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A semi-field experiment was conducted to assess the
response of ten wheat (Triticum aestivum L.)
genotypes to drought applied at booting stage by withholding 25% of field
capacity for three weeks. Flag leaves were checked for their performance under
water sufficient and deficient conditions. Split plot statistical analysis of
data revealed that irrespective of genotype, drought generally caused marked
decrease in leaf biomass, area, water content and succulence; with
non-significant effect on leaf specific area and sclerophylly. Conversely,
drought increased leaf thickness as well as the area of xylem and whole
vascular bundle, while that of phloem was non-significantly affected. Irregular
shape of mesophyll chloroplasts was identified in leaves of drought plants with
unorganized membranous system, less starch grains and more plastoglobules
compared with their well-watered synonyms. Moreover, drought significantly
decreased photosynthesis and transpiration rate as well as stomatal and
mesophyll conductance; with non-significant effect on photosynthetic water use
efficiency, internal CO2 concentration and stomatal limitation.
Significant decrease in polysaccharides was also recorded to accompany the
decrease in chlorophyll a and chlorophyll a/b ratio under drought; with marked
increase in glucose, fructose, sucrose, trehalose, total soluble sugars, total
carbohydrates as well as chlorophyll b, total chlorophyll, carotenoids and
chlorophyll stability index. Furthermore, variations among genotypes
irrespective of watering level besides their individual responses to drought
are specifically discussed. Also, drought-induced changes in the estimated
parameters are correlated. Generally, the Sids genotypes and Shandawel 1 seemed
to have the best leaf agro-histological features and the most efficient
photosynthetic machinery when droughted.
Keywords: Drought,
Gas exchange, Leaf anatomy, Photosynthetic efficacy, Ultrastructure, Wheat
Abbreviations: A:
Photosynthesis Rate; Ca: Ambient CO2 Concentration; Ci:
Intercellular CO2 Concentration; CSI: Chlorophyll Stability Index;
E: Transpiration Rate; gm: Mesophyll Conductance; gs:
Stomatal Conductance; Ls: Stomatal Limitation; pWUE: Photosynthetic
Water Use Efficiency
INTRODUCTION
Not only the plant growth stage at which stress is applied and the
stress severity are the determinant of wheat response to drought, but it is
also the genotype that greatly determines the degree of tolerance or
susceptibility to stress. Thus, there is an urgent need to identify genotypes
with reasonable vegetative traits contributing to improved yield under control
and drought conditions [7]. Therefore, the present investigation was designed
to evaluate the effect of drought on ten wheat genotypes at booting stage. For
that, some agronomic, anatomical and ultra-structural features of their flag
leaves in relation to their photosynthetic pigmentation system, gas exchange
parameters and photo-assimilates were assessed. In addition, intensive
statistical analysis of the data obtained was employed in order to elucidate
the solo effect of each of the watering level and the genotype as well as their
combined effect on the concerned plants. Correlations among the drought-induced
changes in the estimated parameters were also computed along with statistical
ranking of the addressed traits and genotypes according to their response to
drought.
MATERIALS AND
METHODS
Plant materials and
experimental design
Growth vigor of the uppermost leaf was estimated. Some leaf agronomic
features, such as fresh and dry weight, were directly scored; while others
could be calculated according to the following relations:
Water content = (fresh mass - dry mass) / fresh mass
Succulence degree = (fresh mass - dry mass) / area [8]
Sclerophylly degree = dry mass / area [8]
Succulence quotient = succulence degree / sclerophylly degree [9]
Estimation of leaf
anatomy
Firstly leaf area and specific area were determined as following:
Leaf area = length × breadth × 0.75 [10]
Specific area = area / dry mass [11]
Leaves were then fixed in formalin: acetic acid: ethanol (1: 1: 18,
v/v) for 48 h. Dehydration, clearing, staining and mounting procedures were
followed as recommended by Maiti et al. [12]. Sections were examined under
light microscope, photographed and analyzed using "Image J" version
1.38 software.
