|
Revista Científica UDO Agrícola
Universidad de Oriente Press
ISSN: 1317-9152
Vol. 6, Num. 1, 2006, pp. 1-10
|
Revista Científica UDO Agrícola Vol. 6, Núm. 1, 2006, pp. 1-10
Recent advances in
understanding genetic basis of heterosis in rice (Oriza sativa L.)
Avances recientes en el
conocimiento de la base genética de la heterosis en arroz (Oriza sativa L.)
Sofi Parvez
Sher-E-Kashmir University of Agricultural Sciences and Technology of
Kashmir. Shalimar Campus-191 121, Srinagar, Jammu
& Kashmir State, India.
E-mail:
phdpbg@yahoo.com
Received:
07/26/2006
|
Reviewing
ending:
09/07/2006
|
Review
received:
11/14/2006
|
Accepted:
11/28/2006
|
Code Number: cg06001
ABSTRACT
Heterosis is perhaps one of
the greatest practical achievements of the science of plant breeding and has
been extensively used in crop improvement. Therefore, an understanding of its
potential genetic basis is imperative. Extensive studies in crop plants
including rice have been made to elucidate the genetic factors underlying
heterosis. Various research groups have proposed dominance, overdominance and
epistasis as major genetic basis of heterosis and recent advances in molecular
biology have helped to validate these findings in various crop species.
Despite, tremendous advances in molecular marker techniques, QTL analysis and
genomics, conclusive evidence in support of either of these theories is still
elusive, as all of these factors seem to be mutually non-exclusive. Nowadays,
focus is increasingly shifting to study heterosis at genomic level to identify
the genomic regions that evoke heterotic effect and introgress such regions
into elite rice lines to develop high yielding hybrids. Advances have also been
made in expression profiling and relate differences in transposon and repeat
content in parental lines to heterotic effect.
Key
words: Rice, heterosis, genetic basis, molecular markers
RESUMEN
Heterosis es quizás uno de los mayores logros
prácticos de la ciencia del mejoramiento de plantas y ha sido extensivamente
usada en el mejoramiento de los cultivos. Por lo tanto, un conocimiento de su
base genética potencial es imperativo. Se han realizado extensivos estudios en
plantas cultivadas incluyendo el arroz para elucidar los factores genéticos que
causan la heterosis. Varios grupos de investigación han propuesto la
dominancia, la sobredominancia y la epistasis como principales bases genéticas
de la heterosis y avances recientes en biología molecular han ayudado a validar
estos descubrimientos en varias especies cultivadas. A pesar de los avances
tremendos en las técnicas de marcadores moleculares, análisis de QTLs y
análisis genómico, una evidencia conclusiva en soportar una de estas teorías
todavía no se ha definido, como todos estos factores parecen ser mutualmente no
exclusivos. En la actualidad, el enfoque está moviéndose rápidamente hacia el
estudio de la heterosis a nivel genómico para identificar las regiones
genómicas que induzcan el efecto heterótico e introducir tales regiones dentro
de líneas elites de arroz para desarrollar híbridos con altos rendimientos. Se
han realizado también avances en el perfil de
expresión y relacionar diferencias en el contenido repetitivo y del
transposon en líneas parentales para efecto heterótico.
Palabras
clave:
Arroz, heterosis, bases genéticas, marcadores moleculares
INTRODUCTION
The phenomenon of superiority of F1 over its
parents is heterosis (Syn. hybrid vigour). The term heterosis was coined by
Shull (1908) for quantitative measure of superiority of F1 over its
parents. The phenomenon of heterosis has been a powerful force in the evolution
of plants and has been exploited extensively in crop production (Birchler et al. 2003). The successful development
of hybrid maize in 1930 gave great impetus to breeders of other crops including
rice to utilize the principle of hybrid production by exploiting heterosis. In
fact the exploitation of heterosis has been the greatest practical achievement
of the science of genetics and plant breeding (Alam et al. 2004). The impact of this phenomenon can be judged by the
fact that rice in its wild state produces only a few hundred spikelets whereas,
the improved inbred varieties produce about 40,000 filled spikelets and rice
hybrids about 52,000 filled spikelets per square meter (Mir, 2002).
Heterosis is a widely documented phenomenon in diploid
organisms that undergo sexual reproduction. Although rice is a naturally self
pollinated crop, strong heterosis is observed in their F1 hybrids.
Though heterosis has been observed for various morphological, physiological and
biochemical characters, in an applied breeding programme, the concern primarily
with the economic yield potential (Ahmad. 1996). In practical breeding
programmes, usually the standard heterosis is considered, which is defined as
superiority of F1 hybrid as compared to highest yielding check, and
is estimated as:
In rice, heterosis was first
reported by Jones (1926) who observed that some F1 hybrids had more
culms and yield than their parents. Between 1962 and
1967 a
number of suggestions
came from different corners of the world regarding commercial exploitation of
heterosis as a major component of rice improvement programmes at national and
international level. There was, however lack of enthusiasm regarding such
applications by most of the rice breeders because of rice being a strictly
self-pollinated crop.
