Journal of Agricultural Sciences
Vol. 59, No. 3, 2014
Pages 207-226
DOI: 10.2298/JAS1403207R
UDC: 635.33-152.75
Review article
CYTOPLASMIC MALE STERILITY AND INTER AND INTRA SUBGENOMIC
HETEROSIS STUDIES IN BRASSICA SPECIES: A REVIEW
Valiollah Rameeh*
Agricultural and Natural Resources Research Center of Mazandran, Sari, Iran
Abstract: Plants of the genus Brassica comprise a remarkably diverse group
of crops and encompass varieties that are grown as oilseeds, vegetables, condiment
mustards and forages. One of the basic requirements for developing hybrid
varieties in oilseed Brassica is the availability of proven heterosis. The
development of hybrid cultivars has been successful in many Brassica spp. Midparent heterosis and high-parent heterosis (heterobeltiosis) have extensively been
explored and utilized for boosting various quantity and quality traits in rapeseed.
Heterosis is commercially exploited in rapeseed and its potential use has been
demonstrated in turnip rape (B. rapa L.) and Indian mustard (B. juncea L.) for seed
yield and most of the agronomic traits. The oilseed rape plant, B. napus, possesses
two endogenous male sterile cytoplasms, nap and pol. Ogura type of cytoplasmic
male sterility was first discovered in Japanese wild radish and other male-sterile
Brassicas (Ogura bearing cytoplasm) derived from interspecific crosses.
Information concerning the allelic frequencies of restorers can be useful in trying to
understand their evolutionary origins. The ogu, pol and nap cytoplasms of B. napus
induce sterility in all, some, and only a few cultivars, respectively. In this study,
different kinds of male sterility, combining ability and heterosis of qualitative and
quantitative traits in different Brassica species will be reviеwed.
Key words: Brassica, cytoplasm, heterosis, interspecific hybrids, male sterility.
Introduction
The Brassica is an important genus of angiosperms consisting of over 3,200
species with highly diverse morphologies. They are used as nutritious vegetables,
condiments and for producing oil (Nasrin et al., 2011). The development of hybrid
genotypes/high-yielding varieties has an important role to fill the gap between food
production and human population. Heterosis and combining ability studies in
Brassica species lead to the development of the hybrid genotypes/varieties that will
produce better seed yield, plant biomass, oil content, protein content and canola
type traits for good health. Cytoplasmic male sterility (CMS) is one of the most
*
Corresponding author: e-mail: [email protected]
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important approaches to utilize the heterosis in Brassica species. The discovery and
characterization of novel male sterile cytoplasm are always the base for rapeseed
heterosis breeding. Up to now, a lot of rapeseed CMS lines have been found,
among which, Ogura (Ogu) CMS shows very stable and complete sterility.
However, no restorer is available in rapeseed, and it shows chlorosis at low
temperature and under low nectar production. Therefore, it is very necessary to
improve the Ogu CMS to overcome these shortcomings and to breed new Ogu
CMS restorers. Transferring Ogu CMS from Chinese cabbage made an improved
Ogu-NWSUAF CMS. Heterosis can only occur when parental cultivars used for F1
production differ in gene frequencies (Falconer and Mackay, 1997). Heterosis for
different agronomic traits has been reported. A significant positive correlation of
mean performances with heterosis and heterobeltiosis effects for yield components
except 1000-seed weight in rapeseed indicated that the selection of the superior
crosses based on heterosis and heterobeltiosis effects will be effective (Rameeh,
2012d). Schuler et al. (1992) for inter-cultivar F1s of B. rapa reported mid-parent
heterosis (MPH) of 18% for seed yield. Falk et al. (1998) in cultivars of spring
B. rapa reported 25% MPH for seed yield. Kaur et al. (2007) in B. rapa subspecies
of toria, brown sarson and yellow sarson observed 31% heterosis in intra group
crosses and 17% in inter group crosses for seed yield. Wang et al. (2007) in
Chinese B. rapa vegetables reported MPH of 10% for plant leaves, 44% for petiole
fresh weight and 17% for the length of the biggest leaf. One of the most expensive
steps in heterosis utilization is the identification of parental combinations that
produce F1 with superior yield. Therefore, the prediction of F1 performance with
accuracy from morphology or molecular data is important. This could reduce the
cost involved in evaluating parent and crosses in field trials to identify parental
combinations that will give high F1 performance. The predictions of heterosis from
parental genetic distance have been widely studied in many crops though hardly
utilized. Knowledge about the type and amount of genetic effects is required for an
efficient use of genetic variability of crops. The concept of good combining ability
refers to the potential of a parental form to produce by its crossing with another
parent superior offspring for the breeding process and it is widely used in the
breeding of cross-pollinated plants. Information and study on combining ability can
be useful in regard to selection of breeding methods and selection of lines for
hybrid combination. Due to the numerous theoretical and practical advantages of
this method, in recent years, the choice of parental forms on the basis of combining
ability has been extended. Advancement in the yield of Brassica requires certain
information regarding the nature of combining ability of parents available for use
in the hybridization program. Seed yield is a complex trait that includes various
components and finally results in a highly plastic yield structure (Diepenbrock,
2000). Yield per area is the product of population density, the number of pods per
plant, the number of seeds per pod and the individual seed weight. While
Cytoplasmic male sterility and heterosis studies in Brassica species
209
examining the genetic control of grain yield in oilseed rape, both additive and nonadditive gene effects have been found to be involved (Yadav et al., 2005).