Estimation of leaf
ultrastructure
Transmission electron microscopy was carried out following Reynolds
[13]. Square sections of leaves were fixed in 2.5% glutaraldehyde and 2%
paraformaldehyde buffered in 0.1 M sodium phosphate buffer (pH 7.4). The plant
tissues were then processed, cut into ultra-thin sections and rinsed into
copper grids to be examined and photographed at 4000x using JEOL JEM-2100
transmission electron microscope at Electron Microscopy Unit, Mansoura
University, Egypt.
Estimation of
photosynthetic pigments
A known fresh weight of leaves was macerated in 80% chilled acetone in
presence of solid traces of MgCO3, centrifuged and the supernatant
was raised to a total volume. The absorbance (A) was measured at 3 wavelengths
to calculate the amount of photosynthetic pigments in µg ml-1 as
following:
Chlorophyll a = 10.3 A663 - 0.918 A644
Chlorophyll b = 19.7 A644 - 3.87 A663
Carotenoids = 5.02 A480
Estimation of leaf
gas exchange
Portable gas exchange system (LCi, ADC Bio Scientific, UK) was used to
measure some photosynthetic parameters in situ using open flow mode. Leaves
were oriented normally to the incoming radiation with average
photosynthetically active radiation of 700 µmol m-2 s-1,
temperature of 28°C and ambient CO2 concentration (Ca) of 360 µmol
mol-1 within the chamber. Various gas exchange parameters like
photosynthesis rate (A), transpiration rate (E), intercellular CO2
concentration (Ci) and stomatal conductance (gs) could be
directly measured. In addition, other parameters were calculated as following:
Photosynthetic water use efficiency (pWUE) = A / E
Mesophyll conductance (gm) = A / Ci
Stomatal limitation (Ls) = 1- (Ci / Ca) [17]
Estimation of
carbohydrates
A known dry weight of leaves was extracted with 80% ethanol; and the
alcoholic extracts were used to colorimetrically determine the amount of
glucose using O-toluidine reagent [18], fructose using resorcinol reagent [19],
sucrose and total soluble sugars using anthrone reagent [20,21]. Meanwhile,
acidic extracts; trichloroacetic acid extracts for trehalose as recommended by
Fu et al. [22] and perchloric ones for polysaccharides as recommended by
Sadasivam and Manickam [23], were used along with anthrone reagent for both.
STATISTICAL ANALYSIS
Five replicates were taken to assess the agronomic traits, while only
three were used for histological and biochemical assays.
"CoHort/CoStat" version 6.311 software was employed to analyze data
with two sets of analyses. The first set was mainly descriptive to calculate
the means and standard deviations. The second one comprised an analysis of
variance (ANOVA) at p ≤ 0.05 with one way completely randomized (1WCR) and
split plot (SP) designs; and the degree of significance was referred to as ***,
**, * or ns for respective high, medium, low or non-significant variation.
Superscript letters were given so that different superscripts indicate
significant variation. To assess the impact of drought on each of the estimated
parameters, impact index was calculated based on the SP outputs as:
100 × (drought value - control value) / control value
RESULTS AND DISCUSSION
Leaf agronomic traits are among the plant criteria mostly affected by
drought. According to SP analysis of data in Table 1, wheat genotype Sakha 93 seemed to show the maximum leaf
biomass and water content regardless of watering level. SP analysis revealed
also that drought significantly reduced leaf biomass and water content
regardless of genotype. According to 1WCR analysis in Table 1, drought significantly decreased leaf fresh mass of all
genotypes except for Shandawel 1 and Giza 186 where the recorded decrease was
non-significant. Regarding the drought-induced decrease in leaf dry mass, only
Masr 1, Gimmaza 9 and Sids (the two studied genotypes) responded by
non-significant decrease in their leaf dry mass. For leaf water content, the
drought-induced decrease was significant only in five genotypes (Masr, Gimmaza
and Sakha 94). The results recorded herein for leaf agronomic traits of wheat
plants under drought agree with those recorded by Aldesuquy et al. [25]. The
recorded decrease in leaf biomass and water content may be attributed to
drought-induced: (i) drop in cellular turgor pressure that inhibits cell
division, enlargement and differentiation [26], (ii) little assimilates supply
caused by imposed constraints on plant processes especially photosynthesis
[27], (iii) interference with nutrient availability which accompanies little
water supply [28], and/or, (iv) delayed leaf emergence and early leaf
senescence [29]. From another point of view, decreased leaf biomass under
drought can be considered as an adaptive response of the studied wheat plants
to cope with water deficit. In this regard, it was supposed that the first
strategy maintained by some plants to control water loss is to restrict leaf
growth [30].
