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Article

Evaluation of the Effect of Low-Temperature Plasma Treatment on Seed Germination of Long-Term Stored Genetic Resources

by
Martin Matějovič
1,2,
Eva Jozová
1,
Michael Rost
1,
Vladislav Čurn
1,
František Hnilička
3,
Zora Kotíková
3 and
Petra Hlásná Čepková
2,*
1
Faculty of Agriculture and Technology, University of South Bohemia, Branišovská 1645/31a, 370 05 České Budějovice, Czech Republic
2
Crop Research Institute, Drnovská 507, 161 06 Prague Ruzyně, Czech Republic
3
Faculty of Agrobiology, Food and Natural Resources, Czech University of Life Sciences Prague, Kamýcká 129, 165 00 Prague Suchdol, Czech Republic
*
Author to whom correspondence should be addressed.
Agronomy 2024, 14(9), 1918; https://doi.org/10.3390/agronomy14091918
Submission received: 6 August 2024 / Revised: 22 August 2024 / Accepted: 24 August 2024 / Published: 27 August 2024
(This article belongs to the Special Issue Seeds for Future: Conservation and Utilization of Germplasm Resources)
Browse Figures
Versions Notes

Abstract

Low-temperature plasma (LTP) is currently one of the non-invasive and environmentally friendly methods of seed treatment and is massively tested on various types of crops. For the needs of gene banks, the use of LTP technology represents the treatment of seeds before sowing to improve the germination and emergence of long-term stored seed samples. Seeds of four genotypes of wheat, oats, flax, and rapeseed stored in the gene bank for 1, 10, and 20 years were plasma treated for 20, 25, and 30 min. Standard germination parameters (SG3, SG7, GR, MGT, and GI), as well as predictive models, were used to evaluate the effect of plasma treatment on seeds, and the effect on seed metabolism was assessed by superoxide dismutase (SOD) activity. The plasma treatment had different effects on germination and on the enzymatic activity of the tested species, and the result was influenced by both the duration of the treatment and the crop species/genotype. The plasma treatment has a positive effect on germination parameters in flax and rapeseed; in some variants, as in wheat, oats generally reacted negatively. SOD activity was variable in wheat, while higher activity with increasing treatment time was found in other crops. The results of this first study focused on long-term stored seeds and showed the potential of plasma treatment of seeds of plant genetic resources, the possibility of stimulating the germination of stored PGRs, and the need to optimize treatment conditions for individual genotypes.

