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Article

Association of High-Molecular-Weight Glutenin Subunits with Grain and Pasta Quality in Spring Durum Wheat (Triticum turgidum spp. durum L.)

by
Pavel Yu. Kroupin
1,
Ludmila A. Bespalova
2,
Aleksandra Yu. Kroupina
1,†,
Aleksey S. Yanovsky
2,†,
Varvara A. Korobkova
1,
Daniil S. Ulyanov
1,
Gennady I. Karlov
1 and
Mikhail G. Divashuk
1,*
1
All-Russia Research Institute of Agricultural Biotechnology, 127550 Moscow, Russia
2
P.P. Lukyanenko National Grain Centre, Department of Breeding and Seed Production of Wheat and Triticale, Central Estate of KNIISH, 350012 Krasnodar, Russia
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Agronomy 2023, 13(6), 1510; https://doi.org/10.3390/agronomy13061510
Submission received: 19 April 2023 / Revised: 17 May 2023 / Accepted: 27 May 2023 / Published: 30 May 2023
(This article belongs to the Section Crop Breeding and Genetics)
Browse Figure
Versions Notes

Abstract

Spring durum wheat is an important raw material for producing diverse products such as couscous, bulgur, bread, and pasta. The quality of the dough is significantly influenced by high-molecular-weight glutenins, the allelic status of which depends on the region and breeding program. In this study, a collection of 69 cultivars and promising lines of durum wheat were analyzed for the allelic state of Glu-A1 and Glu-B1 using SDS-PAGE and KASP PCR markers. Protein and gluten content, volume increase index, pasta breaking strength, general pasta estimation, SDS, and gluten index were measured for each accession based on a two-year field experiment in the Krasnodar region. The analysis revealed that the Glu-B1al, Glu-B1d, and Glu-B1z* alleles positively influence gluten index, with Glu-B1al increasing protein, gluten, and SDS content, whereas Glu-B1d decreased these traits. Glu-B1e, on average, decreased the gluten index and SDS value but did not affect protein or gluten content. The role of alleles affecting the gluten index and protein content in ensuring the quality of pasta in durum wheat breeding is discussed.

1. Introduction

Durum wheat (Triticum turgidum L. subsp. durum (Desf.) Husn), a tetraploid wheat species (2n = 28) with the genomic composition BBAA, is widely cultivated around the world. The total estimated cropping area of durum wheat is 13.5 million hectares, with the estimated/projected production ranging from 31.3 to 32.8 million tons in 2021–2023 years [1,2]. The main global producers of durum wheat are countries in the Mediterranean basin (Southern Europe, Turkey, and North Africa), Canada, Mexico, Kazakhstan, USA, Argentina, Russia, India, Syria, Australia, and other countries [1,3,4].
The quality of durum wheat plays a vital role in producing various products such as pasta, couscous, bulgur, and bread. Cultivation practices [5,6], weather and climatic conditions [7,8,9,10], and genetic factors [11,12] affect the quality of these durum wheat products. Genetic factors determine the protein content, dough strength, and levels of yellow pigments. Modern breeding has significantly improved the gluten index, SDS values, yellow pigment index, and gliadin/glutenin ratio [13,14,15,16]. Advances in the gluten quality of durum wheat varieties owe much to the development of instrumental gluten quality assessment tools applied at the early stages of breeding, including classic devices such as the alveograph, mixograph, and systems for SDS and gluten index estimation, as well as more modern tools such as the glutograph, glutopeak, and mixolab [17]. Improvements in gluten strength are most likely associated with the replacement of the Glu-B1e allele (Bx20 + By20) with the Glu-B1b (Bx7 + By9) and Glu-B1d (Bx6 + By8) high-molecular-weight glutenins (HMW-GS), the positive effect of low-molecular-weight glutenin (LMW-GS) subunits of the LMW-2 group, and the γ-45 subunit of gliadin associated with high firmness and viscoelasticity of pasta [11,12,13,15,18,19,20]. Identifying alleles (including novel ones) with a positive impact on quality and implementing them into the breeding process is facilitated by classic methods of protein (SDS-PAGE) and molecular genetic analysis (PCR), as well as modern approaches such as Lab-on-a-Chip [21], KASP [22,23], and GWAS-based markers [24,25].
The leading breeding center in Russia, P.P. Lukyanenko National Grain Centre, has been developing high-yielding adaptive durum wheat cultivars for regional producers for a long time [26,27,28]. Despite the commercial success of these cultivars, the breeding of durum wheat in Russia has long been conducted without the use of the gluten index determination method. To enter the global market and increase competitiveness, breeders started using gluten index evaluation methodology. The aim of this study was to assess the effect of HMW-GS allele status on the grain and pasta quality parameters including the gluten index in commercial cultivars and stable lines from the competitive variety testing at the P.P. Lukyanenko National Grain Centre.

