Inheritance of Antioxidant Activity of Triticale under Drought Stress
The objective of this study was to evaluate the inheritance of antioxidant activity of triticale under drought stress. For this study, the F1 seeds of a 7x7 half diallel along with their parents were grown in greenhouse in well watered and drought conditions. For this purpose, seven selected lines from breeding programs conducted previously were used as plant entries of the research. Yield and yield components were taken up to determine the best lines to be candidate for future varieties. After exposure of plants to drought stress, Catalase (CAT), the activity of Ascorbate Peroxidase (APX) and Superoxide Dismutase (SOD) enzymes were measured. Presence of over dominance and greater importance of dominance effects in control of traits was observed. All of traits had very high broad sense heritability. In stress condition among the traits APX had high narrow sense heritability (Hn), followed by moderate Hn for CAT and low Hn for SOD and in normal condition APX had highest Hn, followed by SOD with moderate Hn and CAT with low Hn. Regarding to the significant correlations between drought tolerance and antioxidant activity in the literature and considering the highest heritability of antioxidant enzymes in this experiment, it can be inferred that they can be considered as good yardstick for selecting resistance to drought in triticale.
Received: April 14, 2011;
Accepted: May 31, 2011;
Published: July 28, 2011
Adequate water and nutrient supply are important factors affecting optimal
plant growth and successful crop production. Water stress is one of the severe
limitations of crop growth especially in arid and semiarid regions of the world
as it has a vital role in plant growth and development at all growth stages
(Ahmad et al., 2009). Plants respond to diverse
environmental signals in order to survive stresses such as drought (Pastori
and Foyer, 2002). Drought leads to oxidative stress in plants due to the
production of Reactive Oxygen Species (ROS) such as the super oxide radical,
hydrogen peroxide and hydroxyl radical. Oxidative stress is one of the major
limiting factors in plant productivity. Reactive Oxygen Species (ROS) generated
during metabolic processes damage cellular functions and consequently lead to
disease, senescence and cell death. Plants have evolved an efficient defense
system by which the ROS is scavenged by antioxidant enzymes such as Superoxide
Dismutase (SOD), Calatase (CAT), Peroxidase (POX), Polyphenoloxidase (PPO) and
Glutathione Reductase (GR) (Joseph and Jini, 2010).
Drought stress invariably leads to oxidative stress in the plant cell due to
higher leakage of electrons towards O2 during photosynthetic and
respiratory processes leading to enhancement in activated oxygen species generation
(Stepien and Klobus, 2005). Photosynthesis is particularly
sensitive to water deficit because the stomatal closure to conserve water, depletes
intercellular CO2. This process reduces the availability of CO2
for photosynthesis which can lead to the formation of Reactive Oxygen Species
(ROS) from the misdirecting of electrons in the photosystem (Reddy
et al., 2004). Antioxidants are compounds that inhibit or delay the
oxidation of other molecules by inhibiting the initiation or propagation of
oxidizing chain reactions (Klein and Kurilich, 2000).
Antioxidants function by scavenging free radicals via donation of an electron
or a hydrogen atom, or by deactivation of prooxidant metal ions and singlet
oxygen (Shahidi, 2002). Morello et
al. (2002) stated that the primary role of antioxidants is to prevent
degradation induced by free radical reactions. They noted that antioxidants
function by hydrogen abstraction and metal ion assisted electron transfer. The
antioxidant donates hydrogen atoms to the free radicals, thus inhibiting the
propagation of the autocatalytic chain reaction. Drought-induced process of
stomatal closure increases the oxidative load on the plant tissue. This causing
imbalance in biochemical phatways and consequently formation of Reactive Oxygen
Species (ROS), such as super oxideradicals, hydrogen peroxide, singlet oxygen
and hydroxyl radicals (Luna et al., 2005). Stress
resistance in plants is a complex character that depends on many genes and thus
is determined by the interactions of many morphological, physiological and biochemical
processes. Antioxidative system in plants has been composed of several enzymatic
and non-enzymatic components that are being active in a differential manner
in response to drought stress in different plants (Gholizadeh,
2010). There are different arrays of mechanisms that plant breeders use
to study the adaptive response of different genotypes and as criteria for selection
under unfavorable conditions (Hefny and Abdel-Kader, 2007).
