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Article

Comparison of Structure and Physicochemical Properties of Starches from Hybrid Foxtail Millets and Their Parental Lines

by
Guiying Zhang
1,
Yurong Guo
1,2,
Wenjuan Du
1,
Longbo Jiang
1,
Zhenhua Wang
1,
Gang Tian
1,
Hong Liu
1,
Xin Liu
1,
Xiangyang Zheng
1,
Jie Guo
2 and
Huixia Li
1,2,*
1
Millet Research Institute, Shanxi Agricultural University, Changzhi 046000, China
2
College of Agriculture, Shanxi Agricultural University, Taigu 030801, China
*
Author to whom correspondence should be addressed.
Agronomy 2024, 14(11), 2527; https://doi.org/10.3390/agronomy14112527
Submission received: 11 September 2024 / Revised: 18 October 2024 / Accepted: 25 October 2024 / Published: 28 October 2024
(This article belongs to the Section Crop Breeding and Genetics)
Browse Figures
Versions Notes

Abstract

:
The structure and physicochemical properties of starch were important factors to determine the quality of foxtail millet. While hybrid foxtail millet has made greater progress in yield, it has made slower progress in quality than conventional foxtail millet with a more complex genetic base, which was jointly influenced by the parents. However, there were no reports on the comparison of the starch structure and physicochemical properties of hybrid foxtail millets and their parents. In this study, the amylose content, morphology structure, granule size distribution, X-ray diffraction, short-range ordered structure, pasting properties, and thermal characteristics of starches derived from Changzagu 466 (466), Changzagu 333 (333), Changzagu 2922 (2922) and their parent materials were analyzed. The results showed that compared with male parents, the starches from three hybrid foxtail millets and their female parents had larger average particle size, d(0.1), d(0.5), and gelatinization enthalpy (ΔH), while the amylose content values of three hybrid foxtail millets were 26.0%, 28.8%, and 28.9%, which were between the parents (25.8~27.1%, 25.4~28.8%, and 23.6~29.5%), with conclusion temperature (Tc) being higher than the parents and having a lower breakdown viscosity. The peak viscosity of Changzagu 466 (466) and Changzagu 2922 (2922) was 5235.5 cP and 5190.8 cP, respectively, lower than that of their parents (5321.0~6006.0 cP and 5257.0~5580.7 cP), while the peak viscosity of Changzagu 333 (333) was 5473.8 cP, falling between the parental values (5337.5~5639.5 cP). The cluster analysis results showed that the starch structure and physicochemical properties of hybrid foxtail millet were significantly different from those of female parents, which were mainly influenced by male parents. The findings of this study will establish a theoretical foundation for the enhancement and innovation of high-quality foxtail millet germplasm resources, as well as the development of high-quality hybrid foxtail millet combinations.

1. Introduction

Foxtail millet (Setaria italica (L.) P. Beauv.) was a cereal crop that originated in China and was primarily cultivated in the northern regions of the country. It has a cultivation history of approximately 10,000 years [1,2,3]. Additionally, foxtail millet was a significant food and feed crop and was cultivated in various countries and regions, including China, Japan, India, Africa, the United States, and Central Asia [3,4]. Notably, China and India have the most extensive cultivation areas. In terms of production volume, China ranks second globally in foxtail millet production [5]. Heterosis was a common phenomenon in the biological world, in which F1 hybrids are superior to their parent inbred lines in the target traits [6]. Foxtail millet has made significant advancements in heterosis, leading to a substantial increase in millet yield. However, the quality breeding of foxtail millet started relatively late, resulting in hybrid varieties with lower eating quality compared to conventional foxtail millet varieties [7]. With the improvement in people’s living standards and changes in dietary structures, there was an increasing focus on nutritious, healthy, and palatable food. Therefore, the selection and breeding of high-quality, high-yield millet were crucial for meeting market demands. In addition, quality traits were complex genetic traits controlled by multiple genes and greatly influenced by parental factors [8,9]. Therefore, it was crucial to select high-yielding hybrid foxtail millet with excellent genetic combinations and analyze the quality of its parental lines to breed high-quality, high-yield millet.
The cooking and eating quality of foxtail millet constitutes the primary quality trait to be contemplated in the selection of high-quality foxtail millet, and it also serves as one of the core factors in determining the commodity value of foxtail millet [10], which was predominantly determined by the structure and physicochemical properties of starch [11,12]. Starch served as a crucial raw material within the food industry. Starch was a principal component of foxtail millet, accounting for approximately 70% of the total grains of foxtail millet [13]. It can be utilized as thickeners, stabilizers, and water-retaining agents of products to modify the textural characteristics of food [14], and it can be employed in the food and food-related industries. The structure and physicochemical properties of starch determine its specific application [15]. Therefore, the study of the starch structure and physicochemical properties of hybrid foxtail millets and their parents was of great significance for expanding their application. The composition of starch included amylose and amylopectin, which together form the intricate structure of starch, encompassing granular, crystalline, layered, spiral, and molecular structures [16,17,18]. The amylose content served as a crucial indicator for assessing the sensory and cooking attributes of millet. A higher amylose content was associated with decreased palatability and reduced digestibility of millet [19]. The morphology of starch particles was closely associated with their quality, which in turn depends on their shape, size, and distribution [20]. The relative crystallinity of starch was positively correlated with the short chain of amylopectin, while the opposite was true with amylose. This was due to the fact that amylose disrupts the crystallinity of starch to a certain extent, and on the other hand, amylopectin contributes more to the crystallinity of starch [21]. Studies have shown that the molecular size of amylose and the structure of amylopectin have been found to impact the gelatinization and thermal property of starch, consequently influencing the eating quality of foxtail millet [22]. Therefore, comprehensive consideration of the structure and physicochemical properties of starch was essential for enhancing the quality of hybrid foxtail millet.
In addition to environmental factors, the biosynthesis process of hybrid foxtail millet starch was significantly influenced by parental genetics [23], and the genetic diversity and heterosis of parents were crucial for informing high-quality breeding selection. In recent years, significant progress has been achieved in the investigation of starch structure and physicochemical properties of rice [24], maize [25], and wheat [26] hybrids and their respective parents. Lin et al. [27] discovered in their study that the long branch-chain of amylopectin, degree of order at a short-range scale on the edge of starch granule, amylose content, and gelatinization temperature of inbred maize starch were higher than those of hybrid maize starch; however, the short branch-chain of amylopectin, relative crystallinity, branching degree of amylopectin, and gelatinization enthalpy of inbred maize starch were lower than those of hybrid maize starch. Kang et al. [28] demonstrated that the amylopectin, intermediate component, long branch-chains of amylopectin, and the average chain length (ACL) of hybrid wax sorghum starch were significantly lower than for the inbred waxy sorghum starch. Therefore, the starch structure and physicochemical properties of different crops changed in different ways between hybrids and parents after hybridization. The variations in starch structure and physicochemical properties of different crops and different parental combinations were significantly different. However, there was a lack of research on the starch properties of hybrid foxtail millets and their parental varieties. Previous studies primarily focused on the analysis and comparison of the starch characteristics of hybrid foxtail millets and their parental varieties, including total starch content, amylose content, and amylopectin content. In this study, 466, 333, 2922, and their parents were used as raw materials, among which three hybrid millets were high-yield hybrids selected by our team. They possess good yield performance and strong stress resistance, with an average yield of over 750 g per square meter. They have been extensively promoted and applied in Shanxi, Hebei, Inner Mongolia, and other regions in China. Among them, Changzagu 466 was consistently designated as the main variety in Shanxi Province in China from 2023 to 2024, and large-scale cultivation has been conducted. Although these hybrid foxtail millets possess advantages in terms of yield and broad application prospects, the quality of these widely cultivated hybrid varieties and the causes of their quality differences remain unclear. Therefore, it was of paramount importance to investigate the quality of these three high-yield hybrid millet varieties to achieve the sustainable development of hybrid foxtail millet.