Relationship and origin of the Brassica species
Plants of the genus Brassica comprise a remarkably diverse group of crops
and comprise varieties that are grown as oilseeds, vegetables, condiment mustards
and forages. The cytogenetic and evolutionary associations between the major
oilseed and vegetable species are commonly depicted as U’s triangle, named after
the Korean scientist who first formulated it (U, 1935). U speculated that
B. carinata, B. juncea and B. napus are each allotetraploids formed by interspecific
hybridization events between the parental diploid species B. nigra, B. rapa and
B. oleracea. Thus, hybridization between B. nigra and B. rapa resulted in the
formation of B. carinata, and between B. nigra and B. oleracea in the formation of
B. juncea. B. napus is a hybrid between B. oleracea and B. rapa. The relationships
among these species first assumed by U have since been proved by a large variety
of genetic and molecular analyses. The haploid genomes of B. rapa, B. nigra and
B. oleracea are assigned A, B and C respectively. Thus, diploid B. rapa has two
copies of the A genome within 20 chromosomes (AA, n=10, 2n=20) and diploid
B. napus has also two copies of both the A and C genomes within 38 chromosomes
(AACC, n=19, 2n=38). The diploid species have a long history of domestication
and B. rapa was already cultivated during the Bronze Age in Northern Europe
(Persson et al., 2001), towards the end of the sixteenth century in Holland and
Belgium, and in the eighteenth century in Britain. Molecular and morphological
studies have suggested that B. rapa originated from two independent centers:
Europe and Asia (He et al., 2002; Zhao et al., 2005). The Asian types contain
several subgroups of species which are mainly used as leafy vegetables, while the
European types are used as oilseeds (Reiner and Ebermann, 1995). Based on
vernalization requirement before flowering, B. rapa can be grouped into winter and
spring types and presently for oilseed production in moderate and warm
temperature regions, mainly spring type is cultivated. The Brassica species
together are the second largest oilseed crop produced worldwide (FAO, 2012).
The most important Brassica species is B. napus, but B. rapa is also of special
interest as a progenitor of B. napus and B. juncea. The oil is presently processed, as
natural substance in the petrochemical industry for biodiesel and over 3.9 million
tons of biofuel was produced by the EU in 2005 (EC, 2006). The subspecies
rapifera of B. rapa is cultivated either for its turnips or leaves. In Northern Spain,
Portugal and Southern Italy (Padilla et al., 2005), it is used either as leafy vegetable
for human consumption or as fodder for feeding animals, depending on the
morphotype. The swollen root is consumed by both humans and animals. In China,
different morphotypes of B. rapa are vegetable cultivars, which comprise Chinese
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cabbage (subsp. pekinensis) distinguished by its large leaves with
wrinkled surfaces, and Pak choi (subsp. chinensis) which does not form heads
(Zhao et al., 2005).
B. nigra
BB, 2n=16
B. carinata
BBCC, 2n=34
B. oleracea
CC, 2n=18
B. juncea
AABB, 2n=36
B. napus
AACC, 2n=38
B. rapa
AA, 2n=20
Figure 1. U’s triangle representation of the relationships between the diploid
Brassica species B.nigra, B. rapa and B. oleracea and the allotetraploid species
B. carinata, B. juncea and B. napus. The haploid genomes of the diploid species of
B. rapa, B. nigra and B. oleracea are referred to as A, B and C, respectively.
The concept of subgenome of Brassica
Long years of evolution and artificial selection have made the A and C
genomes in B. napus to some extent different from the A genome in B. rapa and
B. juncea, the C genome in B. oleracea and B. carinata (Li et al., 2010).
To distinguish the difference, the concept of subgenome was introduced to genus
Brassica. Thus, Ar, An and Aj were used to characterize the A genome in B. rapa,
B. napus and B. juncea, Bb, Bj and Bc for the B genome of B. nigra (black
mustard), B. juncea and B. carinata. The Co, Cn and Cc were used for the C genome
of B. oleracea, B. napus and B. carinata (Li et al., 2004, 2005a, 2006b, 2007; Qian
et al., 2007) (Figure 2). B. napus was extensively cultivated in the world. The
limited geographical range of B. napus and its intensive breeding have led to a
relatively narrow genetic basis in this species. Many efforts have focused on
exploring novel B. napus breeding stocks by the hybridization of B. rapa ×
B. oleracea or B. napus × B. juncea, B. carinata × B. nigra (Li et al., 2004). After
that, most interspecific hybrids in Brassica could be considered as intersubgenomic
hybrids, such as ArAnCn (B. napus × B. rapa) and ArBcCc (B. carinata × B. rapa).