Usually, oxidative system is controlled/balanced by antioxidative system during
the normal growth and developments in plant system. Although, plants commonly
activate their total antioxidation machinery in response to drought stress situations
but it has been well shown that different plants exhibit different responses
to stress in terms of various redox enzymes activities. Habibi
et al. (2004) and also Saleh and Plieth (2009)
in theirs studies have been shown that drought stress in plants induces the
oxidative burst that is obviously followed by the activation of their antioxidative
system (Gholizadeh, 2010). Oxidative stress is also
a factor in abiotic and biotic stress phenomena that occurs when there is a
serious imbalance between the production of Reactive Oxygen Species (ROS) and
antioxidant defense. ROS have been considered mainly as dangerous molecules
and their concentrations must be maintained as low as possible (Amirjani,
2010). Chelikani et al. (2004) indicated
that Catalase is a common enzyme found in nearly all living organisms that are
exposed to oxygen, where it functions to catalyze the decomposition of hydrogen
peroxide to water and oxygen. It is a tetramer of four polypeptide chains, each
over 500 amino acids long (Joseph and Jini, 2010). Molecular
genetic maps have been developed for major crop plants, including rice, wheat,
maize, barley, sorghum and potato, which make it possible for scientists to
tag desirable traits using known DNA landmarks. Molecular genetic markers allow
breeders to track genetic loci controlling stress resistance without having
to measure the phenotype, thus reducing the need for extensive field-testing
over time and space. Moreover, gene pyramiding or introgression can be done
more precisely using molecular tags. Together, molecular genetic markers offer
a new strategy known as marker assisted selection. Another molecular strategy
which depends on gene cloning and plant transformation technology, is genetic
engineering of selected genes into elite breeding lines. What makes a particular
goal attainable or unattainable in genetic engineering experiments is the availability
of the following three inputs: (1) the gene of interest, (2) an effective technique
for transferring the desired gene from one species to another and (3) promoter
sequences for regulated expression of that gene. Amongst these, the first is
considered a rate-limiting factor (Joseph and Jini, 2010).
Higher plants have active oxygen scavenging systems consisting of several antioxidant
enzymes, such as Superoxide Dismutase (SOD), Ascorbate Peroxidase (APX), Catalase
(CAT) and Glutathione Reductase (GR) and some low molecules of non-enzyme antioxidants
(Grene, 2002). These cytotoxic oxygen species are highly
reactive and in the absence of any protective mechanism they can seriously disrupt
normal metabolism through oxidative damage resulting in lipid peroxidation and
consequently membrane injury, protein degradation, consequently membrane injury,
protein degradation, enzyme inactivation, pigment bleaching and disruption of
DNA strands (Pan et al., 2006; Quiles
and Lopez, 2004). Antioxidant enzymes can be measured easily and are nondestructive
to whole plant. So they potentially can be considered as selection criteria
if they also have high heritability. The objective of this study was to evaluate
the inheritance of heritability under drought stress.
