1. Introduction
Soya is one of the most valuable crops in the world. The seeds contain about 40% protein with a beneficial amino acid composition and about 20% fat, half of which is unsaturated fatty acids that lower blood cholesterol levels. They are also a source of many valuable compounds such as fibre, lecithin, vitamins, mineral salts and antioxidants [
1]. They are therefore a valuable raw material for the food (oil) and feed (extracted meal) industries. Soybean covers about 29% of the world supply of consumer vegetable oil [
2]. In many countries soybeans are used as a meat substitute, because soy protein contains a set of amino acids in proportions similar to the reference protein (chicken egg) [
3]. Soy is also used in the pharmaceutical and chemical industries [
4,
5]. In addition, oil is one of the basic raw materials for biodiesel production [
6]. Soybean, as a species of the Legume family, brings additional economic and ecological benefits due to nitrogen fixation by the bacteria
Bradyrhizobium japonicum. As a result, it has low requirements for mineral fertilization and additionally increases the yield of successive plants, e.g., cereals [
7,
8]. Thanks to its versatile use, it currently occupies the largest sown area of legumes in the world (in 2018, over 125 million hectares) [
9].
Attempts to introduce thermophilic species such as soybean into cultivation in Poland are connected, among others, with the warming of the climate observed in recent years and the lengthening of the growing season in Poland’s latitude [
10]. Soybean is a short-day plant with high temperature requirements, especially during the flowering stage [
11,
12,
13]. According to Cai et al [
14], photoperiod and temperature are the most important factors affecting the growth and development of soybean, while at the same time severely limiting the cultivation range of this species. Soybean is sensitive to thermal conditions throughout its life cycle, i.e., from emergence to maturity. Câmara et al [
11] state that during the growing season, the average daily temperature should not be lower than 15 °C, as low temperatures slow down the growth of the plants, prevent the production of new leaves, shoots and pods. A drop in temperature below 10 °C may even prevent the soybean from flowering. According to Gass et al [
12], the flowering stage is a critical period associated with a particular sensitivity to low temperatures, where a temperature range of 17 to 18 °C is considered the biological minimum, while 22–25 °C is the optimum. Soybean has lower heat requirements during the maturing period, at the biological minimum of 8 to 14 °C, with an optimum of 14 to 19 °C. In the study of Ohnishi et al [
15], low temperatures (15/10 °C day/night) at 3–4 days before anthesis of soybean, affected the fertilization process and consequently, decreased pod setting and seed yield. There is little research on the response of soybean to low temperatures at earlier developmental stages. Łykowski [
16] states, that temperature 10 °C is the lowest that still ensures normal soybean vegetation.
Research on the effects of stress factors on crops has been carried out for several decades in many centers in Poland and abroad. This is based on breeding methods aimed at consolidating favorable plant traits, especially productivity and resistance to stress factors [
17]. Advanced research is also being conducted on genes related to soybean’s response to low temperatures. Zhang et al [
18] showed that thermal response was controlled by three pairs of major genes and the heritability was as high as 92.66%. However, the complexity of the problem lies in the fact that not only genetic, but also environmental factors determine the sensitivity of plants to stress. Stress factors can disrupt bioenergetic processes, alter plant metabolism, cause damage to cell structures and, as a consequence, inhibit plant growth, reduce yield, and deteriorate plant quality [
19]. Therefore, understanding the mechanism of photothermal sensitivity in soybean can provide a theoretical basis for improving cultivars. Under natural conditions, plants usually acquire low temperature tolerance through acclimatization to cold, i.e., gradual exposure to low, non-freezing temperatures [
20]. This process is linked to multiple mechanisms that include changes in gene expression, cell membrane structure, abscisic acid elevation, or accumulation of water-soluble sugars [
21,
22]. Unfavorable growing conditions restrict the fundamental processes of growth and development of soybean and consequently cause a reduction in yield and its nutritional value [
23].
Varietal variation in soybean in response to cold stress has been reported by many authors. Kołodziej and Pisulewska [
24] found, that of the two soybean cultivars tested, Naviko was more sensitive to adverse weather conditions than Aldana, and an increase in temperature amplitude contributed to an increase in seed and fat yields in both varieties. Gass et al [
12] showed variation among 10 soybean genotypes in cold tolerance by 3 °C between tolerant and susceptible genotypes in the threshold, below which temperatures can be considered to be damaging during flowering (15 and 18 °C). Zhang et al [
18] report that, along with the release years of soybean cultivars in China, the vegetation period was shortened, the reproductive period was prolonged, and the sensitivity to photoperiod was lower in new cultivars than in old ones. The long-term genetic breeding improved the photo-thermal adaptability, yield, agronomic and quality traits of soybean.
