Open AccessArticle

Seed Dressing Containing Gibberellic Acid, Indole-3-Acetic Acid, and Brassinolide Improves Maize Seed Germination and Seedling Growth Under Cold Stress

Jingjing Cui

^1,†,

Liqiang Zhang

^2,†

Qianqian Li

¹,

Yuan Qi

²,

Jiajun Ma

²,

Danyang Guo

¹,

Pengyu Zhang

²,

Yujie Xu

¹,

Yan Gu

^1,* and

Hongyu Wang

^2,*

College of Agriculture, Jilin Agricultural University, Changchun 131008, China

College of Plant Science, Jilin University, Changchun 130012, China

Authors to whom correspondence should be addressed.

^†

These authors contributed equally to this work.

Agronomy 2024, 14(12), 2933; https://doi.org/10.3390/agronomy14122933

Submission received: 24 October 2024 / Revised: 5 December 2024 / Accepted: 7 December 2024 / Published: 9 December 2024

(This article belongs to the Section Plant-Crop Biology and Biochemistry)

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Figure 1
Maize was grown in plastic containers in a climate chamber. (a) Aerial view of the container; (b,c) side view of the container in a climate chamber. "> Figure 2
Effects of GA-IAA-BL WP on the germination rate at different temperatures. The bars represent the mean ± SE, n = 50 replicates. The A, B, and C lettering indicates differences between temperatures under the same treatment (p < 0.05). Lowercase letters (a and b) indicate significant differences between GA-IAA-BL WP treatments at the same temperature (p < 0.05). "> Figure 3
Effect of GA-IAA-BL WP on maize seedling growth at different temperatures. "> Figure 4
Effect of GA-IAA-BL WP on maize seedling shoot (a) and root (b) growth at different temperatures. The bars represent the mean ± SE, n = 50 replicates. The A, B, and C lettering indicates differences between temperatures under the same treatment (p < 0.05). Lowercase letters (a, b, c, and d) indicate significant differences between GA-IAA-BL WP treatments at the same temperature (p < 0.05). "> Figure 5
Effect of temperature and GA-IAA-BL WP seed dressing on the root–shoot ratio of maize seedlings. The bars represent the mean ± SE, n = 50 replicates. The A, B, and C lettering indicates differences between temperatures under the same treatment (p < 0.05). Lowercase letters (a, b, and c) indicate differences between GA-IAA-BL WP treatments at the same temperature (p < 0.05). "> Figure 6
Effect of temperature and GA-IAA-BL WP seed dressing on dry and fresh weights of maize seedling shoots (a,c,e,g,i,k) and roots (b,d,f,h,j,l). The bars represent the mean ± SE, n = 50 replicates. Lowercase letters (a, b, c, and d) indicate differences between GA-IAA-BL WP treatments at the same temperature (p < 0.05). "> Figure 7
Effect of temperature and GA-IAA-BL WP on enzymes. Superoxide dismutase (SOD) (a–c), catalase (CAT) (d–f), and peroxidase (POD) (g–i) activity in maize seedling shoots and roots. The bars represent the mean ± SE, n = 50 replicates. Lowercase letters (a, b, c, and d) indicate differences between GA-IAA-BL WP treatments at the same temperature (p < 0.05). A0–A4 indicate the GA-IAA-BL WP concentration: 0, 50, 100, 150, and 200 mg mL−1, respectively. "> Figure 8
Effect of temperature and GA-IAA-BL WP on proline (Pro) (a–c) and malondialdehyde (MDA) (d–f) in maize seedling shoots and roots. The bars represent the mean ± SE, n = 50 replicates. Lowercase letters (a, b, c, and d) indicate differences between GA-IAA-BL WP treatments at the same temperature (p < 0.05). A0–A4 indicate the GA-IAA-BL WP concentration: 0, 50, 100, 150, and 200 mg mL−1, respectively. "> Figure 9
Effect of temperature and GA-IAA-BL WP on root soluble sugar concentration (a), root soluble protein concentration (b), and root vigor (TTC) (c) of maize seedlings. The bars represent the mean ± SE, n = 50 replicates. The A, B, and C lettering indicates differences between temperatures under the same treatment (p < 0.05). Lowercase letters (a, b, c, and d) indicate differences between GA-IAA-BL WP treatments at the same temperature (p < 0.05). "> Figure 10
Structural equation modeling (SEM) of the effect of GA-IAA-BL WP and temperature on maize seed germination and seedling growth. Blue arrows indicate negative correlations, and red arrows indicate positive correlations between variables (* p < 0.05). The black dotted line indicates no significant correlation (p > 0.05). A1–A4 indicate the GA-IAA-BL WP concentration: 50, 100, 150, and 200 mg mL−1, respectively. Organic matter accumulation includes the dry and fresh weights of maize seedling shoots and roots. Antioxidant enzyme activity includes catalase, superoxide dismutase, and peroxidase. ">

Versions Notes

Abstract

Chemical products, such as seed dressings, are often used to regulate crop growth and development and improve yields. In this study, we investigated a seed dressing containing 0.136% gibberellic acid (GA), indole-3-acetic acid (IAA)-, and brassinolide (BL) as a wettable powder (WP), hereafter referred to as GA-IAA-BL WP. This product is a new plant growth regulator of plant origin that can improve crop stress resistance and yield. However, its effect on maize seed germination and seedling growth under low-temperature stress is unclear. In this study, GA-IAA-BL WP was applied to maize ‘Liukexing 99’ seeds at 50, 100, 150, or 200 mg mL⁻¹, and seeds were germinated in an artificial climatic chamber at 10, 15, or 25 °C for 14 d. Application at 100 mg mL⁻¹ significantly increased the germination rate as well as seedling shoot and root length and dry and fresh weight at all three temperatures. This application rate also increased the contents of proline, malondialdehyde, soluble sugars, and soluble proteins; the activities of catalase, superoxide dismutase, and peroxidase; and root vigor. Our results demonstrate that GA-IAA-BL WP can reduce the negative impacts of low-temperature stress on seed germination and seedling growth.