2. Materials and Methods

2.1. Plant Materials

466, 333, 2922, and their parents were used as experimental materials (Table 1). In late April 2022, these 3 hybrids and their 3 female parents and 3 male parents were planted in the experimental field of the Millet Research Institute of Shanxi Agricultural University (Changzhi, China), using a random block design with 3 repetitions and 1 area in every 4 rows. The area was 13.3 m2, the row spacing was 0.33 m, and the length was 10 m. The experimental fields were managed in accordance with standard field practices, including irrigation, weeding, and pest control. Following ripening, 20 ears of millet were randomly selected from each plot for analysis of starch structure characteristics.
The three hybrid foxtail millets were selected by the “two-line method”, their female parents were all highly male sterile lines, the seeds of the sterile lines were propagated by 5~10% of their self-breeding, and there were no maintenance lines. Among them, F2922 was a middle early-maturity sterile line, and F466 and F333 were middle late-maturity sterile lines. The three male parents were all resistant to Sethoxydim herbicide type, of which K34 and K410 were both medium–late maturing, had a higher plant height, and had excellent millet quality restoration lines, and M22 was a medium–early-maturing, medium–dwarf culm, excellent resistance, good fruiting, and high-cooperativeness excellent restoration line.

2.2. Starch Sample Preparation

The alkali extraction method developed by Li et al. [29] was employed for starch extraction, with necessary adjustments made. The foxtail millet underwent shelling, grinding, and sieving through a 100-mesh sieve. A total of 200 g of millet flour was combined with a 0.1 mol/L NaOH solution at the ratio of material to liquid of 1:5 (w/v), mixed thoroughly, and then stirred for one hour. The resulting mixture was placed in the refrigerator at 4 °C for 12 h; The upper yellow precipitate was discarded, and the remaining solution was passed through a 200-mesh screen and washed until the starch layer was completely removed. The filtrate was collected and centrifuged at 4500 r/min for 10 min; both the supernatant and yellow precipitation were discarded while suspending the starch layer. This process was repeated several times until the upper liquid became clear; subsequently, the supernatant was discarded, and the starch precipitate was placed in the oven to dry at 40 °C before being ground and passed through a 100-mesh sieve for further analysis.

2.3. The Determination of Amylose Content

The content of amylose was determined via the colorimetric method, according to Ministry of Agriculture of the People’s Republic of China. For the determination of the amylose content in rice, the Spectrophotometry Method (NY/T 2639-2014) was used [30]. After achieving water balance, the samples were removed and thoroughly ground in a mortar and sieved through a 100-mesh sieve. In a clean 15 mL centrifuge tube, the 10 mg sample was added, followed by 100 μL of 95% alcohol and 900 μL of NaOH solution; the contents were then vortexed and mixed. The above centrifuge tube was boiled in boiling water for 13 min, and after cooling, it was fixed to 10 mL, shaken thoroughly, and left to sit for 10 min. Then, 0.5 mL of supernatant was taken, and 0.1 mL acetic acid and 0.2 mL potassium iodide solution were added sequentially to fix the volume to 10 mL; the mixture was left to sit at room temperature and protected from the light for 10 min, and the light absorption value was determined at 620 nm.

