Next Article in Journal
Functional Characterization of ABCA4 Missense Variants Linked to Stargardt Macular Degeneration
Next Article in Special Issue
Heteroalleles in Common Wheat: Multiple Differences between Allelic Variants of the Gli-B1 Locus
Previous Article in Journal
Rhus coriaria L. (Sumac) Demonstrates Oncostatic Activity in the Therapeutic and Preventive Model of Breast Carcinoma
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
IJMS
Volume 22
Issue 1
10.3390/ijms22010184
ijms-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

High-Molecular-Weight Glutenin Subunits: Genetics, Structures, and Relation to End Use Qualities

by
Yi Li
1,2,†,
Jiahui Fu
1,†,
Qun Shen
3 and
Dong Yang
1,2,*
1
Beijing Key Laboratory of Functional Food from Plant Resources, College of Food Science & Nutritional Engineering, China Agricultural University, 17 East Tsinghua Rd., Beijing 100083, China
2
Xinghua Industrial Research Centre for Food Science and Human Health, China Agricultural University, Xinghua 225700, China
3
Key Laboratory of Plant Protein and Grain Processing, National Engineering Research Center for Fruit and Vegetable Processing, China Agricultural University, 17 East Tsinghua Rd., Beijing 100083, China
*
Author to whom correspondence should be addressed.
†
These authors share equal co-first contribution.
Int. J. Mol. Sci. 2021, 22(1), 184; https://doi.org/10.3390/ijms22010184
Submission received: 26 November 2020 / Revised: 16 December 2020 / Accepted: 23 December 2020 / Published: 26 December 2020
(This article belongs to the Special Issue Genetics and Breeding of Wheat)
Browse Figures
Versions Notes

Abstract

:
High-molecular-weight glutenin subunits (HMW-GSs) are storage proteins present in the starchy endosperm cells of wheat grain. Encoding the synthesis of HMW-GS, the Glu-1 loci located on the long arms of group 1 chromosomes of the hexaploid wheat (1A, 1B, and 1D) present multiple allelism. In hexaploid wheat cultivars, almost all of them express 3 to 5 HMW-GSs and the 1Ay gene is always silent. Though HMW-GSs are the minor components in gluten, they are crucial for dough properties, and certain HMW-GSs make more positive contributions than others. The HMW-GS acts as a “chain extender” and provides a disulfide-bonded backbone in gluten network. Hydrogen bonds mediated by glutamine side chains are also crucial for stabilizing the gluten structure. In most cases, HMW-GSs with additional or less cysteines are related to the formation of relatively more or less interchain disulfide bonds and HMW-GSs also affect the gluten secondary structures, which in turn impact the end use qualities of dough.

1. Introduction

Wheat is one of the most widely grown cereal crops worldwide with hexaploid wheat (Triticum aestivum L., AABBDD) being a representative one. According to the Agricultural Market Information System (AMIS), the estimate of world wheat production is 764.9 million tons in 2020 to 2021 [1]. Take China as an example, as the world’s largest wheat producer, China produced 131 million tons of wheat and consumed 128 million tons in 2019, among which 67.7% was used for food and 15.0% was used for feed [2]. Protein makes up approximately 8% to 20% of the total mass of mature wheat grains [3]. Based on their solubility, protein in wheat grain can be categorized into four classes: albumin, globulin, gliadin, and glutenin [4]. The latter two, gliadin and glutenin, are the major components of gluten, which are similar in content and together accounts for approximately 80–85% of wheat protein [3]. The protein of wheat grain, especially gluten protein, is generally regarded as one of the most important factors determining dough properties and bread qualities [5,6,7].
Defined as the remaining rubbery mass after gently washing wheat dough to remove the bulk starch granules and water-soluble components, gluten usually contains approximately 75–85% protein on a dry weight basis, depending on the thoroughness of washing [8]. Glutenin subunits are the monomeric component of a gluten polymer in dough through covalent disulfide linkage and noncovalent interactions including hydrogen bonding and hydrophobic interaction, forming a tight gluten network backbone and providing dough elasticity as well as dough strength. On the other hand, most gliadins exist in their monomeric form, affording dough viscosity and extensibility via electrostatic interactions and hydrogen bonding [9,10]. Gliadins can be further separated from gluten by dissolving in 60% to 70% (v/v) ethanol solution. Besides, the solubility of glutenin subunits from gluten would be similar to gliadins in aqueous alcohols if the disulfide bonds are reduced [8]. Based on their electrophoresis mobility on a sodium dodecyl sulfate-polyacrylamide gel electrophoresis (SDS-PAGE), reduced glutenin from dough can be further categorized into High-molecular-weight glutenin subunits (HMW-GSs, MW of 67,000–90,000 Da) and low-molecular-weight glutenin subunits (LMW-GSs, MW of 30,000–45,000 Da) [11,12,13,14]. Though HMW-GSs are minor components in terms of mass (approximately 10% of gluten protein), they are highly related to end use quality [8]. This review aims to describe the genetics and different levels of structures of HMW-GS, and their relationships to dough and bread-making qualities.

2. Genetics of HMW-GS

It is now firmly established that genes named Glu-1 loci encoding the synthesis of HMW-GS (Glu-A1, Glu-B1, and Glu-D1) are located on the long arms of group 1 chromosomes of the hexaploid wheat (1A, 1B, and 1D) (Figure 1) [15,16,17,18]. Each locus includes 2 genes linked together encoding 2 different types of HMW-GS, the x-type subunits with a relatively higher molecular weight and the y-type subunits which exhibit relatively higher electrophoretic mobility on the SDS-PAGE [12,13,14,19,20,21]. Moreover, subloci differences are greater than homoeoallelic differences. For example, differences between Glu-D1x genes (genes encoding x-type subunits) and Glu-D1y genes (genes encoding y-type subunits) are greater than differences between Glu-D1y genes and Glu-B1y genes, as shown in Figure 2 [22,23].

2.1. Allelic Variations of Glu-1 Loci

The Glu-1 loci present multiple allelism: 3 alleles at the Glu-1A loci, 11 alleles at the Glu-1B loci, and 6 alleles at the Glu-1D loci were systematically reported by isolating HMW-GSs from SDS-PAGE in 1983, in which the numbering system developed to identify HMW-GS and provide a chromosomal location of the genes is currently still in use [24]. Polymerase chain reaction (PCR) and immunoassay using specific monoclonal antibodies are alternative ways of isolating novel genes encoding HMW-GS [25,26,27,28]. Since the publication of the catalog of gene symbols for wheat, more than 100 allelic variations at the Glu-1 loci have been identified [29]. According to the collections of the HMW-GS alleles from over 7830 cultivars/lines, there is no doubt that the Glu-1 loci exhibits high genetic polymorphisms [30]. In particular, the Glu-1B and Glu-1D alleles display higher variable frequency while that of the Glu-1A alleles is a much lower. Recently, a number of novel Glu-1 genes from wheat landraces or related species have been identified to be of potential application values to wheat breeding, and efforts have also been made to transfer desirable Glu-1 alleles to cultivated wheat by wide hybridization and chromosomal engineering approaches [14,31,32,33,34,35,36].
Working on HMW-GS allelic variations to improve wheat bread-making qualities has been an attractive research topic in the past several decades. Some allelic variations make greater contributions to dough elasticity and strength as well as loaf volume than others. In general, the Glu-D1 loci exhibited the most significant effect on dough and bread-making properties, followed by Glu-B1 and Glu-A1 [37,38,39]. Furthermore, several studies found that both Glu-D1 and Glu-B1 exhibit significant effects on dough qualities on their own, whereas the effects of Glu-A1 loci depend on the presence of other Glu-1 subunits [40].
As for specific alleles encoding HMW-GSs, the Glu-A1a allele encoding 1Ax1 and the Glu-D1d allele encoding 1Dx5 and 1Dy10 were reported to be associated with better bread-making qualities, and the beneficial effects of these two alleles are additive [19]. Later, in 1987, after analysis of 84 hexaploid wheat varieties, the Glu-1 quality scores assigned to each HMW-GS and corresponding alleles were reported. Among the alleles reported in the research, wheat containing the Glu-D1d allele encoding 1Dx5 and 1Dy10 represents the highest score, corresponding to higher bread-making qualities, while Glu-A1c, Glu-B1a, Glu-B1d, and Glu-D1c represent the lowest scores, corresponding to poor bread-making qualities [16]. By comparing the rapid mix test score from 153 German wheat varieties, it was discovered that the bread-making quality was positively influenced by alleles encoding subunits 1Ax1, 1Ax2*, 1Bx7 + 1By9, 1Bx14 + 1By15, 1Bx17 + 1By18, and 1Dx5 + 1Dy10 [41]. Meanwhile, by studying the deletion of combinations of HMW-GS loci, contributions of each HMW-GS to dough processing properties were ranked in the following order: 1Dx5 + 1Dy10 > 1Bx17 + 1By18 > 1Ax1 + Null [40]. Nevertheless, several studies argue that all HMW-GSs contribute positively to dough or bread-processing quality but only differ in magnitude, since the absence of HMW-GS with weaker effects, such as 1Dx2, 1Dy12, 1Bx20, and 1By20, also led to inferior flour-processing quality in wheat mutants [42,43,44,45,46].

2.2. Gene Expression

The mechanism that regulates HMW-GS expression remains largely unclear [47]. Some conserved cis-acting elements related to the expression of storage proteins have been identified in HMW-GS gene promoters [47,48,49,50]. To date, storage protein activator (SPA), a member of the basic leucine zipper (bZIP) family, has been identified to play a key role in the regulation of wheat grain storage protein synthesis [51,52,53,54,55]. From a theoretical point of view, the hexaploid wheat cultivars could express 6 different HMW-GSs, 1Ax, 1Ay, 1Bx, 1By, 1Dx, and 1Dy, while in fact, owing to gene silencing, almost all of them express 3 to 5 HMW-GSs depending on wheat cultivars except the few hexaploid wheat cultivars expressing all 6 HMW-GSs [56,57,58]. The expression frequencies of 1Dx, 1Dy, and 1Bx are usually the highest, while the 1Ax and 1By subunits sometimes are not expressed at all. On the other hand, the 1Ay subunit is often not expressed in the hexaploid wheat, whereas its expression is frequently reported in diploid and tetraploid wheat [19,59,60,61].