2. Materials and Methods

2.1. Plant Materials

Commercial cultivars and non-segregating perspective breeding lines from the competitive variety trial nursery (CVT, prefinal stage of cultivar assessment preceding its state variety trial and registration) distinguished by stability, uniformity, and distinctness (69 accessions) are presented in Supplementary Table S1; their origin and year of release are indicated.

2.2. Field Experiment

The field experiment was performed on a plot of land at the P.P. Lukyanenko National Grain Centre (45°03′40″ N 38°54′23″ E) in 2020 and 2021. The sowing of spring durum wheat was carried out with peas as a forecrop. Harrowing was performed using a two-disc Catros harrow (Amazone, Osnabrück, Germany). Under the main tillage, the complex fertilizer Azofoska was applied (N16:P16:K16, 200 kg/ha). Plowing was performed to a depth of 25–30 cm with a turn-wrest plow (Lemken GmbH & Co., Alpen, Germany), followed by double cultivation using KPS-4.0 (Tehmash, Lida, Belarus). Sowing was performed using a self-propelled Plotseed TC seed drill (Wintersteiger, Ried, Austria) in 5 m2 plots in double replication. After seedling establishment, top dressing was carried out using ammonia nitrate (100 kg/ha). Harvesting was performed by direct combining using a Classic harvesting machine (Wintersteiger, Ried, Austria).

2.3. Grain and Pasta Quality Estimation

Grain and pasta quality estimation, high molecular glutenin characterization, Glu-A1/Glu-B1 genotyping, and statistical analyses were carried out as described in detail in our recent publication [29]. Therefore, here, we briefly describe the general points. The quality parameters, namely SDS, protein content, and gluten content, were determined using the Infratec™ 1241 grain analyzer (Foss Analytical, Hillerød, Denmark). Gluten index was determined using the Perten Glutomatic® 2100 System (PerkinElmer, Waltham, MA, USA). Pasta breaking strength was determined using the IPM-1 device (VNIIZ, Moscow, Russia). The volume increase index was calculated using a standard method as the ratio of the volume of dry pasta to the volume of pasta after cooking. The overall pasta evaluation assigned scores from “2” (lowest) to “5” (highest) considering pasta color, pasta breaking strength (directly proportional), and volume increase index (inversely proportional).

2.4. High Molecular Glutenin Characterization and Glu-A1/Glu-B1 Genotyping

The allelic state of Glu-B1 and Glu-A1 genes was determined using SDS-PAGE analysis as described in [30] with modifications and KASP markers Glu-Ax1/2*_SNP, distinguishing Glu-A1c (subunit Ax-null) from Glu-A1a/Glu-A1b (subunits Ax1/Ax2*) and BX7OE_866_SNP, distinguishing the Glu-B1al allele (subunit Bx7OE) from the others developed in [31].

2.5. Statistical Analyses

For all observed values expressed in percent (gluten content, protein content, gluten index), logit transformation was applied, and all statistical calculations were performed with the transformed values [32]. The mean observed values for each genotype/HMW GS subunit subcategory were grouped according to Tukey’s criterion. Cross-correlations and internal correlations of the observed values and the input categories, ordered and unordered, were estimated using the Φk coefficient [33]. Correlation and significance matrices were obtained via phik library (https://github.com/KaveIO/PhiK, accessed on 17 May 2023) in Python.
The principal component analysis (PCA) was performed via prince library (https://github.com/MaxHalford/prince, accessed on 17 May 2023) after the logit transformation of percentage data using scipy library. The first three components were used to create 3D reports in html via plotly (https://plotly.com/, accessed on 17 May 2023), showing both data points plotted in the coordinates of principal components and projections of initial numeric variables. The biplots were interpreted based on the angles between resulted vectors visible in html files in Supplementary Figures S1 and S2. The values of angles are shown in Supplementary Table S5. The angle between two vectors (traits) approximates the correlation between the vectors: an angle less than 90° corresponds to a positive correlation; an angle equal to 90° shows no correlation; an angle more than 90° corresponds to a negative correlation.