2.4. Scanning Electron Microscope Analysis

The starch particle image was acquired using scanning electron microscopy. The starch sample was affixed to the conductive adhesive on a copper table and incubated at 37 °C overnight. Subsequently, gold spraying was performed using an ion sputtering instrument before capturing the electron microscope image at 2000-times magnification [31].

2.5. Starch Granule Size Analysis

A 1% (w/w) starch suspension (weigh 100 mg of purified starch and mix with ultra-pure water) was prepared, and the diameter of the starch particles was measured using a laser particle size analyzer, Matersizer 3000 (Malvern Instruments Ltd., Worcestershire, UK), within the range of 0.1–2000 μm.

2.6. X-ray Diffraction Analysis of Starch

The starch sample was analyzed by X-ray diffractometer (Rigaku Corporation, Tokyo, Japan). The test conditions were as follows: the diffraction angle (2θ) scanning range was 4~60°, the step size was 0.02°, and the scanning speed was 4°/min. The X-ray intensity was measured via a NaI crystal scintillation counter. MDI Jade 5.0 software was used for the data analysis to calculate the relative crystallinity of starch [25].

2.7. Fourier-Transform Infrared Spectroscopy Analysis of Starch

It was determined through Fourier-transform infrared spectroscopy (Thermo Fisher Scientific, Inc., Waltham, MA, USA) by mixing potassium bromide and starch samples at a ratio of 100:1 (w:w). The samples were pressed into tablets using a mold and scanned 32 times within the range of 400–4000 cm−1, at a spectral resolution of 4.00 cm−1.

2.8. Pasting Properties

The pasting parameters, including pasting temperature (PT), peak viscosity (PV), trough viscosity (TV), final viscosity (FV), breakdown viscosity (BD), and setback viscosity (SV), were determined using the RVA (Newport Scientific Pty Ltd.,Warriewood, Australia). Following the method described by Siroha [32], 3 g of starch was accurately weighed and then mixed with 25 mL of distilled water in the aluminum cylinder of the RVA. Specific test conditions include maintaining the temperature at 50 °C for 1 min, heating up at a rate of 12 °C/min to reach 95 °C, maintaining this temperature for 10 min, and then cooling down at a rate of 12 °C/min to return to 50 °C and maintaining this temperature for an additional 2 min before concluding the test.

2.9. Thermal Property

A differential scanning calorimeter (TA Instruments, New Castle, DE, USA) was utilized to analyze the thermal properties of starch. A 3.0 mg sample of starch was weighed and mixed with 6.0 mg of deionized water and then equilibrated at 4 °C for 24 h. The temperature was ramped from 30 °C to 105 °C at a rate of 10 °C/min. Thermal transitions of starch were defined as onset temperature (To), peak gelatinization temperature (Tp), conclusion temperature (Tc), and gelatinization enthalpy (ΔH).

2.10. Statistical Analysis

The experiments were conducted three times, and the data were reported as mean and standard deviation (±SD). The one-way ANOVA and Duncan’s test were used to determine significant levels of the data by using SPSS 26 (p < 0.05), data processing and mapping were performed using Origin2021, and a clustering heat map was generated using Heat Map with Dendrogram in the APP.

3. Results

3.1. Basic Components of Isolated Starch

Table 2 presents the moisture content, protein, and fat in the starch of hybrid foxtail millets and their parents. The purity of starch directly affects the structure and physicochemical properties of starch. It can be observed from Table 1 that the protein and fat contents in starch were extremely low, ranging from 0.45% to 0.58% and from 0.05% to 0.23%, respectively, thus indicating the high purity of the starch extracted from the hybrid foxtail millets and their parents.
The amylose content was a crucial parameter for assessing the quality of foxtail millet. The amylose contents of hybrid millets 466, 333, and 2922, as well as their respective parents, were depicted in Figure 1. The amylose content showed significant differences among the parental lines of the three hybrids (p < 0.05). The amylose content of female parents from 466 and 2922 was significantly higher than that of male parents, particularly in the case of 2922, indicating a notable difference between parental levels. In contrast to 466 and 2922, the amylose content of male parent 333 exhibited a significantly higher level compared to that of female parent 333. The amylose content of hybrid foxtail millets 466 and 333 was not significantly different from that of their male parent (p < 0.05). The amylose content of 2922 was much higher than that of the male parent. The amylose content of both 466 and 2922 was lower than that of their female parent, but the amylose content of 333 was higher than that of female parent. The results showed that the amylose content of the three hybrid foxtail millets was higher than that of the male parent and between the parents.

3.2. Morphology Structure and Distribution of Starch Granules

The microscopic morphology of starch in different hybrid foxtail millets and their parents was observed using scanning electron microscopy, as depicted in Figure 2. The morphology of the starch granules of the hybrid foxtail millets and their parents was similar, with the majority exhibiting irregular polygonal shapes, while a minority were spherical. Additionally, the surface of the grain displays deep indentations, consistent with findings from previous studies [16,33]. The granule size of the three hybrid millet varieties, 466, 333, and 2922, was larger than that of their male parent. In conclusion, the granule size of foxtail millet after hybridization was changed compared with that of its parents, but there was no significant difference in granule morphology.
The starch size volume distributions of hybrid foxtail millets and their parents were shown in Figure 3. Except that the M333 volume distribution showed a bimodal distribution, 466, 333, and 2922 and their corresponding other parents showed unimodal distribution. From the volume grain size diagram, the starch particle size of the female parent for three hybrid millets were significantly larger than that of the male parent. After hybridization, the granule size of millet starch in the offspring was found to be larger than that of the male parent. The possible reason was that, in the process of starch biosynthesis, large starch particles have a relatively large influence on the volume distribution of starch, causing the volume distribution of starch to shift to large starch particles [24]. By utilizing the Mastersizer 3000 analysis software v3.81, the acquired data on particle size volume distribution of the collected sample were processed, resulting in the determination of corresponding particle size values for the cumulative distributions of 10% [d(0.1)], 50% [d(0.5)] and 90% [d(0.9)], as presented in Table 3. There were significant differences between hybrid foxtail millet starch d(0.1) and d(0.9) and female parent starch (p < 0.05), but there were no significant differences between medium starch and female parent starch. Compared with male parents, the d(0.1), d(0.5), and d(0.9) of all materials, with the exception of d(0.9) from 466, were found to be higher than that of the male parent. In conclusion, compared with male parents, small, intermediate, and large starch became larger after hybridization (except for 466 large starch).