1. Introduction

The long-term preservation of seeds of genetic resources in the gene bank is an integral part of the protection of plant genetic resources (PGR) ex situ and plays a key role in the protection of the gene pool of cultivated crops [1,2]. Under suitable storage conditions, it is possible to maintain the viability of germplasm for up to tens of years [2]. The problem is that, even if suitable storage conditions are maintained, the viability and germination of the seeds decrease. The guidelines for seed storage then recommend periodic evaluation of the viability of seeds stored in seed banks [3]. However, this is only a check of vitality, not a possible stimulation of germination in less vital seeds.
Various approaches are used to improve seed germination and germination processes: chemical, biological, physiological, and physical. Physiological methods to increase germination include exogenous plant hormones [4] and seed scarification [5]. Chemical seed treatments involve the application of pesticides (fungicides, insecticides, bactericides, nematocides, and rodenticides) to control a range of diseases and pests [6]. Biological and physical methods of seed treatment are described in several studies [7,8,9] where microorganisms (bacteria, fungi) are used for biological seed treatment. However, all these procedures are time- and labor-intensive and, in many cases, lead to chemical residues and environmental pollution [10]. In recent years, various physical methods such as hot water or steam, magnetic field, gamma radiation, laser and electric field, ionizing radiation, ultrasound, light, heat, or vice versa cold [11] or low-temperature plasma—LTP [12] have started to be used for seed treatment and represent an innovative field of research for improving crop yields. These methods are very popular due to the ease of achieving positive biological changes in plants without harming the environment, and many of them are based on the concept of so-called quantum agriculture [13]. Besides them, LTP treatment initiates physiological and biochemical changes that reflect the growth and development processes of plants and ultimately improve yield and production quality [14] and can change indicators of seed vitality such as germination energy, germination, and germination evenness [15].
Seed plasma treatment is divided into two approaches: direct and indirect application, according to the contact of the plasma with the samples [16]. In line with primary treatment, the exposed seeds are directly affected by charged particles, reactive oxygen species, electric fields, and photons in the discharge area. The combination of these components is thought to be a major factor that promotes the germination and growth of plants [17,18]. In alternative treatments, the sample is not exposed to the plasma itself. In this method, a non-equilibrium gas is used, and the samples are still exposed to the long-lived radicals without being exposed to the glowing plasma region [19].
The idea of plasma treatment of seeds of plant genetic resources long-term stored in the Gene Bank is based on the concept of “plasma agriculture” [20], which is a current part of agricultural research trends. In recent years, interest in the use of low-temperature plasma (LTP) has increased, mainly due to its application potential not only in the fields of biology and medicine but also in agriculture and seed production [21]. The beneficial effects of plasma are mainly attributed to its unique mixture of reactive substances, charged particles, an electric field, and ultraviolet radiation, including the thermal component of plasma [22]. In agriculture, LTP is beginning to be used as an effective method of pre-sowing seed treatment with a positive effect on germination [23,24] and with a certain degree of disinfection of the seed surface to remove unwanted microorganisms [25]. Reactive oxygen species (ROS) and reactive nitrogen species (RNS), according to Leti et al. [26], produced by plasma may, however, reduce phytopathogenic microorganisms [27]. ROS can etch the seed coat and thereby positively affect the seed’s absorption of water [28] and nutrients [29]. LTP treatment positively affects the germination index, germination rate, the height of sprouts, root length, as well as the number of roots [30], the activity of enzymes associated with germination [31], photosynthesis rates, stomatal conductivity, and chlorophyll content [32], and chlorophyll and total polyphenol content [33,34]. Dhayal et al. [35] assume that the main cause of the influence of plasma seed treatment on these properties is ‘ion etching.’
Successful germination and development of healthy seedlings are factors playing a crucial role in the reproduction of wild and cultural plant species, population expansion, and rapid recovery from perturbations [36]. Germination is a critical stage in plant development [37], which includes a complex of physiological processes [38], starting with water absorption [39] by a dry, fully matured seed up to embryonic tissue differentiation and axis formation [40] and the perforation of the seed coats by the radicle when seedling development occurs [41]. A variety of chemical compounds and enzymes are associated with the germination process. They are mainly produced by respiratory metabolism and are involved in various types of damage, as well as acting as signal molecules. For example, they are involved in growth elongation, programmed cell death, cell wall rupture, or lignification [42]. During the storage of seeds, the processes associated with respiration are triggered, resulting in the formation of H2O2 or other ROS [43]. Their action can weaken the formation of abscisic acid (ABA), which acts against ROS [44], and thus weaken the dormancy leading to seed aging [45]. During germination, there are reported changes in the activity of superoxide dismutase (SOD) and peroxidase (POD), as well as changes in the content of malonaldehyde (MDA) and soluble protein (SP) in the seeds. These enzymes play a major role in protection against reduced forms of oxygen, create a barrier against stress factors, and play an important role during seed germination and early seedling growth [46].
This study aimed to verify the effect of long-term storage of seeds in the gene bank on their biological quality and the effect of LTP on seed germination parameters. The hypothesis was whether it was possible to use LTP to increase the germination and germination rate of the long-term stored seeds and thus improve the processes of conservation, preservation, and regeneration of plant genetic resources.

2. Materials and Methods

2.1. Genotypes Used in the Study

A set of seeds of selected genotypes of agricultural plants (Table 1) stored in the Gene bank of the Crop Research Institute in Prague, Czech Republic, was used for the experiment. The analyzed samples were stored in the Gene bank for 1 (P1), 10 (P10), and 20 (P20) years at a temperature of −18 °C. Only intact seeds without visible defects or disease germs were used. The seed was divided into control, non-treated variants, and variants treated with LTP. Each sample included 30 seeds with 3 replicates.

2.2. Plasma Treatment

The plasma source was a Plasonic AR-550-M (SurfaceTreat, Turnov, Czech Republic) device generating vacuum low-temperature plasma (LTVP) through a stationary microwave resonator. The process parameters were as follows: microwave discharge pulse duration 60 microseconds, treatment time 20 (T1), 25 (T2), and 30 (T3) minutes, air flow as working gas 50 sccm (standard cubic centimeters), and pressure in the vacuum chamber at the moment of discharge ignition < 50 Pa using the vacuum rotary pump Leybold D16A Trivac (Leybold Vacuum Products Inc., Export, PA, USA). The operating power of the magnetotron was 500 W, frequency 2.45 MHz, and temperature 25 °C. The operating pressure was maintained by simultaneously pumping the vacuum chamber and adding air as working gas using the valve system FV201-Cvh (Bronkhorst High-TechH B.V., Ruurlo, The Netherlands). The working gas flow pushed the active, reactive particles generated in the plasma region toward the treated sample. The treated seeds in glass Petri dishes with a diameter of 9 cm were inserted into the bottom of the vacuum recipient, approximately 15 cm below the plasma entry portal.