3. Results

3.1. Collection Structure

Based on the identification of the allelic state of genes encoding high-molecular-weight glutenins using KASP and SDS PAGE assays, we found that 67 accessions carry the Glu-A1c allele, and 2 accessions carry the Glu-A1b allele (Figure 1). Therefore, we do not describe the influence of the Glu-A1 locus on grain and pasta quality (although the statistical data are shown in Table 1 and Supplementary Materials). The studied collection had the following allelic composition for the Glu-B1 locus: Glu-B1al (7OE + 8), 38 accessions; Glu-B1d (6 + 8), 13 accessions; Glu-B1e (20), 9 accessions; Glu-B1b (7 + 8), 2 accessions. Additionally, in seven accessions, SDS-PAGE analysis revealed Bx7 + By15 subunits, while using the KASP marker BX7OE_866_SNP designed for SNP in the Glu-B1 promoter region showed the “G” call (corresponding to alleles other than Glu-B1al) in two of them and the “C” call (corresponding to Glu-B1al encoding the Bx7OE subunit) in five of them (Figure 1). Consequently, two accessions with “G” were assigned to the Glu-B1z genotype (Bx7 + By15) while the Bx subunit in the other five accessions with “C” was designated as Bx7C, and the coding novel non-typical allele was tentatively designated as Glu-B1z* (Supplementary Table S1).

3.2. Correlations between Quality Traits

In both years of the trials, a strong correlation was found between protein and gluten content. The correlation between SDS value and protein content (Φk 0.87) and between SDS value and gluten content (0.78) in 2021 was stronger than in 2020 (0.36 and 0.51, respectively). As it can be seen from the PCA biplots (Supplementary Figures S1 and S2), all three vectors/traits—protein content, gluten content, and SDS—have a similar direction; the pairwise angle values between them do not exceed 6°, which corresponds to a positive correlation (Supplementary Table S5). In 2021, the pasta breaking strength showed a tendency towards a positive correlation with protein content and gluten content (Φk 0.39 and 0.44, respectively, not statistically significant) and a negative correlation with the gluten index (Φk 0.38; Supplementary Tables S2 and S3). The most reliable correlation between traits within observation years was demonstrated by gluten content (Φk 0.53 at a significance level of 3.11); general pasta evaluation (Φk 0.56), protein content (Φk 0.44), volume increase index (Φk 0.34), and SDS (Φk 0.32) showed a moderate level of correlation at a low level of statistical significance (Supplementary Table S4).

3.3. Effects of HMW-GS on Grain and Pasta Quality

The Glu-B1 gene had a statistically significant influence on SDS value, protein content, and gluten content only in 2020. Genotypes with Glu-B1al (51.2 units) and Glu-B1d (48.3 units) alleles differed significantly in SDS value by 5.7%, while others had intermediate values. The highest gluten content was found in the accessions with Glu-B1z and Glu-B1al genotypes (31.6% and 30.3%, respectively, no significant differences), and the lowest was in the Glu-B1d genotype (28.6%), while other genotypes showed intermediate positions. The maximum protein content was found in the carriers of Glu-B1z, Glu-B1e, and Glu-B1al (16.9%, 16.4%, and 16.2%, respectively, no significant differences), while the minimum was in the Glu-B1d genotype (15.5%), and other genotypes showed intermediate positions (Table 1). In the PCA biplot, dots corresponding to Glu-B1d genotypes are located in the area opposite to the vectors/traits corresponding to gluten and protein content and SDS, which demonstrates a negative effect of Glu-B1d on these parameters (Supplementary Figure S1).
The highest values of gluten index were shown by the genotypes Glu-B1d, Glu-B1al, and Glu-B1z* in both observation years, although statistically significant differences between means were only shown in 2021. The difference between carriers of Glu-B1z*, Glu-B1d, and Glu-B1al alleles, on the one hand, and Glu-B1e, on the other hand, was 17.7 pp, 16.0 pp, and 15.7 pp, respectively; other accessions showed intermediate values (Table 1, Supplementary Figure S1).