3.3. The Crystalline Structure of Starch

The starch granular structure consists primarily of a crystalline zone and an amorphous zone, with the crystalline zone being predominantly composed of amylopectin. The double helix structure was organized in a specific arrangement, leading to the appearance of diffraction peaks in the X-ray diffraction pattern. The amorphous region consists of amylose molecules, and its diffraction pattern exhibits the dispersion diffraction peak [34,35]. The X-ray diffraction patterns of starch in the three hybrid foxtail millets and their parents, as depicted in Figure 4, exhibit a typical A-type starch crystal structure characterized by single diffraction peaks (2θ) at 15° and 23°, as well as double diffraction peaks at 17° and 18°. This was consistent with the previously reported crystal structure type of millet starch [36]. The relative crystallinity of starches of all materials was shown in Table 3. The hybrid exhibited a distinct relative crystallinity compared to that of its parental components. The starch crystallinity of 466 and 333 exhibited a significantly higher level compared to that of the parents (p < 0.05), while the crystallinity of 2922 fell between the levels observed in the parents. The relative crystallinity of starch was inversely associated with amylose content, particularly in high-amylose samples. Amylose has the potential to disrupt the double-helix structure arrangement of starch [37]. The findings of this study were in line with the amylose content results.

3.4. Short-Range Ordered Structure of Starch

The short-range ordered structure of starch in hybrid foxtail millets and their parents was determined using FTIR analysis, as depicted in Figure 5a. In the 400–4000 cm−1 region, the characteristic peaks of hybrid foxtail millets and their parents exhibited similarities, suggesting that there were no changes in the functional groups of millet starch following hybridization. It was observed that the characteristic peaks at 466 and 333 were more closely aligned with those of the male parent, whereas the peaks at 2922 resembled those of the female parent. The short-range ordered structure of starch at 466 and 333 was predominantly influenced by the male parent, while that of 2922 was primarily affected by the female parent. The Fourier-infrared convolution map of hybrid foxtail millet and its parents was depicted in Figure 5b. The infrared absorption peaks at 1047 cm−1 and 1022 cm−1 correspond to the crystalline and amorphous regions of the starch structure, respectively. The presence of the amorphous structure in starch was indicated by an increased absorption peak at 1022 cm−1, while the presence of the crystalline structure was indicated by an increased absorption peak at 1047 cm−1. The ratio of 1047 cm−1/1022 cm−1 (R1047/1022) was utilized to characterize the short-range ordered structure of starch. A higher R1047/1022 value indicates a greater degree of ordering of starch molecules, while a lower value indicates a lower degree of ordering [38,39]. Table 3 displays the infrared spectral peak intensity R1047/1022 values of hybrid millet and its parental varieties. The short-range order degree of three hybrid millet starches was lower than that of the female parent, while the other two hybrid millet starches exhibited a higher degree of order than the male parent, except for 333. This suggested that the order degree of amylose/amylopectin in hybrid foxtail millet starches was generally lower than that of the female parent and falls between that of the parents (except for 333).

3.5. Thermal Property of Starch

The thermal parameters, including gelatinization enthalpy (∆H), onset temperature (To), peak gelatinization temperature (Tp), and conclusion temperature (Tc), of 466, 333, 2922 and their parent starches are presented in Table 4. Compared with parent M466 and F466, 466 starch has an increased ∆H, Tp, and Tc. The ∆H and Tc of starch for 333 were increased, while the To was decreased, in comparison to M333 and F333. Compared to M2922 and F2922, the Tc of 2922 starch increased, while its Tp decreased; in addition, the To values of 466 and 2922 were between those of the parents. The various hybrid foxtail millet starches’ Tp, To, and Tc values exhibit distinct differences, which may be attributed to the stability of their starch structure [40]. Except for the ∆H of 2922 starch, which was between the parents, the ∆H values of 466 and 333 were higher than the parents. Gelatinization enthalpy (∆H) was the amount of energy required to disrupt the crystal structure of starch (the double-helix structure). The value ∆H represents the thermal stability of starch, and a larger ∆H indicates greater resistance to destruction of the crystal structure [41]. Hong et al. [42] demonstrate that ∆H was positively correlated with the crystallinity of starch. The results showed that, compared to the parents, 466 and 333 starches exhibited higher thermal stability, while 2922 showed greater thermal stability than the male parent but lower than the female parent.