MATERIALS AND METHODS
Seven triticale lines (Table 1) were crossed in half diallel
fashion at the experimental farm of Seed and Plant Improvement Institue (SPII),
Iran in 2008. The F1 seeds, along with their parents were grown in greenhouse
in well water and drought conditions using randomized complete block design
with three replications in 2009. Grains of the lines were sown in plastic pots
filled with 12 kg of soil composed of a mixture of garden soil, compost and
sand (1:1:1, v/v). Well-watered plants were irrigated to water-holding capacity
in 3 day intervals.
|| List of lines used in the study
|DR: Drought resistance, R: Resistant, MR: Moderately resistant,
S: Susceptible, GH: Growth habit, W: Winter, F: Facultative, S: Spring
The drought stress was started at the mid-flowering stage. Drought was imposed
by withholding water until 80% soil moisture depletion and then adding only
20% of the water given to the control pots. Two weeks after onset of drought
stress, flag leaves were collected from both control and stress treatments for
Enzyme extraction and determinations of enzymes activity: Leaf tissues
were ground to fine powder in liquid nitrogen, then enzyme extraction was done
according to Sairam et al. (1998). Catalase was
assayed by the method of Maehly and Chance (1954). The
activity of SOD was measured according to the method of Giannopolitis
and Ries (1977). The APX activity was assayed by the method of Nakano
and Asada (1981). The enzyme activities were expressed in terms of specific
activity (Unit/mg Fresh Weight).
Statistical analysis: The diallel analysis was done according to the
theoretical basis developed by Hayman (1954a), adapted
for the half diallel by Walters and Morton (1978). The
goodness of fit of the additive-dominant model was did based on the analysis
of variance of Wr-Vr (difference between array parent-offspring covariance and
array variance) and linear regression of Wr (array parent-offspring covariance)
on Vr (array variance). The genetic components: D, H1, H2, F and h 2 were estimated
by method of Singh and Singh (1984). Standard errors
of these components were calculated from expected and observed values of Wr,
Vr, V r, Vp and (mL1- mL0) over replications. From the estimates of the genetic
components, the genetic parameters presented in Table 4 were
estimated. Broad sense heritability, narrow sense heritability and average degree
of dominance were calculated according to Mather and Jinks
(1971). Analysis of variance of diallel was performed using the DIAL98 software
Ukai (1989) and genetic components were estimated by
electronic spreadsheets in the Excel program (Microsoft® Excel 2003).
In Table 2, it is recognizable that no one from treatments
(seven lines) for CAT, APX and SOD was not significant. For CAT, APX and SOD
Lowest value was 0.00019 related to Rep (for stress condition in CAT and also,
highest value was 1.68 for Rep (Repetition) in stress condition linked to APX
(Table 2). The results of the goodness of fit of the additive-dominant
model are in Table 2 and 4. The Analysis
of variance of the diallel is shown in Table 3. In normal
condition all sources of variation in Table 3 for APX and
SOD were nonsignificant. In Table 3, highest value was 20.69
for b1 (component which measures the mean deviations of the F1s from the mid-parental
values) in stress condition in related to APX and lowest value was 0.00021 for
Rep in normal condition about CAT. Non significant Wr-Vr mean squares for treatment
indicate the adequacy of additive dominant model for all of traits. The b1 component
which measures the mean deviations of the F1s from the mid-parental values was
highly significant for SOD and APX activity. For CAT and APX activities in normal
condition, the slop of linear regression (b) was significantly lower than unit
and additive-dominant model was not satisfied (Table 4).