4. Discussion

The influence of high-molecular-weight glutenins (HMW-GS) on dough properties and pasta quality is an important factor that needs to be considered in the breeding process. Noteworthy, although the main tendencies of HMW-GS to affect grain quality kept stable between years of the present field experiment, in 2020, HMW-GS influenced the gluten index, while in 2021, their effect on protein content, gluten content, and SDS was the most pronounced. This demonstrates that the HMW-GS genetic system may have different ways of impacting grain and protein quality depending on weather conditions that may be explained by the environmental influence on gluten polymerization at grain filling [8,34].
The structure of the world collections based on the allelic composition of Glu-A1 and Glu-B1 genes confirms the impact of certain alleles of HMW-GS on grain quality and final products. Apparently, the more positive influence of the allele on gluten strength and quality parameters, the higher frequency the allele has in the studied collection, especially when modern cultivars are studied. In the present study, for example, almost all accessions had the Glu-A1c allele (Ax-Null), while only two accessions carried Ax2*, which is rare for durum wheat and characteristic of common bread wheat, known for its positive effect on breadmaking quality and dough properties [35]. In the studies of collections of durum wheat cultivars and landraces, all or the vast majority of the accessions also had the Glu-A1c allele, with only a few accessions carrying the Ax2* subunits of Glu-A1b or Ax1 of Glu-A1a alleles [13,18,19,36,37,38,39,40,41]. However, in our recent study of winter durum wheat, 14.5% of the accessions had the Glu-A1a allele [29]; in the collection of varieties from different countries, the Glu-A1b and Glu-A1a alleles accounted for 18.5% and 22.4%, respectively [42], whereas 38.1% of the Mediterranean landrace collection had the Glu-A1a allele [13]. In the present study, Glu-A1b was associated with the Glu-B1al allele (Bx7OE + By8), while in the winter durum wheat collection obtained from NGC, it was mainly associated with the Glu-B1b allele (Bx7 + By8) [29]; in the world collection of durum wheat cultivars, Glu-A1b was associated with the By8 subunit in the absence of Bx [42], whereas in the collection of Mediterranean landraces and old varieties, Glu-A1a was more frequently associated with Glu-B1e and bands 2 + 4 + 15 + 19 at Glu-B3 [43]. Thus, it can be hypothesized that non-null Glu-A1 alleles are still in demand in the breeding of durum wheat and may have a certain advantage if combined with other high- and low-molecular-weight glutenin alleles.
According to the previous study, among Glu-B1 alleles, Glu-B1b (Bx7 + By8), Glu-B1d (Bx6 + By8), and Glu-B1z (Bx7 + By15) are usually indicated as having a positive effect on gluten strength, dough, and pasta quality in durum wheat [12]. In the present study, it was shown that the presence of Glu-B1d, Glu-B1al, and Glu-B1z* alleles positively affects the gluten index in both years of the trials. These genotypes were characterized by the highest gluten index values in both years of the trials, although statistical differences were only detected in 2021.
The Glu-B1al allele has the unique feature of possessing a double copy of the gene encoding the Bx7 subunit [44]. Glu-B1al is generally associated with greater gluten strength (gluten index, SDS sedimentation), extensibility (alveograph L and P/L), and protein content [35,45]. Its possible “predecessor”, the Glu-B1b allele, is associated with medium to strong gluten, high SDS values, gluten index, dough strength, and mixing development time in durum wheat [13,18,19,29,38,39,40,46,47,48,49]. In many studies, the structure of the durum wheat collection was determined without differentiation of Glu-B1b (Bx7 + By8) and Glu-B1al (B7OE + By8), i.e., the Glu-B1b allele in these collections was exclusively determined through SDS-PAGE electrophoresis. To compare our results with literature data, when combining the Glu-B1b and Glu-B1al genotypes into one group, “Glu-B1b”, it turns out that the predominant allele is Glu-B1b (60%), followed by Glu-B1d (18.8%) and Glu-B1e (13%). The significant predominance of the Glu-B1b allele over Glu-B1d by 2–5-fold has also been observed in breeding lines and cultivars from Australia [18], Mediterranean modern cultivars [50], exotic germplasm from various countries [36], and Moroccan modern cultivars [41]. The opposite situation is observed in collections of modern varieties from Canada and the United States, where the frequency of Glu-B1b exceeds that of Glu-B1d by 4–5-fold [18,41], and in Iberian landraces [51]. In the analysis of global collections of modern varieties, the difference between the frequencies of Glu-B1b and Glu-B1d alleles usually is less than twice [19,39,46,48]. Possible differences in the frequencies between “positive” alleles Glu-B1b and Glu-B1d in regional collections may be explained by their different influence on gluten quality under various climatic conditions and in different combinations with Glu-A1 and low-molecular-weight gluten alleles [18].