3.6. Starch Pasting Property

The starch pasting properties of 466, 333, and 2922 and their parents were presented in Table 5. The peak viscosity of starches primarily indicates the water-binding capacity and extent of swelling, serving as a crucial parameter for assessing starch quality [43]. Compared to the parental lines, the peak starch viscosity of 466 and 2922 exhibited a decrease, while the peak starch viscosity of 333 was higher than that of the male parent but lower than that of the female parent. The results indicate a weak starch binding capacity for 466 and 2922, leading to limited expansion potential. The breakdown viscosity was a crucial parameter for assessing the stability of starch hot paste; a higher breakdown viscosity indicates lower hot paste stability. The starch breakdown viscosity of the three hybrid millets was found to be lower compared to that of the parental varieties, except for the female parent and male parent of 2922, as those values were not significantly different (p < 0.05). The female parent of 466 and 333 was significantly higher than that of the male parent (p < 0.05). The findings indicated that the thermal stability of starch in the three hybrid millet varieties was superior, with the male parent starch exhibiting greater strength compared to the female parent starch. The setback viscosity was indicative of the cold paste stability of starch. A higher setback viscosity indicates greater resistance to aging in the starch. The 466 starch’s setback viscosity was lower than that of the parents, 333’s was higher than that of the female parent than that of the male parent, and 2922’s was higher than that of the male parent than that of the female parent. The results showed that there were differences in the pasting characteristics of the three hybrids, probably due to structural differences in the parental and starch from different sources, which affect the starch’s physicochemical properties and, consequently, the starch characteristics of the hybrid foxtail millet [25,44].

3.7. Clustering Heat Maps of Fine Structure and Physicochemical Properties of Hybrid Foxtail Millet and Its Parent Starch

Figure 6 shows the clustered thermograms of the starch structure, pasting characteristics, and thermal properties of hybrid foxtail millets and their parents. The left tree represents the cluster of starch structure, while the upper tree represents the cluster of different hybrid millets and their parents. In this context, blue indicates a high content of the same index, whereas red indicates a low content of the substance. There were differences in starch characteristics among the parents of the three hybrids. Through the analysis of the variety cluster, it was evident that the F466 cluster belongs to class I, while the F333 cluster belongs to class II. The results indicated that the starch structure, pasting property, and thermodynamic properties of female parents were significantly different between the hybrid foxtail millet and male millet. The varieties 466, 333, 2922, F2922, M466, M2922, and M333 were grouped together in class III, suggesting that the starch characteristics of the hybrid millet were predominantly influenced by the male parent. The structure and physicochemical properties of starches 466 and 333 were similar. In conclusion, the results showed that starch structure and physicochemical properties of the hybrid foxtail millets were significantly different from those of their female parents, which were mainly influenced by male parents.

4. Discussion

The composition and structure of starch were the main causative factors for the disparity in foxtail millet quality. Previous studies have demonstrated that the amylose content, the shape and size of the starch granule, the starch crystallinity, and the short-range ordered structure directly influence the starch’s physicochemical properties, which were closely associated with the quality of foxtail millet [13,45,46]. Hybrid breeding was an important way to improve the quality of foxtail millet. Compared with conventional foxtail millet, the genetic basis of hybrid foxtail millet quality was complex and mainly influenced by parents. It was of great significance to compare the starch characteristics of hybrid foxtail millets and their parents for breeding high-quality millet.
Early prediction of heterosis can efficaciously enhance the breeding efficiency of high-quality millet. In the breeding process, amylose content, gel consistency, and gelatinization temperature were frequently employed to assess cereal quality [47]. However, cereals with similar apparent amylose content exhibit notable differences in taste quality [24], which requires an analysis from the perspectives of starch structure and physicochemical properties. The structure and physicochemical properties of starch were the main reasons for the quality difference. In order to comprehensively and systematically analyze the quality differences between hybrid foxtail millets and their parents, this study compared the differences between hybrid foxtail millets and their parents by analyzing the amylose content, morphology structure, granule size distribution, X-ray diffraction, short-range ordered structure, pasting properties, and thermal property of starches. Our further cluster analysis indicated that the starch structure and physicochemical properties of hybrid foxtail millet were predominantly influenced by the male parent, a finding which was in line with the findings of maize [25,48] and rice [47]. Guo et al. [25] compared the physicochemical properties of maize F1 hybrids and their parental starch and found that the male parent played an important determining role in the distribution of amylopectin chain length and relative crystallinity. Zhong et al. [48] demonstrated that the male parent had an impact on the molecular size of amylopectin components and the average chain length of amylose, as well as long amylopectin, in high straight-chain hybrid maize. In rice, for the same sterile line, there were some correlations between the hybrid combinations and restorer lines in terms of short-branch amylopectin chains and amylose [47]. These results indicate that the starch structure of male parent has important practical value in predicting heterosis and parental selection. Therefore, in the process of breeding high-quality hybrids, focusing on the selection of the starch structure of the male parent could enhance the screening probability of the target hybrid, which would offer a reference for the selection of high-quality foxtail millet and other crops.
Amylose content constitutes an essential indicator for cultivating high-quality hybrids, and its content was intimately associated with food quality. Previous studies have shown that the eating and cooking quality value of hybrid rice was negatively correlated with amylose content [47]. Zhang et al. [12] showed that amylose played a major role in the eating quality of foxtail millet congee, and the amylose content was directly correlated with the thermal (To, Tp. R) and textural properties. Previous research has indicated that the inheritance of amylose adheres to incomplete dominance, and the amylose content of the hybrid offspring (F1) lies approximately between that of its parents [49]. In our investigation, it was also discovered that the amylose contents of the hybrid foxtail millets 466, 333, and 2922 were 26.0%, 28.8%, and 28.9%, respectively; these values were similar to the values of amylose content of millet in Xing et al.’s [22] study (24.1~28.3%), as their values were also between that of the parents (23.6~29.5%). Zhou et al.’s [50] study showed that the amylose content of hybrid rice (TY398 and TY871) was between that of the parents. This was consistent with the results of this study. And we also found that the amylose content of the three hybrid foxtail millets was higher than that of the male parent; this might mainly be attributed to the superior activity of starch synthase (such as GBSSI and AGPase) and gene expression involved in amylose synthesis in hybrid foxtail millet compared to that of the male [23]. The distribution of starch granules was a crucial factor influencing grain quality. The granule size of starch was the main factor determining the texture of rice [51]. Peng et al. [24] showed that a greater diversity of forms and sizes of starch granules might influence the eating quality of hybrid rice. In this study, the granules size of the three hybrid millet varieties, 466, 333, and 2922, was larger than that of the male parent. However, there was no significant difference in granules’ morphology between the hybrids and their parents. Similar results were also found in the granule morphology of starch between hybrid and inbred waxy and sweet sorghum [28]. However, Peng et al. studied the granule morphology of hybrid rice plants and their parents and found that the starch granules’ morphology changed significantly after hybridization. It was speculated that the difference in the effect of hybridization on starch granules’ morphology may be caused by the different enzyme activity and gene expression during starch synthesis [23]. In addition, it was discovered that the starch particle size of the female parent was significantly greater than that of the male parent, and the starch granule size of foxtail millet was higher than that of the male parent after hybridization; the possible reason was that, in the process of starch biosynthesis, large starch particles have a relatively large influence on the volume distribution of starch, causing the volume distribution of starch to shift to large starch particles [24]. Starch granule volume is an important factor in determining grain weight, and its volume and granules’ size directly affect grain weight [52]. In addition, starch granules size was related to starch peak viscosity [53], indicating that grain weight and starch functional characteristics after hybridization have changed, which will affect the yield and quality of hybrid foxtail millet. When breeding hybrid foxtail millet featuring a high amylose content and large grain size, suitable male parents can be selected in line with these indexes, which can effectively shorten the breeding process and accomplish the breeding goal.
In conclusion, this study, by analyzing and comparing the starch structure and physicochemical properties of hybrid foxtail millets and their parents, showed that the starch characteristics of hybrid foxtail millets were significantly different from those of their female parents and were greatly influenced by their male parents. However, in the process of breeding good hybrids, it was essential to consider not only quality traits but also high-yield characteristics and excellent agronomic attributes. In the future, the heterosis of hybrid quality traits would be elucidated further through investigations into genetic and metabolic aspects, and the correlation between quality traits and yield traits would be studied to realize the simultaneous improvement of hybrid foxtail millet yield and quality and lay a theoretical foundation for the breeding of high-quality and high-yield hybrid foxtail millet.