2.3. Germination Evaluation

From the control and each variant of plasma treatment, 30 seeds were selected in three repetitions, which were placed in Petri dishes with a diameter of 90 mm. The seeds were covered on both sides with filter paper. The seeds thus covered were moistened with 5 mL of distilled water [47]. The seeds were placed in an air-conditioned chamber, Sanyo Incubator MIR 252 (Sanyo Electric Co., Ltd., Osaka, Japan), and incubated at 20 °C in the dark [3,48]. The number of germinated seeds was recorded every 24 h for 7 days according to the ISTA methodology [3]. The radicle protrusion at 1 mm was recorded as the criterion for germination [48]. Germination parameters—seed germination on the 3rd day (SG3), germination rate (GR), mean germination time (MGT), and germination index (GI)—were calculated according to Aravind et al. [49] in the germination metrics package for R software.

2.4. Determination of Superoxide Dismutase (SOD) Activity

A total of 0.5 g of seed samples were homogenized in 3 mL of 25 mM HEPES buffer (pH 7.8) containing 0.2 mM EDTA and 2% (w/v) polyvinylpyrrolidone. The supernatant was centrifuged for 20 min at 12,000× g, and the resulting supernatant was used for SOD analysis [50]. Absorbance was determined with a Helios Alpha UV–Vis spectrophotometer, and total SOD activity was calculated according to Zhang et al. [51].

2.5. Statistical Analyses

The results were adjusted for statistical evaluation using SW R (version 3.6.3), and statistical analysis was performed using RStudio version 1.2.5019. A one-way analysis of variance (ANOVA) was applied to the data to test whether there was a significant effect of the treatments and periods. The statistically significant differences were verified by a post hoc Tukey HSD test at the level of p < 0.05. Results are expressed as the mean value and the standard deviation of each characteristic. The statistically significant differences are marked with letter indexes in the figures and tables.
To model the time course of an event, in our case, the seed germination of model plant species, we employed the “time-to-event for seed germination” methodology [52], specifically an approach using parametric modeling of the cumulative distribution function (CDF): G t = P T ≤ t .
Here, G(t) corresponds to the proportion of seeds that germinated at time t, or at the time of the control. This approach is also suitable given the nature of the experiment, which inherently contains censored observations, as we do not know the exact moment of germination, or dormant seeds may not germinate at all. This ambiguity is then reflected in the estimation of the error of the regression coefficients.
The selection of a suitable nonlinear regression model was based on the achieved AIC (Akaike Information Criterion) value, with the selection being made from a set of sigmoid regression models suitable for seed germination. e.g., log-logistic model and Weibull’s model.
All numerical estimates of the individual regression parameters in the parametric models were obtained using the maximum likelihood method and numerical optimization using the R 4.3.2 programming environment and the drcte [53] and aomisc [54] libraries. The results are interpreted at a significance level of 0.05. For multiple comparisons, we used Holm’s correction [55].