Due to the difficulty in distinguishing Bx7 and Bx7OE at SDS-PAGE electropherogram, differentiation is possible using MALDI-TOF-MS technology [52], Lab-on-a-Chip [21], high-performance liquid chromatography (RP-HPLC) [53], or with the use of more accessible classical PCR markers or KASP technology markers with primers developed at the 7OE locus [22,31,44,54]. When considering the frequencies of the Glu-B1al and Glu-B1b alleles obtained in the present study separately, it is obvious that the former (55.1%) has an advantage over the latter (2.9%) in the studied spring durum wheat collection of NCC. In our recent study of winter durum wheat from the same breeding center, Glu-B1al was identified in 17.1% and Glu-B1b was detected in 53.9% of accessions [29]. In the study where MALDI-TOF-MS was applied for the identification of the Bx7OE subunit in the collection of durum wheat from different regions, Bx7OE + By8 was found in 16.4% of accessions, Bx7 + By8 in 2.6%, and 9.0% were heterogeneous in Bx7 + By8/Bx7OE + By8, including accessions from the Russian Federation and the former Soviet Union [42]. Thus, it can be concluded that the Glu-B1al allele has been successfully introduced and is being used in the breeding of durum wheat at NCC, owing to its positive effect on the quantity and quality of gluten.
In our study, the Glu-B1d allele (Bx6 + By8) was detected in 13 out of 69 accessions (18.8%), which is consistent with the frequency found in modern varieties from Australia [18], the Mediterranean [50], and Morocco [41]. Glu-B1d had a similar effect in both years of the present experiment: as the gluten index increased, values for SDS, gluten content, and protein decreased (significant in 2020, as a general tendency in 2021). According to the literature, Glu-B1d generally has a positive effect on gluten quality and characteristics, SDS, and gluten index values [18,38,46,47,48] and negatively affects breadmaking quality in hexaploid bread wheat [35].
In the current study, a new allele, tentatively designated as Glu-B1z*, was identified in five accessions, one of which was represented by the Yarina cultivar, while the remaining four were the lines of the competitive variety trial nurseries. On the one hand, they showed bands typical of Bx7 + By15 in SDS-PAGE. On the other hand, the KASP marker BX7OE_866_SNP designed for the SNP G/C in the promoter of the gene encoding the Bx7 subunit [31] showed a call “C” associated with the Glu-B1al allele. The Glu-B1al allele carries a double dose of the gene encoding Bx7, which explains its overexpression [44]. Although the KASP marker BX7OE_866_SNP showed efficiency in detecting Glu-B1al in screening wheat collections [55], it is not causal, i.e., it was not developed directly on the border regions of the Bx7 duplication. Thus, in our atypical case, it cannot be directly concluded that the identified five accessions carry two copies of the Bx7 gene, but only stated the presence of an allele that differs from Glu-B1z in promoter region. It cannot be ruled out that the identified allele Glu-B1z* is a variant of Glu-B1z with a normal Bx copy number, as the promoter of this allele has not been studied before our research as SNPs in the promoter region of Bx are quite common phenomena [54].
The Glu-B1z allele generally shows a relatively low frequency of occurrence among old, intermediate, and modern genotypes in durum wheat germplasm from Argentina, France, Italy, CIMMYT, and Iran [19,37,56,57], as well as in Turkish landraces [58] and synthetic hexaploid cross-combinations [59]. In the collection of 313 rivet wheat accessions (T. turgidum ssp. turgidum), the Glu-B1z allele was detected only in three accessions, whereas among 77 accessions of khorasan wheat (T. turgidum ssp. turanicum), it was found in 52 genotypes [60]. The rareness of this allele in durum wheat might be explained by the frequent use of triticale, emmer, Aegilops, and other related species in breeding programs at NGC, which may lead to the introgression of Glu-B1z in the durum wheat germplasm. Furthermore, Glu-B1z has shown the highest mean values in the SDSS test [19]. In the present study, Glu-B1z and Glu-B1z* alleles have also shown a positive effect on the quality parameters of gluten in spring durum wheat germplasm, as was also shown in other studies [19,61]. The utilization of Glu-B1z and its modification Glu-B1z* in breeding programs may help to increase the genetic diversity of durum wheat and to improve its technological qualities.
In our study, Glu-B1e demonstrated (although not always statistically significant) either minimal or the lowest values for SDS and gluten index in both years of trials. This regularity is consistent with the results of many studies examining SDS and gluten index directly, as well as breadmaking properties and mixograph, alveograph, and farinograph parameters [13,18,19,29,36,38,39,40,46,47,48,49,62]. In our study, which included modern varieties and breeding lines, the frequency of this allele was 13.0%, while in our recent research on winter durum wheat from NGC, it was 14.5%. Subunits Bx20 + By20 have been shown to be progressively replaced by subunits Bx6 + By8 and Bx7 + By8 in Italian-bred varieties and were absent in old Spanish cultivars [13]. The frequency of Glu-B1e in the worldwide collections of wheat varieties or from individual countries is on average about 20%, ranging from 7% to 27% [18,19,39,41,46,48,50]; in landrace collections, its frequency is usually higher and ranges from 34% to 45% [36,41,50,51]. The lack of complete elimination of subunit 20x + 20y from the breeding process can be explained by the interaction of these high-molecular-weight glutenins with low-molecular-weight ones, which can even lead to outstanding SDS values [43,50]. Indeed, despite the generally low levels of SDS and gluten index among carriers of Glu-B1e, accessions x-15 and OSU-3910103/DUREX//OSU were consistently distinguished among other Glu-B1e genotypes by their high values for these traits, as well as their high general past estimation (integrating pasta breaking strength, volume increase index, and color) for both years of observation. Thus, the Glu-B1e allele remains in demand in the breeding process of durum wheat, but it is necessary to take into account the contribution of other genes for storage proteins and starch.