China
was the first country to start extensive research for exploitation of heterosis
for practical applications. It took China, not much time, to harness
the fruits of such effort. The average yield advantage of growing commercial
rice hybrids was about 20%. Presently hybrid rice area in China yield on
an average 6.9t/ha compared to inbred HYVs yielding 5.4 t/ha in similar area
(Virmani, 2004). The results in China
have, in fact, encouraged IRRI and National rice improvement programmes of
countries like India, Vietnam, Philippines,
USA, Bangladesh and Indonesia to start hybrid rice
breeding programmes to exploit heterosis. Hybrid rice technology has made
tremendous impact on food security, rice production efficiency and employment
in China and same is going
to hold true outside China.
The development of super rice series hybrids at IRRI based on NPT or Ideotype
approach are reported to have yield potential of 12 t/ha, which means an increase
of 2.25 t/ha which amounts to increase of 30 Million tones/year. Once the
hybrids with 13 MT/ha are commercialized in 2005, 75 million more people can be
fed annually. China
has already commercialized various hybrids of super rice series such as Liang-You-Pei-Jiu
(LYP 9).
Genetic
basis of heterosis in rice
The genetic basis of heterosis has been a topic of
contentious debate for almost a century now and is still shrouded in mystery.
The earlier workers put forth their suppositions based on quantitative genetic
models but with the advancements in molecular genetics, we have been able to
study this phenomenon in a more refined way. In fact, the recent studies in
maize and rice to attempt an interpretation of heterosis have been greatly
facilitated by molecular markers. The marker data offers an impeccable profile
of genomic regions involved in trait expression and are expected to unravel the
unexplained basis of heterosis (Robin, 2001).
Earlier studies put forth two possible mechanisms of
heterosis: (i) Dominance hypothesis and (ii) over-dominance hypothesis.
Theoretically, the two concepts are based on two different genetic phenomenon
but in most of the situations, both lead to similar expectations (Mukherjee,
1995). In either case, inbreeding leads to a decline in vigour while
out-breeding leads to increased vigour. In case of both dominance and
over-dominance concepts, the decline in vigour is proportional to decrease in
heterozygosity irrespective of the number of dominant and recessive alleles and
degree of dominance. The difficulty of precise demarcation of either of two
basic assumptions arises due to a number of factors.
i)
Distinction between true over-dominance and
pseudo-over dominance. Linkage disequilibrium often causes bias in estimation of
genetic components (non-additive), and as such heterosis may arise from
repulsion phase linkage or complementary epistasis as well.
ii)
Effect of pseudo-alleles which cannot be classified as
dominance or over-dominance.
iii)
Presence or absence of selection pressure may lead to
heterosis due to two different genetic mechanisms.
iv)
Over-simplification of genetic models may lead to
wrong interpretations.
Xu (2003) stated that as a complex character involving
yield and yield components, heterosis should be genetically controlled by many
genes. Although genetic study of quantitative traits has identified a limited
number of QTL, each explaining a relatively large proportion of genetic
variation, much more QTLs could be found when multiple populations are
considered. For a specific hybrid, heterosis is more likely genetically
controlled by a relatively small number of genes; for explanation of heterosis
involved in all hybrids derived from a species, a large number of QTLs will be
needed. Heterozygosity and its related gene interactions are the primary
genetic basis for explanation of heterosis because the hybrid is heterozygous
across all genetic loci that differ between the parents. Thus, the degree of
heterosis depends on which loci are heterozygous and how within locus alleles
and inter-locus alleles interact with each other. Interaction of within-locus
alleles results in dominance, partial dominance, or overdominance, with a
theoretical range of dominance degree from zero (no dominance) to larger than 1
(overdominance). Interaction of inter-locus alleles results in epistasis.
Genetic mapping results have indicated that most QTLs involved in heterosis and
other quantitative traits had a dominance effect. As statistical methods that
can estimate epistasis more efficiently became available, epistasis has been
found more frequently and proven to be a common phenomenon in the genetic
control of quantitative traits including heterosis. With so many genetic loci
involved, it is unlikely that there is no interaction at all between any pair
of them.