3. Results

Altogether, three variants of low-temperature vacuum plasma treatment of seed samples of selected crops were tested. A detailed summary of germination parameters and their statistical evaluation is given in Table S1 (Supplementary Data File S1).
In spring wheat (Triticum aestivum cv. ‘Granny’), the effect of all variants of plasma treatment in all storage periods on SG3 is evident (Figure 1a) when germination was significantly slowed down after LTP treatment. The germination rate (Figure 1b) reached comparable values to the control variant and is not statistically different. However, there is a noticeable trend where seed treatment for 25 min (T2) had a positive effect on seed germination and germination rate. The values of the MGT parameter and GI are highly variable compared to the control. The T2 treatment tends to positively influence and increase GI, while the T3 treatment, on the contrary, has a significantly negative effect on GI (Figure 1c,d).
Oat, Avena sativa cv. ‘Ulan’ showed significant and mostly negative effects of plasma treatment on seed germination tests. The negative effect of longer treatment was statistically significant for variants T2 and T3. Similar to wheat, the LPT treatment affected the retardation of seed germination, and this was manifested by lower values of the SG3 parameter in all treated variants and all seed storage periods (Figure 2a). Treatment for 25 and 30 min (T2 and T3) had a strong negative effect on GR (Figure 2b). This fact was reflected in higher MGT values for these treated variants and a very low GI (Figure 2c,d). The significantly negative effect of LTP treatment on oat grains is also evident in the absolute values of SG3, which in the T3 variant reached only 6.67% (P1), 3.33% (P10), and 2.22% in P20 (Table S1).
In the flax Linum usitatissimum cv. ‘N-9/62/K3/B’, LTP seed treatment had a completely different character than it did in analyzed cereals. A significantly positive effect of seed treatment on SG3 was manifested in the short- and long-term stored seeds (P1 and P20). For medium-term stored seeds (P10), this effect was not statistically significant, but it was still visible as a positive trend (Figure 3a). GR was comparable to the control in all cases (Figure 3b). MGT was also positively affected by longer treatment (Figure 3c). The values of GI were then correlated with the previous parameters (Figure 3d), and the overall positive effect of the flax seed treatment can be seen.
Rapeseed Brassica napus f. napus cv. ‘Skrivenskij’ responded to the LTP seed treatment similarly to flax. There was a delay in SG3 for all variants (Figure 4a); however, the overall GR was positively affected (Figure 4b) for seeds stored for a long time (P20). MTG and GI were positively affected by increasing the time of treatment, especially for P20 seeds (Figure 4c,d).
During germination tests, we recorded an influence on the activity of SOD as a result of physical seed treatment, and the results of the evaluation of the activity of SOD show significant differences between individual crop species. In flax, longer treatment times (T2 and T3) led to a decrease in SOD activity (Figure 5c); in oats, this trend was completely opposite, and in these variants, there was a significant increase in enzyme activity (Figure 5b). The treatment effect was highly variable in wheat and rapeseed. In rapeseed, shorter treatment periods (T1 and T2) affected the reduction in enzyme activity; variant T3 increased SOD activity at all storage times. The highest positive effect was at storage times P1 and P10 (Figure 5d). For wheat, the results were the most fluctuating; for P1 and P20 seeds, the treatment times T1 and T2 had an increasing tendency, and the T3 variant led to a decrease in SOD activity. However, in the storage time P10, the greatest activity was achieved by the variant T3 (Figure 5a).
Based on data obtained from germination tests, predictive models were derived for the germination process of the analyzed crops, depending on the treatment variant and seed storage time. Table 2 presents Akaike information criterion (AIC) values for individual model crop species/genotypes and the parametric models used.
Table 2 clearly indicates that parametric models that feature an asymmetric inflection point demonstrated superior convergence and suitability as numerical models for the description of seed germination. Notably, Weibull’s models W1.2 and W1.3, characterized by a nonlinear regression equation, were identified asusefull:
f x = c + d − c 1 − exp − exp b log x − log e
For the W1.2 two-parameter regression model, parameters c and d were fixed as follows: c = 1, d = 0. For the three-parameter model W1.3, the parameter fixation condition was limited only to parameter c, which was fixed at value 1. The estimated values of parameters b (the slope at the inflection point), e (the abscissa of the inflection point), and potentially d (the asymptote) for the models with the lowest AIC are presented in Table S2. The estimates are classified by crop (Triticum, Avena, Linum, and Brassica), seed storage period (P1, P10, and P20), and plasma treatment variant (C, T1, T2, and T3). Graphical representations of these predictive models are shown in Figure 6.
The prediction of germination models clearly shows the effect of plasma treatment on the course of germination of the seeds of the four tested crops. In rapeseed, a positive effect of plasma treatment can be seen in an earlier increase and better seed germination, especially in long-term stored seed variant P20 (Figure 6d). In the case of flax, a slightly delayed increase in the GR of the treated seeds is noticeable. However, GR is then very high, and the curve of the control variant is exceeded (Figure 6c). The situation is different for the two types of tested cereals. In wheat, plasma treatment leads to a delay in germination; GR is lower, but after the end of the test, most variants achieve the same cumulative germination as the control. Oats, as the second representative of cereals, are very sensitive to treatment; the shortest treatment variant stimulated the onset of seed germination, but the germination rate was lower than in control. Longer treatment times (T2 and T3) then had a strongly negative effect; there was a significant delay in germination, and the overall germination of the seeds was very low. Pairwise comparisons of time-to-event curves reveal that, for each crop/genotype examined, there is at least one curve that differs statistically significantly in its parameters:
  • likelihood ratio test for Triticum aestivum = 241.8502; d.f. = 22; p-value = 6.101 < 0.001;
  • likelihood ratio test for Avena sativa = 1075.7515; d.f. = 33; p-value = 1.063 < 0.001;
  • likelihood ratio test for Linum usitatissimum = 577.8142; d.f. = 22; p-value = 3.911 < 0.001
  • likelihood ratio test for Brassica napus f. napus = 423.8978; d.f. = 22; p-value = 4.733 < 0.
The results of pairwise comparisons for parameters b (indicated as a right superscript), d (indicated as left), and e (indicated as a right subscript) are presented in compact letter display notation in Table S2.