In our present and previous studies of durum wheat genotypes grown under Krasnodar conditions [29], SDS showed a positive correlation with protein content, which is consistent with the results of other studies [63,64]. Indeed, the Glu-B1al allele showed the highest values of SDS, protein, and gluten content, while Glu-B1d showed the lowest values of these parameters in 2019–2020. At the same time, we demonstrated the absence of any significant correlation between SDS and gluten index, whereas such a correlation has been found in many studies [37,49,63,64,65]. Probably, this is due to the fact that the SDS variation in the studied accessions is quite low, despite the overall high values since the breeding for this trait has been directed for many years at NGC, thus achieving its possible maximum. At the same time, evaluation of the gluten index started relatively recently, and selection for this trait was not carried out, which accounts for its high variation. In addition to high-molecular-weight glutenins, low-molecular-weight glutenins and the glutenin/gliadin ratio have been found to affect the gluten index significantly [14,18,49].
Gluten index values should be considered with caution, as selection based solely on this trait does not guarantee the production of pasta varieties with superior technological quality. It has been shown that pasta texture is better only with high protein content in addition to a high gluten index [66]. In the present study in 2021, a weak trend correlation was shown between protein level and pasta breaking strength, a parameter positively affecting the general pasta estimation. However, selection based solely on gluten index cannot lead to higher protein content, as gluten index does not depend on protein content according to many studies [17,39,63]. Modern Spanish and Italian cultivars with higher gluten index and SDS values have lower protein and gluten content compared to old cultivars and landraces [13,15,16]. At the same time, technological qualities such as bread volume, height, and specific volume can be high in old cultivars and landraces even with low gluten index values [67]. Bread baked from ancient Sicilian durum genotypes showed a more pleasant appearance as well as greater diversity in organoleptic and aromatic estimates and the characteristics of the processed products compared to modern cultivars [16]. In our case, for example, in 2021, both high (Glu-B1al and Glu-B1z*)- and low (Glu-B1e)-gluten-index genotypes showed comparable general pasta estimation scores close to 4.8 from a maximum of 5.0. Apparently, there may be an optimum value of gluten index that provides a proper interaction with starch and other macromolecules, resulting in the best cooking and organoleptic qualities of pasta.
Different effects of Glu-B1 on grain and pasta quality are due to different physical and chemical properties of the subunits provided by differences in their amino acid sequences. The presence/absence of extra cystein residues plays a major role in glutenin polymerization and thus may determine dough properties [68,69]. Glu-B1e has been shown to have a detrimental effect on gluten quality due to the substitution of two cysteine residues in the N-terminal domain of subunit Bx20 by tyrosines [70]. Interestingly, the Glu-B1 subunit of durum wheat contains a significantly lower number of negatively and positively charged residues than that of durum wheat [40], which may be associated with the differences in requirements for pasta- and breadmaking technology. Therefore, functional characterization of molecular mechanisms determining the differences between the studies’ alleles would greatly contribute to understanding their role in the breeding process and providing a quality end-product.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/agronomy13061510/s1, Figure S1: Principal component analysis of quality traits in the studied spring durum wheat accessions estimated in 2020. Dots indicate Glu-B1 genotypes; vectors indicate protein content (protein), gluten content (gluten), gluten index (GI), general pasta estimation (GPE), pasta breaking strength (PBS), SDS sedimentation volume (SDS), and volume increase index (VII); Figure S2: Principal component analysis of quality traits in the studied spring durum wheat accessions estimated in 2021. Dots and vectors indicate the same as in Figure S1; Supplementary Table S1: Accessions of the studied durum wheat collection, their Glu-A1 and Glu-B1 allelic state, gluten index, and general pasta estimation, as measured in 2020 and 2021 during the field experiment, with origin and year of release; Supplementary Table S2: Φk correlation indices (A) and their significance (B) between grain quality of durum wheat grown in 2020 and the allelic state of Glu-A1 and Glu-B1; Supplementary Table S3: Φk correlation indices (A) and their significance (B) between grain quality of durum wheat grown in 2021 and the allelic state of Glu-A1 and Glu-B1; Supplementary Table S4: Correlation coefficient between parameters of spring durum wheat measured in 2020 and 2021 during the field experiment; Supplementary Table S5: The values of angles between vectors in principal component analysis biplot.