Keywords:

root vigor; temperature; 0.136% gibberellic acid; indole-3-acetic acid; brassinolide wettable powder; maize yield; growth promoting

1. Introduction

Seed germination is a complex process that begins with water absorption and expansion, progresses through embryonic growth and seed coat rupture, and culminates in the embryonic root breaking through the seed coat, which marks the successful germination of the seed [1]. This process involves a series of physiological and biochemical changes, gene expression, protein biosynthesis, and post-translational modifications [2]. Seed germination is jointly regulated by endogenous factors, such as phytohormones and endosperm decay, and external environmental factors, such as light, temperature, water, and oxygen [3]. Temperature is particularly important in determining seed germination. Most crop seeds germinate at 15–30 °C. Temperatures outside the appropriate range are not conducive to normal water absorption and physiological metabolism and impede seed germination [4]. Low temperatures significantly inhibit seed germination, reduce seedling quality, and ultimately cause serious yield losses [5]. Seeds undergo a series of physiological and metabolic changes under low-temperature stress, including changes in the activities of antioxidant enzymes (catalase (CAT), superoxide dismutase (SOD), peroxidase (POD), etc.) and the contents of non-enzymatic antioxidant substances (ascorbic acid, glutathione, flavonoids), osmotically regulated substances, endogenous phytohormones, and other metabolites [6]. CAT, as a key enzyme in the plant stress response, targets toxic substances, such as reactive oxygen species and phenolic compounds, which in turn affect the growth and development of the plant [7]. SOD defends against damage to the cell membrane system by reactive oxygen species, is important for plant stress responses, and prevents organ senescence [8]. POD activity can also reduce plant senescence [9]. Proline (Pro) aids in regulating cellular permeability and maintaining the structural and functional stability of proteins. The content of Pro can serve as a criterion for assessing stress tolerance [10]. Studies have shown that low-temperature treatment leads to an increase in the Pro content in maize seedlings. The longer the duration of low-temperature stress, the higher the Pro content, thereby alleviating the damage caused by low-temperature stress to maize [11]. Malondialdehyde (MDA) is an important indicator of lipid peroxidation in cell membranes [12]. Low levels of MDA can result in damage to cell membranes, decreasing the content of unsaturated fatty acids in the membrane and reducing membrane fluid [13].

Seed germination is particularly vulnerable to low temperatures [14]. Low temperatures slow down the water absorption rate of seeds, resulting in delayed germination. This exacerbates the adverse effects of other biotic and abiotic factors in the soil on germination, leading to a decline in germination and seedling emergence, affecting the later growth and development of crops, and ultimately reducing crop yields [15]. Rice and maize often suffer from low-temperature stress if they are sown in early spring, and the phenomenon of a lack of trees is broken [16,17]. Wheat and Brassica napus grown in autumn and winter can face low-temperature stress, which can inhibit seed germination, especially due to the rice–oil stubble contradiction intensification. Oilseed rape that is grown late in the season is more likely to suffer from low-temperature stress and seed germination failure, resulting in a large area of arable land in the winter [18,19]. In addition, the inhibition of seed germination at low temperatures limits the geographical distribution of crops, making it difficult to grow crops in the alpine zone [20]. Therefore, improving seed germination under low temperatures will help increase agricultural production.

The Northeast China maize belt starts from the southern part of Heilongjiang Province, includes Jilin Province and the eastern part of the Inner Mongolia Autonomous Region, and extends to the northern part of Liaoning Province. It is known as one of the world’s three ‘Golden Maize Belts’ along with the U.S. and Ukrainian maize belts at the same latitude [21]. Maize is currently used as food, feed, and industrial ethanol, and other uses are being explored. Furthermore, maize is the highest-yielding staple crop [22]. In Jilin Province, there is a large difference between the day and night temperatures in winter; the winter is long and cold [23], and there are high levels of rainfall and snowfall [24]. These conditions have a great impact on the field production of maize. Low temperatures are also persistent in spring [25]. Inversion tillage is common and, because the soil is cold, this can cause low-temperature stress [26]. In autumn, a large area of land is tilled, and more maize is planted in low-lying land. However, in spring, machinery cannot be directly operated [27], which can result in delayed sowing and, therefore, a failure of maize to mature. If farmers sow earlier, while the soil water content is high, this results in lower seedling phosphorus supply [28]. The above factors lead to lower planting densities, weak seedlings, fertility delay, and other issues, which have a great impact on the final maize yields [29].