As shown in prior studies, the positive correlation was detected between genetic
Cytoplasmic male sterility and heterosis studies in Brassica species
211
distance of parents and their F1 mid-parent heterosis for seed yield in B. napus. The
new-typed of B. napus including ArArCcCc or ArArCnCn with normal meiosis can
be created by interspecific hybridization and molecular selection. The heterosis
would be expected in the hybrid of ArCcCnCc or ArAnCnCn if hybridization were
performed between the new typed B. napus with genome composition ArArCcCc or
ArArCnCn and the natural B. napus with genome composition of AnAnCnCn.
ArAnCnCn was generated by the hybridization between ArArCcCc × AnAnCnCn and
ArArCnCn × AnAnCnCn. The method for the creation of new-typed B. napus with
genome composition of ArArCcCc and ArArCnCn is as shown in Figure 2.
B. nigra
BbBb, 2n=16
B. carinata
BcBcCcCc, 2n=34
B. juncea
AjAjBjBj, 2n=36
Brassica
B. oleracea
CoCo, 2n=18
B. napus
AnAnCnCn, 2n=38
B. rapa
ArAr, 2n=20
Figure 2. The letters of subgenome of Brassicas and their relationship.
Gynodioecy
Gynodioecy is the co-existence of hermaphroditic and female (male sterile)
individuals in populations of the same plant species such as Brassica. Male sterility
may have multiple causes. It can result from adverse growth conditions, from
diseases, or from mutations. Naturally occurring genetically male sterile plants in
hermaphrodite species generally maintain fully normal female functions. The
phenotypic expressions of male sterility are very diverse from the complete
absence of male organs, the failure to develop normal sporogenous tissues
(no meiosis), the abortion of pollen at any step of its development, the absence of
stamen dehiscence or the failure of mature pollen to germinate on compatible
stigma. Although multiple causes for pollen abortion exist, cytoplasmic male
sterility, which depends on mitochondrial genes, is the determinant of gynodioecy
most frequently met in natural populations. The molecular data collected over the
last two decades by molecular biologists on sterility inducing mitochondrial genes
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and their expression allow a better understanding of the protection and the role of
this sexual dimorphism in plant species in relation to theoretical models established
by population geneticists (Budar and Pelletier, 2001).
Male sterility
Nuclear male sterilities are generally recessive mutations that affect a huge
number of functions. These mutations may affect for example proteins involved
in male meiosis (Glover et al., 1998), the metabolism of plant hormones, the
biosynthesis of complex lipid molecules or the synthesis of secondary
metabolites (Aarts, 1995). Cytoplasmic male-sterility (CMS) which has been
observed in over 150 plant species is usually identified as “maternally inherited
deficiency in producing viable pollen” and the mitochondria are responsible for
this trait. This characterization leads us to call CMS any mitochondrial mutation,
which impairs the proper functioning of mitochondria, leading to male sterility.
For example, in Nicotiana sylvestris, mitochondrial mutants were obtained from
in vitro culture (Gutierres et al., 1997). They exhibit male sterility, but also many
other have abnormal characters throughout all their development. Such mutated
mitochondrial genomes have not been clearly selected for in natural conditions.
Therefore, a better definition for CMS would be: “maternally inherited male
sterility resulting from a specific (mitochondrial) gene whose expression impairs
the production of viable pollen without otherwise affecting the plant”. The
present information about CMS genes results from studies in several cultivated
species, where this trait is used for F1 hybrid production. The Ogura type of
cytoplasmic male sterility (Ogura, 1968) was first discovered in Japanese wild
radish. The male sterility inducing gene (orf138) was determined (Grelon et al.,
1994) by studying the recombined mitochondrial DNA of ‘cybrids’ (cytoplasmic
hybrids) obtained through protoplast fusion (Pelletier et al., 1983) between fertile
Brassica (napus or oleracea) and male-sterile Brassicas (Ogura bearing
cytoplasm) derived from interspecific crosses (Bannerot et al., 1974). The
‘orf138 locus’ encompasses two open reading frames coding respectively 138and 158-amino-acid polypeptides which are co-transcribed. The latter, also called
orfB, communicates to the subunit 8 of the ATPase complex (Gray et al., 1998),
and the orf138 gene has some similarities with different radish mitochondrial
DNA sequences representing that it is related to intragenomic recombination. The
particular structure of this locus determines the stability of the orf138 gene. In
some of the plants which resulted by protoplat fusion, the male sterility was
unstable due to a frequent loss of the CMS-inducing gene (Bellaoui et al., 1998).
The instability of the CMS is also detected when a second copy of the orfB gene
allows the loss of the copy related to the orf138 gene.