2.2.1. Progress on the Ay Gene

Since 1Ay genes show a high frequency of silence in the hexaploid wheat, researchers have focused on their promoters and coding region structures to explore probable causes. Comparing the 5′ upstream promoter region of the active gene encoding 1By9 with the same region from a silent y-type gene derived from chromosome 1A, it was discovered that there is a deletion of 85 bp bases in the latter, which was also found in the 5′ upstream promoter region of the inactive Ay1d gene from the cultivated emmer (Triticum dicoccum, 2n = 4x = 28, AABB) [62,63]. However, analysis of 141 accessions of diploid and tetraploid wheats found this 85 bp deletion to be present in the promoter regions of all 9 1Ay genes, regardless of whether these genes are active or not [64]. Researchers later constructed two promoter–GUS (β-glucuronidase) reporter gene chimeric vectors, pBI121-Ay-GUS and pBI121-Dx5-GUS, in which the native promoters were replaced by promoters from an inactive 1Ay gene and an active gene encoding 1Dx5, respectively. The transient expression of promoter–GUS constructs indicated that the 1Ay promoter can drive the expression of the GUS gene, verifying that 85 bp deletion in the promoter is not associated with inactivation of 1Ay genes [60].
As for the coding region, an 8-kb insertion retroelement in a cloned pseudo 1Ay gene from wheat cultivar Chinese Spring (Triticum aestivum L., AABBDD), termed wheat insertion sequence-2 (Wis-2), was reported, which interrupts the coding sequence [62]. Similarly, the Ay gene coding sequence in a tetraploid wheat cultivar, T. turgidum (AABB), is also disrupted by an insertion of a Wis retroelement, Wis-3, which may result in silencing of the Ay gene [65]. Besides the above, many scholars have focused on the stop codons in the coding region as well. Translations of three silenced Ay genes from the diploid and tetraploid wheat species, together with silencing of 1Ay (from hexaploid wheat cv. Cheyenne) were disrupted by premature stop codons [64]. This is consistent with a previous study showing that the coding region of an inactive Ay gene, namely Ay1d, contains four stop codons [63]. In conclusion, these genes were highly unlikely to be expressed with full length and defects in the coding regions could be responsible for silencing of the 1Ay genes.
Since the Glu-1Ay gene is usually silenced in hexaploid wheat, the utilization of active 1Ay genes might be an effective strategy for improving flour quality. An active allele encoding 1Ay subunits was successfully integrated from wild emmer wheat (Triticum turgidum ssp. dicoccoides) into the hexaploid wheat (Triticum aestivum) [66]. In this study, the selected line TaAy7-40, which expresses 1Ay subunits stably, was reported to possess better processing quality. Two Swedish hexaploid wheat lines (W29323 and W3879) were found to contain both active 1Ax and 1Ay genes and the corresponding expressed subunits were initially named 21* and 21*y, which were later found inherited as a pair [57]. Moreover, the allele encoding 1Ax21* and 1Ay21* were also integrated into two Australian wheat cultivars and was found to have no significant alterations in their agronomic traits. However, the integration of the Ay subunit showed positive effects in protein and gluten content, protein composition, dough mixing properties, and Zeleny sedimentation values [67]. In 2019, scholars reported that expression of the gene encoding 1Ay21* has the potential to simultaneously increase protein content and grain yield under certain environment [68]. Thus, the active Glu-1Ay allele might be of potential value in breeding aiming to improve wheat flour quality.

2.2.2. Progress on the Bx7 Gene

Among various kinds of alleles, researchers discovered a unique Glu-B1al allele encoding overexpression of 1Bx7 (Bx7OE). This allele is highly associated with improved dough strength, which has been found in many cultivars and landraces [69,70,71,72,73]. However, an Australian cultivar H45, though confirmed to overexpress Bx7 subunits, had relatively low un-extractable polymeric gluten (an indicator of weak dough), the corresponding allele of which was then designated as Glu-B1br [74].
Compared to the gene encoding normal 1Bx7 subunits, the gene encoding 1Bx7OE shows an 18 bp nucleotide duplication in the coding region and a 43 bp insertion in the matrix-attachment region (MAR) upstream to the gene promoter [75,76]. However, evidence indicated that these 18- and 43-bp sequence insertions are not associated with the high expression levels of 1Bx7 because the 18- and 43-bp indels were also found in accessions other than Bx7OE [77]. There is also evidence that the Glu-B1al allele includes two copies of its x-type glutenin gene [71]. Later, by sequencing a bacterial artificial chromosome (BAC) clone encompassing the Glu-B1 locus, scholars reported a 10.3-kb segmental duplication including the Bx7 gene and a flanking long terminal repeat (LTR) retroelement [78]. Meanwhile, according to research collecting a large amount of diploid, tetraploid, and hexaploid accessions, the LTR retroelement/duplication genomic structure was not found in accessions without Bx7 overexpression. These results indicated that gene duplication at the Glu-B1 locus mediated by insertion of a retroelement may lead to overexpression of the Bx7 subunits [77].

3. Structures of HMW-GS

3.1. The Primary Structures

The mature HMW-GSs consist of three structural domains: a nonrepetitive N-terminal domain comprising approximately 81–104 residues and a C-terminal domain of 42 residues, flanking a repetitive central domain with 481 to 872 residues [79]. The repetitive central domain, as the largest part of HMW-GS, is identified by three types of primary repeat units in the x-type subunits and two types of primary repeat units in the y-type subunits. In the x-type subunits, the repeat units are the tripeptides (GQQ), hexapeptides (PGQGQQ), and nonapeptides (GYYPTSPQQ). In the y-type subunits, the repeat units are the hexapeptides (PGQGQQ) and nonapeptides (GYYPTSLQQ) [80,81,82]. Note that the tripeptide and hexapeptides of the x-type subunit are always present in tandem with each other [83]. While the N- and C-terminal regions are quite conservative, variations in the central repetitive domain, particularly the number of tripeptides and hexapeptides, are the main causes of differences in subunit size [79,82,84,85]. Meanwhile, as indicated by the amino acid composition, the central repetitive domain exhibited hydrophilic properties while the N-terminal and C-terminal domain exhibited hydrophobic characteristics [81,82]. A recent study shows that the central repetitive domain could be folded in the action of wheat protein disulfide isomerase, which serves as the basis of dough extension [86].

3.2. Cysteine Residues and Disulfide Bonds

The distribution of cysteine residues in typical x-type and y-type subunits are shown in Figure 3. In general, most x-type subunits contain four cysteines, three in the N-terminal domain and one in the C-terminal domain [31,82]. The 1Dx5 subunit contains an additional cysteine at the beginning of the repetitive domain, while the 1Bx14 and 1Bx20 subunits contain only two cysteine residues, one in the N-terminal region and the other in the C-terminal domain [87,88,89,90,91]. A typical y-type subunit contains seven cysteines: five in N-terminal domains, one in the central repetitive domain, and one in the C-terminal domain [22,31]. Cysteine residues in the central domain of all y-type subunits usually do not exist in the x-type subunits.
Though cysteines are less abundant in HMW-GS, they are extremely crucial to the structure and functions of gluten [92]. Cysteines in the HMW-GSs form either intrachain disulfide bonds or interchain disulfide bonds with other HMW-GSs or LMW-GSs through oxidation, e.g., by catalysis of wheat protein disulfide isomerase [6,83,93,94]. In general, the HMW-GS acts as the “chain extender” of the gluten network owing to the fact that, in most cases, each HMW-GS can provide at least two cysteines participating in the formation of interchain disulfide bonds to form larger gluten aggregates, and it can be further improved by the addition of a so-called flour improver, which are oxidants in nature (e.g., azodicarbonamide and ascorbic acid) [8,95]. According to a structural model for wheat gluten, the HMW-GS provides a disulfide-bonded backbone which forms the basis for “branches” of LMW-GS linked by interchain disulfide bonds and interacts with gliadins by noncovalent interactions [96]. In addition, interchain disulfide bonds play an important role in stabilizing HMW-GS polymers [97]. For these contributing to gluten formation, the disulfides bonds are called “rheologically active” and others are “rheologically inactive”, and the former is catalyzed by wheat protein disulfide isomerase [98]. In FT-Raman Spectroscopy, the band appearing at 497 cm−1 is related to the interchain disulfide bond. Studies have shown that the content of interchain disulfide bond is positively associated with dough properties [99,100,101]. However, up to now, interchain bonds related to HMW-GS extracted from gluten have only been found: (1) between cysteines in a y-type HMW-GS N-terminal domain and the corresponding residue of another y-type HMW-GS, which are connected in parallel; (2) between the cysteine of a y-type HMW-GS repetitive central domain and a cysteine in LMW-GS; (3) and between the additional cysteine of 1Dx5 and the cysteine of an x-type HMW-GS C-terminal domain. Intrachain disulfide bonds related to HMW-GS extracted from gluten have only been between the adjacent cysteines of the N-terminal domain of 1Bx7, which is in line with a molecular model [102,103,104,105]. Other scholars have also proposed two possible patterns of disulfide bond formation according to the homology modeling and molecular dynamics simulations of the N-terminal domain of 1Dy10 [106]. Later in 2017, disulfide linkages in a recombinant N-terminal domain of 1Dx5 (1Dx5-N), which contains three cysteine residues (Cys10, Cys25, and Cys40), were dissected by site-directed mutagenesis and liquid chromatograph-mass spectrometer/mass spectrometry (LC-MS/MS). According to the LC-MS/MS results, intermolecular linkages were found in many combinations among Cys10, Cys25, and Cys40, indicating that the disulfide linkages between Cys10, Cys25, and Cys40 were not conserved strictly. Meanwhile, it was identified that Cys10 and Cys40 were the active sites for intermolecular linkages and that intramolecular linkages were only found between Cys25 and Cys40, which is contradictory to a molecular model of 1Dx5-N with no formation of intramolecular disulfide bonds by prediction [105,107]. Besides, the addition of 1Dx5-N greatly enhanced the formation of a gluten network through disulfide bonds cross-linking and hydrophobic interactions, which exerted a synergistic effect and thus contributed to the superior improvement in dough qualities [108].
It has been reported that, in most cases, HMW-GSs with additional or less cysteines were supposed to give rise to relatively higher or poorer qualities. The additional cysteine in 1Dx5, which might form another interchain bond, is supposed to be responsible for the superior bread properties exhibited in cultivars expressing 1Dx5 subunits [101,103,109]. As for HMW-GSs with less cysteine residues, scholars compared the effects of 1Bx20 subunit with two cysteine residues versus subunit 1Bx7 containing four cysteine residues and discovered that the wheat line carrying a 1Bx20 subunit exhibited less large glutenin polymer formation and poorer mixographic parameters [110]. Similar results have been obtained that incorporation of 1Bx20 subunits to base flour only resulted in small effects, either positive or negative, on dough strength and stability [25]. Meanwhile, 1Bx14*, which contains only two cysteine residues resulting in less formation of intermolecular disulfide bonds, is suggested to be partially the reason of poor milling quality [111]. These experiments fully demonstrated a role of the number of cysteine residues in determining the formation of glutenin polymers and subsequent rheology parameters of dough.
In addition to cysteine, glutathione (GSH), which is naturally present in wheat flour, also plays a critical role in polymerization. GSH contains one cysteine and can easily be oxidized to form GSSG or protein bound glutathione (PSSG, Equation (1)) [112].
GSH + PSSP → PSSG + PSH
That is to say, GSH may cleave the SS bonds of glutenin polymers and promote free cysteine formation, resulting in the trigger of SH/SS interchange reactions. Meanwhile, GSSG reacts with free sulfhydryl groups of aggregated glutenins during polymerization and generates PSSG. Finally, the average molecular weight of gluten network proteins decreases and dough softening occurs [112,113].