Maize is a food crop, and human populations rely on high maize yields. Planting density directly affects the yield of maize [30]. Seed germination is influenced by environmental and intrinsic conditions [31]. Under normal temperature conditions (25 °C), maize seeds start germinating on the second day after soaking [32]. The time required for germination increases with decreasing temperature, with a minimum temperature of 10 °C for germination [33]. If the temperature drops below 10 °C, cells and tissues will suffer irreversible damage [34]. With global climate anomalies, cold weather has become more elusive, and cold spells last longer in late spring, which can have a significant inhibitory effect on seed germination and plant growth [35]. In summary, low-temperature conditions affect plant respiration, water uptake, enzyme activity, organic matter conversion, and phytohormone content, thereby limiting plant growth and yield.

Current research has focused on improving the low-temperature stress resistance of plants and clarifying the molecular mechanisms involved in this resistance [36,37]. Recent studies have shown that the application of growth-regulating substances, such as jasmonic acid [38], melatonin, and salicylic acid [39], can effectively alleviate abiotic stress in plants. Under normal conditions, seed germination is mainly regulated by the antagonism of gibberellic acid (GA) and abscisic acid (ABA). In addition to GA and ABA, a variety of hormones including ethylene (ETH) [40], auxins, such as indole-3-acetic acid (IAA) [41], and brassinosteroids (BRs) [42] also affect seed germination under low-temperature conditions.

A plant growth regulator containing GA, IAA, and the BR brassinolide (BL) at 0.136% in a wettable powder (WP), hereafter referred to as GA-IAA-BL WP [43], has recently been produced. However, there are few reports on the effects of this product as a seed dressing on maize seed germination and seedling growth under low-temperature stress [44]. GA-IAA-BL WP was applied to seeds at different concentrations, and seeds were incubated at different temperatures for 14 d. The objectives of this study were to (1) attempt to reveal the response mechanism of maize seed germination and seedling growth to GA-IAA-BL WP under low-temperature stress; (2) determine the germination, seedling shoot and root growth, and physiological and biochemical indexes; and (3) determine the optimal concentration of GA-IAA-BL WP under low temperature stress. The results of this study provide a theoretical reference for the comprehensive understanding of GA-IAA-BL WP in agricultural production.

2. Materials and Methods

2.1. Chemicals and Maize Seeds

GA-IAA-BL WP was purchased from Beijing Chenghe Jiaxin Agricultural Trading Co., Ltd. (Beijing, China), and maize ‘Liukexing 99’ seeds were purchased from Jilin Yuntianhua Seed Industry Development Co., Ltd. (Changchun, China).

2.2. Seed Dressing Treatments

The total concentration of GA, IAA, and BL in the powder was 0.136%, and the concentrations of the specific compounds were 0.00031%, 0.00052%, and 0.135%, respectively. Maize seeds were mixed with deionized water (A0), or a solution containing GA-IAA-BL WP at 50 (A1), 100 (A2), 150 (A3), or 200 mg mL⁻¹ (A4). The seeds were dried naturally after mixing.

2.3. Maize Culture

After seed dressing was applied, the seeds were placed in a plastic container with sterilized quartz sand in an artificial climate chamber at either 10, 15, or 25 °C and 60% humidity. There were three replicates of 50 seeds per treatment (Figure 1). Samples were taken at 14 d of treatment, at which time the seedlings had grown to the three-leaf stage at 25 °C. The quartz sand served as a delimiter, with the biomass above the quartz sand representing the aboveground biomass and the biomass below representing the belowground biomass. The root–shoot ratio was calculated as the ratio of the fresh belowground biomass to the fresh aboveground biomass. The number of germinated seeds at 14 d was used to calculate the germination rate. The surface of the maize seedlings was dried with absorbent paper before measuring the fresh weight. The samples were placed in an oven at 105 °C for 30 min and then adjusted to 80 °C for drying to a constant weight before the dry weight was measured. The fresh roots and leaves of maize seedlings were collected and frozen for 5 min in liquid nitrogen and stored at −80 °C for subsequent analysis of enzyme activities; proline (Pro), malondialdehyde (MDA), soluble protein, and soluble sugar contents; and root vigor.

2.4. Determination of Physiological Parameters

MDA accumulation was determined using a commercial MDA assay kit (Solarbio, Beijing, China) following Fan et al. (2014) [45]. Maize leaves or roots (0.1 g) were ground and blended with 10% (v/v) trichloroacetic acid. After centrifuging for 20 min at 12,000× g, an aliquot of the supernatant was mixed with an equal amount of thiobarbituric acid and incubated at 95 °C for 40 min. The homogenate was centrifuged for 15 min at 10,000× g after quickly cooling on ice. The absorbances of the supernatant were detected at 600, 532, and 450 nm, and the final results were calculated according to the protocol of the commercial assay kit (Solarbio, Beijing, China).

For the detection of the Pro content, a reported protocol was used [46]. About 100 mg of maize roots or leaves were ground and blended with sulfosalicylic acid (3%; v/v), and the mixture was centrifuged for 20 min at 12,000× g. The supernatant was then blended and vortexed with the same amount of acidic ninhydrin and glacial acetic acid and then incubated for 90 min at 100 °C. The mixture was blended with toluene to separate the samples from the aqueous phase after fast cooling on ice. The absorbance of the supernatant was detected at 520 nm, and a standard curve was used to calculate the Pro content.

The activities of major antioxidant enzymes, SOD [47], CAT [48], and POD [49], and root vigor [50] were measured using commercial assay kits (Solarbio, Beijing, China), as previously reported. The activities of the antioxidant enzymes were standardized according to the descriptions published by Dai et al. (2021) [51].

The soluble sugar content was determined using anthrone colorimetry [52], and the soluble protein content was determined using the Coomassie Brilliant Blue G-250 method [53].

2.5. Statistical Analysis

Two-way ANOVA was used to compare the effects of different concentrations and temperatures on maize seed germination and seedling growth. After evaluating the significant differences between the sample means via one-way ANOVA, Duncan’s test, which is a post hoc test, was used to determine which specific group means were significantly different from each other. ANOVA and Duncan’s test were performed in SPSS 22.0 (Armonk, NY, USA: IBM Corp). Structural equation modeling (SEM) of the effects of different concentrations and temperatures on maize seed germination and seedling growth was implemented using the ‘Lavaan’ package in R v4.3.1.

3. Results

3.1. Germination Rate, Seedling Shoot, and Root Length

All GA-IAA-BL WP concentrations increased the germination rate of maize seeds compared with no GA-IAA-BL WP (Figure 2). At 10, 15, and 25 °C, compared to 0 mg mL⁻¹, the germination rate increased by an average of 18.85%, 11.63%, and 4.31%, respectively. Additionally, under all three temperature conditions, the highest germination rate was observed at 100 mg mL⁻¹, with the most significant increase at 10 °C, where it was an average of 30.09% higher than in other treatments.

The shoot and root lengths of maize seedlings were significantly reduced at 10 and 15 °C (Figure 3 and Figure 4); however, different concentrations of GA-IAA-BL WP could increase seedling shoot and root length.

Under the three temperature conditions (10, 15, and 20 °C), the shoot length and root length with the GA-IAA-BL WP treatment (50, 100, 150, 200 mg mL⁻¹) were higher than those with the control treatment (0 mg mL⁻¹). The 100 mg mL⁻¹ concentration had the most significant effect on shoot length and root length (Figure 4a,b). Compared with the control group, the shoot and root length increased by 64.56% and 52.23%, respectively, at 10 °C; by 220.40% and 27.76%, respectively, at 15 °C; and by 19.15% and 91.97%, respectively, at 25 °C. The 50 and 150 mg mL⁻¹ treatments resulted in greater shoot and root lengths than the 200 mg mL⁻¹ treatment.

3.2. Root–Shoot Ratio

The root–shoot ratio increased with decreasing temperatures; however, GA-IAA-BL WP treatment reduced the root–shoot ratio. The root–shoot ratio first decreased and then increased with increasing GA-IAA-BL WP concentration at the same temperature (Figure 5), indicating that GA-IAA-BL WP has a positive effect if applied at the appropriate concentration but a toxic effect if applied at a higher concentration. Specifically, GA-IAA-BL WP at 100 mg mL⁻¹ at 10, 15, and 25 °C significantly reduced the root–shoot ratio by 25.00%, 12.35%, and 33.05%, respectively, compared with the control.

3.3. Maize Seedling Shoot and Root Dry and Fresh Weights

Maize seedling shoot fresh weight (Figure 6a,e,i), shoot dry weight (Figure 6b,f,j), root fresh weight (Figure 6c,g,k), and root dry weight (Figure 6d,h,l) decreased gradually with decreasing temperatures. However, GA-IAA-BL WP treatment generally increased shoot and root weights compared to the control seeds, with varying degrees of increase. The seedling shoot and root weights first increased and then decreased with increasing GA-IAA-BL WP concentration. Specifically, the 100 mg mL⁻¹ treatment was the most effective, resulting in an increase in seedling shoot fresh weight, shoot dry weight, root fresh weight, and root dry weight compared with the control by 87.32%, 173.68%, 117.64%, and 105.36%, respectively, at 10 °C; by 45.19%, 38.64%, 91.20%, and 21.50%, respectively, at 15 °C; and by 100.43%, 134.85%, 59.32%, and 57.84%, respectively, at 25 °C.

3.4. Antioxidant Enzyme Activity in Maize Seedlings

The SOD (Figure 7a–c), POD (Figure 7d–f), and CAT (Figure 7g–i) activities generally increased and then decreased with increasing GA-IAA-BL WP concentration, peaking at 100 mg mL⁻¹ under all temperatures. In the 100 mg mL⁻¹ GA-IAA-BL WP treatment at 10 °C, the SOD, POD, and CAT activities in shoots were 189.63%, 114.34%, and 136.11% higher than in the control, respectively, and the SOD, POD, and CAT activities in roots were 273.84%, 124.80%, and 110.47% higher than the control, respectively. At 15 °C, the activities of SOD, POD, and CAT in shoots were 161.89%, 149.93%, and 106.16% higher than in the control, and the activities of each of them in roots were 237.28%, 199.53%, and 162.50% higher than in the control, respectively. At 25 °C, the activities of SOD, POD, and CAT in leaves were 150.12%, 160.42%, and 212.82% higher than in the control, and the activities of each of them in roots were 132.59%, 94.48%, and 180.00% higher than in the control, respectively.

3.5. Pro and MDA Content of Maize Seedlings

The contents of Pro and MDA in shoots and roots generally increased and then decreased with increasing GA-IAA-BL WP concentration under each temperature (Figure 8a–f). GA-IAA-BL WP treatment at 50 mg mL⁻¹ increased the MDA content, but not significantly. GA-IAA-BL WP treatment at 100 mg mL⁻¹ significantly increased MDA content and improved the cold resistance of shoots and roots under moderate (25 °C) and low (10 and 15 °C) temperatures. The shoot MDA content increased by 90.67%, 66.31%, and 100.71% at 10, 15, and 25 °C, respectively, and the root MDA content increased by 97.24%, 94.64%, and 466.60%, respectively, compared with the control. The MDA contents were also higher in the 150 and 200 mg mL⁻¹ treatments compared to the control, but the contents were lower compared to the 100 mg mL⁻¹ treatment, indicating that applications over 100 mg mL⁻¹ would waste the product.

The Pro content was highest in the GA-IAA-BL WP treatment at 100 mg mL⁻¹ for all temperatures, with the shoot Pro content increasing by 115.53%, 117.66%, and 196.23% and the root Pro content increasing by 80.35%, 352.95%, and 334.56% compared with the control at 10, 15, and 25 °C, respectively. These results indicate that the seed dressing is beneficial for the seedling Pro content after germination, which could help maintain the normal osmotic pressure of the cells, ensuring normal material transportation and maintaining the integrity of the cell membrane, thus alleviating cold temperature stress.

3.6. Root Soluble Sugar, Soluble Protein Concentrations, and Root Vigor

Low-temperature stress caused a gradual decrease in root soluble sugar (Figure 9a) and soluble protein concentrations (Figure 9b) and a gradual decrease in root vigor (Figure 9c) in maize seedlings. The soluble sugar and protein concentrations and root vigor first increased and then decreased with increasing GA-IAA-BL WP concentration. The optimum concentration was 100 mg mL⁻¹, increasing the root soluble sugar concentration, root soluble protein concentration, and root vigor by 65.72%, 8.19%, and 107.69%, respectively, compared with the control at 10 °C; by 40.02%, 8.24%, and 75.90%, respectively, compared with the control at 15 °C; and by 46.30%, 39.62%, and 42.17%, respectively, compared with the control at 25 °C.

3.7. Pathways by Which GA-IAA-BL WP and Temperature Affect Maize Seed Germination and Seedling Shoot Growth

Structural equation modeling (SEM) was used to determine the main pathways of influence of GA-IAA-BL WP and temperature on maize seed germination and seedling shoot growth (Figure 10). GA-IAA-BL WP had a direct positive effect on maize seed germination and seedling shoot growth (loading coefficient: 0.39). In addition, there were three other pathways by which GA-IAA-BL WP positively affected maize seed germination and seedling shoot growth: organic matter accumulation, seedling antioxidant enzyme activity, and root vigor. Temperature directly positively affected the maize seed germination rate and seedling shoot growth (loading coefficient: 0.46). However, temperature negatively affected antioxidant enzyme activity (loading coefficient: −0.40), which in turn weakened the seed germination rate and seedling shoot length. In summary, GA-IAA-BL WP treatment can reduce the negative effect of cold temperatures on maize seed germination and seedling shoot growth.

The individual effects of different concentrations of GA-IAA-BL WP and temperatures on the target variables were also determined (Table 1). All concentrations of GA-IAA-BL WP were positively related to organic matter accumulation, antioxidant enzyme activity, root vigor, seed germination rate, and shoot and root length, with 100 mg mL⁻¹ resulting in the highest loading coefficient. For temperature, the 10 °C treatment was negatively associated with all target variables, and the loading coefficients tended to increase with increasing temperature.

4. Discussion

4.1. Low Temperatures Inhibit Maize Seed Germination and Seedling Growth

The process of seed germination is sensitive to external environmental changes, such as low temperatures, and is the period of weakest resistance [11]. The growth of the seed at germination determines the quality of the seedling and thus its ability to develop into a normal plant; it, therefore, has an important effect on the later stages of fertility and yield [54]. In the present study, maize seed germination and seedling shoot and root length, fresh weight, and dry weight were significantly reduced at low-temperature stress (10 and 15 °C) compared to at 25 °C. Low temperatures during germination can lead to membrane lipid phase change and damage to seed cell membranes, resulting in dysfunctional respiration and metabolism and diminished enzyme activity, leading to slow or even no seed germination [55].

The root system is an important part of the crop, and the maize root system is more sensitive to temperature than that of other crops [56]. Low temperatures can affect the morphological characteristics of the plant root system; for example, by reducing the root length, root surface area, and root dry matter [57,58,59]. Therefore, low temperatures affect the ability of the plant root system to access, absorb, and utilize nutrients from the soil, thereby adversely affecting plant growth and development [60]. In general, the development of the root system is one of the key factors affecting plant growth and yield. If the root system is more developed, it can better absorb water and nutrients from the soil while protecting the plant from external environmental interference, thus providing a good growth environment for the aboveground part [61]. Therefore, the development of the root system directly affects the growth and yield performance of the plant. It is of great theoretical significance and practical application value to improve the resistance of different plant species and root morphology characteristics to the effects of low temperature on growth [62]. The physiological effects of low temperatures on crop roots are significant, mainly manifested as decreased root activity, weakened respiration, decreased ATPase activity, and decreased cell membrane permeability. Meanwhile, low temperatures can significantly affect the absorption capacity of crop roots, limiting their ability to absorb nutrients [63]. Overall, a series of physiological changes caused by low temperatures can seriously affect the growth and development of crops, thereby limiting their yield and quality. Therefore, studying the physiological impact mechanism of low temperatures on crop roots has important theoretical and practical significance for addressing the effects of low temperatures on crop yield and quality [64].

4.2. Appropriate GA-IAA-BL WP Treatment Reduces the Negative Effect of Low-Temperature Stress on Maize Seed Germination and Seedling Growth

Chemical regulation, as an effective measure that is widely used, can significantly promote root growth and development and improve the absorption capacity of nutrients, water, and trace elements in crops under low-temperature stress, which leads to a decrease in root vitality and an impact on absorption capacity [65]. In this study, GA-IAA-BL WP was found to increase shoot and root lengths, particularly at a concentration of 100 mg mL⁻¹, where it significantly increased shoot and root lengths by 19.15–220.40% and 27.76–91.97%, respectively (Figure 3 and Figure 4). Therefore, in the process of high-yield cultivation, good results can be achieved by reasonably regulating the growth and development of crop roots in response to adverse stress such as low temperatures, drought, pests, and diseases during the growth period [66]. Moreover, under low-temperature conditions, chemical regulation can effectively improve the vitality of crop roots (in this study by 42.17–107.69%) (Figure 9c), enhance their ability to absorb nutrients and water, and thus increase crop accumulation and yield [67]. This study showed that compared with a water control, GA-IAA-BL WP application increased the seedling fresh weight (by 45.19–100.43%), root fresh weight (by 91.2–173.68%), seedling dry weight (by 38.60–134.85%), and root dry weight (by 21.50–105.46%) under low and normal temperatures (Figure 6). A previous study showed that soaking peanut seeds in GA can increase the activity of antioxidant enzymes, increase the content of osmoregulatory substances, and promote peanut seed germination [68]. A study found that spraying GA and benzyladenine (BA) 800 times on the leaves during the period of apricot bud expansion can reduce the degree of frost damage to apricot flower organs, lower the content of POD in flower buds, increase the content of proline in flower organs, increase the activity of SOD, CAT, and POD in apricot flower organs, and enhance the cold resistance of dried apricots [69]. In addition, studies have found that after continuous low-temperature damage to cherries, spraying GA, abscisic acid, salicylic acid, and glycine betaine 10,000 times separately or in combination with CaCl₂ can restore their floral organs to a certain extent and improve their cold resistance [70].

Gibberellic acid (GA) and indole-3-acetic acid (IAA) act as endogenous hormones, regulating the growth and development of a wide range of plants. The hormonal balance between GA and IAA may underlie the material basis for differences in seed germination [71,72]. Brassinolide (BL) is known as the sixth major class of plant growth regulators and has been shown to improve crop resistance and promote crop growth [73]. Both GA and IAA can lift seed dormancy and promote seed germination [74]. In this study, GA-IAA-BL WP was found to increase the germination rate of maize seeds by 4.31–18.85%, with the highest germination rate observed at a concentration of 100 mg mL⁻¹. The increase in the germination rate was most significant at low temperatures (10 °C), averaging 30.09% higher than other treatments (Figure 2). The DELLA family of proteins are key negative regulators in the GA signaling pathway, inhibiting gene expression and thus inhibiting seed germination; however, this inhibition can be lifted by exogenous GA [75]. In addition, at certain concentrations, GA and IAA have a corrosive effect on the wax layer of the seed coat, and after soaking the seed, they can improve the water permeability and air permeability of the seed coat, enhance the physiological and biochemical processes and respiration within the seed, and promote the growth of the embryo, which in turn can promote the germination of the seed [76]. Previous studies have found that soaking Leymus chinensis seeds in a 300 μg g⁻¹ GA solution for 48 h effectively promotes seed germination, the germination index, germination potential, and the vigor index and results in an effective increase in seedling height [77]. Treatment of Medicago sativa seeds at different concentrations of GA solution revealed that germination potential, germination percentage, germination index, germination rate, and root length increased with increasing concentrations of GA, and the best results were obtained when the GA concentration was 200 mg L⁻¹ [78]. It was found that exogenous GA, IAA, and BL could inhibit plant senescence by increasing SOD and CAT activities and regulating lipid peroxidation [79]. In this study, the application of GA-IAA-BL WP significantly increased the activities of SOD, CAT, and POD in both shoots and roots, with an average increase of 146.70–169.70%. The most significant increase in the activities of these three enzymes was observed at a concentration of 100 mg mL⁻¹ (Figure 7). Previous findings revealed that the damage caused by low-temperature stress on seedlings could be significantly alleviated by the exogenous application of GA and BL to cotton seeds, which was attributed to the fact that GA and BL could significantly increase the activities of antioxidant enzymes, such as CAT and SOD, and decrease the content of MDA in the leaves, thus effectively alleviating the process of membrane lipid peroxidation and improving the plant’s cold resistance [80]. After exogenous spraying of GA and IAA, the content of MDA in plants was significantly reduced, which effectively prevented the destruction of protective enzymes by reactive oxygen radicals and delayed the senescence of the membrane system [81]. In this study, under low-temperature (10 °C) stress, GA-IAA-BL WP promoted the accumulation of MDA in maize seedlings, thereby mitigating the damage caused by the low temperature and enhancing cold resistance. At 25 °C, the MDA content in the shoots was 3–10 times higher than that in the roots. This is because maize seedlings at 25 °C had already entered the three-leaf stage, while leaves at 10–15 °C had not yet unfolded. At the three-leaf stage, the shoots (stems and leaves) are more susceptible to external environmental factors, such as stress from light, temperature, and moisture (Figure 8a). These factors intensify membrane lipid peroxidation, leading to a sharp increase in MDA content. Proline has strong water solubility. When plants are subjected to cold stress, they accumulate free proline, which helps cells or tissues maintain their water content, prevent dehydration, reduce the damage caused by dehydration, and maintain normal cellular functions [82]. In this study, the optimal GA-IAA-BL WP concentration for increasing proline levels was 100 mg mL⁻¹ across all three temperatures, resulting in an increase from 80.35% to 352.95% (Figure 8b).

In summary, GA-IAA-BL WP significantly promoted the growth of maize seedlings at 25 °C. Moreover, GA-IAA-BL WP reduced the negative effects of low temperatures (10 and 15 °C). Specifically, compared with the control, GA-IAA-BL WP treatment under 10 and 15 °C increased seed germination, seedling shoot and root weight, seedling shoot and root biomass, root soluble protein and sugar content, and root vigor. A GA-IAA-BL WP concentration of 100 mg mL⁻¹ was most beneficial, while higher concentrations generally had a lower or no effect compared with the control. Excessive seed mixing concentration is not conducive to the establishment of root morphology, and to some extent inhibits the growth of roots. This indicates that using GA-IAA-BL WP at an appropriate concentration for seed mixing can promote the growth of maize roots under low-temperature stress, thereby promoting the growth and development of maize aboveground parts and the formation of yield. Excessive GA-IAA-BL WP seed mixing affects the normal growth of roots, thereby reducing their absorption capacity and leading to a decrease in belowground and aboveground dry matter accumulation.

5. Conclusions

The seed dressing GA-IAA-BL WP improved seed germination and seedling growth (shoot and root weight and length) at 10, 15, and 25 °C. GA-IAA-BL WP improved seedling growth under low temperatures; the growth was still much lower than under optimal temperatures, and more research is needed. The seed dressing also increased the Pro content and the CAT, SOD, and POD activities of seedlings, which likely helped regulate osmotic pressure, maintain the cell status, and remove peroxidation products, alleviating the damage caused by cold stress. The most effective seed dressing concentration was 100 mg mL⁻¹. These results suggest that the application of GA-IAA-BL WP to seeds in the field during sowing could improve the cold tolerance of maize seeds and promote the growth and development of maize seedlings.

Author Contributions

Investigation, Q.L., Y.Q., J.M. and Y.X.; writing—original draft preparation, J.C. and L.Z.; writing—review and editing, L.Z. and H.W.; visualization, P.Z. and D.G.; supervision, Y.G. All authors have read and agreed to the published version of the manuscript.

Funding

The work was supported by the Young and Middle-aged Science and Technology Innovation and Entrepreneurship Excellence Talent Team Programme (project Nos. 20230508003RC), the National Key Research and Development Programme (project Nos. 2023YFD2301702), the Jilin Provincial Agricultural Major Technology Synergistic Extension Project (project Nos. 2024XT0107), and the Jilin Province Agricultural Key Core Technology Demonstration and Promotion Project (project Nos. JARS-2024-0102).

Data Availability Statement

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

Acknowledgments

We wish to thank Chunsheng Wu and Jinhu Cui for their valuable and encouraging discussions. We appreciate the efforts of the anonymous reviewers and the editors’ valuable suggestions in earlier versions of this manuscript.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Maize was grown in plastic containers in a climate chamber. (a) Aerial view of the container; (b,c) side view of the container in a climate chamber.

Figure 2. Effects of GA-IAA-BL WP on the germination rate at different temperatures. The bars represent the mean ± SE, n = 50 replicates. The A, B, and C lettering indicates differences between temperatures under the same treatment (p < 0.05). Lowercase letters (a and b) indicate significant differences between GA-IAA-BL WP treatments at the same temperature (p < 0.05).

Figure 3. Effect of GA-IAA-BL WP on maize seedling growth at different temperatures.

Figure 4. Effect of GA-IAA-BL WP on maize seedling shoot (a) and root (b) growth at different temperatures. The bars represent the mean ± SE, n = 50 replicates. The A, B, and C lettering indicates differences between temperatures under the same treatment (p < 0.05). Lowercase letters (a, b, c, and d) indicate significant differences between GA-IAA-BL WP treatments at the same temperature (p < 0.05).

Figure 5. Effect of temperature and GA-IAA-BL WP seed dressing on the root–shoot ratio of maize seedlings. The bars represent the mean ± SE, n = 50 replicates. The A, B, and C lettering indicates differences between temperatures under the same treatment (p < 0.05). Lowercase letters (a, b, and c) indicate differences between GA-IAA-BL WP treatments at the same temperature (p < 0.05).