Cytoplasmic male sterility and heterosis studies in Brassica species
213
The possible role of CMS and restorer genes in evolution
In alloplasmic situations, the observed phenotype is often complex, resulting
from the association of both chloroplastic and mitochondrial genomes with an alien
nuclear counterpart. Some of the CMS induced by alloplasmic situations could also
be a revival of ancient CMS in the cytoplasm donor species, which have been
silenced by fixation of nuclear restorers in these species. A new nuclear
background, which has never selected restorer genes for this CMS, allows the
cytoplasm to induce sterility again. One can expect to detect the CMS inducing
gene in such alloplasmic situations by looking for an ORF, present but silent in the
cytoplasm donor species and expressed (and probably co-transcribed with an
indispensable mitochondrial gene) in the species where CMS is expressed. This is
observed in the case of the alloplasmic B. napus and B. juncea plants carrying
B. tournefortii cytoplasm. In the B. tournefortii mitochondrial genome, a chimaeric
ORF (orf263) is related to the atp6 gene, but it is not expressed. In alloplasmic
lines of B. napus or B. juncea carrying the B. tournefortii cytoplasm, orf263 is
co-transcribed with atp6 and the bicistronic mRNA is accumulated (Landgren et
al., 1996). Although the responsibility of orf263 in the male sterile phenotype of
alloplasmic plants remains to be proven, the expression behavior of this
mitochondrial gene in different nuclear backgrounds conforms to what is expected
from a ‘silent’ CMS gene reactivated in an alloplasmic context. One of the most
intriguing features of CMS, still open to hypotheses, is the precise localisation in
the development of the phenotype induced by a mitochondrial gene which, in all
cases except the bean pvs gene (Abad et al., 1995), is constitutively expressed. This
observation is not so surprising when one considers that these genes have recruited
expression signals from other mitochondrial genes and are therefore submitted to
the same controls. One can expect that CMS genes which have been maintained for
a long time (and probably selected for) in natural populations, such as the Ogura
CMS present in different Rhaphanus species (Yamagishi et al., 1996; 1997) or the
bean CMS determinant present in different Phaseolus species will have an effect
strictly limited to pollen production. Hence, the limited phenotype induced by these
genes must result from a specific ‘activity’ in male organs. It is likely that the
possible means of impairing male gametogenesis via a mitochondrial defect
without affecting the female fitness of the plant are limited. This remark might
appear to be in disagreement with the observed absence of homology between
CMS gene sequences. However, it is noteworthy that at least one hydrophobic
domain and a possible or shown relationship to the mitochondrial membrane are
shared between the encoded proteins (Schnable and Wise, 1998). Some stretches of
amino acids are sometimes shared by these otherwise unrelated proteins (Tang et
al., 1996; L’Homme et al., 1997), but an interpretation of this latter observation in
terms of function of the encoded proteins is still premature.
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Population genetics of restorers
Information concerning the allelic frequencies of restorers can be useful in
trying to understand their evolutionary origins. The ogu, pol and nap cytoplasms of
B. napus induce sterility in all, some, and only a few cultivars, respectively. Hence,
one might realize that the ogu restorer (Rfo) is absent from B. napus germplasm,
pol restorers are rare, and nap restorers are more common. Higher-plant
mitochondrial genomes are thought to exist in the form of multiple circular DNA
molecules capable of recombining with one another at high frequency across
specific recombination repeat sequences generally greater than 2 kb in size.
Infrequent recombination events across shorter repeat sequences can also happen,
and rearrangements resulting from such rare events represent the major form of
evolutionary change occurring in the molecule. In some cases these rare
recombination events have created chimeric genes that are associated with
cytoplasmic male sterility (CMS) (Hanson, 1991; Hanson and Folkerts, 1992;
Bonen and Brown, 1993). CMS is a widespread, maternally inherited trait of higher
plants that results in pollen abortion. The expression of these chimeric genes can
often be influenced by specific nuclear genes, termed restorers of fertility (Rf) that
suppress male sterility and allow for normal pollen development. It remains to be
explained how the expression of these novel genes specially alters pollen
development. CMS in B. napus can be given either by alien cytoplasms, such as the
Ogura cytoplasm of radish, or by endogenous cytoplasms established within
cultivated varieties (Shiga and Baba, 1980). The endogenous systems entail an
unusual set of interactions between different nuclear and mitochondrial genotypes.
Male fertility of most nuclear genotypes is unaffected by the cytoplasm assigned
nap found in most B. napus cultivars. The nap cytoplasm can, however, give male
sterility on a limited number of cultivars that lack corresponding Rf genes, such as
the cultivar ‘Bronowski’ (Shiga and Baba, 1980). Male-fertile ‘maintainers’ of
such cultivars possess a cytoplasm designated cam that is thought to be derived
from B. campestris, one of the diploid progenitor species of the amphidiploid
B. napus. A third cytoplasm, ‘Polima’ or pol, confers male sterility on most
B. napus cultivars (Fan et al., 1986). A few genotypes can restore fertility to pol
male-sterile cytoplasms, and restoration may take place through the action of either
of two unlinked dominant alleles (Fang and McVetty, 1989). Both nap and pol
cytoplasms can therefore induce male sterility in appropriate nuclear backgrounds,
whereas the cam cytoplasm appears unable to induce male sterility in B. napus.