3.3. Secondary Structures of HMW-GS

The N- and C-terminal domains are both considered to be rich in α-helixes [114,115]. As for the central repetitive domains, β-reverse turns were initially proposed to be the dominant structural feature, as supported by the circular dichroism (CD) and Fourier transform infrared spectra (FTIR) study of synthetic peptides designed with the consensus peptides PGQGQQ and GYYPTSPQQ of HMW-GS [80,115,116,117]. These regularly repeated β-turns in the HMW-GS were organized into a β-spiral structure, supported by scanning tunneling microscopy images of 1Dx5 [116,118,119,120]. Analyses of the data from viscometric and small angle X-ray scattering also indicated that the structure of both reduced (no formation of disulfide bond) and alkylated HMW-GS are rod-shaped [119,120]. Despite β-turns, FTIR of HMW-GS in the hydrated solid state also indicated the presence of intermolecular β-sheet structures owing to the formation of extensive hydrogen bonds, which may be promoted by the N- and C-terminal domains [114,119,120]. The content of β-sheets was reported to change according to water content and temperature [121,122].
Although interchain disulfide bonds are crucial for stabilizing the HMW-GS polymers, nuclear magnetic resonance (NMR) studies indicate that hydrogen bonds mediated by glutamine side chains may also play an important role in stabilizing the gluten structure [121]. A “loop and train” model has been proposed for the contribution of such hydrogen bonding to gluten elasticity, in which HMW-GS has unbonded mobile regions (loops) and bonded regions (trains) at intermediate moisture contents [123]. The loops can be stretched, and when the stress is removed, reestablishment of the loop-train equilibrium provides the elastic restoring force; as a result, extension of the dough will result in stretching of the “loops” and “unzipping” of the “trains” [10]. The formation of interchain hydrogen bonds between glutamine residues may account for this observation as well [124,125]. Later, this model was further supported by many studies. NMR experiments showed that some parts of a purified HMW-GS chain were held in a much less mobile state, even at higher water contents [121]. According to the carbon and proton solid-state NMR study, regions rich in glutamine and glycine residues may form more mobile (or loop) parts of the network whereas regions containing high amount of hydrophobic residues intermingled with glutamines residues may form the junction zones (trains) [126]. In addition, the ratio of these “loops” and “trains” vary with the hydration level and with the length as well as sequence of the repetitive domain [121,127,128]. As the hydration level increases, the system is plasticized, allowing the orientation of β-turns in adjacent β-spirals to form structures that resemble an “interchain” β-sheet. Further extension will disrupt these “trains”, while release from the extension will result in reformation of the equilibrium balance, resulting in elastic recoil. Support for this hypothesis comes from a study in which changes in gluten-protein conformation were determined by FTIR spectroscopy during protein deformation [128].

4. Relationship to End Use Qualities

It has been reported that different HMW-GSs affect the proportion of gluten secondary structures, and higher contents of β-sheets and β-turns of gluten are generally considered to be associated with better dough qualities [101,108,122,129]. A near-isogenic line with the highest content of β-turns was reported to yield the greatest dough viscoelasticity, while another with the highest content of β-sheets exhibited the greatest wheat dough strength. Meanwhile, it was also mentioned that significant differences in the secondary structures of different wheat lines were mainly caused by their HMW-GSs [129]. Similar results from another research reported that the proportion of secondary structure of gluten in three wheat near-isogenic lines mainly resulted from the different HMW-GS compositions encoded by Glu-A1 and Glu-D1 loci and that the content of β-sheets in gluten has a significant relationship with dough rheological properties [101]. Compared with the normal Bx7 subunits, Bx7OE subunits of a wheat near-isogenic line were also reported to yield increased content of β-sheets in gluten secondary structure and were related to superior dough rheological properties [130]. Besides, HMW-GSs with higher content of β-strands, indicated by secondary structure prediction, may be helpful to form a better gluten structure [131]. A longer repetitive domain or a higher proportion of repeats units of HMW-GSs may produce more β-turns, which confer elasticity to the polymers and are supposed to be positively related to dough and bread-making qualities [33,132,133,134,135,136].
Currently, scholars hold different views on the effect of α-helixes content on the dough quality. Compared with subunits from hexaploid wheat, subunits from TD-256, a cultivar with poor flour quality, possess less α-helixes quantity according to a secondary structure prediction study [111]. This indicated that the α-helixes content of HMW-GSs may exhibit positive effects on dough quality, supported by many other studies [131,133]. However, the content of α-helixes of gluten was reported to be negatively correlated with that of β-sheets, which could be explained by the transformation between α-helixes and β-sheets under certain conditions [122,129]. More α-helixes lead to less β-sheets, and the latter correlates positively with dough quality. Scholars further argue that α-helix content showed a negative correlation with dough quality [122]. In fact, significant correlations were found between the percentage of unextractable polymeric protein and the secondary structures mentioned above, so these secondary structures could be used as indicators for end product quality of dough [137].

5. Conclusions

HMW-GSs of wheat grain play a key role in determining rheological dough properties and end use properties. Both the interchain disulfide bonds and hydrogen bonds mediated by glutamine side chains are crucial for stabilizing the gluten structure. Specific alleles encoding HMW-GSs make greater contributions. In most cases, HMW-GSs with additional or less cysteines were supposed to give rise to relatively more or less formation of interchain disulfide bonds. As for secondary structures, HMW-GSs affect dough qualities by acting on the secondary structures’ composition of gluten. Though cumulative work has been carried out for the relationship between the genetics/structures of HMW-GSs and dough end use qualities, it is essential to explore the mechanism of crosslinking via disulfide bonds among different types of HMW-GS and other gluten components more specifically to establish an accurate model for the role that HMW-GSs play in the dough. The number of cysteine residues, the length of the repetitive domain, and the secondary structure content could be used as predictors to evaluate the quality of novel HMW-GSs for molecular breeding. Meanwhile, more efforts should be made to transfer desirable Glu-1 alleles to cultivated wheat via hybridization and chromosomal engineering approaches.

Author Contributions

Conceptualization, Y.L., J.F., Q.S., and D.Y.; writing—original draft preparation, Y.L. and J.F.; writing—review and editing, Q.S. and D.Y. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the National Natural Science Foundation of China, grant number 31801482; by the National Key Research and Development Program of China, grant number 2019YFC1605000; and by the National Laboratory of Biomacromolecules, grant number 2018kf09.

Acknowledgments

The authors are grateful to Chih-chen Wang at the Institute of Biophysics, Chinese Academy of Sciences for her support and encouragement in our research.

Conflicts of Interest

The authors declare no conflict of interest.