Author Contributions

Conceptualization, L.A.B., A.S.Y. and M.G.D.; methodology, A.Y.K., A.S.Y., V.A.K. and M.G.D.; software, D.S.U.; validation, A.Y.K., A.S.Y., V.A.K. and D.S.U.; formal analysis, D.S.U.; investigation, A.Y.K., A.S.Y. and V.A.K.; resources, L.A.B., A.S.Y., G.I.K. and M.G.D.; data curation, D.S.U.; writing—original draft preparation, P.Y.K., A.Y.K., A.S.Y. and D.S.U.; writing—review and editing, P.Y.K., L.A.B., A.S.Y., G.I.K. and M.G.D.; visualization, A.Y.K. and D.S.U.; supervision, L.A.B., A.S.Y., G.I.K. and M.G.D.; project administration, L.A.B., G.I.K. and M.G.D.; funding acquisition, M.G.D. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Russian Science Foundation, grant 21-16-00121.

Data Availability Statement

Data are contained within the article and Supplementary Materials.

Conflicts of Interest

The authors declare no conflict of interest.

References

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Agronomy 13 01510 g001
Figure 1. Scatter plots for Glu-Ax1/x2*_SNP and BX7OE_866_SNP assays showing clustering of durum wheat accessions on the X-(FAM) and Y-(HEX) axes. (A) Orange dots, Ax1/Ax2* allele; blue dots, Ax-null allele. (B) Orange dots, non-Bx7OE allele; blue dots, Bx7OE allele. Black dots show negative control (water).
Figure 1. Scatter plots for Glu-Ax1/x2*_SNP and BX7OE_866_SNP assays showing clustering of durum wheat accessions on the X-(FAM) and Y-(HEX) axes. (A) Orange dots, Ax1/Ax2* allele; blue dots, Ax-null allele. (B) Orange dots, non-Bx7OE allele; blue dots, Bx7OE allele. Black dots show negative control (water).
Agronomy 13 01510 g001
Table 1. Mean values of quality traits of 69 spring durum wheat accessions. Mean values designated with the same letters have no significant differences within each group, as calculated using Tukey’s criterion. N, number of accessions of a corresponding group.
Table 1. Mean values of quality traits of 69 spring durum wheat accessions. Mean values designated with the same letters have no significant differences within each group, as calculated using Tukey’s criterion. N, number of accessions of a corresponding group.
Locus/ProteinAllele/SubunitNVolume Increase IndexPasta Breaking StrengthGeneral Pasta EstimationGluten Index, %SDSGluten Content, %Protein Content, %
20202021202020212020202120202021202020212020202120202021
Glu-A1Glu-A1b23.853.958388394.304.8546.079.351.647.732.6 b28.517.4 b15.2
Glu-A1c673.733.908288234.364.8074.295.350.542.729.9 a26.816.1 a14.6
Glu-B1Glu-B1al383.733.938328094.374.7576.896.2 a51.2 a42.430.3 a26.816.2 a14.5