Several lines of evidence suggest that the region of the pol mitochondrial genome
surrounding the atp6 gene is associated with the CMS trait. It is the only region for
which transcript differences have been identified among fertile pol CMS, and
fertility restored pol plants (Singh and Brown, 1991; Witt et al., 1991). This region
is also organized differently between the sterile pol and fertile cam mitochondrial
Cytoplasmic male sterility and heterosis studies in Brassica species
215
genomes (L’Homme and Brown, 1993), and it is the only region that is genetically
correlated with CMS in somatic hybrids (Wang et al., 1995). Singh and Brown
(1991) found that the pol atp6 gene is co-transcribed with a chimeric gene, orf224.
The first 58 codons and the 5¢ noncoding region of this chimeric gene resulted
from a common mitochondrial gene of unknown function termed orfB. The pol
mitochondrial genome contains a 4.5-kb DNA segment immediately upstream of
atp6 that is missing in cam mtDNA and spans orf224. An apparently intact copy of
this segment was also established near the atp6 gene in the nap mitochondrial
genome. However, this copy is 5 kb further upstream of atp6, and nap atp6
transcripts are monocistronic. Since the genomic environments in which the 4.5-kb
segment is located differ between pol and nap mtDNAs, it was suggested that the
segment should be transposed since the divergence of lineages leads to the two
mitochondrial genomes (L’Homme and Brown, 1993). Nothing associated with
this transposition was detected in the pol mitochondrial genome, of approximately
1 kb of DNA from a region immediately upstream of atp6. The finding of an
mtDNA segment containing a sequence related with pol CMS at a distinct site in
the nap mitochondrial genome suggested that the sequence might also be
associated with the nap CMS. To address this issue, we have sequenced the nap
and pol 4.5-kb segments, the regions upstream of atp6 in the cam and nap mtDNAs
that are missing from the pol mitochondrial genome, and the regions neighboring
the sites of these rearrangements. An open reading frame (ORF) homologous to,
but divergent from, orf224 was found at the matching site in the nap 4.5-kb
segment. This open reading frame, orf222, is co-transcribed with the trans-spliced
exon c of the nad5 gene and another ORF. We present results indicating that
expression of the orf222 region is uniquely associated with the male sterility
induced by the nap cytoplasm. This study reveals several rearrangements that have
occurred during the evolution of the nap, cam and pol mitochondrial genomes in
addition to those previously identified (L’Homme and Brown, 1993), all involving
the transposed nap and pol 4.5-kb segments. The two segments, though highly
similar in sequence over most of their length, each contain an internal region not
found in the other. In addition, 603 bp of the pol segment most distal to the
chimeric ORF are missing in the nap segment. The most striking difference
between the nap and pol segments, however, is the extensive degree of sequence
divergence at the 3¢ ends of the respective ORFs. The absence of the terminal
region of the nap segment, and especially the extensive degree of change in the
open reading frames, indicate that simple transposition of the 4.5-kb segment is not
sufficient to account for the changes observed. Among the Brassica mtDNAs in
general (L’Homme and Brown, 1993), it seems unlikely that the widespread
divergence observed in the 3¢ ends of these sequences is the result of changes that
occurred separately subsequent to the divergence of the nap and pol lineages.
Under slightly reduced hybridization stringency conditions, a probe derived
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entirely from the non orfB-homologous portion of orf222 detects over ten different
fragments in southern hybridizations to detect the cam, nap and pol Brassica
mtDNAs, representing that the sequences from this region are present at multiple
sites on the mitochondrial genome in each of these mtDNAs (Small et al., 1989).