Abbreviations

HMW-GSHigh-molecular-weight glutenin subunit
SDS-PAGESodium dodecyl sulfate-polyacrylamide gel electrophoresis
LMW-GSLow-molecular-weight glutenin subunit
PCRPolymerase chain reaction
GUSβ-glucuronidase
WisWheat insertion sequence
LTRLong terminal repeat
1Dx5-NN-terminal domain of 1Dx5
LC-MS/MSliquid chromatograph-mass spectrometer/mass spectrometry
GSHglutathione
PSSGprotein bound glutathione
FTIRFourier transform infrared spectroscopy
NMRNuclear magnetic resonance

References

  1. Agricultural Market Information System. Available online: http://www.amis-outlook.org/#jfmulticontent_c363419-2 (accessed on 8 October 2020).
  2. Organisation for Economic Co-operation and Development and Food and Agriculture Organization of United Nations Agricultural Outlook 2019–2028. Available online: https://stats.oecd.org/viewhtml.aspx?datasetcode=HIGH_AGLINK_2019&lang=en# (accessed on 16 July 2019).
  3. Anjum, F.M.; Khan, M.R.; Din, A.; Saeed, M.; Pasha, I.; Arshad, M.U. Wheat Gluten: High Molecular Weight Glutenin Subunits–Structure, Genetics, and Relation to Dough Elasticity. J. Food Sci. 2007, 72, R56–R63. [Google Scholar] [CrossRef] [PubMed]
  4. Osborne, T.B. The Vegetable Proteins, 2nd ed.; Longmans Green and Co.: London, UK, 1924. [Google Scholar]
  5. MacRitchie, F. Evaluation of Contributions from Wheat Protein Fractions to Dough Mixing and Breadmaking. J. Cereal Sci. 1987, 6, 259–268. [Google Scholar] [CrossRef]
  6. MacRitchie, F. Physicochemical properties of wheat proteins in relation to functionality. Adv. Food Nutr. Res. 1992, 36, 1–87. [Google Scholar]
  7. Weegels, P.L.; Hamer, R.J.; Schofield, J.D. Functional Properties of Wheat Glutenin. J. Cereal Sci. 1996, 23, 1–18. [Google Scholar] [CrossRef]
  8. Wieser, H. Chemistry of gluten proteins. Food Microbiol. 2007, 24, 115–119. [Google Scholar] [CrossRef] [PubMed]
  9. Lambourne, J.; Tosi, P.; Marsh, J.; Bhandari, D.; Green, R.; Frazier, R.; Shewry, P.R. Characterisation of an s-type low molecular weight glutenin subunit of wheat and its proline and glutamine-rich repetitive domain. J. Cereal Sci. 2010, 51, 96–104. [Google Scholar] [CrossRef]
  10. Belton, P.S. Mini review: On the Elasticity of Wheat Gluten. J. Cereal Sci. 1999, 29, 103–107. [Google Scholar] [CrossRef]
  11. D’Oovidio, R. The low-molecular-weight glutenin subunits of wheat gluten. J. Cereal Sci. 2004, 39, 321–339. [Google Scholar] [CrossRef]
  12. Zhang, Q.; Dong, Y.M.; An, X.L.; Wang, A.; Zhang, Y.Z.; Li, X.H.; Gao, L.Y.; Xia, X.C.; He, Z.H.; Yan, Y.M. Characterization of HMW glutenin subunits in common wheat and related species by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI-TOF-MS). J. Cereal Sci. 2008, 47, 252–261. [Google Scholar] [CrossRef]
  13. Liu, L.; Wang, A.L.; Appels, R.; Ma, J.H.; Xia, X.C.; Lan, P.; He, Z.H.; Bekes, F.; Yan, Y.M.; Ma, W.J. A MALDI-TOF based analysis of high molecular weight glutenin subunits for wheat breeding. J. Cereal Sci. 2009, 50, 295–301. [Google Scholar] [CrossRef] [Green Version]
  14. Peng, Y.C.; Yu, K.; Zhang, Y.J.; Islam, S.; Sun, D.F.; Ma, W.J. Two novel y-type high molecular weight glutenin genes in Chinese wheat landraces of the Yangtze-River region. PLoS ONE 2015, 10, e0142348. [Google Scholar] [CrossRef] [PubMed]
  15. Bietz, J.A.; Shepherd, K.W.; Wall, J.S. Single-kernel analysis of glutenin: Use in wheat genetics and breeding. Cereal Chem. 1975, 52, 513–532. [Google Scholar]
  16. Payne, P.I.; Nightingale, M.A.; Krattiger, A.F.; Holt, L.M. The relationship between HMW glutenin subunit composition and the bread-making quality of British-grown wheat varieties. J. Sci. Food Agric. 1987, 40, 51–65. [Google Scholar] [CrossRef]
  17. Payne, P.I.; Holt, L.M.; Jackson, E.A.; Law, C. Wheat storage proteins: Their genetics and their potential for manipulation by plant breeding. Philos. Trans. R. Soc. Lond. B Biol. Sci. 1984, 304, 359–371. [Google Scholar]
  18. Lawrence, G.J.; Shepherd, K.W. Chromosomal location of genes controlling seed proteins in species related to wheat. Theor. Appl. Genet. 1981, 59, 25–31. [Google Scholar] [CrossRef]
  19. Payne, P.I.; Corfield, K.G.; Holt, L.M.; Blackman, J.A. Correlations between the inheritance of certain high-molecular weight subunits of glutenin and bread-making quality in progenies of six crosses of bread wheat. J. Sci. Food Agric. 1981, 32, 51–60. [Google Scholar] [CrossRef]
  20. Payne, P.I.; Holt, L.M.; Lawrence, G.J.; Law, C.N. The genetics of gliadin and glutenin, the major storage proteins of the wheat endosperm. Plant Foods Hum. Nutr. 1982, 31, 229–241. [Google Scholar] [CrossRef]
  21. Shewry, P.R.; Lafiandra, D.; Tamás, L.; Békés, F. Genetic manipulation of gluten structure and function. In Gliadin and Glutenin the Unique Balance of Wheat Quality; Wrigley, C., Békés, F., Bushuk, W., Eds.; American Association of Cereal Chemists, Inc. (AACC): St. Paul, MN, USA, 2006; pp. 363–385. [Google Scholar]
  22. Thompson, R.D.; Bartels, D.; Harberd, N.P. Nucleotide sequence of a gene from chromosome 1D of wheat encoding a HMW-glutenin subunit. Nucleic Acids Res. 1985, 13, 6833–6846. [Google Scholar] [CrossRef] [Green Version]
  23. Halford, N.G.; Forde, J.; Anderson, O.D.; Greene, F.C.; Shewry, P.R. The nucleotide and deduced amino acid sequences of an HMW glutenin subunit gene from chromosome 1B of bread wheat (Triticum aestivum L.) and comparison with those of genes from chromosomes 1A and 1D. Theor. Appl. Genet. 1987, 75, 117–126. [Google Scholar] [CrossRef]
  24. Payne, P.I.; Lawrence, G.J. Catalogue of alleles for the complex gene loci, Glu-A1, Glu-B1, and Glu-D1 which code for high-molecular-weight subunits of glutenin in hexaploid wheat. Cereal Res. Comm. 1983, 11, 29–35. [Google Scholar]
  25. Shewry, P.R.; Gilbert, S.M.; Savage, A.W.; Tatham, A.S.; Wan, Y.F.; Belton, P.S.; Wellner, N.; D’Ovidio, R.; Bekes, F.; Halford, N.G. Sequence and properties of HMW subunit 1Bx20 from pasta wheat (Triticum durum) which is associated with poor end use properties. Theor. Appl. Genet. 2003, 106, 744–750. [Google Scholar] [CrossRef] [PubMed]
  26. Wan, Y.; Wang, D.; Shewry, P.R.; Halford, N.G. Isolation and characterization of five novel high molecular weight subunit of glutenin genes from Triticum timopheevi and Aegilops cylindrica. Theor. Appl. Genet. 2002, 104, 828–839. [Google Scholar] [CrossRef] [PubMed]
  27. Liu, Z.; Yan, Z.; Wan, Y.; Liu, K.; Zheng, Y.; Wang, D. Analysis of HMW glutenin subunits and their coding sequences in two diploid Aegilops species. Theor. Appl. Genet. 2003, 106, 1368–1378. [Google Scholar] [CrossRef] [PubMed]
  28. Wang, H.Q.; Zhang, X.Y. An approach for isolating high-molecular-weight glutenin subunit genes using monoclonal antibodies. Genome 2006, 49, 181–189. [Google Scholar] [CrossRef]
  29. McIntosh, R.A.; Yamazaki, Y.; Devos, K.M.; Dubcovsky, J.; Rogers, W.J.; Appels, R. Catalogue of gene symbols for wheat. In Proceedings of the 10th International Wheat Genetics Symposium, SIMI, Rome, Italy, 1–6 September 2003. [Google Scholar]
  30. Bekes, F.; Cavanagh, C.R.; Martinov, S.; Bushuk, S.; Wrigley, C.W.F. PART II. Composition table for the HMW subunits of glutenin. In The Gluten Composition of Wheat Varieties and Genotypes; AACC International: St. Paul, MN, USA, 2008. [Google Scholar]
  31. Li, X.; Liu, D.C.; Sun, J.Z.; Yang, W.L.; Guo, X.L.; Wang, D.W.; Zhang, A.M. Characterization of novel high-molecular-weight glutenin subunits and their coding sequences in Aegilops markgrafii. J. Cereal Sci. 2015, 65, 9–18. [Google Scholar] [CrossRef]
  32. Du, X.; Zhang, X. Molecular cloning and functional characterization of two novel high molecular weight glutenin subunit genes in Aegilops markgrafii. J. Genet. 2017, 96, 563–570. [Google Scholar] [CrossRef]