Syed and Chen (2005)
indicated that Arabidopsis thaliana
Col and Ler ecotypes share similar genetic backgrounds and, indeed, the
performance of RILs for most of the traits examined remained within mean values
of the two parents (Col and Ler) ruling out dominance complementation for the
majority of traits. However, a large amount of variation was observed in the F1
(or backcross) hybrids derived from each of the RILs and its parent,
Col or Ler. These F1
lines showed low and high performance for all of the traits studied, it is
notable that high F1 performance was observed in F1 lines
derived from RILs x Col
or Ler. The reciprocal hybrids between Col
and Ler did not show a comparable superiority over the two parents. Moreover,
total heterozygosity is not as important as heterozygosity in individual
chromosomes or segments for the observed heterosis. The data suggest that
differential heterozygosity combined with epistasis may be the reason for the
observed heterosis. Furthermore, the hybrid vigor occurred between two closely
related ecotypes, and provides a general mechanism for novel variation
generated between genetically similar materials.
Swanson-Wagner et
al. (2006) state among other mechanisms, one attractive hypothesis for the
existence of underdominant and overdominant gene action invokes the action of
small interfering RNAs (siRNAs). siRNAs are typically derived from transposons
and repeats, although some genes and other sequences can generate siRNAs.
siRNAs can regulate gene expression by cleaving target mRNAs and via
transcriptional silencing. Maize inbreds differ radically in transposon and
repeat content. Hence, inbreds are likely to differ in their complement of
siRNAs. If siRNAs from one inbred do not match genes from the other inbred, the
resulting hybrid could exhibit novel patterns of gene expression, including
overdominance or underdominance. Overall, the results are consistent with the
hypothesis that multiple molecular mechanisms contribute to heterosis.
Guo et al. (2004)
found that the allelic expression variation occurred frequently in maize
hybrids. The differential expression between the alleles could potentially
result in hybrids surpassing the inbred parents in expression in different
dimensions, such as (1) expression level, (2) expression timing/duration, and
(3) response to developmental and environmental cues. The data suggest that the
two parental alleles in maize hybrids may be regulated differentially during
plant development and in response to environmental signals. Although only a
small number of genes were analyzed using one each of the hybrid, distinct
allelic expression patterns were found between a modern and an old hybrid. This
work demonstrates that the maize hybrid is an excellent system to study allele
expression variation because alleles are compared within the same genotype of a
hybrid and equally affected by genetic background or environmental factors.
Auger et al. (2005) concluded from their data that nonadditive gene
expression is quite prevalent in hybrids. The question arises as to whether and
how these nonadditive expression levels contribute to heterosis. The triploid
data indicate that allelic dosage affects the nonadditivity and therefore gene
regulatory interactions are involved. Further work will be required to
determine what spectrum of gene expression, if any, is correlated with
heterosis.
Dominance as
major genetic basis of heterosis
The dominance hypothesis was promulgated by Davenport (1908), Bruce
(1910), Keeble and Pellew (1910) and later elaborated by Jones. This hypothesis
assumes that heterosis is due to non-expression of deleterious recessive
alleles in presence of beneficial dominant alleles in the resulting F1 from
two parents. Therefore the F1 produced from such a cross possesses
superior characters because of the contribution of dominant alleles from one
parent (Budak et al. 2002). Thus
based on the dominance hypothesis, breeders should be able to fix the inbred
lines with favourable alleles, and likely produce inbreds equivalent to F1
hybrids. However, the isolation of such inbreds has been difficult likely due
to a large number of loci differing between two parents. In fact the opponents
of dominance hypothesis put this point as a major evidence against such an
explanation of heterosis.
Recent advancements in molecular genetics have made it
possible to detect and individually analyze the loci underlying heterosis (Xiao
et al. 1995). Molecular linkage maps
coupled with quantitative genetic analysis help in getting a better perspective
of genetic basis of heterosis. Stuber et
al. (1992) were first to use QTL analysis for detecting genomic regions
(QTLs) contributing to heterosis. In rice Xiao et al. (1995) used F1 of an indica variety (9024) and a
Japonica variety (LH422) and developed Recombinant Inbred Lines (RILs) and
back-cross Inbred lines (BC1 F7 and BC2 F7;
Table 1). All the traits studied were subjected to QTL analysis by single point
basis and interval mapping. Using QTL data from all these combined populations,
they estimated the differences in phenotypic means of heterozygotes and
homozygotes over all portions of genome. From the overall results of their
study they found that:
- Most of the QTLs (73 %) were detected in only one of
two backcross generations. In 82% of these cases heterozygotes had higher
phenotype (F1 plants have a higher value of each phenotypic trait
measured in comparison to either parent) as compared to the respective
homozygotes.
- 23 % of QTLs were detected in both backcross
populations and each pair was mapped to same chromosomal location. In all these
cases heterozygotes fell between two homozygotes. This finding suggested that
complementation of dominant (or partially dominant) alleles at different loci
in F1 was major contributor to F1 heterosis for different
traits.