Combining ability
Selection of parents for synthetic or hybrid breeding is based on their
combining ability. Combining ability is the ability of a parent to generate superior
progeny and it is divided into general and specific combining abilities (GCA and
SCA, respectively). The GCA effect of a population is an indicator of the relative
value of the population in terms of frequency of favorable genes as compared to the
other populations. The SCA effects of two populations express the differences of
gene frequencies between them and their divergence, as compared to the diallel
populations (Viana, 2000). The mating designs often employed in the assessment
of combining ability are line x tester and diallel crosses (Griffing, 1956; Gardner
and Eberhart, 1966). These permit the selection of superior pure lines for
hybridization and, in cross-pollinating species, screening of populations for use
within and between population breeding programs. Studies on combining ability
for traits such as yield and other agronomic traits are available in different Brassica
species with diallel analysis. Most of the studies in Brassica napus showed
significant GCA and SCA effects for yield and its component characters indicating
that both additive and non-additive gene actions were important in the inheritance
of these traits (Rameeh, 2010; 2011a; 2011b; 2011c; 2011d). Qian et al. (2003)
evaluated intraspecific hybrid between B. rapa × B. napus for biomass yield in two
years. A significant variation observed for both GCA and SCA indicates that both
additive and non-additive effects influenced biomass yield production. The ratios
of variance component for GCA to SCA were 89% in 1999 and 88% in 2000,
showing that GCA had more important role though both were significant. Wang et
al. (2007) studied combining ability for different traits in subspecies of Chinese
B. rapa. They observed that yield per plant and length of main inflorescence were
mainly controlled by SCA; plant height, number of primary branches, siliques of
primary branches, seeds per silique and 1000-seed weight were controlled by both
GCA and SCA; and number of secondary branches, siliques of secondary branches
and siliques per plant were mainly controlled by GCA. Combining ability of
15 subspecies of B. rapa was estimated by using diallel including reciprocals for
12 characters related to yield and oil content (Singh and Murty, 1980). Gene action
was predominantly controlled by SCA effects with GCA effects playing a minor
role in the traits including oil content and 50% of flowering. Yadav et al. (1988) in
nine inbred lines of brown sarson used as females and three other cultivars as males
examined the combining ability of their 27 hybrids. Specific combining ability was
Cytoplasmic male sterility and heterosis studies in Brassica species
217
observed to control all traits when the hybrids were evaluated for plant height,
number of branches per plant, number of seeds per pot, 1000-seed weight and seed
yield per plant (Rameeh, 2012a; 2012b; 2012c; 2012e; 2013a; 2013b).
Heterosis
Heterosis, the term that followed “heterozygosis” which was first used at the
beginning of the 20th century, was defined by Shull (1948) as “the increased size,
the excessive kinetic energy, the increased productiveness, resistance to disease or
to unfavorable conditions of the environment, the stimulating effects of hybridity
which may be observed in cross-bred organisms when compared with
corresponding inbred or comparatively more pure-bred organisms”. In short,
heterosis is “the increase in size or rate of growth of progeny over parents”
(Duvick, 1999; Chen, 2010; Jahnke et al., 2010). This is a phenotypic description
and heterosis is generally observed as a property of quantitative traits, therefore the
first theoretical explanation of heterosis was given through quantitative genetics.
Heterosis can be described in different ways. One formulation is the difference
between the hybrid and the mean of the two parents, known as mid-parent
heterosis. Falconer and Mackay (1997) explained the theoretical background of
mid-parent heterosis based on the relationship between genetic distance and
dominance effect. Later, Lamkey and Edwards (1998; 1999), based on a theoretical
framework described by Willham and Pollak (1985), revisited and refined the
theoretical relationship by differentiating heterosis at the population level and in an
inbred line cross system. The previous could be derived from the genetic
architecture of both parents, whether they were from random-mating or inbred
populations. The concepts of baseline heterosis are panmictic mid-parent heterosis,
and inbred mid-parent heterosis. The inbred mid-parent heterosis, which is the sum
of baseline heterosis and panmictic mid-parent heterosis, has been generally
exploited in the production of hybrid cultivars. Another particularly important
point that appeared from the theoretical concerns of heterosis is that the
performance of an F1 hybrid is a function of dominance and unlinked dominance
interacting via dominance epistasis at loci showing genetic divergence. The first
hypothesis proposed as an explanation of heterosis was the theory of
overdominance presented by East (1936). This idea assumed that “vigor is
promoted when the genes at certain loci are unlike”. On the other hand, Jones
(1917) showed that heterosis “could result from normal gene action and be a
phenomenon accompanying hybridity”. This observation led to a second
hypothesis named “dominance theory”, although it can be better described as
“avoidance of recessive harmful genes” since the idea is based on heterozygous
loci that prevent deleterious effects brought about by recessive genes. Rasmusson
(1933) proposed a gene interaction hypothesis, which was later called “epistasis
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theory”. In a quantitative genetic sense, estimation of heterosis effects is actually a
breakdown of genetic architecture into its components, dissecting phenotypic
variation into additive genetic and dominance gene actions and their epistatic
interactions (Comstock and Robinson, 1948; Griffing, 1956; Mather and Jinks,
1972). Within a properly set mating design to develop certain types of generations,
the heterosis effect is often treated as an effect of dominance, or the “specific
combining ability” effect, especially when epistasis is ignored in the model.
In Indian mustard (Brassica juncea), Yadava et al. (1974) reported heterosis
of 239 per cent over better parent for seed yield per plant. A wide range of positive
heterosis for the number of primary and secondary branches per plant, plant height
and seeds per siliqua were also reported (Rawat, 1975). In another study of partial
diallel analysis of mustard, significant heterosis for yield per plant, number of
primary and secondary branches, length of siliqua, 1000-seed weight were reported
(Ram et al., 1976). Banga and Labana (1984) reported up to 200 per cent heterosis
in B. juncea. It was further verified that some of the crosses exhibited
heterobeltiosis. Verma et al. (2000) reported a significant degree of heterobeltiosis
in several varieties of Indian mustard.