5. Conclusions

The fine structure and physicochemical properties of starch in three hybrid foxtail millet varieties (466, 333, and 2922) and their respective parents were compared in this study. The results showed that the male parent starch had a lower-volume average particle size, d(0.1), d(0.5), relative crystallinity, ∆H, and pasting temperature compared to the female parent. Compared to the male parent, hybrid foxtail millet starch exhibited an increase in amylose content, volume mean grain size, d(0.1), d(0.5), ∆H, relative crystallinity, and Tc, as well as a decrease in breakdown viscosity, all of which were crucial indicators of starch quality. The starch crystal structure of hybrid foxtail millet and parent starch was typical “A” type. There were significant differences in starch characteristics between different hybrid foxtail millets and their parents. The R1047/1022 of the three hybrid foxtail millet starches was between that of the parents; the Tc was higher than that of the parents; and the breakdown viscosity was lower than that of the parents, where 466 and 2922 had lower peak viscosities than their parents, while 333 had peak viscosity between the parents. Our analysis of the clustering results showed that the starch characteristics of the female parent were significant differences between the hybrid foxtail millet and the male parent, and the male parent had a greater influence on the starch structure and physicochemical properties of the hybrid foxtail millet. The results of this study provide an important reference for the breeding of hybrid foxtail millet and the rational utilization of hybrid foxtail millet starch in the industrial field.

Author Contributions

Conceptualization, G.Z.; methodology, G.Z., W.D. and L.J.; investigation, H.L. (Hong Liu), Y.G., Z.W. and X.Z.; resources, G.T., H.L. (Huixia Li) and X.L.; writing—original draft preparation, G.Z. and Y.G.; writing—review and editing, G.Z., H.L. (Huixia Li) and J.G. All authors have read and agreed to the published version of the manuscript.

Funding

Key Research and Development Program of Shanxi Province (202102140601003, 2022ZDYF107); General Youth Fund Project of Shanxi Province (202203021212463); Biological Breeding Engineering Programme, Shanxi Agricultural University (YZGC027); Supported by Science and Technology Development Funding Programme for the Central Guided Local Funds (YDZJSX2022A048); Shanxi Millet Industry Technology System (2024CYJSTX04-06); Shanxi Provincial Science and Technology Innovation Team (2015013001-09); and Technology Achievement Transformation Project of Shanxi Province (202104021301043).

Data Availability Statement

Data is contained within the article.

Acknowledgments

Starch pasting properties were determined in the Millet Research Institute, Shanxi Agricultural University. We thank K.C.’s team for providing the experimental instruments of RVA.

Conflicts of Interest

The authors declare no conflicts of interest. The funders had no role in the experimental design, data collection and analysis, decision to publish, or preparation of the manuscript.