Figure 6. Effect of temperature and GA-IAA-BL WP seed dressing on dry and fresh weights of maize seedling shoots (a,c,e,g,i,k) and roots (b,d,f,h,j,l). The bars represent the mean ± SE, n = 50 replicates. Lowercase letters (a, b, c, and d) indicate differences between GA-IAA-BL WP treatments at the same temperature (p < 0.05).

Figure 7. Effect of temperature and GA-IAA-BL WP on enzymes. Superoxide dismutase (SOD) (a–c), catalase (CAT) (d–f), and peroxidase (POD) (g–i) activity in maize seedling shoots and roots. The bars represent the mean ± SE, n = 50 replicates. Lowercase letters (a, b, c, and d) indicate differences between GA-IAA-BL WP treatments at the same temperature (p < 0.05). A0–A4 indicate the GA-IAA-BL WP concentration: 0, 50, 100, 150, and 200 mg mL⁻¹, respectively.

Figure 8. Effect of temperature and GA-IAA-BL WP on proline (Pro) (a–c) and malondialdehyde (MDA) (d–f) in maize seedling shoots and roots. The bars represent the mean ± SE, n = 50 replicates. Lowercase letters (a, b, c, and d) indicate differences between GA-IAA-BL WP treatments at the same temperature (p < 0.05). A0–A4 indicate the GA-IAA-BL WP concentration: 0, 50, 100, 150, and 200 mg mL⁻¹, respectively.

Figure 9. Effect of temperature and GA-IAA-BL WP on root soluble sugar concentration (a), root soluble protein concentration (b), and root vigor (TTC) (c) of maize seedlings. The bars represent the mean ± SE, n = 50 replicates. The A, B, and C lettering indicates differences between temperatures under the same treatment (p < 0.05). Lowercase letters (a, b, c, and d) indicate differences between GA-IAA-BL WP treatments at the same temperature (p < 0.05).

Figure 10. Structural equation modeling (SEM) of the effect of GA-IAA-BL WP and temperature on maize seed germination and seedling growth. Blue arrows indicate negative correlations, and red arrows indicate positive correlations between variables (* p < 0.05). The black dotted line indicates no significant correlation (p > 0.05). A1–A4 indicate the GA-IAA-BL WP concentration: 50, 100, 150, and 200 mg mL⁻¹, respectively. Organic matter accumulation includes the dry and fresh weights of maize seedling shoots and roots. Antioxidant enzyme activity includes catalase, superoxide dismutase, and peroxidase.

Table 1. Relationships of concentrations and temperatures with target variables. Organic matter accumulation includes the dry and fresh weights of maize seedling shoots and roots. Antioxidant enzyme activity includes catalase, superoxide dismutase, and peroxidase. “×” represents the interaction between target variables.

Concentration (mg mL⁻¹)		Target Variable	Loading Coefficient	Temperature (℃)		Target Variable	Loading Coefficient
50	×	Organic matter accumulation	0.39	10	×	Organic matter accumulation	−0.16
100			0.57	15			0.45
150			0.45	20			0.78
200			0.35
50	×	Antioxidant enzyme activity	0.27	10	×	Antioxidant enzyme activity	−0.82
100			0.42	15			−0.59
150			0.39	20			0.21
200			0.36
50	×	Root vigor	0.28	10	×	Root vigor	−0.43
100			0.39	15			−0.25
150			0.33	20			0.46
200			0.31
50	×	Maize seed germination rate, shoot and root length	0.34	10	×	Maize seed germination rate, shoot and root length	−0.22
100			0.47	15			0.65
150			0.38	20			0.95
200			0.37

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MDPI and ACS Style

Cui, J.; Zhang, L.; Li, Q.; Qi, Y.; Ma, J.; Guo, D.; Zhang, P.; Xu, Y.; Gu, Y.; Wang, H. Seed Dressing Containing Gibberellic Acid, Indole-3-Acetic Acid, and Brassinolide Improves Maize Seed Germination and Seedling Growth Under Cold Stress. Agronomy 2024, 14, 2933. https://doi.org/10.3390/agronomy14122933

AMA Style

Cui J, Zhang L, Li Q, Qi Y, Ma J, Guo D, Zhang P, Xu Y, Gu Y, Wang H. Seed Dressing Containing Gibberellic Acid, Indole-3-Acetic Acid, and Brassinolide Improves Maize Seed Germination and Seedling Growth Under Cold Stress. Agronomy. 2024; 14(12):2933. https://doi.org/10.3390/agronomy14122933

Chicago/Turabian Style

Cui, Jingjing, Liqiang Zhang, Qianqian Li, Yuan Qi, Jiajun Ma, Danyang Guo, Pengyu Zhang, Yujie Xu, Yan Gu, and Hongyu Wang. 2024. "Seed Dressing Containing Gibberellic Acid, Indole-3-Acetic Acid, and Brassinolide Improves Maize Seed Germination and Seedling Growth Under Cold Stress" Agronomy 14, no. 12: 2933. https://doi.org/10.3390/agronomy14122933

APA Style

Cui, J., Zhang, L., Li, Q., Qi, Y., Ma, J., Guo, D., Zhang, P., Xu, Y., Gu, Y., & Wang, H. (2024). Seed Dressing Containing Gibberellic Acid, Indole-3-Acetic Acid, and Brassinolide Improves Maize Seed Germination and Seedling Growth Under Cold Stress. Agronomy, 14(12), 2933. https://doi.org/10.3390/agronomy14122933

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