Table 1. Correlation
Coefficients between Genome heterozygosity and trait value (Xiao et al., 1995).
|
Trait
|
BC1
|
BC2
|
Plant height
|
0.204
**
|
0.081
|
Days to heading
|
-0.004
|
0.021
|
Days to maturity
|
-0.027
|
0.026
|
Panicle length
|
0.143*
|
-0.021
|
Panicles per plant
|
-0.082
|
-0.048
|
Spikelets per panicle
|
0.062
|
-0.013
|
Grains per panicle
|
0.069
|
-0.026
|
Percent seed set
|
0.028
|
-0.016
|
1000-grain weight
|
0.068
|
0.099
|
Spikeletes per plant
|
0.026
|
-0.041
|
Grains per plant
|
0.037
|
-0.057
|
Grain yield
|
0.091
|
0.017
|
* p < 0.05 and ** p <
0.01
|
This conclusion is
supported by two important findings.
The correlation coefficient between genome heterozygosity
and trait values by regressing the trait value of each BC1 F7
family on its percentage of genome heterozygosity should reflect the importance
of heterozygosity per se to the
expression of a particular trait. The values of the correlation coefficient (r)
for most of the traits was very low and non significant. Even some of the
heterozygotes had lower phenotypes than respective homozygotes. Thus
heterozygosity is not an essential feature of heterosis as proposed in
over-dominance theory.
The table reveals that except for plant
height and panicle length correlation coefficients for all traits are
non-significant which implies that heterozygosity is not essential for heterosis.
All other traits for both populations and plant height and panicle length for
BC/LH422 showed no relationship between the genome heterozygosity and trait
performance, indicating thereby that overall genome heterozygosity alone had
little effect on trait expression.
One of the important assumption of dominance hypothesis
is that we should be able to isolate, from segregating populations, a true
breeding individual which is as vigorous as F1 (because in dominance
hypothesis AA = Aa). In their experiment Xiao et al. (1995) observed two recombinant inbred lines whose phenotype
exceeded that of F1, and true breeding individuals as vigorous as F1
were observed for all traits including grain yield.
Digenic interactions between markers associated with significant
QTLs and all other markers were not significant. Thus epistasis cannot be
attributed as the cause of F1 heterosis. However, due to inherent
inefficiencies and low resolution of marker based QTL studies in detecting
epistasis (Tanksley. 1993), the possibility of occurrence of some level of
epistasis cannot be totally excluded.
The analysis of QTL x E interactions revealed that gene
action of a QTL did not change from dominance to recessiveness or partial
dominance to over-dominance from one environment to other.
These lines of evidence reinforce the conclusion that
dominance is the major genetic basis of heterosis in rice. Although the same
results do not come out with QTL analysis in maize even though both rice and
maize belong to Gramineae, share many orthologous genes and have evolved from a
common ancestor. Stuber et al (1992)
concluded that over-dominance is major genetic basis of heterosis in maize. The possible explanations of this contrast are:
a)
Maize possess a large number of genes for which
alleles interact in a truly over-dominant manner whereas rice does not.
b)
The observed over-dominant gene action may be due to
pseudo-over-dominance or occurrence of dominant and recessive alleles in
coupling phase linkage (Crow, 1952).
c)
QTL mapping at present is a low resolution process.
The evidence for
dominance as a major genetic basis of heterosis was also provided by Hua et al (2002) who performed a QTL
analysis using F2 populations. They found that correlation between
genotype heterozygosity and trait performance was very low, implying thereby
that heterozygotes are not always advantageous for performance. They also
concluded that dominance is a major genetic basis of heterosis in rice. Singh et al. (2004) studied the components of
heterosis in rice and concluded that dominance is the chief cause of heterosis.
Over-dominance
as major genetic basis of heterosis
The hypothesis
advocating over-dominance as major genetic basis of heterosis was first proposed
by Shull (1910) and East (1908). The same concept was later advocated by
Gustafsson (1938), Stadler (1939) and Hull
(1945). This theory proposes heterozygosity as basic cause of heterosis by
providing physiological stimulus to improved development. Over-dominance theory
is also called as Single gene heterosis; Superdominance or Cumulative
action of divergent alleles. Hull
(1945) strongly advocated this concept and proposed that F1
heterosis in maize cannot be accounted for by dominant genes acting additively
but can be better explained by over-dominance. But one of the biggest lacuna of
this concept is that majority of evidences have been worked out in cases of single locus heterosis while as most of quantitative traits
including yield is governed by a number of genes. The overdominance hypothesis
for heterosis involves alleles acting in dosage adjustment manner in which
neither homozygote is better than heterozygote. With this explanation, it is
assumed that heterozygosity alone is the major genetic basis of heterosis. At
the molecular level, the preferable level of gene product by combination effect
in heterozygous state results in better catalysis of metabolic pathways that
lead to increased growth and yield.