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Figure 1. Amylose content of hybrid foxtail millets and their parental lines. H, hybrid foxtail millet; M, male parent; F, female parent; different letters signify significant differences between hybrids and their parents within the identical breed (p < 0.05).
Figure 1. Amylose content of hybrid foxtail millets and their parental lines. H, hybrid foxtail millet; M, male parent; F, female parent; different letters signify significant differences between hybrids and their parents within the identical breed (p < 0.05).
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Figure 2. Images of starch from hybrid foxtail millets and their parental lines obtained using scanning electron microscopy (×2000); scale = 10 μm.
Figure 2. Images of starch from hybrid foxtail millets and their parental lines obtained using scanning electron microscopy (×2000); scale = 10 μm.
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Figure 3. Volume distributions of starch granules for hybrid foxtail millets and their parental lines.
Figure 3. Volume distributions of starch granules for hybrid foxtail millets and their parental lines.
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Figure 4. XRD pattern of starch from hybrid foxtail millets and their parental lines.
Figure 4. XRD pattern of starch from hybrid foxtail millets and their parental lines.
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Figure 5. Fourier-transform infrared spectroscopy (a) and deconvolution (b) of starch from hybrid foxtail millets and their parental lines.
Figure 5. Fourier-transform infrared spectroscopy (a) and deconvolution (b) of starch from hybrid foxtail millets and their parental lines.
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Figure 6. Heat map displaying starch structure, pasting properties, and thermal properties of hybrid foxtail millets and their parental lines. AC, amylose content; RC, relative crystallinity; PV, peak viscosity; TV, trough viscosity; BD, breakdown viscosity; FV, final viscosity; SB, setback viscosity; PT, pasting temperature; To, onset temperature; Tp, peak temperature; Tc, conclusion temperature; ΔH, gelatinization enthalpy.
Figure 6. Heat map displaying starch structure, pasting properties, and thermal properties of hybrid foxtail millets and their parental lines. AC, amylose content; RC, relative crystallinity; PV, peak viscosity; TV, trough viscosity; BD, breakdown viscosity; FV, final viscosity; SB, setback viscosity; PT, pasting temperature; To, onset temperature; Tp, peak temperature; Tc, conclusion temperature; ΔH, gelatinization enthalpy.
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Table 1. Female and male parents of the studied varieties.
Table 1. Female and male parents of the studied varieties.
VarietyFemale ParentMale Parent
466 (Changzagu466)F466 (Gu3A)M466 (K34)
333 (Changzagu333)F333 (Gao51A) M333 (K410)
2922 (Changzagu2922)F2922 (Jin29A)M2922 (M22)
Table 2. Basic impurities of starch from hybrid foxtail millets and their parental lines.
Table 2. Basic impurities of starch from hybrid foxtail millets and their parental lines.
VarietyMoisture Content (%)Protein (%)Fat (%)
4668.27 ± 0.07 a0.53 ± 0.01 b0.09 ± 0.01 def
M4667.52 ± 0.17 b0.53 ± 0.03 b0.07 ± 0.01 efg
F4667.00 ± 0.13 d0.52 ± 0.01 b0.14 ± 0.02 b
3336.96 ± 0.21 d0.51 ± 0.02 b0.06 ± 0.00 gf
M3335.77 ± 0.02 f0.45 ± 0.02 c0.05 ± 0.01 g
F3337.55 ± 0.24 b0.53 ± 0.02 b0.23 ± 0.01 a
29227.20 ± 0.06 cd0.53 ± 0.02 b0.11 ± 0.03 bcd
M29227.33 ± 0.12 bc0.54 ± 0.01 ab0.10 ± 0.01 cde
F29226.07 ± 0.04 e0.58 ± 0.04 a0.13 ± 0.00 bc
Mean values in the same experiment in the same column followed by different letters were significantly different (p < 0.05).
Table 3. The granule size, relative crystallinity, and R1047/1022 of starch from hybrid foxtail millets and their parental lines.
Table 3. The granule size, relative crystallinity, and R1047/1022 of starch from hybrid foxtail millets and their parental lines.
Varietyd0.1 (μm)d0.5 (μm)d0.9 (μm)d[4, 3] (μm)d[3, 2] (μm)RC (%)R1047/1022
4667.83 ± 0.01 a 11.90 ± 0.00 b18.00 ± 0.00 gf12.50 ± 0.10 b11.30 ± 0.10 b22.12 ± 0.08 b0.86 ± 0.01 b
M4666.11 ± 0.01 e 10.40 ± 0.00 e18.30 ± 0.10 ef11.50 ± 0.00 c9.66 ± 0.01 d21.11 ± 0.03 d0.80 ± 0.01 c
F4667.40 ± 0.20 b 12.80 ± 0.10 a23.00 ± 0.10 a14.10 ± 0.10 a11.80 ± 0.00 a21.58 ± 0.10 c0.90 ± 0.01 a
3336.94 ± 0.04 c 11.50 ± 0.20 c19.10 ± 0.10 c12.40 ± 0.10 b10.70 ± 0.10 c20.17 ± 0.01 f0.86 ± 0.01 b
M3335.71 ± 0.01 f9.93 ± 0.02 f18.50 ± 0.10 de11.20 ± 0.00 d9.21 ± 0.01 e16.99 ± 0.05 h0.90 ± 0.00 a
F3337.73 ± 0.03 a 11.70 ± 0.00 bc17.80 ± 0.10 g12.30 ± 0.20 b11.10 ± 0.10 b18.72 ± 0.03 g0.89 ± 0.00 a
29226.67 ± 0.06 d 11.20 ± 0.20 d19.40 ± 0.20 c12.30 ± 0.30 b10.40 ± 0.30 c21.14 ± 0.02 d0.86 ± 0.01 b
M29226.06 ± 0.06 e 10.40 ± 0.00 e18.70 ± 0.40 d11.60 ± 0.00 c9.67 ± 0.04 d20.39 ± 0.13 e0.81 ± 0.00 c
F29226.60 ± 0.10 d11.20 ± 0.20 d20.00 ± 0.00 b12.40 ± 0.10 b10.40 ± 0.30 c22.93 ± 0.05 a0.90 ± 0.02 a
Mean values in the same experiment in the same column followed by different letters are significantly different (p < 0.05). RC, relative crystallinity.
Table 4. The thermal properties of starch from hybrid foxtail millets and their parental lines.
Table 4. The thermal properties of starch from hybrid foxtail millets and their parental lines.
Variety∆H (J/g)Tp (°C)To (°C)Tc (°C)
46612.73 ± 0.16 c74.12 ± 0.21 c68.52 ± 0.31 b82.11 ± 0.21 ab
M46612.21 ± 0.08 e73.64 ± 0.68 cde68.63 ± 0.54 b80.10 ± 0.27 d
F46612.68 ± 0.07 cd73.59 ± 0.48 cde67.28 ± 0.37 c80.27 ± 0.26 cd
33313.42 ± 0.05 a73.06 ± 0.32 de66.50 ± 0.38 d82.46 ± 0.53 a
M33312.55 ± 0.08 d72.81 ± 0.71 e67.13 ± 0.36 cd79.30 ± 0.07 e
F33313.13 ± 0.02 b76.85 ± 0.53 a72.26 ± 0.12 a81.68 ± 0.44 b
292211.85 ± 0.07 g73.86 ± 0.65 cd66.91 ± 0.21 cd81.67 ± 0.13 b
M292211.48 ± 0.05 h74.37 ± 0.34 bc66.79 ± 0.33 cd80.93 ± 0.67 c
F292212.03 ± 0.06 f75.22 ± 0.31 b68.63 ± 0.33 b80.55 ± 0.15 cd
Mean values in the same experiment in the same column followed by different letters were significantly different (p < 0.05). To, onset temperature; Tp, peak temperature; Tc, conclusion temperature; ΔH, gelatinization enthalpy.
Table 5. The pasting properties of starch from hybrid foxtail millets and their parental lines.
Table 5. The pasting properties of starch from hybrid foxtail millets and their parental lines.
VarietyPV (cP)TV (cP)BD (cP)FV (cP)SB (cP)PT (°C)
4665235.5 ± 4.5 de1978.0 ± 82.0 abcd3257.5 ± 77.5 c3951.0 ± 91.0 e1973.0 ± 9.0 d75.0 ± 0.40 cd
M4665321.0 ± 35.0 d1947.0 ± 71.0 bcd3374.0 ± 36.0 c4066.5 ± 88.5 de2119.5 ± 17.5 cd74.9 ± 0.40 cd
F4666006.0 ± 38.0 a2086.0 ± 91.0 ab3920.0 ± 53.0 a4278.5 ± 178.7 cd2192.5 ± 89.9 c75.0 ± 0.40 cd
3335473.8 ± 76.0 c1999.5 ± 3.5 abc3474.3 ± 79.3 b4432.0 ± 73.7 bc2432.5 ± 77.0 b74.1 ± 0.48 e
M3335337.5 ± 47.5 d1851.5 ± 67.5 de3486.0 ± 115.0 b4649.5 ± 5.5 a2798.0 ± 73.0 a74.9 ± 0.43 cd
F3335639.5 ± 62.5 b1882.5 ± 98.5 cde3757.0 ± 161.0 a3964.5 ± 79.5 e2082.0 ± 178.0 cd78.1 ± 0.43 a
29225190.8 ± 55.3 e1931.0 ± 54.0 cde3259.8 ± 108.2 c4672.0 ± 23.0 a2741.0 ± 77.0 a75.4 ± 0.05 c
M29225580.7 ± 98.7 bc2115.0 ± 16.0 a3466.67 ± 114.4 b4335.5 ± 97.5 c2220.5 ± 81.5 c74.6 ± 0.05 de
F29225257.0 ± 60.0 de1799.3 ± 97.7 e3464.0 ± 47.0 b4622.5 ± 175.5 ab2823.2 ± 78.2 a76.9 ± 0.03 b
Mean values in the same experiment in the same column followed by different letters are significantly different (p < 0.05). PV, peak viscosity; TV, trough viscosity; BD, breakdown viscosity; FV, final viscosity; SB, setback viscosity; PT, pasting temperature; cP, centipoise.
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MDPI and ACS Style