4. Discussion

The seed treatment by low-temperature plasma has been tested on different, mainly agriculturally important plant species such as wheat [30], barley [12], rapeseed [23], or on model plants such as goosefoot [56]. Due to the different climatic conditions in Europe, the potential for breeding and developing resistant varieties lies in particular in the regional indigenous crop varieties that possess traits such as drought, disease, and pest resistance [57]. For these materials, it is crucial to ensure their germination and thus enable the regeneration of valuable materials stored in the Gene Bank [58]. The application of low-temperature plasma and its effect on seed samples stored for a long time in Gene Bank conditions have not yet been tested, and this study was focused on this issue.
The results of evaluating the effect of plasma discharge in different technical/technological layouts may give different results. In this study, the Plasonic vacuum plasma generator was selected to evaluate the effect of plasma discharge, which is more suitable for application to small-seeded and oilseed plant species. Other methods and technological approaches, such as DBD plasma (dielectric barrier discharge plasma) [59,60] and gliding Arc [18,61], work with a carrier gas stream applied directly to plant seeds. When used, seed samples may be defragmented and mixed, and the use of these devices was not appropriate for the species tested in this study.
The effect (positive and negative) of low-temperature vacuum plasma treatment on seed germination and young plant development of all species tested was demonstrated. These results corresponded with the findings of Monica et al. [62] in Foxtail millet (Setaria italica L.), where seed germination was accelerated after plasma treatment. In several other studies [63,64], a positive effect of plasma seed treatment was found, and there is a shortening of the time of germination and emergence, as reported by Priatama et al. [24] and Song et al. [65].
It is also evident that the degree of influence of the plasma treatment manifests itself differently depending on the length of the treatment, the age of the seeds, and the length of storage time in the gene bank. The positive effect of plasma treatment was recorded in this study in flax. Also, for rapeseed and wheat, the overall GR is increased, but the SG3 is lower. However, a very negative effect was observed in oats. A positive effect on germination was reported by Perea-Brenes et al. [66], who observed a positive effect of plasma discharge of DBD 72 h after treatment, with 75% of seeds germinating compared to the control (60%). In several previous studies, variable responses to seed plasma treatment in different crops and genotypes/varieties have been described [67,68]. This phenomenon may be due to an interaction between genotype and treatment type, as also reported by Bozhanova et al. [67]. Similarly, Jezek et al. [25] reported different responses of winter and spring wheat varieties to plasma treatment. These differences were probably due to different amounts of flavonoids in the seed. These compounds protect the plant from oxidative stress and help to reduce the damaging effects of free radicals [45]. Higher germination rates have been described by Perea-Brenes et al. [66] for seeds and seedlings exposed to low temperatures (5 °C). Plasma-treated seeds and, subsequently, plants showed higher GR and better growth in young plants. However, the conditions of this experiment were standardized for use by the gene banks according to the ISTA methodology [3] and Li et al. [48], and therefore, the temperature was uniform (20 °C) for all experimental treatments.
A whole range of parameters is used to assess the seed value. Bozhanova et al. [67] evaluated the effect of plasma treatment on the germination of seeds in three cultivars of durum wheat (Triticum durum L.). They found that germination after three days was similar in two varieties (94%), and only one variety showed a significant decrease in germination. In the wheat cultivar ‘Granny,’ the oat cultivar ‘Ulan,’ and the rapeseed cultivar ‘Skrivenskii,’ longer treatment time affected slowing down germination and reducing SG3 values, similar to the study [67]. The opposite reaction was recorded in the GR parameter, where plasma-treated variants showed higher values. The initial retardation of the development of treated variants of flax and rapeseed, with a lower value for SG3, was fully compensated, and the GR reached higher values than the untreated control. Also, Šerá et al. [69] described a similar response in hemp seeds (Cannabis sativa L.), where on the fifth day after sowing, significantly lower germination of treated seed samples was recorded than untreated controls. Similarly, Tong et al. [70] and Li et al. [48] presented a significant increase in GI values in rapeseed. On the other hand, the oat variety ‘Ulan’ responded significantly differently. There was a rapid decrease in GI values with increasing length of plasma treatment, and the decrease in GI values also reflected a significant reduction in GR. Other studies devoted to oats also did not yield clear results. Šerá et al. [71] reported that after plasma treatment, there was a slight reduction in germination. In wheat, GI values are variable and inconsistent, similar to the study by Bozhanova et al. [67]. The T2 treatment variant significantly stimulated the increase in GI; however, this variant resulted in prolonged MGT and reduced overall germination. The decrease in germination rate with increasing treatment time was also reported by Roy et al. [47]. Based on the evaluation of the germination parameters, it is clear that the plasma treatment has a positive effect on flax and rapeseed. In some variants, a positive effect is also observed in wheat and oats; short treatment times do not differ from the control, and longer treatment times have a significantly negative effect on germination and seed vigor. Due to the different behavior of individual crops or varieties, optimizing the time and intensity of plasma treatment for each crop type and genotype seems to be a key issue.
The influence of plasma treatment on the germination of long-term stored seeds was investigated using time-to-event analysis. This approach was recently developed by Onofri [52] for evaluating seed germination and seed quality parameters. The germination process was modeled using two- and three-parameter nonlinear regression models. The graphical representation of these models supports the results obtained from standard seed quality parameters. Our results demonstrate that plasma treatment significantly alters the germination curves, specifically shifting the inflection point and modifying the slope at this point. These findings are in agreement with the previous studies of Bozhanova et al. [67] and Perea-Brenes et al. [66], indicating a positive effect of plasma treatment, especially for crops with small oilseeds such as flax and rapeseed.
In addition to the standard parameters used in the evaluation of seed quality/value, the effect of plasma treatment on the activity of enzymes associated with germination processes was investigated. Qu et al. [46] reported superoxide dismutase (SOD) as a key enzyme involved in germination processes. The evaluation of SOD activity is often reported from the roots and sprouts of plasma-treated seeds [72]. Plasma can affect SOD activity both positively and negatively, depending on the time of seed treatment, as shown by the results of this study. The control variant of oat cv. ‘Ulan’ had the lowest SOD activity in all periods, while with increasing treatment time, SOD activity increased and reached the highest values in the T3 variant. An extreme increase in SOD activity was observed for the combination of the T3 treatment variant and P20 storage time. This variant also showed the lowest values of germination rate and total germination and was strongly negatively affected by plasma treatment. A similar result of the increase in SOD activity with longer plasma treatment was observed in peas [72], maize [73], and papaya seedlings [74]. In the wheat ‘Granny,’ higher variability of SOD activity was found within the treatment variant as well as within the storage period. In the T2 variant and the P1 and P3 periods, the highest activity was found, and a decrease in SOD activity occurred in the T3 variant. Similarly, Hossain et al. [75] found that there was an increase in SOD activity in maize seedlings with an increasing plasma treatment period (1-3 min). On the contrary, when plasma was applied for 4 min, there was a conclusive decrease in SOD activity, as in this study. In rapeseed, the trend of changes in SOD activity was similar to that of oats, with an increase in SOD activity with increasing treatment time in all seed storage periods. However, in contrast to oats, there was no deterioration in germination parameters. The opposite trend was observed for flax, where for storage periods P1 and P20, longer treatment times (T2 and T3) led to a decrease in SOD activity. Valderrama et al. [76] reported that SOD activities increased in environments with higher ROS/RNS abundance. The changes in SOD activity are explained by the different intensities of the diffusion of reactive oxygen species through the biomembranes of cells and their subsequent effect on the activity of SOD or other enzymes such as catalase or ascorbate peroxidase [20]. SOD can degrade oxygen radicals and can therefore be referred to as an enzyme enabling plants to adapt to environmental stress [77]. It is evident that plasma treatments do not have the same effect on SOD activity in the tested crops, and this variability may be due to the different anatomical/morphological characteristics of the seeds and their chemical composition. The results of this experiment showed that there was a shift in SOD activity with an increasing storage period compared to the control, depending on the treatment period. Based on the findings of Leprince et al. [78], Bowler et al. [77], or Wojtyla et al. [79] and the results of this experiment, it would be useful to focus on the determination of SOD activity in relation to other enzymes and different types of metabolism concerning the length of seed storage in the gene banks and the length of plasma treatment.