  33. Hou, W.Q.; Feng, W.; Yu, G.H.; Du, X.Y.; Ren, M.J. Cloning and functional analysis of a novel x-type high-molecular-weight glutenin subunit with altered cysteine residues from Aegilops umbellulata. Crop Pasture Sci. 2017, 68, 409–414. [Google Scholar] [CrossRef]
  34. Hu, J.X.; Wang, J.; Deng, X.; Yan, Y.M. Cloning and characterization of special HMW glutenin subunit genes from Aegilops longissima L. and their potential for wheat quality improvement. 3 Biotech 2019, 9, 267. [Google Scholar] [CrossRef]
  35. Wang, H.J.; Zhang, H.J.; Li, B.; Yu, Z.H.; Li, G.R.; Zhang, J.; Yang, Z.J. Molecular cytogenetic characterization of new wheat—Dasypyrum breviaristatum introgression lines for improving grain quality of wheat. Front. Plant Sci. 2018, 9, 365. [Google Scholar] [CrossRef]
  36. Du, X.Y.; Jia, Z.; Yu, Y.; Wang, S.; Che, B.J.; Ni, F.; Bao, Y.G. A wheat-Aegilops umbellulata addition line improves wheat agronomic traits and processing quality. Breeding Sci. 2019, 69, 503–507. [Google Scholar] [CrossRef] [Green Version]
  37. Yang, Y.H.; Li, S.M.; Zhang, K.P.; Dong, Z.Y.; Li, Y.W.; An, X.L.; Chen, J.; Chen, Q.F.; Jiao, Z.; Liu, X.; et al. Efficient isolation of ion beam-induced mutants for homoeologous loci in common wheat and comparison of the contributions of Glu-1 loci to gluten functionality. Theor. Appl. Genet. 2014, 127, 359–372. [Google Scholar] [CrossRef] [PubMed]
  38. Lawrence, G.J.; MacRitchie, F.; Wrigley, C.W. Dough and baking quality of wheat lines deficient in glutenin subunits controlled by the Glu-A1, Glu-B1 and Glu-D1 loci. J. Cereal Sci. 1988, 7, 109–112. [Google Scholar] [CrossRef]
  39. Zhang, L.J.; Chen, Q.F.; Su, M.J.; Yan, B.; Zhang, X.Q.; Jiao, Z. High-molecular-weight glutenin subunit-deficient mutants induced by ion beam and the effects of Glu-1 loci deletion on wheat quality properties. J. Food Sci. Agric. 2015, 96, 1289–1296. [Google Scholar] [CrossRef] [PubMed]
  40. Jiang, P.H.; Xue, J.S.; Duan, L.N.; Gu, Y.S.; Mu, J.Y.; Han, S.C.; Chen, L.; Li, Y.X.; Ma, W.J.; Yan, Y.M.; et al. Effects of high-molecular-weight glutenin subunit combination in common wheat on the quality of crumb structure. J. Sci. Food Agric. 2019, 99, 1501–1508. [Google Scholar] [CrossRef] [PubMed]
  41. Brönneke, V.; Zimmermann, G.; Killermann, B. Effect of high molecular weight glutenins and D-zone gliadins on bread-making quality in German wheat varieties. Cereal Res. Commun. 2000, 28, 187–194. [Google Scholar] [CrossRef]
  42. Liu, H.Y.; Wang, K.; Xiao, L.L.; Wang, S.L.; Du, L.P.; Cao, X.Y.; Zhang, X.X.; Zhou, Y.; Yan, Y.M.; Ye, X.G. Comprehensive identification and bread-making quality evaluation of common wheat somatic variation line AS208 on glutenin composition. PLoS ONE 2016, 11, e0146933. [Google Scholar] [CrossRef] [Green Version]
  43. Wang, Z.J.; Li, Y.W.; Yang, Y.H.; Liu, X.; Qin, H.J.; Dong, Z.Y.; Zheng, S.H.; Zhang, K.P.; Wang, D.W. New insight into the function of wheat glutenin proteins as investigated with two series of genetic mutants. Sci. Rep. 2017, 7, 1–14. [Google Scholar] [CrossRef] [Green Version]
  44. Gao, X.; Liu, T.H.; Ding, M.Y.; Wang, J.; Li, C.L.; Wang, Z.H.; Li, X.J. Effects of HMW-GS Ax1 or Dx2 absence on the glutenin polymerization and gluten micro structure of wheat (Triticum aestivum L.). Food Chem. 2018, 240, 626–633. [Google Scholar] [CrossRef]
  45. Song, L.J.; Li, L.Q.; Zhao, L.Y.; Liu, Z.Z.; Xie, T.T.; Li, X.J. Absence of Dx2 at Glu-D1 locus weakens gluten quality potentially regulated by expression of nitrogen metabolism enzymes and glutenin-related genes in wheat. Int. J. Mol. Sci. 2020, 21, 1383. [Google Scholar] [CrossRef] [Green Version]
  46. Chen, H.Q.; Li, S.J.; Liu, Y.W.; Liu, J.X.; Ma, X.L.; Du, L.P.; Wang, K.; Ye, X.G. Effects of 1Dy12 subunit silencing on seed storage protein accumulation and flour-processing quality in a common wheat somatic variation line. Food Chem. 2021, 335, 127663. [Google Scholar] [CrossRef]
  47. Duan, L.N.; Han, S.C.; Wang, K.; Jiang, P.H.; Gu, Y.S.; Chen, L.; Mu, J.Y.; Ye, X.G.; Li, Y.X.; Yan, Y.M.; et al. Analyzing the action of evolutionarily conserved modules on HMW-GS 1Ax1 promoter activity. Plant Mol. Biol. 2019, 102, 225–237. [Google Scholar] [CrossRef] [PubMed]
  48. Wang, K.; Zhang, X.; Zhao, Y.; Chen, F.G.; Xia, G.M. Structure, variation and expression analysis of glutenin gene promoters from Triticum aestivum cultivar Chinese Spring shows the distal region of promoter 1Bx7 is key regulatory sequence. Gene 2013, 527, 484–490. [Google Scholar] [CrossRef] [PubMed]
  49. Ravel, C.; Fiquet, S.; Boudet, J.; Dardevet, M.; Vincent, J.; Merlino, M.; Michard, R.; Martre, P. Conserved cis-regulatory modules in promoters of genes encoding wheat high-molecular-weight glutenin subunits. Front. Plant Sci. 2014, 5, 621. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  50. Makai, S.; Éva, C.; Tamás, L.; Juhász, A. Multiple elements controlling the expression of wheat high molecular weight glutenin paralogs. Funct. Integr. Genomics 2015, 15, 661–672. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  51. Albani, D.; Hammond-Kosack, M.C.; Smith, C.; Conlan, S.; Colot, V.; Holdsworth, M.; Bevan, M.W. The Wheat Transcriptional Activator SPA: A Seed-Specific bZIP Protein That Recognizes the GCN4-like Motif in the Bifactorial Endosperm Box of Prolamin Genes. Plant Cell 1997, 9, 171–184. [Google Scholar]
  52. Ravel, C.; Martre, P.; Romeuf, I.; Dardevet, M.; El-Malki, R.; Bordes, J.; Duchateau, N.; Brunel, D.; Balfourier, F.; Charmet, G. Nucleotide polymorphism in the wheat transcriptional activator Spa influences its pattern of expression and has pleiotropic effects on grain protein composition, dough viscoelasticity, and grain hardness. Plant Physiol. 2009, 151, 2133–2144. [Google Scholar] [CrossRef] [Green Version]
  53. Kumar, A.; Jaiswal, J.P.; Sharma, N.; Gupta, S.; Kumar, A. Understanding the molecular basis of differential grain protein accumulation in wheat (Triticum aestivum L.) through expression profiling of transcription factors related to seed nutrients storage. 3 Biotech 2018, 8, 112. [Google Scholar] [CrossRef]
  54. Guo, D.D.; Hou, Q.L.; Zhang, R.Q.; Lou, H.Y.; Li, Y.H.; Zhang, Y.F.; You, M.S.; Xie, C.J.; Liang, R.Q.; Li, B.Y. Over-Expressing TaSPA-B Reduces Prolamin and Starch Accumulation in Wheat (Triticum aestivum L.) Grains. Int. J. Mol. Sci. 2020, 21, 3257. [Google Scholar] [CrossRef]
  55. Boudet, J.; Merlino, M.; Plessis, A.; Gaudin, J.C.; Dardevet, M.; Perrochon, S.; Alvarez, D.; Risacher, T.; Martre, P.; Ravel, C. The bZIP transcription factor SPA Heterodimerizing Protein represses glutenin synthesis in Triticum aestivum. Plant J. 2019, 97, 858–871. [Google Scholar] [CrossRef] [Green Version]
  56. Johansson, E.; Henriksson, P.; Svensson, G.; Heneen, W. Detection, chromosomal location and evaluation of the functional value of a novel high Mr glutenin subunit found in Swedish wheats. J. Cereal Sci. 1993, 17, 237–245. [Google Scholar] [CrossRef]
  57. Margiotta, B.; Urbano, M.; Colaprico, G.; Johansson, E.; Buonocore, F.; D’Ovidio, R.; Lafiandra, D. Detection of y-type subunit at the Glu-A1 locus in some Swedish bread wheat lines. J. Cereal Sci. 1996, 23, 203–212. [Google Scholar] [CrossRef]
  58. Anjum, F.M.; Lookhart, G.L.; Walker, C.E. Electrophoretic identification of hard white spring wheats grown at different locations in Pakistan in different years. J. Sci. Food Agric. 2000, 80, 1155–1161. [Google Scholar] [CrossRef]
  59. Ciaffi, M.; Lafiandra, D.; Porceddu, E.; Benedettelli, S. Storage-protein variation in wild emmer wheat (Triticum turgidum ssp. dicoccoides) from Jordan and Turkey. I. Electrophoretic characterization of genotypes. Theor. Appl. Genet. 1993, 86, 474–480. [Google Scholar]
  60. Jiang, Q.T.; Ma, J.; Zhao, S.; Zhao, Q.Z.; Lan, X.J.; Dai, S.F.; Lu, Z.X.; Zheng, Y.L.; Wei, Y.M. Characterization of HMW-GSs and their gene inaction in tetraploid wheat. Genetica 2012, 140, 325–335. [Google Scholar] [CrossRef] [PubMed]