|| Goodness of fit of additive-dominant model based on ANOVA
|ns: Non-significant, *and**: Significant at p<0.05 and
|| Analysis of variance of the diallel tables for the evaluated
|S.V: Source of variation, ns: Non-significant, *and** significant
at p<0.05 and 0.01, respectively. a: Additive variance, b: Dominant genetic
effects, b1: Component which measures the mean deviations of the F1s from
the mid-parental values, b2: Indicator presence of asymmetry in the distribution
of alleles among the parents, b3: Specific combining ability variance
|| Estimates of genetic components and related statistics in
|ns: Bon-significant, *and** significant at p<0.05 and 0.01,
respectively, D: Additive genetic variance, H1: Uncorrected dominance genetic
variance, H2: Corrected dominancevarianc , F: Average covariation of additive
and dominance effects, h: Dominance effects (as algebraic sum over all loci
in 2 heterozygous phase in all crosses), Averaged: Average degree of dominance,
H2/4 H1: Relative distribution of positive and negative genes among parents,
KD/KR: Relative distribution of dominant and recessive genesamong parents,
h2/H: The number of effective factors that showed ominance, Hb: Broad senseheritability,
Hn: Narrow sense heritability, E: Environmental variance (errormeans quare
of simple ANOVA divided by number of replications), rYr( Wr+Vr): Relation
between the favorable alleles and dominance, F1-P: Magnitudeofdominance
b (Wr/Vr): Slope of regression line of Wr on Vr
For CAT and APX activity, additive variance (a component) was highly significant
in stress condition, indicating the presence of additive effects in the control
of these traits. However, this component was not significant in activity of
SOD. The significance of a (additive variance) in Table 2
was elegant with the significance of additive effects (D component) in Table
4. Significance of b1 part was generally in accordance with higher magnitude
of dominance ( ) and this indicated that F1s (all hybrids) had higher enzymatic
activity than their parents under stress. The b source of variation (dominant
genetic effects) also showed highly significant effects for all of traits under
stress condition. This proves the importance of dominant genetic effects as
well as additive effects in the control of all of traits. The b2 (component
that measures average heterosis) section was significant only for APX activity
under stress. The proportion of positive and negative genes was calculated by
(H2/4H1) in Table 4. This ratio was lower than 0.25 in CAT
activity and APX (under stress), indicating the presence of asymmetry in the
distribution of the positive and negative alleles in the parents. The b3 component
which is synonym with specific combining ability variance was significant for
all of traits under stress. Positive values for F substantiated by KD/KR (relative
distribution of dominant and recessive genes among parents) being greater than
1 and vice versa. The estimate of the genetic component F was non significant
in all cases which is an indication of symmetry in the distribution of dominant
and recessive alleles in the parents. However, the ratio of the total number
of dominant and recessive alleles in the parents (KD/KR) was higher than 1 for
CAT activity, indicates a higher frequency of dominant alleles in the parents,
this ratio was lower than 1 in the case of APX (under stress) and SOD activity.
For all of traits positively significant h (dominance effects (as algebraic
sum over all loci inheterozygous phase in all crosses) alues were recorded (Table
4). The degree of average dominance was higher than 1, indicating the presence
of over dominance in control of these chracterss. Contribution of over dominance
also confirmed by higher heterosis (117%) in SOD activity (Table
4). The number of groups of genes that control the trait and exhibit dominance
(h2/H2) ranged from 0.195 to 5.327 (H2 = corrected dominance variance). In general
SOD had the highest number of dominant genes followed by APX and CAT activity.
The values of the broad sense heritability (Hb) ranged from 0.461-0.930. The
differences observed between the Hn and Hb reflected the presence of the dominant
effects. Narrow sense heritability of traits ranged from 0.117 to 0.627. Among
the traits CAT activity had the highest Hn, followed by APX with moderate Hn
and SOD with low Hn (under stress) and in normal condition APX had highest Hn,
followed by SOD with moderate Hn and CAT with low Hn. Non-significant correlation
coefficients between the parental means and order of dominance rYr (Wr+Vr) were
observed for all characterss indicating that there is not a strong relation
between dominance and isotropic of traits.
The degree of average dominance also was shown by the intercept point between origin and regression line. As shown in Table 4, only the intercept of SOD activity (under drought stress) was significantly lower than zero proving its over dominance.
Drought stress cause molecular damage to plant cells, that directly or indirectly
the reason for the formation of Actived Oxygen Species (AOS). Moreover, it inactivates
antioxidant enzymes which are very important for H2O2
scavenging such as catalases (Kono and Fridovich, 1983)
and peroxides (Esfandiari et al., 2007). Drought
stress increased the superoxide level in cells. If this radical is not scavenged
by SOD, it disturbs vital bimolecular (Mittler, 2002).