Difficulties in
discriminating true over-dominance from pseudo-overdominance are major
opposition to this hypothesis. Jones (1917) was first to propose that linkage
causes great problems in identification of overdominance and in fact
pseudo-overdominance arising out of repulsion phase linkage may often be
misinterpreted as true overdominance. In such a situation the pair of linked
loci would mimic a single overdominant locus thereby skewing the measure of
true overdominance (Budak et al.
2002).
Brewbaker (1964) described four theories to explain
over-dominance:
- Supplementary allelic action
- Alternative pathways
- Optimal amount
- Hybrid substance
Jinks (1983) was a
strong opponent of over-dominance as genetic basis of heterosis in crops like
rice where according to him great improvements have been made in
performance of inbred lines by
alternating cycles of hybridization and reextraction (pedigree selection). However it is difficult
to exclude role of overdominance in heterosis in both autogamous and allogamous
crops.
Several recent studies on genetic basis of heterosis in
rice have came up with strong evidences in support of over-dominance.
Li et al.
(2001) studied the genetic basis of heterosis and inbreeding depression in rice
by using five interrelated mapping populations comprising a Lemont (japonica)/Teqing (indica) RIL, two BC and two test cross populations using Zhong 413
and IR64 as testers. The non-additive
gene action accounted for 62 % of trait variation while additive gene action
accounted for 28.1 % of trait variation of F1 mean values. They
found that most of the QTLs (~ 90%) contributing to heterosis were
over-dominant especially for grain yield, biomass, panicles per plant and
grains per panicle. One of the important findings of the study was that there
was no evidence of pseudo-over-dominance from repulsion phase linkage of
completely or partially dominant QTLs for yield components as proposed by Crow
(1952). Similar results were reported by Luo et al. (2001) using similar set of mapping populations. They
concluded that over-dominant loci are the major genetic basis of inbreeding
depression and heterosis in rice, especially for panicle per plant and grains
per panicle. They stated that pronounced over-dominance resulting from
epistasis by multi-locus genotypes appears to explain the longstanding dilemma
of how inbreeding could arise from over-dominant genes. Hua et al. (2003) detected many heterotic
loci in RILs from a cross between parents of Shanyou 63 and found high degree
of over-dominance in many heterotic loci. Suresh et al. (2004) studied molecular marker heterozygosity and heterosis
using a set of SSR and RAPD markers and found significant positive correlation
between marker heterozygosity and heterosis in relation to traits such as
productive tillers/plant, biomass yield and grain yield per plant.
Epistatis as
a major genetic basis of heterosis
Dominance
and over-dominance (both proposed in 1808) remained the major genetic
understandings of the cause of heterosis even though both faced contradictions.
The advent of molecular marker systems
such as isozymes, RFLP, AFLP and high
density molecular linkage maps made it possible to dissect the loci causing heterosis, in terms of
effects and dominance relationships, with more precision and reliability.
Both dominance and over-dominance concepts are based on
single-locus model. But Wright (1968) proposed that most of the quantitative
traits are conditioned by many loci and as such each gene replacement may have
effects on many characters because genes invariably do interact with each
other. He visualized a net-like
structure of population genotypes such that the variations of most characters
are affected by many loci such that each gene replacement may have effects on
many characters. Based on such a perspective, epistasis should be one of the
major genetic components in case of quantitative traits. Hallauer and Miranda
(1988) also proposed that epistasis should contribute significantly to
heterosis.
A classical study
in rice by Yu et al. 1997 using F3
population derived from bagged F2 plants from a cross between
Zhenshan 97 and Minghui 63 (Parents of Shanyou 63, the best hybrid in China
accounting for 25 % of hybrid rice acreage) (Tables 2 and 3), the most striking
finding of the study was the prevalence of epistasis in rice, with three
pronounced features.
Table 2. Summary of the
significant (p < 0.01) interactions identified in 1994 and 1995 by
searching all possible two locus interactions.
|
Trait
|
Interaction (traits)
|
1994
|
1995
|
Common
|
Yield
|
AA
|
60
|
91
|
9
|
|
AD/DA
|
51
|
73
|
3
|
|
DD
|
4
|
18
|
0
|
Tillers/plant
|
AA
|
79
|
105
|
17
|
|
AD/DA
|
28
|
42
|
1
|
|
DD
|
10
|
6
|
0
|
Grains/panicle
|
AA
|
52
|
80
|
9
|
|
AD/DA
|
56
|
74
|
10
|
|
DD
|
4
|
16
|
0
|
Grain weight
|
AA
|
84
|
102
|
27
|
|
AD/DA
|
47
|
71
|
19
|
|
DD
|
15
|
16
|
9
|
Number of Tests
|
|
7585
|
7681
|
|
Source : Yu et al. 1997
|
Table 3. Two locus
interactions for grain per panicle simultaneously detected by two-way
analysis of variance at P < 0.1 in 1994 and 1995.