  61. Luo, G.B.; Song, S.Y.; Zhao, L.R.; Shen, L.S.; Song, Y.H.; Wang, X.; Yu, K.; Liu, Z.Y.; Li, Y.W.; Yang, W.L. Mechanisms, origin and heredity of Glu-1Ay silencing in wheat evolution and domestication. Theor. Appl. Genet. 2018, 131, 1561–1575. [Google Scholar] [CrossRef] [PubMed]
  62. Harberd, N.P.; Flavell, R.B.; Thompson, R.D. Identification of a transposon-like insertion in a Glu-1 allele of wheat. Mol. Gen. Genet. 1987, 209, 326–332. [Google Scholar] [CrossRef] [PubMed]
  63. Sun, M.M.; Yan, Y.M.; Jiang, Y.; Xiao, Y.H.; Hu, Y.K.; Cai, M.H.; Li, Y.X.; Hsam, S.L.K.; Zeller, F.J. Molecular cloning and comparative analysis of a y-type inactive HMW glutenin subunit gene from cultivated emmer wheat (Triticum dicoccum L.). Hereditas 2004, 141, 46–54. [Google Scholar] [CrossRef]
  64. Jiang, Q.T.; Wei, Y.M.; Wang, F.; Wang, J.R.; Yan, Z.H.; Zheng, Y.L. Characterization and comparative analysis of HMW glutenin 1Ay alleles with differential expressions. BMC Plant Biol. 2009, 9, 16. [Google Scholar] [CrossRef] [Green Version]
  65. Gu, Y.Q.; Coleman-Derr, D.; Kong, X.Y.; Anderson, O.D. Rapid genome evolution revealed by comparative sequence analysis of orthologous regions from four triticeae genomes. Plant Physiol. 2004, 135, 459–470. [Google Scholar] [CrossRef] [Green Version]
  66. Wang, Z.Z.; Huang, L.; Wu, B.H.; Hu, J.L.; Jiang, Z.L.; Qi, P.F.; Zheng, Y.L.; Liu, D.C. Characterization of an Integrated Active Glu-1Ay Allele in Common Wheat from Wild Emmer and Its Potential Role in Flour Improvement. Int. J. Mol. Sci. 2018, 19, 923. [Google Scholar] [CrossRef] [Green Version]
  67. Roy, N.; Islam, S.; Ma, J.; Lu, M.; Torok, K.; Tomoskozi, S.; Bekes, F.; Lafiandra, D.; Appels, R.; Ma, W.J. Expressed Ay HMW glutenin subunit in Australian wheat cultivars indicates a positive effect on wheat quality. J. Cereal Sci. 2017, 79, 494–500. [Google Scholar] [CrossRef]
  68. Roy, N.; Islam, S.; Yu, Z.T.; Lu, M.Q.; Lafiandra, D.; Zhao, Y.; Anwar, M.; Mayer, J.E.; Ma, W.J. Introgression of an expressed HMW 1Ay glutenin subunit allele into bread wheat cv. Lincoln increases grain protein content and breadmaking quality without yield penalty. Theor. Appl. Genet. 2019, 133, 517–528. [Google Scholar] [CrossRef] [PubMed]
  69. Marchylo, B.A.; Lukow, O.M.; Kruger, J.E. Quantitative variation in high molecular weight glutenin subunit 7 in some Canadian wheats. J. Cereal Sci. 1992, 15, 29–37. [Google Scholar] [CrossRef]
  70. Lukow, O.M.; Forsyth, S.A.; Payne, P.I. Over-production of HMW [High Molecular Weight] glutenin subunits coded on chromosome 1B in common wheat—Triticum aestivum [in Israel and Canada]. J. Genet. Breeding Sci. 1992, 46, 187–192. [Google Scholar]
  71. D’Ovidio, R.; Masci, S.; Porceddu1, E.; Kasarda, D.D. Duplication of the Bx7 high-molecular-weight glutenin subunit gene in bread wheat (Triticum aestivum L.) cultivar‘Red River 68’. Plant Breeding 1997, 116, 525–531. [Google Scholar] [CrossRef]
  72. Juhàsz, A.; Larroque, O.R.; Tamas, L.; Hsam, S.L.K.; Zeller, F.J.; Békés, F.; Bedo, Z. Bánkúti 1201-an old Hungarian wheat variety with special storage protein composition. Theor. Appl. Genet. 2003, 107, 697–704. [Google Scholar] [CrossRef]
  73. Radovanovic, N.; Cloutier, S.; Brown, D.; Humphreys, D.G.; Lukow, O.M. Genetic Variance for Gluten Strength Contributed by High Molecular Weight Glutenin Proteins. Cereal Chem. 2002, 79, 843–849. [Google Scholar] [CrossRef]
  74. Gao, X.; Appelbee, M.J.; Mekuria, G.T.; Chalmers, K.J.; Mather, D.E. A second ‘overexpression’ allele at the Glu-B1 high-molecular-weight glutenin locus of wheat: Sequence characterisation and functional effects. Theor. Appl. Genet. 2012, 124, 333–343. [Google Scholar] [CrossRef]
  75. Butow, B.J.; Gras, P.W.; Haraszi, R.; Bekes, F. Effects of different salts on mixing and extension parameters on a diverse group of wheat cultivars using 2-g mixograph and extensigraph methods. Cereal Chem. 2002, 79, 826–833. [Google Scholar] [CrossRef]
  76. Butow, B.J.; Ma, W.; Gale, K.R.; Cornish, G.B.; Rampling, L.; Larroque, O.; Morell, M.K.; Bekes, F. Molecular discrimination of Bx7 alleles demonstrates that a highly expressed high molecular weight glutenin allele has a major impact on wheat flour dough strength. Theor. Appl. Genet. 2003, 107, 1524–1532. [Google Scholar] [CrossRef]
  77. Ragupathy, R.; Naeem, H.A.; Reimer, E.; Lukow, O.M.; Sapirstein, H.D.; Cloutier, S. Evolutionary origin of the segmental duplication encompassing the wheat GLU-B1 locus encoding the overexpressed Bx7 (Bx7OE) high molecular weight glutenin subunit. Theor. Appl. Genet. 2007, 116, 283–296. [Google Scholar] [CrossRef] [PubMed]
  78. Cloutier, S.; Banks, T.; Nilmalgoda, S. Molecular understanding of wheat evolution at the Glu-B1 locus. In Proceedings of the International Conference on Plant Genomics and Biotechnology: Challenges and Opportunities, Raipur, India, 26–28 October 2005; p. 40. [Google Scholar]
  79. Shewry, P.R.; Halford, N.G.; Tatham, A.S. High molecular weight subunits of wheat glutenin. J. Cereal Sci. 1992, 15, 105–120. [Google Scholar] [CrossRef]
  80. Tatham, A.S.; Drake, A.F.; Shewry, P.R. Conformational studies of synthetic peptides corresponding to the repetitive regions of the high molecular weight (HMW) glutenin subunits of wheat. J. Cereal Sci. 1990, 11, 189–200. [Google Scholar] [CrossRef]
  81. Shewry, P.R.; Halford, N.G.; Tatham, A.S. The high molecular weight subunits of wheat, barley and rye: Genetics, molecular biology, chemistry and role in wheat gluten structure and functionality. In Oxford Surveys of Plant and Molecular Cell Biology; Miflin, B.J., Ed.; Oxford University Press: London, UK, 1989; pp. 163–219. [Google Scholar]
  82. Anderson, O.D.; Greene, F.C. The characterization and comparative analysis of high-molecular-weight glutenin genes from genomes A and B of a hexaploid bread wheat. Theor. Appl. Genet. 1989, 77, 689–700. [Google Scholar] [CrossRef] [PubMed]
  83. Shewry, P.R.; Halford, N.G.; Tatham, A.S.; Popineau, Y.; Lafiandra, D.; Belton, P.S. The high molecular weight subunits of wheat glutenin and their role in determining wheat processing properties. Adv. Food Nutr. Res. 2003, 45, 219–302. [Google Scholar] [PubMed]
  84. D’Ovidio, R.; Masci, S.; Porceddu, E. Development of a set of oligonucleotide primers specific for genes at the Glu-1 complex loci of wheat. Theor. Appl. Genet. 1995, 91, 189–194. [Google Scholar] [CrossRef]
  85. Halford, N.G.; Field, J.M.; Blair, H.; Urwin, P.; Moore, K.; Robert, L.; Thompson, R.; Flavell, R.B.; Tatham, A.S.; Shewry, P.R. Analysis of HMW glutenin subunits encoded by chromosome 1A of bread wheat (Triticum aestivum L.) indicates quantitative effects on grain quality. Theor. Appl. Genet. 1992, 83, 373–378. [Google Scholar] [CrossRef]
  86. Gao, J.H.; Yu, P.X.; Liang, H.R.; Fu, J.H.; Luo, Z.Y.; Yang, D. The wPDI Redox Cycle Coupled Conformational Change of the Repetitive Domain of the HMW-GS 1Dx5-A Computational Study. Molecules 2020, 25, 4393. [Google Scholar] [CrossRef]
  87. Anderson, O.D.; Greene, F.C.; Yip, R.E.; Halford, N.G.; Shewry, P.R.; Malpica-Romero, J. Nucleotide sequences of the two high-molecular-weight glutenin genes from the D-genome of a hexaploid bread wheat, Triticum aestivum L. cv Cheyenne. Nucleic Acids Res. 1989, 17, 461–462. [Google Scholar] [CrossRef] [Green Version]
  88. Kasarda, D.D. Glutenin structure in relation to wheat quality. In Wheat is Unique; Pomeranz, Y., Ed.; AACC: St. Paul, MN, USA, 1989; Volume 277, pp. 277–302. [Google Scholar]
  89. Buonocore, F.; Caporale, C.; Lafiandra, D. Purification and Characterisation of High Mr Glutenin Subunit 20 and its Linked y-type Subunit from Durum Wheat. J. Cereal Sci. 1996, 23, 195–201. [Google Scholar] [CrossRef]