Agriculture is one of the economic branches that is most dependent on weather and climate conditions. Counteracting stress is, therefore, one of the main ways of ensuring yield stability in crop production. According to Anioł et al [
25], the difference between the potential yield of currently cultivated crops in Poland and the real yield may reach as much as 70%; therefore, from the cognitive and economic point of view, any research aimed at elucidating the basis of plant resistance to stresses is highly desirable. The aim of this study was to identify the response to cold stress applied at very early developmental stages of 16 soybean cultivars by evaluating emergence, yield, and chemical composition of seeds.
4. Discussion
Latitude determines the length of day and temperature, the most important factors to take into account when selecting a region for soybean cultivation. Climatic conditions in Poland are characterized by a relatively cool spring, which is very important from the point of view of the thermal requirements of soybean; hence, sowing is carried out only at the end of April to the beginning of May. The long duration of plant vegetation means, however, that delaying sowing carries a risk of plants not ripening and being harvested before autumn frosts, especially in the case of late cultivars. Therefore, the sowing date is very important, especially in the event of a cool spring.
The study showed that cold stress (12/6 °C day/night) did not largely reduce soybean emergence. A short-term 3-day stress, inflicted immediately after sowing and also after 3 and 6 days after sowing, reduced emergence by 6–10% on average. A longer 9-day cold stress did delay emergence by 9 days, but the number of germinated seeds was only 5% lower than in the control, which means that temperature drops of a few days were not the cause of much worse emergence. On the basis of research conducted in Switzerland [
12], it was found that low temperature after sowing soybean may cause prolonged germination, rotting of some seeds, while the emergency of the remaining seeds is slowed down and delayed. In our research, the cold stress caused a prolonged germination and delayed emergence, and a few percent reduction in emergence could have been caused by some of the seeds rotting. However, it should be noted that varietal variation in germination may reflect the capacity of particular lot of seeds used for this study. On the other hand, earlier sowing of soybeans can be beneficial in terms of extending the growing season. Hinson and Hartwig [
32] found that soybean seeds can germinate at temperatures from 5 to 40 °C. The study showed that a drop in temperature to 6 °C at night for a period of 9 days, inhibited plant emergence, but when the temperature rose, the plants emerged evenly, which means that they had not been damaged. According to certain authors, spring chill for soybean is not so harmful as heavy rains, which especially on heavy soils, cause soil crusting and consequently problems with emergence and optimal plant density [
33] and weed infestation in the early growth stages of soybean [
34,
35,
36].
The study showed that cold stress had a positive effect on soybean yield. After a short overcooling of germinating seeds (treatments B and C) only two cultivars showed a significant increase in yield, but after a longer chilling of seeds (treatment D), the yield was significantly higher in 12 cultivars, and in the remaining four cultivars such a tendency was recorded. This means that temperature drops immediately after sowing, even for a longer time, do not limit plant growth and development but, on the contrary, they increase plant vitality and have a positive effect on yield. Many authors consider early sowing of soybean as a key agronomic element in achieving high seed yield. Egli and Cornelius [
37] showed that in the southern states of the USA, earlier sowing of soybean causes a significant increase in yield, while delaying it until the end of May and the beginning of June significantly reduces it. According to the authors, an earlier sowing date is associated with earlier flowering of plants, which allows to avoid late summer drought and reduces disease and pest pressure. However, early sowing must be conditioned by favorable field conditions (rainfall, temperature). A study by Pedersen and Lauer [
38] showed that an earlier sowing date for soybean resulted in a higher number of pods and seeds and consequently a higher yield than a later date. According to Egli and Bruening [
39], late sowing of soybean shortens plant vegetation due to the complex effects of temperature and photoperiod. This can result in shorter plants, fewer nodes, lower vegetative weight at the beginning of seed filling and reduced flowering. Documented increases in soybean yield associated with earlier sowing are also presented by other authors [
40,
41,
42]. Meyer and Badaruddin [
43] found that early sowing should be a prudent management practice leading to increased soybean yields, especially in cooler regions, because it can expose the soybean to spring frosts, in which resow may be necessary. Therefore, in the northern U.S. states, where spring starts later and there are earlier fall frosts that limit the growing season, soybean producers are more cautious about the optimal seeding date that also minimizes the risks associated with cold, wet soils and seed pathogens [
44]. In the USA, soybeans are sown immediately after maize, when soil temperatures reach 10 °C, which, in the northern part of this country, generally falls at the end of May [
40]. On the other hand, sowing in late spring is associated with lower water resources in the soil and poorer seed germination, or heavy rains that encrust the soil [
45]. Therefore, in certain years, unfavorable spring conditions can reduce plant density and consequently yield, regardless of the sowing date [
44]. De Bruin and Pedersen [
40] report that in cool spring climates, soybean growers can increase yields by sowing soybeans 1 to 2 weeks earlier than the recommended optimum dates.