Heterosis is the difference in performance between F1 generation and midparent or high-parent and has been a major breeding tool for plant productivity
improvement. Preferably, inbred lines with genetically different backgrounds are
used as parents for F1 production. It makes maximum use of heterosis by
combining favorable alleles of the individual homozygous parents. In populations
such as B. rapa, a part of heterosis is already utilized in base population due to
their open pollination with plants being partly heterozygous. However, it can take
advantage of the homozygous plants within the population for heterosis, and also
heterotic increase which could result by crossing heterozygous plants. Parental
populations with different genetic make-up such as cultivars (Shuler et al., 1992),
synthetics (Falk et al., 1998), and subspecies (Wang et al., 2007) have been used in
heterosis studies in B. rapa. For estimating heterosis in crosses between population,
Lamkey and Edwards (1999) suggested the term panmictic mid-parent heterosis for
the difference between the mean of two random mating populations and the mean
of a hybrid population produced by crossing individual plants of the two
populations. Dominance, overdominance and epistasis are the three principal
genetic explanations for heterosis. The dominance hypothesis stipulated that
heterosis is contributed by favorable alleles of both parents. Overdominance is a
condition where loci in the heterozygous state are superior to parents and epistasis
defined as complex interactions of favorable alleles of the two parents (Xiong et
al., 1998; Crow, 1999; Tian and Dai, 2004; Sun et al., 2004). Heterosis can only
occur when parental cultivars used for F1 production differ in gene frequencies
(Falconer and Mackay, 1996). Heterosis for different agronomic traits has been
reported. Significant positive correlation of mean performances with heterosis and
Cytoplasmic male sterility and heterosis studies in Brassica species
219
heterobeltiosis effects for yield components except 1000-seed weight in rapeseed
indicated that selection of the superior crosses based on heterosis and
heterobeltiosis effects will be effective for their mean performances improving for
these traits except 1000-seed weight (Rameeh, 2012d). Schuler et al. (1992) in
inter-cultivar F1s of B. rapa reported mid-parent heterosis (MPH) of 18% for seed
yield. Falk et al. (1998) in cultivars of spring B. rapa reported 25% MPH in seed
yield. Kaur et al. (2007) in B. rapa subspecies of toria, brown sarson and yellow
sarson observed 31% heterosis in intra group crosses and 17% in inter group
crosses for seed yield. Wang et al. (2007) in Chinese B. rapa vegetables reported
MPH of 10% for plant leaves, 44% for petiole fresh weight and 17% for the length
of the biggest leaf. One of the most expensive steps in heterosis utilization is the
identification of parental combinations that produce F1 with superior yield.
Therefore, the prediction of F1 performance with accuracy from morphology or
molecular data is important. This could reduce the cost involved in evaluating
parent and crosses in field trials to identify parental combinations that will give
high F1 performance. The predictions of heterosis from parental genetic distance
have been widely studied in many crops though hardly utilized. It is estimated by
calculating distances of molecular or phenotypic data for prediction of the heterosis
from field experiments (Wang et al., 1995). Reports on the extent of correlation
between genetic distance and heterosis have varied for traits and studies. Qian et al.
(2003) in interspecific hybrids between B. rapa and B. napus reported a larger
genetic distance based on molecular marker and a higher biomass yield. Qian et al.
(2007) observed a weak correlation between genetic distance and heterosis for
interspecific crosses of European spring and Chinese semi winter lines. Kaur et al.
(2007) observed a negative correlation between genetic diversity and hybrid
performance in diverse morphotypes of B. rapa.
The possible mechanism for production of heterosis in
intersubgenomic hybrids
Interaction between different genomes of Brassicas might be the reason for
production of heterosis. Liu et al. (2002) revealed that some DNA fragments of Ar
were significantly associated with biomass production in trigenomic hybrids
(ArAnCn), but those DNA fragments had no direct relationship with the heterosis
of yield. Qian et al. (2007) detected that some DNA segments that introgressed
from Ar had positive effects on seed yield of intersubgenomic hybrids of
ArAnCnCn. Li et al. (2006a) indicated that seed yield of intersubgenomic hybrids
of ArAnCcCn was positively correlated with the genomic proportion of Ar, Cc and
Ar + Cc in the new-typed B. napus. The above-mentioned phenomena suggested
that the increasing subgenome portion of Ar and Cc in the new-typed B. napus
might further strengthen the intersubgenomic heterosis for seed yield. Allelic
220
Valiollah Rameeh
combinations present in hybrids might result in the alteration of allele expression
profiles, production of novel allelic interactions, genesis of beneficial adaptations
in the hybrids and give rise to heterotic phenotypes (Springer and Stupar, 2007;
Chen et al., 2008). Chen et al. (2008) also found that the introgression of Ar and
Cc subgenomes of B. rapa (ArAr) and B. carinata (BcBcCcCc) could lead to
considerable differences in the gene expression profiles of the partial new-typed
B. napus (Ar/nAr/nCc/nCc/n) compared with their parents. Chen et al. (2008)
considered that dominance and overdominance effects were important in the
intersubgenomic hybrids (Huang et al., 2006; Ju et al., 2006). About 15.04% and
0.66% of the transcript-derived fragments (TDFs) that were differentially
expressed between the intersubgenomic hybrids and their parents showed a
significant correlation with at least one or over two of analyzed traits of yield.