  90. Li, W.; Wan, Y.; Liu, Z.; Liu, K.; Liu, X.; Li, B.; Li, Z.; Zhang, X.; Dong, Y.; Wang, D. Molecular characterization of HMW glutenin subunit allele 1Bx14: Further insights into the evolution of Glu-B1-1 alleles in wheat and related species. Theor. Appl. Genet. 2004, 109, 1093–1104. [Google Scholar] [CrossRef] [PubMed]
  91. Tatham, A.S.; Field, J.M.; Keen, J.N.; Jackson, P.J.; Shewry, P.R. Purification and characterization of HMW glutenin subunits encoded by chromosome 1B of durum wheat (Triticum durum). J. Cereal Sci. 1991, 14, 111–116. [Google Scholar] [CrossRef]
  92. Grosch, W.; Wieser, H. Redox Reactions in Wheat Dough as Affected by Ascorbic Acid. J. Cereal Sci. 1999, 29, 1–16. [Google Scholar] [CrossRef]
  93. Wrigley, C.W. Giant proteins with flour power. Nature 1996, 72, 738–739. [Google Scholar] [CrossRef]
  94. Wang, L.; Yu, J.J.; Wang, C.C. Protein disulfide isomerase is regulated in multiple ways: Consequences for conformation, activities, and pathophysiological functions. BioEssays 2020. [Google Scholar] [CrossRef]
  95. Wieser, H. The use of redox agents in breadmaking. In Breadmaking, 2nd ed.; Cauvain, S.P., Ed.; Woodhead Publishing: Sawston, UK, 2012; pp. 447–469. [Google Scholar]
  96. Shewry, P.R.; Popineau, Y.; Lafiandra, D.; Belton, P. Wheat glutenin subunits and dough elasticity: Findings of the EUROWHEAT project. Trends Food Sci. Technol. 2001, 11, 433–441. [Google Scholar] [CrossRef] [Green Version]
  97. Humphris, A.D.L.; McMaster, T.J.; Miles, M.J.; Gilbert, S.M.; Shewry, P.R.; Tatham, A.S. Atomic Force Microscopy (AFM) Study of Interactions of HMW Subunits of Wheat Glutenin. Cereal Chem. 2000, 77, 107–110. [Google Scholar] [CrossRef]
  98. Zhao, C.F.; Luo, Z.Y.; Li, M.Z.; Gao, J.H.; Liang, Z.X.; Sun, S.Y.; Wang, X.; Yang, D. Wheat protein disulfide isomerase improves bread properties via different mechanisms. Food Chem. 2020, 315, 126242. [Google Scholar] [CrossRef]
  99. Lindsay, M.P.; Tamas, L.; Appels, R.; Skerritt, J.H. Direct Evidence that the Number and Location of Cysteine Residues affect Glutenin Polymer Structure. J. Cereal Sci. 2000, 31, 321–333. [Google Scholar] [CrossRef]
  100. Ferrer, E.G.; Gómez, A.V.; Añón, M.C.; Puppo, M.C. Structural changes in gluten protein structure after addition of emulsifier. A Raman spectroscopy study. Spectrochimi. Acta A 2011, 79, 278–281. [Google Scholar] [CrossRef]
  101. Li, X.J.; Liu, T.H.; Song, L.J.; Zhang, H.; Li, L.Q.; Gao, X. Influence of high-molecular-weight glutenin subunit composition at Glu-A1 and Glu-D1 loci on secondary and micro structures of gluten in wheat (Triticum aestivum L.). Food Chem. 2016, 213, 728–734. [Google Scholar] [CrossRef] [PubMed]
  102. Keck, B.; Köhler, P.; Wieser, H. Disulphide bonds in wheat gluten: Cystine peptides derived from gluten proteins following peptic and thermolytic digestion. Z. Lebensm. Unters. F. 1995, 200, 432–439. [Google Scholar] [CrossRef] [PubMed]
  103. Lutz, E.; Wieser, H.; Koehler, P. Identification of disulfide bonds in wheat gluten proteins by means of mass spectrometry/electron transfer dissociation. J. Agric. Food Chem. 2012, 60, 3708–3716. [Google Scholar] [CrossRef] [PubMed]
  104. Köhler, P.; Belitz, H.-D.; Wieser, H. Disulphide bonds in wheat gluten: Further cystine peptides from high molecular weight (HMW) and low molecular weight (LMW) subunits of glutenin and from γ-gliadins. Z. Lebensm. Unters. F. 1993, 196, 239–247. [Google Scholar] [CrossRef] [PubMed]
  105. Köhler, P.; Bettina, K.G.; Wieser, H.; Kasarda, D.D. Molecular Modeling of the N-terminal Regions of High Molecular Weight Glutenin Subunits 7 and 5 in Relation to Intramolecular Disulfide Bond Formation. Cereal Chem. 1997, 74, 154–158. [Google Scholar] [CrossRef]
  106. Cazalis, R.; Aussenac, T.; Rhazi, L.; Marin, A.; Gibrat, J.F. Homology modeling and molecular dynamics simulations of the N-terminal domain of wheat high molecular weight glutenin subunit 10. Protein Sci. 2003, 12, 34–43. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  107. Wang, J.J.; Liu, G.; Huang, Y.B.; Zeng, Q.H.; Hu, S.Q. Dissecting the disulfide linkage of the N-terminal domain of HMW 1Dx5 and its contributions to dough functionality. J. Agric. Food Chem. 2017, 65, 6264. [Google Scholar] [CrossRef]
  108. Wang, J.J.; Liu, G.; Huang, Y.B.; Zeng, Q.H.; Song, G.S.; Hou, Y.; Li, L.; Hu, S.Q. Role of N-terminal domain of HMW 1Dx5 in the functional and structural properties of wheat dough. Food Chem. 2016, 213, 682–690. [Google Scholar] [CrossRef]
  109. Popineau, Y.; Deshayes, G.; Lefebvre, J.; Fido, R.; Tatham, A.S.; Shewry, P.R. Prolamin aggregation, gluten viscoelasticity, and mixing properties of transgenic wheat lines expressing 1Ax and 1Dx high molecular weight glutenin subunit transgenes. J. Agric. Food Chem. 2001, 49, 395–401. [Google Scholar] [CrossRef]
  110. Margiotta, B.; Pfluger, L.; Roth, M.R.; MacRitchie, F.; Lafiandra, D. Isogenic bread wheat lines differing in number and type of high Mr glutenin subunits. In Proceedings of the 7th International Workshop Gluten 2000, Bristol, UK, 2–6 April 2000; pp. 29–33. [Google Scholar]
  111. Zhang, D.L.; He, T.T.; Liang, H.H.; Huang, L.Y.; Su, Y.Z.; Li, Y.G.; Li, S.P. Flour quality and related molecular characterization of high molecular weight glutenin subunit genes from wild emmer wheat accession TD-256. J. Agric. Food Chem. 2016, 64, 5128–5136. [Google Scholar] [CrossRef]
  112. Joye, I.J.; Lagrain, B.; Delcour, J.A. Endogenous redox agents and enzymes that affect protein network formation during breadmaking—A review. J. Cereal Sci. 2009, 50, 1–10. [Google Scholar] [CrossRef]
  113. Li, W.L.; Tsiami, A.A.; Schofield, J.D. Redox Reactions during Dough Mixing and Dough Resting: Effect of Reduced and Oxidised Glutathione and L-Ascorbic Acid on Rheological Properties of Gluten. In Wheat Gluten; Shewry, P.R., Tatham, A.S., Eds.; The Royal Society of Chemistry: Cambridge, UK, 2000; pp. 239–243. [Google Scholar]
  114. Gilbert, S.M.; Wellner, N.; Belton, P.S.; Greenfield, J.A.; Siligardi, G.; Shewry, P.R.; Tatham, A.S. Expression and characterisation of a highly repetitive peptide derived from a wheat seed storage protein. BBA-Protein Struct. Mol. Enzym. 2000, 1479, 135–146. [Google Scholar] [CrossRef]
  115. Tatham, A.S.; Shewry, P.R.; Miflin, B.J. Wheat gluten elasticity: A similar molecular basis to elastin? FEBS Lett. 1984, 177, 205–208. [Google Scholar] [CrossRef] [Green Version]
  116. Tatham, A.S.; Miflin, B.J.; Shewry, P.R. The β-turn conformation in wheat gluten proteins: Relationship to gluten elasticity. Cereal Chem. 1985, 62, 405–412. [Google Scholar]
  117. Van Dijk, A.A.; Van Wijk, L.L.; Van Swieten, E.; Robillard, G.T.; Vliet, A.V.; Tesser, G.I.; Haris, P. Structure characterization of the central repetitive domain of high molecular weight gluten proteins. I. Model studies using cyclic and linear peptides. Protein Sci. 1997, 6, 637–648. [Google Scholar] [CrossRef] [Green Version]
  118. Miles, M.J.; Carr, H.J.; McMaster, T.C.; I’Anson, K.J.; Belton, P.S.; Morris, V.J.; Field, J.M.; Shewry, P.R.; Tatham, A.S. Scanning tunneling microscopy of a wheat seed storage protein reveals details of an unusual supersecondary structure. PNAS 1991, 88, 68–71. [Google Scholar] [CrossRef] [Green Version]
  119. Field, J.M.; Tatham, A.S.; Shewry, P.R. The structure of a high-Mr subunit of durum-wheat (Triticum durum) gluten. Biochem. J. 1987, 247, 215–221. [Google Scholar] [CrossRef] [Green Version]
  120. Matsushima, N.; Danno, G.I.; Sasaki, N.; Izumi, Y. Small-angle X-ray scattering study by synchrotron orbital radiation reveals that high molecular weight subunit of glutenin is a very anisotropic molecule. Biochem. Biophys. Res. Commun. 1992, 186, 1057–1064. [Google Scholar] [CrossRef]
  121. Belton, P.S.; Colquhoun, I.J.; Grant, A.; Wellner, N.; Field, J.M.; Shewry, P.R.; Tatham, A.S. FTIR and NMR studies on the hydration of a high-Mr subunit of glutenin. Int. J. Biol. Macromol. 1995, 17, 74–80. [Google Scholar] [CrossRef]