|
Locus 1
|
Locus 2
|
Type
(1994)
|
Type
(1995)
|
RG532 (1)
|
RM 4 (11)
|
AA
|
AA
|
RG173 (1)
|
RM203 (3)
|
AA
|
AA
|
C547x (1)
|
RG 634 (2)
|
AA
|
AA
|
RG236 (1)
|
R1440 (7)
|
AD
DA
|
AD
DA
|
C112 (1)
|
G389a (11)
|
AA
|
AA
|
MX 7b (2)
|
Waxy (6)
|
DA
|
DA
|
C1447 (5)
|
C677 (10)
|
AA
DA
|
AA
---
|
C1447 (5)
|
G389 a (11)
|
AA
|
AA
|
G1458 x (5)
|
G342 (6)
|
AA
|
AA
|
G193 x (5)
|
G 342 (6)
|
AA
|
AA
|
RG360 (5)
|
RG653 (6)
|
AD
DA
|
AD
DA
|
RG360 (5)
|
G343 (6)
|
AD
|
AD
|
R830 (5)
|
RZ404 (9)
|
AA
DD
|
AA
DD
|
C1023 (7)
|
C794 (11)
|
DA
|
DA
|
Numbers
in parenthesis represent chromosomal
locations
|
Source : Yu et al. 1997
|
1) Two-locus analysis resolved larger number of
loci contributing to trait expression. For grains per panicle only, counting
interactions simultaneously, the significant two-locus interactions detected 25
QTLs on 9 of 12 rice chromosomes compared with 5 and 7 QTLs detected in two
years for this trait.
2) All the three
types of interactions i.e. A x A, A x D and D x D occurred among various
two-locus combinations.
3) Multiple interaction terms were found in a
considerable proportion of interacting two-locus combinations in all traits.
Lack of correlation between genotype heterozygosity and
trait expression was also observed in this study, which implies that,
collectively, the effect of dominance and/or overdominance made only limited
contributions to the heterosis. Dominant interactions (DD) were most relevant
to F1 data but AA was more commonly detected than AD and DA types.
The
study also suggested possibility of higher-order interactions at least for most
complex trait (grain yield). There are some lines of evidence implying existence
of higher-order interactions.
- Fewer QTLs were detected for yield than other traits
and smaller amount of phenotypic variation was accounted for by them.
- At the two-locus level, the numbers of interactions
detected for yield were less than component traits. This suggests involvement of genetic
components not resolved by either single locus or two- locus analysis.
- Significant
two-locus interactions revealed Chain-like relationship among interacting
two-locus combinations such that locus 1 interacted with locus 2, which in turn
interacted with locus 3 and so on and so
forth (Table 2). This implies
higher-order multi-locus interactions.
Luo et al
(2001) also found many epistatic QTL pairs for yield and yield components. Most
epistasis occurred between complementary loci, suggesting that grain yield
components were associated more with multi-locus genotypes than with specific
alleles at the individual loci.
More recently, Hua et al. (2003) studied immortalized F2 population produced by randomly intermitting
RILs derived from Zhenshan 97/Minghui 63 which are the parents of Shanyou 63,
which is the best
hybrid in China. They observed significant two-locus interactions by
two-way ANOVA across entire genome, DD interaction occurred at predominantly
high frequency, followed by AD/DA, with AA being the least frequent.
CONCLUSION
The understanding of the
phenomenon of heterosis in terms of its genetic basis is far from adequate even
after molecular dissection of the process and factors contributing to it. The
majority of the earlier studies speculated dominance and over-dominance as the
genetic mechanism of heterosis but the recent studies have revealed that
linkage and epistasis may also have a role to play (Budak et al. 2002). However, one common observation in all the studies
has been that no single hypothesis holds true for all the experiments and
crops. It is, thus likely that the heterosis is crop dependant and population
dependant. This seems to resolve the conflicting reports from experiments designed
to study the genetic basis of heterosis. Different studies which focused on
understanding genetic basis of heterosis have came up with conclusions
regarding different genetic elements such as dominance, over-dominance and
epistasis as possible genetic mechanisms responsible for heterosis. The
challenge now is how to put the pieces together to frame a comprehensive
picture (Hua et al. 2003). In case of
rice there was a strong case for dominance as depicted by Xiao et al. (1995) because there were many
points regarding over-dominance such as pseudo over-dominance or repulsion
phase linkage of dominant alleles. However, recent study of Yu et al. (1997) provided strong evidence
for two-locus and multi-locus interactions (epistasis) especially for traits
such as grain yield, which are complex in nature. They found that heterosis is
not controlled by single locus alone, whether the locus behaves in dominant or
over-dominant fashion, linkage and epistasis has a major role. Even net like
gene interaction is prevalent for most of traits including even seemingly
simple traits like days to heading.
Thus, the effects of dominance, over-dominance and
epistasis of various forms are not mutually exclusive in the genetic basis of
heterosis, as opposed to what was previously debated in favour of different
hypothesis (Allard, 1960). All of these
components have a role to play depending
upon the genetic architecture of the population (Hua et al. 2003) i. e. single-locus
heterotic effects (caused by partial, full-and over-dominance), all three forms
of digenic interactions (AA/AD/DA and
DD) and probably multi-locus interactions. Thus, these results may help
reconcile the century long debate on the role of dominance, over-dominance and
epistasis as genetic basis of heterosis.
Two different types of allele interaction, both
within-locus and inter-locus, each should play an important role in the genetic
control of heterosis. Contribution of a specific locus to heterosis could be due
to any single type of these interactions. When multiple loci are involved that
were not taken into account in the early 1900s, various combinations of
within-locus and inter-locus interactions (especially dominance x dominance
interaction) could contribute to the genetic control of heterosis. A full
understanding of heterosis will depend on cloning and functional analysis of
all genes that are related to heterosis. This process would be very similar to
that for understanding disease resistance genes that functionally appear much
simpler than heterosis (Xu, 2003).
The current research on molecular breeding with heterosis
aims at identification of specific
genomic regions in crop plants like rice (heterotic chromosome blocks)
wherein specific genomic regions
conditioning heterotic expression are to be identified in diverse lines in
parents which can be used for
development of superior hybrids. Already
in maize, the pioneer Hi-Bred International Inc. is approaching the dissection
of heterosis in maize using a Gene Calling technology. This approach uses
molecular biology and bioinformatics to dissect expressed DNA sequences
responsible for hybrid vigour. Advances in rice genomics and molecular markers
will help devise similar systems for dissection of heterosis at DNA level to
precisely understand its genetic basis for practical application in hybrid rice
development.
LITERATURE
CITED
- Alam
M. F.; M. M. R. Khan; M. Nuruzzaman; S. Parvez; A. M. Swaraz; I. Alam; N.
Ahsan. 2004.
Genetic basis of heterosis and inbreeding depression in rice (Oryza sativa L.). Journal of Zhejiang University (Science) 5 (4): 406-411.
- Allard,
R. W. 1960. Principles of Plant Breeding. John Wiley & Sons Inc.
- Ahmad,
M. I. 1996. Hybrid rice production technology. DRR, Hyderabad.
- Auger,
D. L. A. D. Gray; T. S. Ream; A. Kato; E. H. Coe, Jr. and J. A. Birchler. 2005.
Nonadditive gene expression in diploid and triploid hybrids of maize. Genetics
169: 389397.
- Birchler,
J. A.; L. A. Donald and N. Riddle. 2003. In search of molecular basis of
heterosis. Plant Cell. 15: 2236-2239
- Brewbaker,
J. L. 1964. Agricultural genetics. Prentice Hall Inc. New Jersey
- Bruce,
A. B. 1910. The Mendelian theory of heredity and augmentation of vigour.
Science 32: 627-628.
- Budak,
H.; L. Cesurer; Y. Bolek; T. Dokuyuku and A. Akaya. 2002. Understanding of
heterosis . Journal of Science and Engineering 5 (2): 68-75.
- Collins,
G. N. 1921. Dominance and vigour of first generation hybrids. American
Naturalist. 55: 116-133
- Crow,
J. F. 1952. Dominance and overdominance. In: Heterosis. Ed. J. W. Gowen. Iowa
State College Press, Ames. 282-297.
- Davenport, C. B. 1908.
Degeneration , albinism and inbreeding. Science 28: 454-455.
- East,
E. M. 1908. Inbreeding in corn. Report of Connecticut
- Agricultural Experimental
Station. 1907: 419-428.
- Guo, M.;
M. A. Rupe; C. Zinselmeier; J. Habben; B. A. Bowen and O. S. Smith. 2004. Allelic
variation of gene expression in maize hybrids. The Plant Cell 16: 17071716.
- Gustafsson,
A. 1938. Studies on genetic basis of chlorophyll formation and mechanism of
induced mutations. Hereditas. 24: 33-93
- Hallauer, A. R. and J. B. Miranda. 1988. Quantitative genetics in Maize Breeding. Iowa State College Press, Ames. 468 pp.
- Hua, J. P.; Y. Z. Xing; C. Xu; X. L. Sun; S. B. Yu and Q. Zhang. 2002. Genetic dissection of an elite rice hybrid revealed that heterozygotes are not always advantageous for performance. Genetics. 162: 1885-1895.
- Hua, J. P.; Y. Z. Xing; W. Wu; C. G. Xu; X. L. Sun; S. B. Yu and Q. Zhang. 2003. Single locus heterotic effects and dominance by dominance interaction can adequately explain the genetic basis of heterosis in an elite rice hybrid. Proceedings of the National Academy of Sciences of the United States of America 100: 2574-2579.