Zhang, G.; Guo, Y.; Du, W.; Jiang, L.; Wang, Z.; Tian, G.; Liu, H.; Liu, X.; Zheng, X.; Guo, J.; et al. Comparison of Structure and Physicochemical Properties of Starches from Hybrid Foxtail Millets and Their Parental Lines. Agronomy 2024, 14, 2527. https://doi.org/10.3390/agronomy14112527

AMA Style

Zhang G, Guo Y, Du W, Jiang L, Wang Z, Tian G, Liu H, Liu X, Zheng X, Guo J, et al. Comparison of Structure and Physicochemical Properties of Starches from Hybrid Foxtail Millets and Their Parental Lines. Agronomy. 2024; 14(11):2527. https://doi.org/10.3390/agronomy14112527

Chicago/Turabian Style

Zhang, Guiying, Yurong Guo, Wenjuan Du, Longbo Jiang, Zhenhua Wang, Gang Tian, Hong Liu, Xin Liu, Xiangyang Zheng, Jie Guo, and et al. 2024. "Comparison of Structure and Physicochemical Properties of Starches from Hybrid Foxtail Millets and Their Parental Lines" Agronomy 14, no. 11: 2527. https://doi.org/10.3390/agronomy14112527

APA Style

Zhang, G., Guo, Y., Du, W., Jiang, L., Wang, Z., Tian, G., Liu, H., Liu, X., Zheng, X., Guo, J., & Li, H. (2024). Comparison of Structure and Physicochemical Properties of Starches from Hybrid Foxtail Millets and Their Parental Lines. Agronomy, 14(11), 2527. https://doi.org/10.3390/agronomy14112527

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