, 0.2, 0.5, and 1%, with 1% emulsifier added [21]. The emulsifier PEG-40 hydrogenated castor oil and distilled water-H2O were used as controls [22].

Three-year (Y1–Y3) Althea officinalis seeds were treated with each oil (A) at concentrations (0.002, 0.02, 0.2, 0.5 and 1%) for 24 h in an airtight box [23, 24]. The seeds were then sown in boxes (dimensions: 22 cm long, 15 cm wide, 5 cm deep), which were filled with sand. The sand was of a uniform grade (0.3–0.5 mm) and sterilised in 100 °C oven. Throught the germination period, the sand humidity (60–80%) was high enough to permit air flow through the substrate, with pH levels ranging from 6.0 to 7.5 [25]. Following seed treatment and sowing, the boxes were placed in a germination chamber (temperature 20/30 °C; 8 h light at 0.03 µmol/s/m2 and 16 h dark; 100 seeds in four replications). After 21 days, seed quality parameters were determined: dormant seeds-DS%, germinated seeds-GS%, dead seeds-DeS%, and abnormal seedlings-AS%. Dormant and dead seeds were subjected to the Tetrazolium test. The red colour that occurs in seed tissue is a positive indicator of seed viability by indicating respiration at the cellular level. Non-viable seed tissues do not react with Tetrazolium and, as a result, do not stain [26]. Seedling quality parameters: seedling stem (cm) and radicle growth (cm) were measured with a ruler on all normally developed seedlings [27], while percentages of seedlings infected with pathogens: Mucor, Alternaria, Fusarium, and Penicillium spp. were obtained following the ISTA Rules [28].

The tests were simultaneously performed following the same procedures in two accredited laboratories: Laboratory for Testing the Quality of Seeds and Planting Material at the Institute for Plant Protection and Environment in Topčider, Belgrade and the National Reference Laboratory, located in Batajnica, Belgrade (factor C).

Gas chromatography/mass spectrometry (GC/MS) and gas chromatography/flame ionization detection (GC/FID) analyses

GC/MS analysis was performed on Agilent Technologies 7890B gas chromatograph [29], equipped with a nonpolar, silica capillary column, HP-5MS (5% diphenyl- and 95% dimethyl-polysiloxane, 30 m × 0.25 mm, 0.25 μm film thickness; (Agilent Technologies, Santa Clara, CA, USA) and coupled with inert, selective 5977A mass detector [30] of the same company. Essential oils were dissolved in diethyl ether. One microlitre of the solution was injected into the GC column through a split/splitless inlet set at 250 °C in 40:1 split mode. Helium was used as the carrier gas, at the constant flow rate of 1 cm3/min. The oven temperature increased from 60 °C to 246 °C at the rate of 3 °C/min. Temperatures of the MSD transfer line, ion source and the quadrupole mass analyser were set at 300 °C, 230 °C and 150 °C, respectively. The ionization voltage was 70 eV and the mass range was 41–415 m/z.

The GC/FID analysis was carried out under identical experimental conditions as GC/MS. The flows of the carrier gas (He), make-up gas (N2), fuel gas (H2), and oxidizing gas (air) were 1, 25, 30, and 400 cm3/min, respectively. The temperature of the flame-ionization detector (FID) was set at 300 °C.

Data processing was performed using the following softwares: MSD ChemStation, Mass Hunter Qualitative Analysis and AMDIS_32 software (Agilent Technologies, USA). Retention indices of components from the sample were experimentally determined using a homologous series of n-alkanes from C8–C20 as standards and analysed under identical GC/MS and GC/FID conditions. The identification of Eo constituents was based on the comparison of their retention indices (RIexp) with those (RIlit) available in the literature [31]. Their mass spectra were compared with those of the authentic standards as well as with those from Willey 6, NIST2011 and RTLPEST3 libraries, and by co-injection with the authentic standards (Sigma Chemical Company, St. Louis, MO, USA). A particular component`s percentage composition of the Eo was determined based on an area percentage report (uncalibrated calculation procedure), which was generated by Agilent ChemStation software.

Statistical analysis

Analysis of variance (F test) was performed in the first phase of a three-factor factorial design [32]. Treatment effects were tested using Tukey’s multiple range test. Standard error of the mean differences (± SED) was calculated for deviation from the mean values. The relative dependence of traits was determined by Pearson’s coefficient and the multiple regression coefficients [33]. Transformations have been applied to percentage values [34].

Results

Impact of investigated factors

According to analysis of variance (ANOVA) of the impact of the following factors: essential oils (A), seed age (Y) and their interactions (A × Y) on seed quality, seedling growth and pathogen presence in seedlings had significant effects (p ≤ 0.05; p ≤ 0.001; p ≤ 0.001). On the other hand, the laboratory-based effects, factor C, and the interaction between factors A and Y, were not significant (p ≥ 0.05) (Table 1). Mean values from the two laboratories are shown below.