Candan and Tarhan (2003), Martinez
et al. (2001), Zhao et al. (2006)
and Esfandiari et al. (2007) had similar findings
and expressed that the increase in SOD activity and decrease in oxidative damage
were closely related. Cloned plant genes and transgenic plants have become a
standard tool in plant-stress biology. These technologies have mainly been applied
to model systems and have greatly enlarged the knowledge of mechanisms of tolerance.
The various abiotic stresses cause changes in plant processes at all levels
of organization (morphological, physiological, biochemical and molecular). In
recent years, attention has focused on alterations in gene expression. The list
of genes whose transcription is upregulated in response to stress is rapidly
increasing. Functions for some of these polypeptides are close to being identified
and their likely role in stress physiology is being determined. The understanding
of mechanisms that regulate gene expression and the ability to transfer genes
from other organisms into plants will expand the ways in which plants can be
utilized (Joseph and Jini, 2010). Due to the importance
of dominance in the control of characters in this experiment, especially APX
and CAT activity, it was suggested that the evaluations of lines must be done
at advanced generations of inbreeding. Costa et al.
(2005) found increase in CAT activity when sorghum plants subjected to 75
mM NaCl and the increase was more conspicuous in tolerant than in sensitive
genotype. Sairam et al. (2002) stated that scavenging
of H2O2 as represented by GR and CAT is limited and less
efficient in susceptible wheat genotypes leading to higher H2O2
accumulation and increasing in lipid peroxidation under water limited environments
(Hefny and Abdel-Kader, 2007). Based on the results
of this study it was concluded that the activity of antioxidant enzymes under
drought stress adequately can be described by additive-dominance model. For
APX and CAT activity under stress, additive effects as well as dominant effects
were significant. However, in SOD activity, additive effects were not significant.
Since the degree of average dominance was higher than 1, the presence of over
dominance and greater importance of dominance effects in control of traits was
suggested. In general, all of traits had high broad sense heritability and its
magnitude was higher under stress than normal conditions but such trend did
not observed in narrow sense heritability. Since CAT and APX were controlled
by relatively fewer numbers of dominant genes than SOD, it seems that they can
be more easily manipulated in plant breeding programs. The results also showed
that, effect dominance was predominantly in one direction except for CAT activity,
indicating the presence of heterosis in the control of these two traits. These
findings get support from previous studies on wheat by Nayyar
and Gupta (2006) and Angra et al. (2010).
According to Bernardo (2002), individual plant measurements
of quantitative traits are prone to large nongenetic effects making estimates
of heritability higher. The significance of the b1 component indicates that
the dominance was predominantly in one direction and measures average heterosis
(Singh and Singh, 1984). The significance of the b2
portion indicated that the mean dominance deviations of the Fs from their mid
parental values differed significantly over the F arrays; this proves the presence
of asymmetry in the distribution of alleles among the parents (Hayman,
1954b). This means that there was evidence that some parents had a significantly
better performance than others (Ramalho et al., 1993).
Results obtained about this study from other reviewers are in support ours study
but only Saleh and Plieth (2009) reported that the activity
of peroxidase has been already reported to be remarkably increased in the case
of pea, while its activity is highly decreased in gardencress pepperweed plant
Regarding to the highest heritability of antioxidant enzymes in this study,
it can be concluded that they can be considered as good criterion for selecting
drought tolerance in tritcale. Since CAT and APX were controlled by relatively
fewer numbers of dominant genes than SOD, it seems that they can be more easily
manipulated in plant breeding programs. The results also showed that, effect
dominance was predominantly in one direction except for CAT activity, indicating
the presence of heterosis in the control of these two traits. Antioxidative
mechanism seems to be not enough to protect plants from the elevated environmental
stresses such as drought. Transgenic plants over expressing single transgene
of SOD, APX and GR separately in chloroplast or other compartment of plant cell
were generated and displayed increased tolerance against the oxidative stress.
The authors would like to thank from SSII for providing the plant material.
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