  122. Georget, D.M.R.; Belton, P.S. Effects of temperature and water content on the secondary structure of wheat gluten studied by FTIR spectroscopy. Biomacromolecules 2006, 7, 469–475. [Google Scholar] [CrossRef]
  123. Belton, P.S. A hypothesis concerning the elasticity of high molecular weight subunits. In Wheat Kernel Proteins: Molecular Functional Aspects; Universita della Tuscia: Viterbo, Italy, 1994; pp. 159–165. [Google Scholar]
  124. Mita, T.; Matsumoto, H. Flow properties of aqueous gluten and gluten methyl ester dispersions. Cereal Chem. 1981, 58, 57–61. [Google Scholar]
  125. Bushuk, W. Interactions in wheat doughs. In The Keys to Cereal Quality; American Assn. of Cereal Chemists: St. Paul, MN, USA, 1998; pp. 1–16. [Google Scholar]
  126. Alberti, E.; Gilbert, S.M.; Tatham, A.S.; Shewry, P.R.; Gil, A.M. Study of high molecular weight wheat glutenin subunit 1Dx5 by 13C and 1H solid-state NMR spectroscopy. I. Role of covalent crosslinking. Biopolymers 2002, 67, 487–498. [Google Scholar] [CrossRef] [PubMed]
  127. Feeney, K.A.; Wellner, N.; Gilbert, S.M.; Halford, N.G.; Tatham, A.S.; Shewry, P.R.; Belton, P.S. Molecular structures and interactions of repetitive peptides based on wheat glutenin subunits depend on chain length. Biopolymers 2003, 72, 123–131. [Google Scholar] [CrossRef] [PubMed]
  128. Wellner, N.; Mills, E.N.C.; Brownsey, G.; Wilson, R.H.; Brown, N.; Freeman, J.; Halford, N.G.; Shewry, P.R.; Belton, P.S. Changes in Protein Secondary Structure during Gluten Deformation Studied by Dynamic Fourier Transform Infrared Spectroscopy. Biomacromolecules 2005, 6, 255–261. [Google Scholar] [CrossRef] [PubMed]
  129. Gao, X.; Liu, T.H.; Yu, J.; Li, L.Q.; Feng, Y.; Li, X.J. Influence of high-molecular-weight glutenin subunit composition at Glu-B1 locus on secondary and micro structures of gluten in wheat (Triticum aestivum L.). Food Chem. 2016, 197, 1184–1190. [Google Scholar] [CrossRef] [PubMed]
  130. Li, S.P.; Liu, Y.C.; Tong, J.Y.; Yu, L.W.; Ding, M.Y.; Zhang, Z.M.; Rehman, A.-u.; Majzoobi, M.; Wang, Z.H.; Gao, X. The overexpression of high-molecular-weight glutenin subunit Bx7 improves the dough rheological properties by altering secondary and micro-structures of wheat gluten. Food Res. Int. 2020, 130, 108914. [Google Scholar] [CrossRef]
  131. Jin, M.; Xie, Z.Z.; Ge, P.; Li, J.; Jiang, S.S.; Subburaj, S.; Li, X.H.; Zeller, F.J.; Hsam, S.L.K.; Yan, Y.M. Identification and molecular characterisation of HMW glutenin subunit 1By16* in wild emmer. J. Appl. Genet. 2012, 53, 249–258. [Google Scholar] [CrossRef]
  132. Flavell, R.B.; Goldsbrough, A.P.; Robert, L.S.; Schnick, D.; Thompson, R.D. Genetic variation in wheat HMW glutenin subunits and the molecular basis of bread-making quality. Bio/Technology 1989, 7, 1281–1285. [Google Scholar] [CrossRef]
  133. Wang, K.; An, X.L.; Pan, L.P.; Dong, K.; Gao, L.Y.; Wang, S.L.; Xie, Z.Z.; Zhang, Z.; Appels, R.; Ma, W.; et al. Molecular characterization of HMW-GS 1Dx3t and 1Dx4t genes from Aegilops tauschii and their potential value for wheat quality improvement. Hereditas 2012, 149, 41–49. [Google Scholar] [CrossRef]
  134. Wang, S.; Yu, Z.T.; Cao, M.; Shen, X.X.; Li, N.; Li, X.H.; Ma, W.J.; Weißgerber, H.; Zeller, F.; Hsam, S.; et al. Molecular mechanisms of HMW glutenin subunits from 1Sl genome of Aegilops longissima positively affecting wheat breadmaking quality. PLoS ONE 2013, 8, e58947. [Google Scholar] [CrossRef] [Green Version]
  135. Gianibelli, M.C.; Larroque, O.R.; MacRitchie, F.; Wrigley, C.W. Biochemical, Genetic, and Molecular Characterization of Wheat Glutenin and Its Component Subunits. Cereal Chem. 2001, 78, 635–646. [Google Scholar] [CrossRef]
  136. Li, X.Y.; Li, Y.; Karim, H.; Li, Y.; Zhong, X.J.; Tang, H.P.; Qi, P.F.; Ma, J.; Wang, J.R.; Chen, G.Y.; et al. The production of wheat-Aegilops sharonensis 1Ssh chromosome substitution lines harboring alien novel high-molecular-weight glutenin subunits. Genome 2019, 63, 155–167. [Google Scholar] [CrossRef] [PubMed]
  137. Liu, T.; Gao, X.; Li, L.; Du, D.; Cheng, X.; Zhao, Y.; Liu, Y.; Li, X. Effects of HMW-GS at Glu-B1 locus on the polymerization of glutenin during grain development and on the secondary and micro-structures of gluten in wheat (Triticum aestivum L.). J. Cereal Sci. 2016, 72, 101–107. [Google Scholar] [CrossRef]
Ijms 22 00184 g001 550
Figure 1. Schematic diagram of the gene loci of a high-molecular-weight glutenin subunit (HMW-GS) in wheat chromosome 1: the genes coding the synthesis of HMW-GS are located on the long arms of group 1 chromosomes 1A, 1B, and 1D.
Figure 1. Schematic diagram of the gene loci of a high-molecular-weight glutenin subunit (HMW-GS) in wheat chromosome 1: the genes coding the synthesis of HMW-GS are located on the long arms of group 1 chromosomes 1A, 1B, and 1D.
Ijms 22 00184 g001
Ijms 22 00184 g002 550
Figure 2. “*” indicates identical amino acid residues, “꞉” indicates similar amino acid residues, and “ꞏ” indicates less similar amino acid residues. Yellow indicates amino acid residues G, P, C, H, Y; red indicates amino acid residues T, S, N, Q, E, D, K, R; green indicates amino acid residues W, L, V, I, F, A, M, C.
Figure 2. “*” indicates identical amino acid residues, “꞉” indicates similar amino acid residues, and “ꞏ” indicates less similar amino acid residues. Yellow indicates amino acid residues G, P, C, H, Y; red indicates amino acid residues T, S, N, Q, E, D, K, R; green indicates amino acid residues W, L, V, I, F, A, M, C.
Ijms 22 00184 g002
Ijms 22 00184 g003 550
Figure 3. Schematic representation of the distribution of cysteine residues in x- and y-type HMW-GSs: the HMW-GS is comprised of three domains, the N- and C- terminal domains where most cysteine residues (red lines) are located, flanking a central repetitive domain. Two cysteine residues in the N-terminal of the y-type HMW-GSs are absent in the x-type. In HMW-GS 1Dx5, there is one additional cysteine residue in the repetitive domain near the N-terminal side, and there is an additional cysteine residue in the repetitive domain of the HWM-GSs 1By and 1Dy near the C-terminal side.
Figure 3. Schematic representation of the distribution of cysteine residues in x- and y-type HMW-GSs: the HMW-GS is comprised of three domains, the N- and C- terminal domains where most cysteine residues (red lines) are located, flanking a central repetitive domain. Two cysteine residues in the N-terminal of the y-type HMW-GSs are absent in the x-type. In HMW-GS 1Dx5, there is one additional cysteine residue in the repetitive domain near the N-terminal side, and there is an additional cysteine residue in the repetitive domain of the HWM-GSs 1By and 1Dy near the C-terminal side.
Ijms 22 00184 g003
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Li, Y.; Fu, J.; Shen, Q.; Yang, D. High-Molecular-Weight Glutenin Subunits: Genetics, Structures, and Relation to End Use Qualities. Int. J. Mol. Sci. 2021, 22, 184. https://doi.org/10.3390/ijms22010184

AMA Style

Li Y, Fu J, Shen Q, Yang D. High-Molecular-Weight Glutenin Subunits: Genetics, Structures, and Relation to End Use Qualities. International Journal of Molecular Sciences. 2021; 22(1):184. https://doi.org/10.3390/ijms22010184

Chicago/Turabian Style

Li, Yi, Jiahui Fu, Qun Shen, and Dong Yang. 2021. "High-Molecular-Weight Glutenin Subunits: Genetics, Structures, and Relation to End Use Qualities" International Journal of Molecular Sciences 22, no. 1: 184. https://doi.org/10.3390/ijms22010184

APA Style

Li, Y., Fu, J., Shen, Q., & Yang, D. (2021). High-Molecular-Weight Glutenin Subunits: Genetics, Structures, and Relation to End Use Qualities. International Journal of Molecular Sciences, 22(1), 184. https://doi.org/10.3390/ijms22010184

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop