全 文 ：植物生理学报 Plant Physiology Journal 2011, 47 (6): 531~539 531
Received 2011-04-14 Accepted 2011-04-29
This work was supported by the Natural Science Foundation of
China (31000568 and 30871320), the National Transgenic Project
(2009ZX08002-014B) and the Doctoral Foundation of Shandong Prov-
ince (BS2010NY013).
* Corresponding author (E-mail: xiagm@sdu.edu.cn; Tel: 0531-88364525).
Genetic Variation of High Molecular Weight Glutenin Subunits Associated with
Processing Quality Improvements in Wheat
LIU Shu-Wei, XIA Guang-Min*
The Key Laboratory of Plant Cell Engineering and Germplasm Innovation, Ministry of Education, School of Life Sciences, Shan-
dong University, Jinan 250100, China
Abstract: High-molecular-weight glutenin subunits (HMW-GS) are polymeric protein components of wheat
endosperm which could form the glutenin polymers through the inter-molecular disulphide bonds with each
other and/or with low-molecular-weight glutenin subunits (LMW-GS) in dough. Due to their particular impor-
tance for dough viscosity and elasticity in wheat processing, a majority of studies on the gluten proteins associ-
ated with wheat processing quality have focused on the HMW-GS in the past few decades. Abundant research
results have been achieved in recent years on the characterization of HMW-GS and their encoding genes, the
variation of these genes and their roles in wheat processing quality. This review will concern the recent research
results on the HMW-GS and focus on the variation of HMW-GS proteins and their potential role in wheat qual-
ity breeding.
Key words: wheat; genetic variation; HMW-GS; processing quality
小麦高分子量麦谷蛋白亚基的遗传变异与小麦加工品质改良
刘树伟, 夏光敏*
山东大学生命科学学院, 植物细胞工程与种质创新教育部重点实验室, 济南250100
摘要: 高分子量麦谷蛋白亚基(HMW-GS)是小麦胚乳中一种具有多态性的蛋白质组分, 在面团中它们可以通过相互之间或
与低分子量麦谷蛋白亚基(LMW-GS)之间形成二硫键来组成麦谷蛋白多聚体。由于其在小麦面粉加工所需的粘性和弹力
方面具有极其重要的作用, 过去几十年间在小麦加工品质相关蛋白研究方面的工作大多数集中在高分子量麦谷蛋白亚基
上。近几年在高分子量麦谷蛋白亚基及其编码基因的鉴定、基因的遗传变异以及不同变异在小麦加工品质中的作用方面
进行了大量研究。本文对近几年在HMW-GS领域的研究进展进行综述并且重点讨论HMW-GS的变异及其对小麦品质育种
的重要意义。
关键词: 小麦; 遗传变异; 高分子量麦谷蛋白亚基; 加工品质
特约综述 Invited Review
Wheat is one of the most important crops in the
world due to its high production (678 million tons in
2009, FAO), wide geographical range and high pro-
portion of human consumption (Shewry et al. 2003a).
Unlike rice and maize, wheat can be processed into a
wide range of foods like bread, cake, cookies, noo-
dles, pasta, and other products, which is determined
by a group of wheat specific proteins, the gluten pro-
teins. Gluten is commonly produced by washing
dough with water and it is mainly comprised of alco-
hol-soluble gliadins and insoluble glutenins. The gli-
adins consist of monomeric proteins, which are sepa-
rated into α, β, γ, and ω groups by polyacrylamide
gel electrophoresis at low pH. The glutenins are poly-
meric proteins consisting of two groups of glutenin
subunits called high molecular weight glutenin sub-
units (HMW-GS) and low molecular weight glutenin
subunits (LMW-GS), which are stabilized through
植物生理学报532
the inter-chain disulphide bonds. The LMW-GS
could be further classified into B-, C- and D-types,
while the HMW-GS comprised x- and y-type sub-
units based on their different mobilities during elec-
trophoresis.