This indicated that allelic variation introduced from Ar/Cc subgenome may lead
to many positive allelic combinations in the intersubgenomic hybrids (Chen et
al., 2008). Some TDFs, such as Copia-like TDF, were activated in new-typed
B. napus. It indicated that the DNA methylation and chromatin remodeling might
be involved in the production of intersubgenomic heterosis (Hirochika et al.,
2000; Zilberman et al., 2007; Chen et al., 2008). Further research revealed that 12
TDF-markers were mapped to 12 different linkage groups within the one DH
population developed by Qiu et al. (2006). Four of these TDFs were located
within the confidence intervals of eight quantitative trait loci (QTLs) for yieldrelated traits, which could explain the phenotype variation from 4.41% to 13.45%
in the TN DH population.
Conclusion
Studies on combining ability for traits such as yield and other agronomic traits
are available for the different Brassica species with different genetic designs. Most
of the studies in Brassica napus showed significant GCA and SCA effects for yield
and its component characters indicating that both additive and non-additive gene
actions were important in the inheritance of these traits and their performance
heterosis. Heterosis is the difference in performance between F1 generation and
mid-parent or high-parent and has been a major breeding tool for Brassica species
productivity improvement. Heterosis is commercially exploited in rapeseed and its
potential use has been demonstrated in turnip rape (B. rapa L.) and Indian mustard
(B. juncea L.) for seed yield and most of the agronomic traits. The oilseed rape
plant, B. napus, possesses two endogenous male sterile cytoplasms, nap and pol.
They were used along with their respected restorer genes for commercial hybrid
production. Interaction between different genomes of Brassicas might be another
reason for production of heterosis, therefore the concept of subgenome was
introduced to the genus Brassica.
Cytoplasmic male sterility and heterosis studies in Brassica species
221
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Received: May 9, 2014
Accepted: June 20, 2014
226
Valiollah Rameeh
CITOPLAZMATSKA MUŠKA STERILNOST I INTER I INTRA
SUBGENOMSKI HETEROZIS KOD VRSTA RODA BRASSICA: PREGLED
Valiollah Rameeh*
Istraživački centar za poljoprivredne i prirodne resurse u Mazandranu, Sari, Iran
Rezime
Biljke roda Brassica obuhvataju izuzetno raznovrsnu grupu gajenih biljaka i
uključuju sorte koje se uzgajaju kao uljarice, povrće, začinske slačice i krmno bilje.
Jedan od osnovnih zahteva za stvaranje hibridnih sorti kod uljarica iz roda Brassica
je primena utvrđenog heterozisa. Stvaranje hibridnih sorti je bilo uspešno kod
mnogih vrsta roda Brassica. Heterozis u odnosu na srednjeg roditelja i u odnosu na
boljeg roditelja (heterobeltiozis) su intenzivno istraživani i korišćeni za poboljšanje
različitih kvantitativnih i kvalitativnih osobina kod uljane repice. Heterozis se
komercijalno koristi kod uljane repice, a njegova potencijalna primena je uočena i
kod repe ugarnjače (B. rapa L.) i indijske slačice (B. juncea L.) za prinos semena i
većinu drugih agronomskih osobina. Kod biljaka uljane repice, B. napus, utvrđena
su dva tipa endogene muški sterilne citoplazme, nap i pol. Ogura tip
citoplazmatske muške sterilnosti je uočen prvo kod japanske divlje rotkve i drugih
muško sterilnih biljaka roda Brassica (sa ogura citoplazmom) dobijenih
međuvrsnim ukrštanjima. Podaci o frekvenciji alela restorera mogu biti korisni u
tumačenju njihovog evolucionog porekla. Tip citoplazme ogu indukuje sterilnost
kod svih sorti, tip pol kod nekih sorti, a tip nap samo kod nekoliko sorti uljane
repice. U ovom radu dat je pregled različitih vrsta muške sterilnosti, kombinacionih
sposobnosti i heterozisa za kvalitativne i kvantitativne osobine kod različitih vrsta
iz roda Brassica.
Ključne reči: Brassica, citoplazma, heterozis, međuvrsni hibridi, muška
sterilnost.
Primljeno: 9. maja 2014.
Odobreno: 20. juna 2014.
*
Autor za kontakt: e-mail: [email protected]