5. Conclusions

Plasma treatment of seeds is a subject of intensive research and finds practical applications in seed production. However, the effects of plasma treatment on long-term stored seeds of valuable plant genetic resources remain unexplored. This study represents the first attempt to evaluate the impact of plasma treatment on the seeds of crops stored for long-term periods in a gene bank. Four different crops, varying in seed size and anatomical structure, were tested. The results indicated diverse responses among individual crops, ranging from positive to negative, and revealed a significant dependence on treatment conditions, such as plasma exposure duration and seed storage time. Positive responses to plasma seed treatment were observed in flax and rapeseed, characterized by improved germination parameters. However, these crops exhibited distinct behaviors in terms of the SOD enzyme, another biomarker. The two cereals examined displayed contrasting outcomes: wheat generally responded positively, while oats exhibited a pronounced negative response to plasma treatment. Utilizing the novel “time-to-event for seed germination” methodology, the effects of plasma treatment on long-term stored seeds were assessed, and the germination process was modeled using appropriate nonlinear regression models. The findings indicate that plasma treatment significantly alters the germination course, notably shifting the inflection point and modifying the curve’s slope at this point. The study results highlight the potential of plasma treatment for enhancing the germination of plant genetic resources, stimulating stored PGRs, and the necessity of optimizing treatment conditions for individual genotypes.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/agronomy14091918/s1, Table S1: (summary of germination tests for all used genotypes and variants). Statistical evaluation using the HSD Tukey test for p < 0.05) and Table S2: (the estimated values of parameters b (the slope at the inflection point), e (the abscissa of the inflection point), and potentially d (asymptote) for the models with the lowest AIC for individual tested crops/genotypes, period of seed storage, and plasma treatment variant). Table S3: Calculation of germination parameters.

Author Contributions

Conceptualization, V.Č., F.H. and P.H.Č.; methodology, M.M. and E.J.; validation, M.M. and P.H.Č.; formal analysis, P.H.Č.; investigation, M.M., E.J. and Z.K.; resources, M.M., E.J. and Z.K.; data curation, M.M. and M.R.; writing—original draft preparation, V.Č.; writing—review and editing, F.H., M.M. and P.H.Č.; visualization, M.M.; supervision, V.Č.; project administration, V.Č.; funding acquisition, V.Č. and P.H.Č. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the University of South Bohemia, grant number GAJU 080/2022/Z, by the Ministry of Agriculture of the Czech Republic (No. RO0423), and by the S project of the Ministry of Education, Youth, and Sports of the Czech Republic.

Data Availability Statement

The data presented in this study are available in Supplementary Tables S1–S3, further inquiries can be directed to the corresponding author/s.

Acknowledgments

We gratefully acknowledge the National Programme for the Conservation and Use of Plant Genetic Resources and Agrobiodiversity (no. MZE-62216/2022-13113) for providing plant material.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Effect of low-temperature vacuum plasma seed treatment on germination parameters in Triticum aestivum cv. ‘Granny’: (a) SG3—seed germination on the third day; (b) GR—germination rate; (c) MGT—mean germination time; (d) GI—germination index. P1, P10, and P20 represent the seed storage times. Letters indicate the statistical significance of the HSD Tukey test at the significance level of p < 0.05.
Figure 1. Effect of low-temperature vacuum plasma seed treatment on germination parameters in Triticum aestivum cv. ‘Granny’: (a) SG3—seed germination on the third day; (b) GR—germination rate; (c) MGT—mean germination time; (d) GI—germination index. P1, P10, and P20 represent the seed storage times. Letters indicate the statistical significance of the HSD Tukey test at the significance level of p < 0.05.
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Figure 2. Effect of low-temperature vacuum plasma seed treatment on germination parameters in Avena sativa cv. ‘Ulan’: (a) SG3—seed germination on the third day; (b) GR—germination rate; (c) MGT—mean germination time; (d) GI—germination index. P1, P10, and P20 represent the seed storage times. Letters indicate the statistical significance of the HSD Tukey test at the significance level of p < 0.05.
Figure 2. Effect of low-temperature vacuum plasma seed treatment on germination parameters in Avena sativa cv. ‘Ulan’: (a) SG3—seed germination on the third day; (b) GR—germination rate; (c) MGT—mean germination time; (d) GI—germination index. P1, P10, and P20 represent the seed storage times. Letters indicate the statistical significance of the HSD Tukey test at the significance level of p < 0.05.
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Figure 3. Effect of low-temperature vacuum plasma seed treatment on germination parameters in Linum usitatissimum cv. ‘N-9/62/K3/B’: (a) SG3—seed germination on the third day; (b) GR—germination rate; (c) MGT—mean germination time; (d) GI—germination index. P1, P10, and P20 represent the seed storage times. Letters indicate the statistical significance of the HSD Tukey test at the significance level of p < 0.05.
Figure 3. Effect of low-temperature vacuum plasma seed treatment on germination parameters in Linum usitatissimum cv. ‘N-9/62/K3/B’: (a) SG3—seed germination on the third day; (b) GR—germination rate; (c) MGT—mean germination time; (d) GI—germination index. P1, P10, and P20 represent the seed storage times. Letters indicate the statistical significance of the HSD Tukey test at the significance level of p < 0.05.
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Figure 4. Effect of low-temperature vacuum plasma seed treatment on germination parameters in Brassica napus f. napus cv. ‘Skrivenskij’: (a) SG3—seed germination on the third day; (b) GR—germination rate; (c) MGT—mean germination time; (d) GI—germination index. P1, P10, and P20 represent the seed storage times. Letters indicate the statistical significance of the HSD Tukey test at the significance level of p < 0.05.
Figure 4. Effect of low-temperature vacuum plasma seed treatment on germination parameters in Brassica napus f. napus cv. ‘Skrivenskij’: (a) SG3—seed germination on the third day; (b) GR—germination rate; (c) MGT—mean germination time; (d) GI—germination index. P1, P10, and P20 represent the seed storage times. Letters indicate the statistical significance of the HSD Tukey test at the significance level of p < 0.05.
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Figure 5. Effect of low-temperature vacuum plasma seed treatment on SOD activity (U/g DW) in Triticum aestivum cv. Granny (a), Avena sativa cv. Ulan (b), Linum usitatissimum cv. N-9/62/K3/B (c), and Brassica napus f. napus cv. Skrivenskij (d). P1, P10, and P20 represent the seed storage times. Letters indicate the statistical significance of the HSD Tukey test at the significance level of p < 0.05.
Figure 5. Effect of low-temperature vacuum plasma seed treatment on SOD activity (U/g DW) in Triticum aestivum cv. Granny (a), Avena sativa cv. Ulan (b), Linum usitatissimum cv. N-9/62/K3/B (c), and Brassica napus f. napus cv. Skrivenskij (d). P1, P10, and P20 represent the seed storage times. Letters indicate the statistical significance of the HSD Tukey test at the significance level of p < 0.05.
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Figure 6. The course of germination, graphical presentations of Weibull’s models for individual tested crops: (a) wheat, (b) oat, (c) flax, and (d) rapeseed. P1, P10, and P20 correspond to the period of seed storage.
Figure 6. The course of germination, graphical presentations of Weibull’s models for individual tested crops: (a) wheat, (b) oat, (c) flax, and (d) rapeseed. P1, P10, and P20 correspond to the period of seed storage.
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Table 1. Characteristics of genotypes used in experiments.
Table 1. Characteristics of genotypes used in experiments.
Genotype NumberECNPlant SpeciesCultivar
TA_101C0100139Triticum aestivumGranny
AS_203C0700959Avena sativaUlan
LU_305X1100390Linum usitatissimumN-9/62/K3/B
BN_415O0100097Brassica napus f. napusSkrivenskij
ECN—registration national code of the gene bank accession.
Table 2. Overview of AIC values for tested model crops and the parametric models.
Table 2. Overview of AIC values for tested model crops and the parametric models.
ModelAIC Values for Analyzed Genotypes
Triticum aestivumAvena sativaLinum usitatissimumBrassica napus f. napus
GrannyUlanN-9/62/K3/BSkrivenskij
LL.2775.4792Convergence failed2615.2982903.903
LL.3Convergence failed2306.946Convergence failedConvergence failed
LL.4Convergence failedConvergence failedConvergence failedConvergence failed
LN.2779.0403Convergence failed2627.5862945.571
LN.3Convergence failed2316.164Convergence failedConvergence failed
W1.2734.5158Convergence failed2468.9592818.281
W1.3Convergence failed2266.246Convergence failedConvergence failed
W2.2Convergence failed2679.1612884.3223108.13
W2.3Convergence failed2387.964Convergence failedConvergence failed
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MDPI and ACS Style

Matějovič, M.; Jozová, E.; Rost, M.; Čurn, V.; Hnilička, F.; Kotíková, Z.; Hlásná Čepková, P. Evaluation of the Effect of Low-Temperature Plasma Treatment on Seed Germination of Long-Term Stored Genetic Resources. Agronomy 2024, 14, 1918. https://doi.org/10.3390/agronomy14091918

AMA Style

Matějovič M, Jozová E, Rost M, Čurn V, Hnilička F, Kotíková Z, Hlásná Čepková P. Evaluation of the Effect of Low-Temperature Plasma Treatment on Seed Germination of Long-Term Stored Genetic Resources. Agronomy. 2024; 14(9):1918. https://doi.org/10.3390/agronomy14091918

Chicago/Turabian Style

Matějovič, Martin, Eva Jozová, Michael Rost, Vladislav Čurn, František Hnilička, Zora Kotíková, and Petra Hlásná Čepková. 2024. "Evaluation of the Effect of Low-Temperature Plasma Treatment on Seed Germination of Long-Term Stored Genetic Resources" Agronomy 14, no. 9: 1918. https://doi.org/10.3390/agronomy14091918

APA Style

Matějovič, M., Jozová, E., Rost, M., Čurn, V., Hnilička, F., Kotíková, Z., & Hlásná Čepková, P. (2024). Evaluation of the Effect of Low-Temperature Plasma Treatment on Seed Germination of Long-Term Stored Genetic Resources. Agronomy, 14(9), 1918. https://doi.org/10.3390/agronomy14091918

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