On
contrary, SP analysis in Table 1
revealed that drought non-significantly increased leaf sclerophylly degree (dry
mass per unit leaf area); with the two Gimmaza genotypes exhibiting the maximum
leaf sclerophylly. Also, 1WCR data analysis revealed that drought caused
non-significant increase in leaf sclerophylly in all genotypes (Table 1). In this connection, Edwards
et al. [32] discussed the significance of sclerophylly on the basis of three
hypotheses that center on sclerophylly as: (i) an adaptation to water stress,
(ii) an adaptation to, or consequence of, low nutrient supply and (iii)
improvement of leaf longevity by protecting leaf and increasing its carbon gain.
Correlation among the traits addressed herein revealed that the recorded
drought-induced change in leaf sclerophylly of the ten genotypes was strongly
and negatively correlated with the change in leaf specific area (r=-0.88) (Figure 1); indicating that the
recorded non-significant increase in leaf sclerophylly in response to drought
can be attributed to the recorded non-significant decrease in leaf specific
area. Matching these results, Chartzoulakis et al. [33] recorded that olive
plants could overcome water deficit with by increasing leaf sclerophylly.
General pattern of ultrastructural alterations in response to drought
was similarly recorded elsewhere [37,38]. Disruption of leaf ultrastructure
under stress is frequently attributed to over-production of reactive oxygen
species (ROS); where chloroplasts are the major site for generating ROS as
by-products of photosynthesis. Under normal conditions, ROS are produced in
limited amounts as signaling molecules. However, ROS accumulated under stress
are highly active causing oxidative stress; with cell membranes, organelles and
biomolecules being their main targets [39]. As a consequence, serious membrane
injury along with enzyme inactivation and organelles malformations are usually
clear signs of stress. Also, the obvious appearance of plastoglobules
(lipoprotein particles regulating plastid lipid metabolism within chloroplasts)
is another indicator of stress [40]. Fewer starch grains within chloroplasts of
droughted plants can be ascribed to: (i) less water supply that may suppress
photosynthesis, (ii) adverse effect of ROS on photosystems and enzymes involved
in photosynthesis, and/or, (iii) damage of starch grains by ROS. Fat-storing
oleosomes may also appear, enlarge or increase in number to store lipids more
assembled under stress [41].
For stomatal conductance (gs) that refers to the rate of water movement out of leaf into air through stomata, its pattern of change in the present study in response to drought was typically similar to that recorded for A and E; but with higher impact index (Table 4). Reduction in gs under water stress was previously reported for other plants [59,62]. In this connection, Yang et al. [63] reported that changes in gs were closely related to leaf senescence. Furthermore, gs decreased with increasing CO2 under low water supplies; indicating that higher CO2 limited the stomata opening [34]. For that, it was found that the drought-induced change in gs in the genotypes studied herein was strongly correlated with that in A (r=0.92) and E (r=0.90) (Figure 1). Matching these results, strong positive correlations was recorded by Agnihotri et al. [61] between A and gs as well as between E and gs. Regarding mesophyll conductance (gm) that refers to the conductance of CO2 transfer from leaf intercellular air-spaces into chloroplasts, a pattern of change similar to that in gs was recorded for gm; with Sids 13 ranked in the second order after Gimmaza 9 with the maximum gm value (Table 4). Other studies showed decreased gm in different plants suffering water stress [64,65]. In this context, it was argued that significant genotypic differences in gm of wheat flag leaves under stress might result from the differences in RuBisCO activity and the anatomical features of leaves [64]. However, gm may notably have an effect on both photosynthesis and water use efficiency of plants under drought situations. Olsovska et al. [66] reported that restriction of gm may also lead to limited carboxylation efficiency. Coinciding with this assumption, the drought-induced change in gm of the studied wheat genotypes was found to be strongly correlated with that in A (r=0.86) (Figure 1).