Within the context of improving protein quality (e.g.
high extensibility and appropriate dough strength) by
wheat breeding, research has conclusively shown the
importance of glutenin, particularly with emphasis on
those subunits with high molecular weights (Payne et
al. 1981a, 1987; Branlard and Dardevet 1985; Gupta
and MacRitchie 1994; Popineau et al. 1994). In the
past few decades, a majority of studies on the gluten
proteins associated with wheat processing quality
have focused on the HMW-GS, not only due to their
accessibility for analysis (They appear at the top of
the electrophoresis gel pattern and are well separated
from all the other gluten protein subunits.), but also
due to their particular importance for dough viscosity
and elasticity in wheat processing (Shewry et al.
1992, 1997). The HMW-GS only account for about
12% of the total protein in the endosperm of common
wheat (Triticum aestivum L.), while their allelic vari-
ation explain about 45% to 70% of the variation in
bread making performance within European wheat
cultivars (Branlard and Dardevet 1985; Payne et al.
1987, 1988). There have been some excellent reviews
on their genetics, structure and relationship with
wheat processing properties (Shewry et al. 1995,
2003a, b). Abundant research results have been
achieved in recent years on the characterization of
HMW-GS and their encoding genes, the variation of
these genes and their roles in wheat processing quali-
ty, thus, this review will primarily build on recent re-
search results and focus on the variation of HMW-GS
proteins and their potential role in wheat quality
breeding.
1 Characterization of HMW-GS proteins
Genetic studies indicate that the HMW-GS protein
genes exhibit simple co-dominant Mendelian inheri-
tance (Payne et al. 1981b; Payne 1987), and the genes
encoding the HMW subunits are located on the long
arms of the homoeologous group 1 chromosomes of
hexaploid bread wheat (1AL, 1BL, 1DL) at the loci
designated Glu-1 (Lawrence and Shepherd 1980;
Payne et al. 1980). Each locus contains two tightly
linked genes encoding two types of subunits. The
greater one is named x-type and the smaller one y-
type (Harberd et al. 1986). Bread wheat cultivars
contain a large number of allelic forms of the sub-
units encoded by each locus. SDS-PAGE electropho-
retic analyses of about 300 wheat varieties identified
a total of 3 alleles at the Glu-A1 locus, 11 at the Glu-
B1 locus and 5 at the Glu-D1 locus. A numbering
system to designate the different alleles was proposed
based on the relative mobilities of the subunits in
SDS-PAGE (Payne and Lawrence 1983). Subsequent
analyses of the different wheat cultivars and tetra-
ploid or diploid wheat have resulted in continuing in-
creases in the number of alleles detected at each of
the three loci.
Because electrophoresis is simple and easy to per-
form, SDS-PAGE has become a widely used method
for screening HMW-glutenin subunits around the
world. However, it still has obvious disadvantages
because the identification of the HMW-GS is based
on their relative mobilities during SDS-PAGE. Some-
times it is difficult to correctly identify subunits that
have very similar physical and chemical properties
such as 1Ax2* and 1Dx2 (Gao et al. 2010). In recent
years, some new techniques, such as acid polyacryl-
amide gel electrophoresis (A-PAGE), capillary elec-
trophoresis (CE), reversed phase-high performance
liquid chromatography (RP-HPLC) and matrix-as-
sisted laser desorption/ionization time-of-flight mass
spectrometry (MALDI-TOF-MS), were used to better
characterize HMW-GS with the improvement of res-
olution and accuracy (Marchylo et al. 1989; Morel
1994; Werner et al. 1994; Sutton and Bietz 1997;
Dworschak et al. 1998; Garozzo et al. 1999; Foti et
al. 2000), which led to the characterization of many
刘树伟等: 小麦高分子量麦谷蛋白亚基的遗传变异与小麦加工品质改良 533
novel HMW-GS.
For example, several bread wheat HMW-GS with
similar mobilities on SDS-PAGE, such as 1Bx7 and
1Bx7*, 1By8 and 1By8*, 1Dx2 and 1Ax2*, 1Bx6
and 1Bx6.1, were found to be well separated with
RP-HPLC (Dong et al. 2009). Through one and two-
dimensional polyacrylamide gel electrophoresis com-
bined with capillary electrophoresis, the allelic com-
positions of HMW-GS among European spelt
(Triticum spelta L.) and related hexaploid and tetra-
ploid Triticum species were investigated and some
novel alleles encoding subunits 1Ax2.1*, 1Bx6.1,
1Bx13*, 1By19*, 1By22*, 1By22.1 were detected,
which had not been found in previous investigations
on common bread wheat (Yan et al. 2003a, 2004). In
another study, the HMW-GS compositions of 205 ac-
cessions of cultivated emmer wheat (Triticum tur-
gidum ssp. dicoccum Schrank) were examined using
the same techniques, and two novel alleles at Glu-A1
encoding 1Ax1.1 and 1Ax2.1′ were found while sev-
en new subunits (1Bx17*, 1Bx6′, 1Bx13′, 1Bx20*,
1By9*, 1By14.1, and 1By8.1) at the Glu-B1 locus
were detected (Li et al. 2006).
As the genetic base of modern wheat cultivars is
generally narrow, the wild progenitors and relatives
of wheat are potentially rich resources of useful
genes for improvements in wheat quality due to their
high variability in the composition of their seed stor-
age proteins (Nevo and Payne 1987; Ciaffi et al.
1993). Through SDS-PAGE analysis, more than 14
allelic variations at the Glu-Dt1 locus of Triticum
tauschii were detected (Lagudah and Halloran 1988;
William et al. 1993). Through analyzing a large col-
lection of accessions of T. tauschii, a large range of
allelic variation was found and some novel subunits
were observed in both the x- and y-type glutenin sub-
units, including x- or y-type null forms (Gianibelli et
al. 2001). Recently the use of high resolution meth-
ods such as CE, RP-HPLC and MALDI-TOF-MS
contributed to the identification of some novel HMW-
GS in Aegilops tauschii, which had slightly different
mobilities compared to those of bread wheat such as
1Dy10.4 t, 1Dy10.3* t, 1Dy12.1* t, 1Dy12.2* t,
1Dy12.4*t, 1Dy12.5t, 1Dy12.1t, 1Dy10.1t, 1Dy12.2t,
1Dx5*t and 1Dx5.1*t (Yan et al. 2003b, 2004; Zhang
et al. 2006, 2008, 2009). The HMW-GS have also
been characterized for some other wild relatives such
as rye, Ae. umbellulata, Ae. caudate, Ae. searsii, Ae.
cylindrical, Agropyron elongatum (Thinopyrum elon-
gatum), Lophopyrum elongatum, Pseudoroegneria
stipifolia and Australopyrum retrofractum (De Bustos
et al. 2001; Liu et al. 2002, 2003, 2008a, b, 2010;
Wan et al. 2002; Sun et al. 2006; Li et al. 2008).
2 The exploration of HMW-GS encoding genes
Due to the particular importance of HMW-GS to the
processing quality of wheat, exploring the genes en-
coding these subunits will not only enable the identi-
fication of specific residues that are associated with
good or poor breadmaking quality but will also im-
prove wheat quality through genetic manipulation.
The first full length HMW glutenin subunit gene se-
quences were isolated from the genomic library of
common wheat in 1985 which encoded silent Glu-
Aly, Glu-1Dx2 and Glu-1Dy12 (Forde et al. 1985;
Sugiyama et al. 1985; Thompson et al. 1985). The
gene sequences for Glu-1By9, Glu-1Ax2*, Glu-1-
Bx7, Glu-1Dx5, Glu-1Dy10, Glu-1Ax1 and Glu-1-
Bx17 were subsequently isolated and sequenced
(Halford et al. 1987; Anderson and Greene 1989; An-
derson et al. 1989; Halford et al. 1992; Reddy and
Appels 1993).
The huge size of the wheat genome makes it labori-
ous to perform library construction and screening,
while the length of the HMW subunit genes (typically
greater than 2 kb) and repetitive structure makes it
difficult to amplify the sequences with the poly-
merase chain reaction (Shewry et al. 2003a). Howev-
er, these difficulties have been overcome due to the
availability of more reliable and robust polymerases
(D’Ovidio et al. 1995; Wan et al. 2002), which, in
turn, makes PCR a more efficient method than library
植物生理学报534
screening for the characterization of HMW-GS genes.
The employment of PCR has led to the identification
of abundant HMW-GS genes from wheat cultivars,
the wild progenitors and relatives of wheat in recent
years, including HMW-GS genes from the A, B, D, R,
Ee, St, K, Ta and W genomes (D’Ovidio et al. 1996;
Mackie et al. 1996a, b; De Bustos et al. 2001; Liu et
al. 2002, 2003, 2008a, b, 2010; Wan et al. 2002,
2005; Shewry et al. 2003c; Bai et al. 2004; Li et al.
2004, 2008; Guo et al. 2005; Sun et al. 2006; Yan et
al. 2006; Yang et al. 2006; Pang and Zhang 2008; Ji-
ang et al. 2009).
The availability of a large number of HMW-GS
genes from cultivated wheat, their wild progenitors
and their relatives enabled a detailed comparison of
their amino acid sequences. All of these proteins pos-
sess highly conserved structures, with each subunit
containing a long repetitive region flanking two high-
ly conserved terminal nonrepetitive domains, N and
C. The N-terminal domain of the x-type subunits
contains 81–89 amino acid residues while that of the
y-type subunits contains 104 or 105 residues. The
central repetitive domains of both x- and y-type sub-
units comprise hexapeptide and nonapeptide motifs
while the x-type subunits also contain tripeptide mo-
tifs. The similarity in structures of different HMW
glutenin subunits indicates that they likely evolved
from the same ancestor (Shewry and Tatham 1990;
Shewry et al. 1995). The first step in the evolutionary
process of HMW subunits was the duplication of a
single ancestral gene into two closely linked copies
and these copies diverged to be distinguishable (x-
and y-type) before the speciation of wheat and wheat-
related species (Wan et al. 2002; Shewry et al.
2003b). The Glu-1 gene duplication event was tenta-
tively dated at 7.2–10.0 million years ago (MYA)
while the origin of the A, B, D and G genomes at
5.0–6.9 MYA (Allaby et al. 1999)
The recently characterized HMW-GS from A. ret-
rofractum comprised a novel type of repeat motif
containing 12 residues in this subunit, which was the
fourth type of repeat motif presented in HMW-GS
(Liu et al. 2010). This subunit also contains some
other special modifications when compared with
known subunit from other species and it separated
from both published x- and y-type subunit genes with
phylogenetic analysis, which indicated that the W ge-
nome underwent a special evolutionary process dif-
ferent from other Triticeae species (Liu et al. 2010).
Moreover, some y-type HMW-GS from the E and St
genomes had more similarity with the x-type subunits
when the phylogenetic tree was constructed based on
the C-terminal sequences, which indicated they were
an intermediate state in the divergence between the x-
and y-type subunits.
3 Induced variation in HMW-GS
Even though a large number of HMW-GS and their
encoding genes have been characterized from wheat
and related species, most studies to improve wheat
quality by wheat breeding focus on those HMW-GS
con t ro l l ed by the D genome , pa r t i cu l a r ly
1Dx5+1Dy10. One of the reasons for this might due
to the lack of more superior subunits than 1Dx5+
1Dy10 in cultivated wheat varieties, which could be
more easily used for plant breeding through hybrid-
ization. Searching for other high quality subunits in
wheat still remains a huge challenge due to the nar-
row genetic range of cultivated wheat varieties. How-
ever, inducing novel variations in HMW-GS might be
a convenient and feasible route for exploring high
quality subunits and some progress has been made at
this area in recent years.
It has been proposed that the plant cell culture itself
could generate heritable somaclonal variation, which
provides a novel source of variability for plant im-
provement (Larkin and Scowcroft 1981). Extensive
variations including the variation of gliadin proteins
have been observed among 142 regenerants of a
Mexican breeding line Yaqui 50E and their progeny
(Larkin et al. 1984). Similar variations have also been
detected in regenerated plants of the winter wheat
刘树伟等: 小麦高分子量麦谷蛋白亚基的遗传变异与小麦加工品质改良 535
line ND7532, except that gliadin changes occurred
less frequently in ND7532 than in Yaqui 50E (Cooper
et al. 1986). Significant changes in bands of gliadins
and glutenins in seeds of wheat regenerated from im-
mature embryo cultures included the appearance of
new bands, the loss of specific protein bands and
changes of band intensity relative to the parent (Hu et
al. 1998). SDS-PAGE analysis revealed the HMW-
GS composition of some seeds from wheat plants re-
generated from tissue culture variation from the
1Ax1, 1Bx7+1By8, 1Dx2+1Dy12 to 1Bx7+1By8,
1Dx2+1Dy12 and 1Bx7, 1Dx2+1Dy12 (Zhang et al.
1997). Similar phenomenon was also observed in the
progeny of regenerated plants derived from a single
cell culture in spring wheat NE7742 (HMW-GS com-
position 1Ax1, 1Bx7+1By8, 1Dx2+1Dy12) where
three kinds of novel HMW-GS combinations were
detected and 8 lines expressed 1Bx7+1By8,
1Dx2+1Dy12, one line expressed 1Bx7, 1Dx2+
1Dy12 and 5 lines expressed 1Bx7+1By9, 1Dx2+
1Dy12 (Hu et al. 2002).
In addition to somaclonal variation, changes in
HMW-GS have also been induced by other approach-
es such as chemical and/or physical mutagenesis and
introducing exogenous DNA into the wheat. Chemi-
cal mutagenesis of wheat cv. Viginta using nitroso-
ethylurea provided a mutant line with altered compo-
sition of HMW-GS where the 7+9 subunits encoded
by Glu-B1 locus changed to 6 (Svec et al. 1999).
Four somaclones were derived from gamma ray irra-
diated immature embryos of wheat and lost the sub-
units encoded by Glu-A1, Glu-B1, and/or Glu-1Dy
(Zhang et al. 2002). Introducing the total DNA from
sorghum into spring wheat Ganmai No. 8 also in-
duced variation in the HMW-GS in one of the proge-
ny where subunits 2+12 of Ganmai No. 8 were sub-
stituted by 5+10 in progeny 89144 (Wang et al.
2000). Chemical mutagenesis of an elite Chinese
wheat variety Xiaoyan 54 led to a mutant where the
expression of the 1Bx14 subunit was specifically
blocked and the silencing of this subunit might due to
a base substitution that resulted in a premature stop
codon in the mutant ORF (Zhu et al. 2005).
4 Genetic variation in HMW-GS induced by so-
matic hybridization
For the purpose of quality improvement, the genera-
tion of novel HMW-GS was more significant com-
pared to the loss of subunits. However, all of the
above-mentioned studies indicated less frequent gen-
eration of novel variation of HMW-GS than those
lost and no explanations were presented to describe
how the novel HMW-GS were created. Fortunately,
high frequency generation of novel HMW-GS was
reported in the introgression lines of somatic hybrids
between wheat and tall wheatgrass. Moreover, the
mechanisms of novel HMW-GS formation were dis-
cussed (Zhao et al. 2003; Feng et al. 2004; Liu et al.
2006, 2007, 2009; Gao et al. 2010).
Asymmetric somatic hybridization between the pro-
toplast of common wheat (T. aestivum L cv. Jinan
177) and the UV-irradiated protoplast of A. elonga-
tum generated fertile introgression lines with superior
agronomic traits. In particular the bread making qual-
ity was improved (Xia et al. 2003; Zhao et al. 2003;
Liu et al. 2006). SDS-PAGE analysis of the seeds of
175 somatic hybrid lines indicated that about 35% of
the hybrid lines express novel high quality HMW-GS
not present in Jinan177 or either parents. Six novel
HMW-GS 1Ax1, 1Ax2*, 1Bx13, 1By16, 1By8,
1Dx5, and three allelic HMW-GS combinations
1Bx13+1By16, 1Bx7+1By8, and 1Dx5+1Dy12 oc-
curred in the hybrids (Zhao et al. 2003). More impor-
tantly, most of these novel HMW-GS or combina-
tions correlated with higher flour processing quality
than the parent wheat (Liu et al. 2006) and they could
be stably inherited (Liu et al. 2009). Characterization
of the coding sequences of the novel subunits indi-
cated that additional cysteine residues were present
in at least three novel subunits, which could partially
explain the higher flour processing quality of some
novel subunits (Feng et al. 2004; Liu et al. 2009).
植物生理学报536
Through sequence alignments of the novel subunits
with those of both parents, the mechanisms of how
these new subunits were created were elucidated (Liu
et al. 2007, 2008, 2009). Except for two genes direct-
ly introgressed from the donor parent A. elongatum,
most of the novel hybrid HMW-GS genes were de-
rived from point mutations and replication slippage
of the parental genes. Six subunit genes were pro-
duced by point mutations and 10 subunit genes re-
sulted from unequal crossover or slippage of the pa-
rental wheat genes (Liu et al. 2007, 2009). In addition
to the above mechanisms, reactivation of transposons
and shuffling of parent genes to produce novel chi-
meric HMW-GS genes was also found to be respon-
sible for the generation of novel subunits (Liu et al.
2007, 2009). Novel HMW-GS were also present in
the fertile regenerants of symmetric somatic hybrid-
ization between the protoplasts of common wheat (T.
aestivum L cv. Jinan 177) and A. elongatum, which
are morphologically similar to tall wheatgrass, but
contain some introgression segments from wheat (Cui
et al. 2009; Gao et al. 2010). We would expect there
to be similar mechanisms for the generation of these
novel subunits in symmetric somatic hybrids with
those that occured in asymmetric somatic hybrids,
and this similarity between different hybrids indicates
that the response to genomic shock triggered by the
merger and interaction of biparent genomes might be
mainly responsible for the sequence variation of
HMW-GS genes in the introgression lines (Gao et al.
2010).
The formation of these novel hybrid genes has simi-
larity to the evolutionary mechanisms of natural
HMW-GS genes mentioned by Anderson and Greene
(1989), which include: (a) single base changes, (b)
deletions or additions within a repeat, (c) single re-
peat changes, and (d) deletions or duplications of
blocks of repeats. The results suggest that asymmet-
ric somatic hybridization is a unique pathway to rap-
idly produce novel HMW-GS alleles that can be used
for wheat quality improvement and this technique
may represent a valuable means of extending the
variation at these functionally important genes.
5 Conclusions
The importance of wheat in food processing and the
tight correlation between HMW-GS composition and
flour processing quality has stimulated a massive vol-
ume of studies on the HMW-GS and their encoding
genes. Transformation of wheat with HMW-GS
genes has been widely used over the past decade to
modify the functional properties of dough. However,
the choice of target subunits has also almost certainly
been restricted to 1Ax1, 1Dx5 and 1Dy10 due to the
limited availability of high quality subunits (Altpeter
et al. 1996; Blechl and Anderson 1996; Barro et al.
1997; He et al. 1999, 2005; Pastori et al. 2000; Alva-
rez et al. 2001). The exploration of novel high quality
subunits from cultivated wheat, the wild progenitors,
and relatives of wheat together with chemical, physi-
cal and/or biological inducement of novel subunits
has significantly expanded the gene pool that could
be used for wheat quality improvement by genetic
engineering technology.
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