Table 1 Results of analysis of variance (ANOVA) for seed quality: abnormal seedlings (AS) growth of embryonic stems and roots, presence of pathogens, GS—germinated seeds, DS—dormant seeds, DeS%—dead seeds
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Impact of essential oils on seed quality of Althea officinalis

Seed germination

Percentages of germinated seeds in oil treatments at a concentration of 0.002%, ranged from 32% (oregano, basil, caraway) to 34% (mint) in 1-year-old seeds. In 2-year-old seeds, percentages of germinated seeds ranged from 33% (lavender) to 36% (oregano, mint), whereas in 3-year-old seeds, percentages of germinated seeds varied between 31% (cinnamon) and 34% (caraway) Eos. No treatment was statistically different from controls (Fig. 1a). Percentages of germinated seeds at a concentration of 0.02%, ranged from 2% (oregano, basil) to 10% (lavender) in 1-year-old seeds, and were statistically different from controls. In 2-year-old seeds, percentages of germinated seeds ranged from 4% (oregano) to 11% (lavender), whereas both Eos were statistically different from controls, while in 3-year-old seeds, percentages of germinated seeds varied between 28% (oregano) and 46% (lavender) Eos, and were statistically different from the control treatments (Fig. 1b). No germinated seeds were observed when 1-, 2- and 3-year old seeds were treated with a concentration of 0.2% Eos, whereas control treatments varied between 32 and 34% (Fig. 1c). The same results were obtained after applying all tested Eos at concentrations of 0.5% (Fig. 1d) and 1% (Fig. 1e), suggesting that concentrations above 0.2% are too high to promote germination.

Fig. 1
figure 1

Impact of different concentrations of Eos on seed germination of A. officinalis of different ages: a 0.002%; b 0.02%; c 0.2%; d 0.5%; e 1%. Seed age: 1 year (2020‒Y1), 2 years (2019‒Y2) and 3 years (2018–Y3). Eos: oregano Eo, cinnamon Eo, basil Eo, caraway Eo, mint Eo, lavender Eo; E—emulsifier PEG-40 hydrogenated castor oil; W—Water, H2O Ø. For all seed ages, Tukey's Multiple Range test a, b,… x, significant effect p ≤ 0.05; standard error of the differences of means (± SED)

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Seed dormancy

Percentages of dormant seeds in oil treatments at a concentration of 0.002%, ranged from 36% (oregano, cinnamon) to 38% (caraway, mint, lavender) in 1-year-old seeds. Control treatments were 40%. In 2-year-old seeds, percentages of dormant seeds ranged from 33% (cinnamon) to 36% (mint) Eos, while control treatments ranged from 36 to 37%. In 3-year-old seeds, percentages of dormant seeds varied between 13% (oregano, cinnamon, basil) and 14% (caraway, mint, lavender) Eos. Control treatments were 15%. No treatments were statistically different from controls (Fig. 2a). Percentages of dormant seeds at a concentration of 0.02%, varied between 32% (caraway) and 37% (basil). Other Eos, except cinnamon and basil, were statistically different from controls in 1-year-old seeds. The control treatments were in the range: 38–40%. In the case of 2-year-old seeds, the lowest percentages of dormant seeds (20% and 21%) were recorded in the lavender and mint oil treatments respectively, which were statistically different from controls, while the remaining treatments of Eos had higher percentages (24–27%) of dormant seeds, that were not statistically different from controls. The control treatments were in the range: 36–38%. Percentages of dormant seeds in 3-year-old seeds ranged from 0% (oregano) to 4% (lavender) Eos. All treatments, except oregano and basil Eos, were not statistically different from controls. The control treatments were in the range: 15–16% (Fig. 2b). Application of Eos at a concentration of 0.2%, resulted in seed dormancy rates ranging from 13% (oregano) to 20% (lavender) in 1-year-old seeds. All treatments were statistically different from controls. Control treatments were 39–40%. Dormancy in 2-year-old seeds ranged from 10% (oregano and cinnamon) to 16% (lavender). Control treatments were 35–36% and all treatments were statistically different from controls. Corresponding values for 3-year-old seeds varied from 6% (oregano), to 13% (lavender) and were statistically different from controls. Control treatments were 15–16% (Fig. 2c). After application of all types of Eos at a concentration of 0.5%, percentages of dormant seeds varied from 3% (oregano) to 8% (lavender) in 1-year-old seeds, compared to the control treatments of 39–40%. In 2-year-old seeds, percentages of dormant seeds were between 4% (oregano and cinnamon) and 7% (lavender) compared to the control treatments of 35–36%, whereas in 3-year-old seeds, percentages of dormant seeds ranged from 3% (oregano, cinnamon) to 5% (lavender, mint) Eos. Control treatments were: 15–16%. All treatments were statistically different from controls (Fig. 2d). Treatments of all Eo types at a concentration of 1%, resulted in 0% dormant seeds, which was statistically different from controls. Control treatments varied between 15 and 41% (Fig. 2e).

Fig. 2
figure 2

Impact of different concentrations of Eos on seed dormancy of A. officinalis of different ages: a 0.002%; b 0.02%; c 0.2%; d 0.5%; e 1%. Seed age: 1 year (2020-Y1), 2 years (2019-Y2) and 3 years (2018-Y3). Eos: oregano Eo, cinnamon Eo, basil Eo, caraway Eo, mint Eo, lavender Eo; E—emulsifier PEG-40 hydrogenated castor oil; W—Water, H2O Ø; For all seed ages, Tukey's Multiple Range test a, b,… x, significant effect p ≤ 0.05; standard error of the differences of means (± SED)

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Dead seeds

Percentages of dead seeds in oil treatments at a concentration of 0.002%, ranged from 20% (mint, lavender) to 23% (oregano, cinnamon, basil) in 1-year-old seeds. In 2-year-old seeds, percentages of dead seeds ranged from 17% (caraway, mint, basil) to 18% (oregano, lavender, cinnamon), whereas in 3-year-old seeds, percentages of dead seeds varied between 27% (lavender, cinnamon) and 29% (basil) Eos. Control treatments were not significantly different from oil treatments in all years (Fig. 3a). Regarding the 1-year-old seeds treated with the tested oils at a concentration of 0.02%, percentages of dead seeds varied from 42% (basil, cinnamon) to 45% (oregano, mint) Eos and were significantly different from controls. Control treatments varied between 17 and 20%. In 2-year-old seeds, percentages of dead seeds ranged from 42% (basil, cinnamon) to 45% (lavender) Eos, representing a significant difference from the control treatments. Controls were 15–17%. In 3-year-old seeds, percentages of dead seeds varied between 31% (lavender) and 51% (caraway) Eos, and were significantly different from the control treatments. Controls ranged from 25 to 28% (Fig. 3b). Percentages of dead seeds in oil treatments at a concentration of 0.2%, ranged from 78% (lavender) to 87% (oregano) in 1-year-old seeds. Controls were 17–20%. In 2-year-old seeds, percentages of dead seeds ranged from 81% (lavender) to 90% (oregano and cinnamon) Eos, compared to controls: 15–17%, whereas in 3-year-old seeds, percentages of dead seeds varied between 80% (lavender) and 94% (oregano) Eos. Controls were 26–27%. All treatments were significantly different from controls (Fig. 3c). Treatments with all Eo types at a concentration of 0.5% resulted in more than 90% of dead seeds in all years. This was significantly different from controls which ranged from 15 to 27% (Fig. 3d). At a concentration of 1% all Eos (Fig. 3e), 100% dead seeds were obtained, which was significantly different from controls (15–25%).

Fig. 3
figure 3

Impact of different concentrations of Eos on dead seeds of A. officinalis of different ages: a 0.002%; b 0.02%; c 0.2%; d 0.5%; e 1%. Seed age: 1 year (2020‒Y1), 2 years (2019‒Y2) and 3 years (2018‒Y3). Eos: oregano Eo, cinnamon Eo, basil Eo, caraway Eo, mint Eo, lavender Eo; E—emulsifier PEG-40 hydrogenated castor oil; W—Water, H2O Ø. For all seed ages, Tukey's Multiple Range test a, b… x, significant effect p ≤ 0.05; standard error of the differences of means (± SED)

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Abnormal seedlings

Percentages of abnormal seedlings in oil treatments at a concentration of 0.002%, ranged from 8% (mint) to 9% (all other Eos) in 1-year-old seeds. Controls were at 7%. In 2-year-old seeds, percentages of abnormal seedlings ranged from 11% (mint) to 15% (lavender, cinnamon, basil). Controls varied from 12 to 13%; while in 3-year-old seeds, percentages of abnormal seedlings varied from 24% (caraway) to 29% (cinnamon) Eos. Controls were 26‒28%. All treatments were not significantly different from controls (Fig. 4a). Percentages of abnormal seedlings in 1-year-old seeds varied from 12% (lavender) to 20% (caraway, cinnamon, oregano) Eos, when applied at a concentration of 0.02%. Controls were 8% to 9%. In 2-year-old seeds percentages of abnormal seedlings ranged from 15% (lavender) to 24% (basil), compared to controls (12–13%). Oil treatments in 1- and 2-year-old seeds were significantly different from controls. In 3-year-old seeds percentages of abnormal seedlings varied from 19% (lavender, mint) to 24% (oregano), and were not significantly different from controls. Controls were 24–25% (Fig. 4b). Treatments of seeds with Eos at a concentration of 0.2% resulted in the occurrence of abnormal seedlings: 2% in 1-year-old seeds treated with lavender oil (controls: 6‒9%), then 1–3% in 2-year-old seeds treated with mint and lavender Eos, respectively (controls: 13‒16%), and 3–7% in 3-year-old seeds also treated with mint and lavender oil, respectively (controls: 24‒25%). No abnormal seedlings were found in other oil treatments. All treatments were significantly different from controls (Fig. 4c). After the application of lavender Eo at a concentration of 0.5% only one, i.e., two abnormal seedlings were found in one‒i.e., 2-year-old seeds, respectively (controls ranged from 9‒10% to 12‒16% respectively). No abnormal seedlings were found in any of the other treatments. In 3-year-old seeds, no abnormal seedlings were found in all oil treatments, whereas in the control treatments results ranged from 24 to 25%. All treatments were significantly different from controls (Fig. 4d). At a 1% oil concentration, abnormal seedlings were 0%. Control treatments were: 9‒11%, 12‒16% and 23‒27% in the first, second, and third year of seed age, respectively. All treatments were significantly different from controls (Fig. 4e). According to the ISTA Rules 2020 [21], abnormal seedlings are not accepted as germinated seeds because they do not develop into normal plants in the field.

Fig. 4
figure 4

Impact of different concentrations of Eos on abnormal seedlings of A. officinalis of different ages: a 0.002%; b 0.02%; c 0.2%; d 0.5%; e 1%. Seed age: 1 year (2020Y1), 2 years (2019Y2) and 3 years (2018Y3). Eos: oregano Eo, cinnamon Eo, basil Eo, caraway Eo, mint Eo, lavender Eo; Eemulsifier PEG40 hydrogenated castor oil; W Water, H2O Ø. For all seed ages, Tucey's Multiple Range test a, b,… x, significant effect p ≤ 0.05; standard error of the differences of means (± SED)

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Seedling growth

After applying oil treatments at a concentration of 0.02% the stem and root (radicle) growth values were significantly lower in 1- and 2-year-old seeds than those determined in the control treatments (Table 2). Seedling stem growth in 3-year-old seeds treated with lavender Eo was faster and stems were longer 0.87 cm and 0.88 cm, i.e., 24–26% than the stems in controls. In addition, roots were 0.68 and 0.70 cm longer, i.e., 35% longer in comparison to root lengths determined in the control treatments. Similar results were obtained when the mint oil treatment was applied. Seedling stems and roots were longer 0.35 and 0.36 cm i.e., 10%, and 0.26 and 0.28 cm i.e., 11%, respectively. However, these differences were not significantly different from controls. The treatments with caraway and basil Eos on seedling growth were at the same level as that of the control treatments. Cinnamon as well as oregano Eos had a detrimental effect on stem and root growth, compared to that of the control treatments (Table 2).

Table 2 Results of seedling growth after the treatment with essential oils at the concentration of 0.02% on A. officinalis seeds of different ages
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Impact of essential oils on seed-borne fungal pathogens of Althea officinalis

Mucor sp.

Percentages of Mucor sp. in the oil treatments at a concentration of 0.002%, ranged from 13% (lavender) to 15% (mint) in 1-year-old seeds. Controls were at 16%. In 2-year-old seeds, percentages of Mucor sp. ranged from 17% (lavender, oregano) to 18% (mint, basil) Eos compared to controls (19–20%), whereas in 3-year-old seeds, percentages of Mucor sp. varied between 13% (oregano) and 15% (mint) Eos. The control treatments were 16–17%. In 3-year-old seeds all treatments, except oregano Eo were not significantly different from controls (Fig. 5a). Treatment with cinnamon oil at a concentration of 0.02% was the most effective regarding the incidence of Mucor sp. in 1-year-old seeds (4%), in contrast to seeds treated with oregano (10%), mint (10%) and lavender (12%) Eos. Control treatments were 16‒17%. In 2-year-old seeds percentages of Mucor sp. ranged from 2% (cinnamon) to 9% (caraway) Eos. Controls were 19‒20%. In 3-year-old seeds, percentages of fungal growth varied from 7% (lavender) to 10% (oregano, cinnamon) Eos, while controls were 15–16%. All Eos treatments were significantly different from controls (Fig. 5b). At a concentration of 0.2%, which completely inhibited Mucor growth, the most effective treatments were achieved with oregano, cinnamon, caraway, and mint Eos in 1-year-old seeds. The control treatments were 16‒17%. The same effect was observed in 2-year-old seeds treated with oregano, cinnamon, caraway, and basil Eos. Controls were 18–20%. In 3-year-old seeds, treatments with oregano, cinnamon, caraway, and mint Eos completely inhibited Mucor growth. Controls were 15‒16%. All treatments were significantly different from controls (Fig. 5c). All types of Eos (oregano, cinnamon, basil, caraway, mint, and lavender), at concentrations of 0.5% (Fig. 5d) and 1% (Fig. 5e), were 100% effective in suppressing Mucor sp. and results were significantly different from control values (15–18%).

Fig. 5
figure 5

Impact of different concentrations of Eos on the presence of Mucor sp. on seedlings of A. officinalis of different ages: a 0.002%; b 0.02%; c 0.2%; d 0.5%; e 1%. Seed age: 1 year (2020Y1), 2 years (2019Y2) and 3 years (2018Y3). Eos: oregano Eo, cinnamon Eo, basil Eo, caraway Eo, mint Eo, lavender Eo; E—emulsifier PEG-40 hydrogenated castor oil; W—water, H2O Ø. For all seed ages, Tukey's Multiple Range test a, b,… x, significant effect P ≤ 0.05; standard error of the differences of means (± SED)

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Alternaria sp.

Percentages of Alternaria sp. in oil treatments at a concentration of 0.002%, ranged from 31% (lavender, mint) to 34% (basil) Eos in 1-year-old seeds. In 2-year-old seeds, percentages of Alternaria sp. ranged from 30% (basil, cinnamon, lavender) to 32% (mint) Eos, whereas in 3-year-old seeds, percentages of Alternaria sp. varied between 31% (basil, oregano) and 33% (caraway) Eos. All treatments were not significantly different from controls, which were 32‒35% (Fig. 6a). Treatment with lavender oil at a concentration of 0.02% in 1-year-old seeds was the most effective in reducing Alternaria sp. (fungal growth was 19%), compared to the maximal level of 29%, achieved with mint Eo. In 2-year-old seeds, treatment with cinnamon Eo was the most effective (19%), while treatments with caraway and oregano Eos were the least effective (23%). In addition, in 3-year-old seeds, treatment with cinnamon Eo was the most effective (4%) and treatment with oregano was the least effective (11%). In all years, controls varied from 33 to 35%, whereas all treatments were significantly different from controls (Fig. 6b). The most effective treatments at a concentration of 0.2%, were achieved with oregano, cinnamon, and mint Eos, resulting in complete inhibition of Alternaria in 1-year-old seeds. The same effect was observed in 2-year-old seeds whereas treatments with oregano, cinnamon, caraway, and mint Eos completely inhibited Alternaria growth in 3-year-old seeds. In all years, controls varied between 33 and 35% and all treatments were significantly different from controls (Fig. 6c). All types of Eos at concentrations of 0.5% (Fig. 6d) and 1% (Fig. 6e) were 100% effective in suppressing Alternaria sp. and all treatments were significantly different from controls which were 9‒12% in all years.

Fig. 6
figure 6

Impact of different concentrations of Eos on the presence of Alternaria sp. on seedlings of A. officinalis of different ages: a 0.002%; b 0.02%; c 0.2%; d 0.5%; e 1%. Seed age: 1 year (2020Y1), 2 years (2019Y2) and 3 years (2018Y3). Eos: oregano Eo, cinnamon Eo, basil Eo, caraway Eo, mint Eo, lavender Eo; E‒emulsifier PEG‒40 hydrogenated castor oil; W Water, H2O Ø. For all seed ages, Tukey's Multiple Range test a, b,… x, significant effect p ≤ 0.05; standard error of the differences of means (± SED)

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Fusarium sp.

Percentages of Fusarium sp. in oil treatments at a concentration of 0.002%, ranged from 9% (basil, caraway, cinnamon, lavender) to 10% (mint) Eos in 1-year-old seeds. Controls were at 11%. In 2-year-old seeds, percentages of Fusarium sp. ranged from 8% (lavender) to 9% (all other Eos). Controls were 10‒11%. In 3-year-old seeds, percentages of Fusarium sp. varied between 9% (oregano) and 12% (mint) Eos. Controls were 12‒13%. In 3-year-old seeds, all treatments, except oregano Eo, were not significantly different from controls (Fig. 7a). Percentages of Fusarium sp. in oil treatments at a concentration of 0.02%, ranged from 7% (lavender) to 10% (mint) Eos, (controls: 11%), in 1-year-old seeds. In 2-year-old seeds, percentages were between 2% (oregano) and 7% (cinnamon), compared to the control values 10–11%. In 3-year-old seeds, percentages of Fusarium varied from 2% (lavender) to 7% (cinnamon) Eos, compared to 12% of control values. In one-year-old seeds, all treatments, except mint Eo, were significantly different from controls (Fig. 7b). The most effective treatments, resulting in complete inhibition of Fusarium were achieved with oregano, cinnamon, caraway and mint Eos, at a concentration of 0.2% in 1-year-old seeds. Controls were at 11%. Complete inhibition of Fusarium (100%) was observed in 2-year-old seeds treated with oregano, cinnamon, caraway, mint, and basil Eos, up to 99% inhibition of Fusarium treated with lavender Eo. Controls were 10–11%. In 3-year-old seeds, percentages of Fusarium growth varied from 0% (oregano, cinnamon, caraway, mint, lavender) to 2% (basil) Eos, compared to 12% of the control values. All treatments were significantly different from controls (Fig. 7c). All types of essential oils at concentrations of 0.5% (Fig. 7d) and 1% (Fig. 7e), were 100% effective in suppressing Fusarium growth. All treatments were significantly different from controls which were 9 12%.

Fig. 7
figure 7

Impact of different concentrations of Eos on the presence of Fusarium sp. on seedlings of A. officinalis of different ages: a 0.002%; b 0.02%; c 0.2%; d 0.5%; e 1%. Seed age: 1 year (2020‒Y1), 2 years (2019‒Y2) and 3 years (2018‒Y3). Eos: oregano Eo, cinnamon Eo, basil Eo, caraway Eo, mint Eo, lavender Eo; E‒emulsifier PEG-40 hydrogenated castor oil; W—Water, H2O Ø. For all seed ages, Tukey's Multiple Range test a, b,… x, significant effect p ≤ 0.05; standard error of the differences of means (± SED)

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Penicillium sp.

Percentages of Penicillium sp. in oil treatments at a concentration of 0.002%, ranged from 8% (oregano, lavender) to 11% (basil, caraway, mint) in 1-year-old seeds. In 2-year-old seeds, percentages of Penicillium sp. ranged from 8% (lavender) to 11% (caraway), whereas in 3-year-old seeds, percentages of Penicillium sp. varied between 8% (oregano) and 10% (mint, lavender) Eos. Controls varied from 10 to 11%, in all years, and all treatments were not significantly different from controls (Fig. 8a). In 1-year-old seeds, percentages of Penicillium sp. in the oil treatments at a concentration of 0.02%, varied from 1% (basil, lavender, caraway) to 4% (oregano) Eos. In 2-year-old seeds, percentages of Penicillium sp. were between 0% (lavender, basil, mint, and oregano) and 1% (cinnamon, caraway). In 3-year-old seeds, the most effective treatments, resulting in complete inhibition of Penicillium sp., were achieved with lavender, caraway, oregano, and mint Eos, whereas cinnamon and basil Eos inhibited 97% and 98% Penicillium, respectively. All treatments were significantly different from controls (Fig. 8b). The most effective treatments resulting in complete inhibition of the Penicillium growth, at a concentration of 0.2%, were achieved with oregano, cinnamon, caraway, mint, and lavender Eos, in 1-year-old seeds. In 2-year-old seeds, complete inhibition of Penicillium was caused by treatments with all Eos. In 3-year-old seeds, complete inhibition of Penicillium growth was achieved with oregano, cinnamon, caraway, mint, and lavender Eos, while 1% of the fungal growth, was achieved with basil Eo. Controls varied from 10 to 11% in all years. All treatments were significantly different from controls (Fig. 8c). No single pathogen was detected after application of all Eos at concentrations of 0.5% (Fig. 8d) and 1% (Fig. 8e) in all years. Controls were 9‒13%, in all years. All treatments were significantly different from controls.

Fig. 8
figure 8

Impact of different concentrations of Eos on the presence of Penicillium sp. on seedlings of A. officinalis of different ages: a 0.002%; b 0.02%; c 0.2%; d 0.5%; e 1%. Seed age: 1 year (2020Y1), 2 years (2019Y2) and 3 years (2018Y3). Eos: oregano Eo, cinnamon Eo, basil Eo, caraway Eo, mint Eo, lavender Eo; Eemulsifier PEG40 hydrogenated castor oil; W—Water, H2O Ø. For all seed ages, Tukey's Multiple Range test a, b,… x, significant effect p ≤ 0.05; standard error of the differences of means (± SED)

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Impact of essential oils on the relationship between seed germination and the presence of seed‒borne fungal pathogens

The relationship between the two major cultivation factors of A. officinalis, namely, of seed germination and pathogen presence was influenced by different Eos (mean values), and are presented as a scatter diagram, shown in Fig. 9. The best results were obtained with oregano, lavender, and cinnamon Eos, in relation to Penicillium, Alternaria and Fusarium spp. respectively, shown in the upper left corner of the diagram. Percentages of fungal pathogens were up to 5%, while the germination rate peaked at 36%. The best result was achieved with lavender Eo.

Fig. 9
figure 9

Impact of essential oils on the relationship between seed germination and the presence of seed-borne fungal pathogens (Penicillium, Mucor, Alternaria, and Fusarium spp.) in Althea officinalis seeds (mean values)

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Chemical composition of essential oils

Cinnamon, oregano and lavender oils had the highest degree of fungal growth inhibition, so therefore their chemical composition was analysed. According to the GC/MS and GC/FID analyses, 19 compounds, representing 100% of the total cinnamon Eo composition, were identified. Its main components were cinnamaldehyde and methoxy-cinnamaldehyde (95.9%), while cinnamyl acetate was the third major compound in the total essential oil composition (Table 3).

Table 3 Chemical composition of cinnamon Eo
Full size table

The chemical analysis of oregano Eo identified 18 compounds, representing 99.9% of the total essential oil composition, with the greatest number of aromatic compounds, contributing with 88.4%, followed by monoterpene hydrocarbons (4.6%) and oxygen-containing monoterpenes (4.3%). Carvacrol was the representative of aromatic, i.e., phenolic compounds contributing with 77.9%, while α-pinene and linalool were major compounds of monoterpene hydrocarbons and oxygen-containing monoterpenes, respectively (Table 4).

Table 4 Chemical composition of oregano Eo
Full size table

Twenty-nine compounds were identified in lavender Eo, representing 100% of the total essential oil composition. The main components were linalool and linalyl acetate, as the representatives of oxygen-containing monoterpenes (Table 5).

Table 5 Chemical composition of lavender Eo
Full size table

Pearson correlation coefficients (r) among studied traits

Taking into consideration 240 pairs (eight oil treatments, five oil concentration levels, three seed ages, and two laboratories), the strongest positive correlation was established between the germination rate and the seedling stem growth (r = 998), and the radicle growth (r = 999), as well as between the seedling stem and radicle growth (r = 999). As expected, a negative and highly significant (p ≤ 0.001) correlation was established between dead seeds and the remaining tested traits of seed and seedling qualities (Table 6). A strong negative correlation was also determined between dormant and dead seeds (r = 816).

Table 6 Pearson correlation coefficients (r) of the tested traits after the oil treatment was applied to A. officinalis seeds (n = 240)
Full size table

Discussion

The germination rate of A. officinalis seeds averaged approximately 33% in controls and varied slightly, independent of seed age. The increase in Eo concentration, resulted in a decrease of the germination rate, indicating the damage of seeds and embryos by high oil concentrations [35]. The germination rate, and conditions under which seeds germinate can increase during post-ripening [36]. Treatment of Eos at a concentration of 0.02% showed full efficacy and the germination rate was increased by 13%, in 3-year-old seeds. On the other hand, full efficacy of the same treatment was not achieved in 1- and 2-year-old seeds, due to the high percentage of dormant seeds. Seed dormancy is a biological trait that allows seeds to germinate when environmental conditions are favourable [37]. Many species survive in nature due to this trait [7]. Storage or post-ripening is the most economical way to break dormancy [38]. Although seed dormancy is one of the most studied traits, not all aspects of the complex mechanisms of seed dormancy are known [35]. Malvaceous seed dormancy is both physical and physiological [39,40,41]. Physical dormancy is based on the impermeable seed coat. The seed coat serves to protect seed germination capacity and longevity [42]. Scarification is an effective measure that reduces the percentage of dormant seeds and increase seed germination in the Malvaceae family [43, 44], as well as in other families [45, 46]. In this study, marshmallow seeds were initially dormant, whereby dormancy decreased from the youngest to the oldest seeds. However, it is important to find an optimal treatment according to the duration of scarification, the concentration of the solution, etc. [46]. Our study clearly shows the scarification effect of lavender Eo at a concentration of 0.02%, in which seed dormancy was reduced by 11%, while the germination rate was increased by 13%. In 1- and 2-year-old seeds, there were higher percentages of dormant seeds and lower percentages of dead seeds. In contrast, 3-year-old seeds had a higher percentage of dead seeds and a lower percentage of dormant seeds. Essential oil concentrations above 0.02%, decreased number of dormant seeds and increased number of dead seeds, indicating damage to embryos due to high oil concentrations. Effective application improved seedling quality, resulting in rapid growth of stems and radicles by 24‒35%, respectively. This is also indicated by the strongest correlation between germination rate and seedling stem and root growth, consistent with the results obtained by other researchers [47,48,49]. Increasing the Eo concentration above 0.02% decreased number of abnormal seedlings, and increased number of dead seeds. The highest concentrations (0.5% and 1%) yielded 0% abnormal seedlings and 100% dead seeds, indicating the damage of seed embryos. Low oil concentration indirectly affected stem and root growth. The higher the seed coat permeability, the faster the seed germination and the better seedlings development [50]. The results of Nishida et al. [51] show that the presence of lipid globules at increased oil concentrations causes anatomical changes in seedlings, such as a decrease in mitochondria and deterioration of the seed coat. Membranes of root cells undergo structural changes that limit root growth [52, 53].

Pathogens may be present in seeds, depending on the variety, sowing date, and environmental factors [54]. Fungal growth was completely or significantly inhibited in seeds treated with Eo concentrations of 0.5% and 1%. Low concentrations of Eos failed to prevent fungal growth of Alternaria, Aspergillus, Fusarium, and Penicillium similarly to the study of Karaca et al. [55]. According to Tanović et al. [56], mint and basil Eos used at concentrations of 0.04‒0.65 μL/mL (air), were found to partially or completely inhibit the growth of Fusarium. Regarding the susceptibility of fungal pathogens to Eos, in our study, Penicillium, then Fusarium and Mucor. were the most susceptible fungal species. Alternaria sp. was the most resistant species, except in 2018 when the fungus responded similarly to Fusarium and Mucor spp. Mucor sp., isolated from 1- and 2-year-old seeds was the most susceptible to cinnamon Eo, while the same fungus detected in 3-year-old seeds was proven to be the most susceptible to lavender Eos. Alternaria and Fusarium determined in seeds of all ages were the most susceptible to cinnamon and oregano oil, respectively. Furthermore, Penicillium detected in seeds of all ages was the most susceptible to lavender essential oil. The presence of pathogens varied slightly between the seed years, which was in correlation with meteorological data (Additional file 1: Table S1), similarly to the data of Poole et al. [57].