Glu-B1b23.653.808998614.504.9552.268.4 ab51.5 ab47.429.8 ab27.116.2 ab15.0
Glu-B1d133.713.958198324.404.8573.096.5 a48.3 b42.528.6 b26.415.5 b14.6
Glu-B1e93.803.868178504.264.8252.180.5 b50.3 ab42.330.0 ab26.516.4 a14.6
Glu-B1z23.703.657888624.305.0028.884.7 ab51.6 ab47.331.6 a28.216.9 a15.1
Glu-B1z*53.723.868388384.284.8893.198.2 a51.8 ab44.530.5 ab27.516.3 ab14.7
Glu-A1 + Glu-B1Glu-A1b Glu-B1al23.853.958388394.304.8546.079.3 ab51.6 ab47.732.7 a28.517.4 a15.2
Glu-A1c Glu-B1al363.723.938328074.384.7478.296.6 a51.1 a42.130.2 a26.716.2 b14.5
Glu-A1c Glu-B1b23.653.808998614.504.9552.268.4 ab51.5 ab47.429.8 ab27.116.2 abc15.0
Glu-A1c Glu-B1d133.713.958198324.404.8573.096.5 ab48.3 b42.528.6 b26.415.5 c14.6
Glu-A1c Glu-B1e93.803.868178504.264.8252.180.5 b50.3 ab42.330.0 ab26.516.4 ab14.6
Glu-A1c Glu-B1z23.703.657888624.305.0028.884.7 ab51.6 ab47.331.6 a28.216.9 ab15.1
Glu-A1c Glu-B1z*53.723.868388384.284.8893.198.2 a51.8 ab44.530.5 ab27.516.3 abc14.7
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Kroupin, P.Y.; Bespalova, L.A.; Kroupina, A.Y.; Yanovsky, A.S.; Korobkova, V.A.; Ulyanov, D.S.; Karlov, G.I.; Divashuk, M.G. Association of High-Molecular-Weight Glutenin Subunits with Grain and Pasta Quality in Spring Durum Wheat (Triticum turgidum spp. durum L.). Agronomy 2023, 13, 1510. https://doi.org/10.3390/agronomy13061510

AMA Style

Kroupin PY, Bespalova LA, Kroupina AY, Yanovsky AS, Korobkova VA, Ulyanov DS, Karlov GI, Divashuk MG. Association of High-Molecular-Weight Glutenin Subunits with Grain and Pasta Quality in Spring Durum Wheat (Triticum turgidum spp. durum L.). Agronomy. 2023; 13(6):1510. https://doi.org/10.3390/agronomy13061510

Chicago/Turabian Style

Kroupin, Pavel Yu., Ludmila A. Bespalova, Aleksandra Yu. Kroupina, Aleksey S. Yanovsky, Varvara A. Korobkova, Daniil S. Ulyanov, Gennady I. Karlov, and Mikhail G. Divashuk. 2023. "Association of High-Molecular-Weight Glutenin Subunits with Grain and Pasta Quality in Spring Durum Wheat (Triticum turgidum spp. durum L.)" Agronomy 13, no. 6: 1510. https://doi.org/10.3390/agronomy13061510

APA Style

Kroupin, P. Y., Bespalova, L. A., Kroupina, A. Y., Yanovsky, A. S., Korobkova, V. A., Ulyanov, D. S., Karlov, G. I., & Divashuk, M. G. (2023). Association of High-Molecular-Weight Glutenin Subunits with Grain and Pasta Quality in Spring Durum Wheat (Triticum turgidum spp. durum L.). Agronomy, 13(6), 1510. https://doi.org/10.3390/agronomy13061510

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