Soybean cultivars respond unevenly to seed overcooling associated with earlier sowing. In the conducted research, early and very early cultivars responded best to prolonged overcooling of seeds, while a slightly smaller yield increase was recorded in semi-late and late cultivars. In a study of Mourtzinis et al [
33], the highest seed yield was obtained from early sowing of cultivars belonging to earliness group MG2, while cultivars from groups MG0.6-1.2 responded poorly to sowing date. Salmeron et al [
46] found that combining early sowing with cultivars from the MG4 and MG5 groups gave favorable yield results in the US Midsouth. The yield reduction associated with later sowing (late May/early June) compared to earlier sowing (April/early May) was 6–18% depending on the cultivar. The selection of the cultivar to be grown is therefore crucial, as the response to environmental factors, especially stresses, can vary even within a single earliness group, as shown in the study. For example, in the late cultivars Madlen and Lissabon, the increase in seed yield after prolonged cold stress was 34.3 and 10.5%, respectively, while in the early cultivars Annushka and Paradis, it was 41.7 and 15.5%, respectively.
The results obtained show that cold stress applied after sowing of soybean did not significantly affect the quality of seed yield, indicating a larger influence of habitat and weather factors during the growing season on this trait. Research conducted under field conditions showed that earlier sowing of soybean (in April) resulted in higher crude fat, oleic acid, and sucrose content in seeds, while later sowing (in June) resulted in higher protein and linolenic acid contents [
1]. However, according to the authors, these changes may have been due to variability in environmental factors during the growing season, primarily drought and high temperatures. In particular, the increase in sugar content may have been related to the response to environmental stress. Kane et al [
47] showed that delayed soybean sowing increased protein and linolenic acid content and decreased crude fat and oleic acid content, whereas it did not affect palmitic, stearic and linoleic acid levels. In contrast, higher temperatures during seed filling associated with earlier sowing of soybean were strongly correlated with increased crude fat and oleic acid content and decreased linolenic acid levels in the soybean cultivars tested. Additionally, Kołodziej and Pisulewska [
24] found that the yield and fat content of soybean seeds depended on the weather conditions during the growing season, especially on air temperature. High thermal requirements of this species were demonstrated, among others, by the Aldana cultivar, in which the value of the correlation coefficient of seed yield with the maximum temperature amplitude was 0.999 at the significance level
p = 0.01, and with the minimum temperature 0.788 at the significance level
p = 0.05. Air temperature did not significantly affect the fat content in seeds of the cultivars studied. A significant effect of high temperature on fat accumulation and a decrease in protein content in soybean seeds was demonstrated by other authors [
48,
49]. In turn, Hou et al [
19] found that the fat content in the seed and the ratio of saturated to unsaturated acids are more affected by the extreme minimum daily temperatures during September seed filling than by the average or maximum air temperature and the geographical location.
In the study conducted, the chemical composition of soybean seeds significantly depended on the genetic factor (cultivar), which confirms the results of other authors. Piper and Boote [
50] showed variation in nutrient content in 20 soybean cultivars, with protein content significantly dependent only on cultivar, while fat content was equally affected by cultivar and temperature related to latitude. Kozak et al [
51] found, however, that the chemical composition of soybean seeds depended to the greatest extent on climatic conditions, followed by the varietal factor. In a study of Biel et al [
52], the varietal factor had a significant effect on fat and ash content (the Merlin cultivar contained more fat than Aldana). In turn, Nascimento et al [
53] showed a coefficient of variation (CV) of 6.9% for fat content in 15 soybean genotypes. They also indicated a strong interaction of genotype with habitat conditions. A significant interaction of temperature and cultivar on seed yield and the contents of protein, fat, fatty acid, and carbohydrates (raffinose and stachyose), was also demonstrated by Alsajri et al [
54].
5. Conclusions
Sowing date and soybean cultivar can have a major impact on the quantity and quality of the soybean seed yield, and can therefore increase or decrease overall farm profitability. Low temperatures during soybean sowing (6 °C at night) lasting for a period of 9 days delayed, but did not significantly reduce plant emergence, but in contrast, increased the yields of almost all the soybean cultivars studied. Spring cold stress, on the other hand, did not significantly affect the chemical composition of seeds. These results indicate that acceleration of soybean sowing by 1–2 weeks, depending on the region and field conditions (temperature, precipitation), may bring measurable benefits related to higher soybean yield, which may be of great importance in terms of soybean cultivation management. It should also be noted that other factors influencing germination and initial plant growth, such as weed competition, pest infestation or disease, should be considered when facing soybean emergence problems.
The research carried out comparing 16 soybean cultivars under controlled and partially controlled conditions is of great diagnostic importance but, on the other hand, we are aware that the results obtained cannot be validated for field conditions. Therefore, in order to provide more accurate recommendations to a wider range of producers, environmental studies in different points of Poland are needed to capture the environmental variability in important soybean production areas in this country.