In general, Mucor and Alternaria were the most susceptible to cinnamon Eo, Fusarium to oregano, and Penicillium was the most susceptible to lavender Eo. Lavender oil at a concentration of 0.02% was the most effective in the simultaneous inhibition of the fungal growth and the stimulation of seed germination. Golijan-Pantović and Sečanski [58] demonstrated that essential oils have stimulating properties. The results point out that oregano oil at a concentration of 3.2 mL/L increased the proportion of healthy seedlings (69.8%) in contaminated soil compared to the control. Cinnamaldehyde was the major prevalent component of cinnamon Eo, whereas carvacrol was the major compound of oregano Eo, according to GC/MS and GC/FID analyses. Linalool and linalyl acetate were the main components of lavender Eo. Sing and Chittenden [59] reported inhibition of Mucor growth on panel products by cinnamaldehyde. Carvacrol is the phenolic component of oregano Eo and like other natural phenolic compounds, has been proven to have potent antifungal properties [60]. Both cinnamaldehyde and phenol may be important factors in inhibiting fungal growth in this study. Aldehydes and phenols are chemicals that can be transformed into highly toxic compounds in living cells [61]. Linalool and its ester linalyl acetate have low acute oral and dermal toxicity [62, 63], and are low toxic compounds. Consequently, they may not damage seed embryo. Therefore, lavender Eo performed the best among all other Eos at a concentration of 0.02%, without damaging the embryos and enhancing seed germination.

Conclusions

The impact of Eos on Althea officinalis seed quality and seed health depends on the Eo species, its concentration as well as seed age. Increase in Eo concentrations above 0.02%, resulted in lower germination, fewer dormant seeds and abnormal seedlings and more dead seeds, which indicates damage of seeds and embryos. In 1-and 2-year-old seeds, a high percentage of dormant seeds under optimal treatment of Eos prevented an increase in the germination rate. Concentrations of 0.5% and 1% Eos were 100% effective in suppressing pathogens, while completely inhibiting seed germination.

The most optimal treatment was the application of lavender Eo in 3-year-old A. officinalis seeds at a concentration of 0.02%. The treatment increased the seed germination rate by 13%, significantly increased seedling stem and radicle growth (24‒35%), and significantly reduced the presence of the pathogens Mucor, Fusarium, Alternaria, and Penicillium spp., in the range from 53 to 100%. This is the first discovery of the stimulating effect of lavender Eo on the seed quality parameters that demonstrates its potential use in seed processing in the organic production of marshmallows, which should be confirmed in future field study trials.

Availability of data and materials

The datasets used during the current study are available from the corresponding author on reasonable request.

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Acknowledgements

The authors thank the Ministry of Science, Technological Development and Innovations, Republic of Serbia, for the financial support, and thank all their laboratory teams for their support and suggestions.

Funding

Supported by the Ministry of Science, Technological Development and Innovations; Republic of Serbia, Contracts No. 451-03-47/2023-01/20010; 451-03-47/2023-01/200383; 451-03-47/2023-01/2040.

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Authors and Affiliations

  1. Faculty of Agriculture, University of Niš, Kosančićeva 4, 37000, Kruševac, Serbia

    Dragan Terzić

  2. Maize Research Institute Zemun Polje, Slobodana Bajića 1, 11185, Belgrade-Zemun, Serbia

    Marijenka Tabaković

  3. Institute for Plant Protection and Environment, Teodora Drajzera 9, 11040, Belgrade, Serbia

    Violeta Oro, Dobrivoj Poštić, Ratibor Štrbanović & Rade Stanisavljević

  4. Institute for Medicinal Plants Research “Dr Josif Pančić”, Tadeuša Košćuška 1, 11000, Belgrade, Serbia

    Vladimir Filipović

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  1. Dragan Terzić
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  2. Marijenka Tabaković
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  3. Violeta Oro
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  4. Dobrivoj Poštić
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  7. Rade Stanisavljević
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Contributions

RS, VO and MT wrote the manuscript. RS, VO, VF and MT prepared methodology, MT, VO and RS prepared figures. VO, VF and DT analysed and interpreted data, DT, RŠ, VF, and DP designed the work, RS and MT performed formal analyses, DP and RŠ performed investigation, DP, VF and RŠ carried out data curation, DP, RŠ and DT edited manuscript, DT and RS supervised the work. Funding acquisition was done by DT. All authors have read and agreed to the published version of the manuscript. All authors reviewed the manuscript. All authors read and approved the final manuscript.

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Correspondence to Dragan Terzić.

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Supplementary Information

Additional file 1

: Table S1.Sum of precipitation and max and min temperature during IV to VIII months in surroundings of the city of Pancevo - 44°50'01'' N; 20°44'46'' E and 85 m above sea level during 2018, 2019, 2020 years.

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Terzić, D., Tabaković, M., Oro, V. et al. Impact of essential oils on seed quality and seed-borne pathogens of Althea officinalis seeds of different ages. Chem. Biol. Technol. Agric. 10, 33 (2023). https://doi.org/10.1186/s40538-023-00405-8

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