- Hull, F. H. 1945. Recurrent selection for specific combining ability in corn. Journal of the American Society of Agronomy 37: 134-145.
- Jinks, J. L. 1983. Biometrical genetics of heterosis. Theoretical and Applied Genetics 6: 1-46.
- Jones, D. F. 1917. Dominance of linked factors as a means of accounting for heterosis. Genetics. 2: 466-469.
- Jones, J. W. 1926. Hybrid vigor in rice. Journal of the American Society of Agronomy. 18: 423-428.
- Keeble, F. and C. Pellew. 1910. The mode of inheritance of stature and time of flowering in pea. Genetics. 1: 47-56
- Li, Z.; L. J. Luo; H. Mei; D. L. Wang; Q. L. Shu; R. Tabein; D. Zhong; J. W. Stansel; G. S Khush and A. H. Paterson. 2001. Genetic basis of inbreeding depression and heterosis in rice. Genetics. 158: 1737-1753
- Luo, L. J.; Z. Li; H. Mei; Q. L Shu; R. Tabein; D. Zhong; C. S. Ying; J. W. Stansel; G. S. Khush and A. H. Paterson. 2001. Overdominant epistatic loci are the primary genetic basis of inbreeding depression and heterosis in rice. II. Grain yield components. Genetics. 158 (4): 1755-1771
- Mir, G. N. 2002. Development of commercial hybrids for hills-problems, present status and future scope. In: Recent advances in rice production technology in hills, SKUAST-K. pp. 107-111
- Mukherjee, B. K. 1995. The heterosis phenomenon. Kalyani Publishers, India. 130 pp.
- Robin, S. 2001. Genetic basis of heterosis as explained by molecular markers. Paper presented in training Programme on "Harnessing hybrid vigour in crop plants", organised by Center for Plant Breeding and Genetics, TNAU, Coimbatore. Sept. 13-Oct. 3, 2001.
- Shull, G. H. 1908. The composition of a field of maize. Rep. of American Breed. Assoc. 4: 296-301
- Singh, P; N. R. Gupta and P. K. Singh. 2004. Analysis of components of yield heterosis in rice. In: Extended summaries of Intl. Symposium on rice- From Green Revolution to Gene Revolution. Oct 4-6, 2004, DRR, Hyderabad, India.
- Stadler, L. J. 1939. Some observations on gene variability and spontaneous mutations. Sprague Memorial Lecture, Michigan State College.
pp. 1-15.
- Stuber, C. W.; S. E. Lincoln; D. W. Wolf; T. Helenjarisand and E. S. Lander. 1992. Identification of factors contributing to heterosis in a hybrid from two elite maize inbred lines using molecular markers. Genetics. 132: 823-839
- Suresh, R.; P. Shanmugasundaram; R. C. Babu; S. Satishkumar and M. M. Gomez. 2004. Molecular marker heterozygosity in relation to heterosis for yield and drought traits in rice. In: Extended summaries of Intl. Symposium on rice- From Green Revolution to Gene Revolution. Oct 4-6, 2004, DRR, Hyderabad, India.
- Syed. N. H. and Z. J. Chen. 2005. Molecular marker genotypes, heterozygosity and genetic interactions explain heterosis in Arabidopsis thaliana. Heredity 94: 295–304.
- Swanson-Wagner, R. A.; Y. Jia; R. De Cook; L. A. Borsuk; D. Nettleton and P. S. Schnable. 2006. All possible modes of gene action are observed in a global comparison of gene expression in a maize F1 hybrid and its inbred parents. Proceedings of the National Academy of Sciences of the United States of America 103: 6805-6810.
- Tanksley, S. D. 1993. Mapping polygenes. Annual Review of Genetics 27: 205-233
- Virmani, S. S. 2004. Opportunity and challenges of developing and disseminating hybrid rice. In: Extended summaries of Intl. Symposium on rice- From Green Revolution to Gene Revolution. Oct 4-6, 2004, DRR, Hyderabad, India
- Wright, S. 1968. Evolution and genetics of population. University of Chicago Press, Chicago.
- Xiao, J.; J. Li; L. Yuan and S. D. Tanksley. 1995. Dominance is the major genetic basis of heterosis in rice as revealed by QTL analysis and molecular markers. Genetics. 140: 745-754-
- Xu, Y. 2003. Developing marker-assisted selection strategies for breeding hybrid rice. Plant Breeding Reviews. 23: 73-174.
- Yu, S. B.; K. Li; C. G. Xu; Y. F. Tan; Y. J. Gao; X. H. Li; Q. Zhang and M. A. Maroof. 1997. Importance of epistasis as genetic basis of heterosis in an elite rice hybrid. Proceedings of the National Academy of Sciences of the United States of America 94: 9226-9231.
Copyright 2006 - Revista Científica UDO Agrícola
|