With respect to intercellular CO2 concentration (Ci),
SP analysis revealed that drought caused non-significant increase in Ci;
with Shandawel 1 followed by Sids 13 showing the maximum Ci values.
Via 1WCR analysis, drought increased Ci values of most genotypes;
but it decreased such value in Sids 13 and Shandawel 1. The same trend was
observed for ratio of Ci to ambient CO2 concentration (Ci/Ca)
(unenclosed data) and the reverse with stomatal limitation (Ls = 1 - (Ci / Ca))
(Table 4). Also, correlation matrix
revealed a highly negative correlation between the drought-induced change in Ci
and that in Ls (r=-0.94) (Figure
1). The results reported in the present study regarding the increase in Ci
under the effect of drought are to somewhat similar to those obtained by
Siddique et al. [67] and Inoue et al. [68]. Adversely, the decrease in Ci
as a result of drought in some genotypes was reported in other studies [69,70].
In this regard, increased Ci with decreased gs may refer
to difficulty in chloroplast efficiency; since distorted chloroplast metabolism
was suggested to decrease the demand for CO2 [71]. Therefore, Inoue
et al. [68] explained that lower Ci in droughted plants might be due
to higher chloroplast activity to fix CO2 than that of
well-irrigated ones. In addition, lowered Ci might be related to
enhance photosynthetic rate in droughted plants; and thus it could be
considered as a strategy for drought tolerance. For Ci/gs,
drought caused significant increase in this ratio with Shandawel 1 having the
maximum Ci/gs value. Drought could increase Ci/gs
in all genotypes except for Masr 2; where its Ci/gs value
decreased in response to drought (Table
4). Matching such finding, Agnihotri et al. [61] while examining drought
tolerance of different rice genotypes observed that plants with high A titers
possessed low Ci/gs values and vice versa with a strong
negative correlation between these two parameters; taking into consideration
that low mesophyll efficiency can be indicated by high Ci/gs
values. Thus, drought caused significant reduction in mesophyll efficiency of
all wheat genotypes except for Masr 2. Drought-induced change in Ci/gs
of the genotypes studied herein was found to be positively correlated with the
drought-induced change in pWUE (r=0.82) but negatively correlated with gm
(r=-0.79) (Figure 1).
As the main photosynthetic product, carbohydrates represent one of the main organic components of the plant cell dry matter. However, the amount of carbohydrates in plants is usually affected by water stress. In the present study, SP analysis showed that the genotype Sids 13 had almost the highest amount of glucose, fructose, sucrose, trehalose, total soluble sugars, polysaccharides and total carbohydrates (Table 5). Irrespective of genotype, drought caused significant increase in the amount of all the assessed carbohydrates fractions and their total amount except for polysaccharides whose amount was significantly decreased under drought. Via 1WCR data analysis in Table 5, drought caused significant decrease in polysaccharides content of almost all the studied genotypes except for Sids 13 and Sakha 94 (significant increase). For the eight genotypes in which polysaccharides content decreased by drought, four of them (Masr 1, Gimmaza 11, Sids 12 and Giza 186) exhibited significant decrease in polysaccharides content while in the other four, the recorded decrease was non-significant. Similarly, Alsokari [21] recorded that water stress could reduce polysaccharides amount in cowpea plants. The stress-induced reduction in chlorophyll content along with the suppression of carbon gain and photosynthetic efficiency may account for the reduced polysaccharides amount recorded herein as a result of drought. In this regard, a strong correlation was recorded between the drought-induced decrease in polysaccharides content of the ten genotypes and the drought-induced change in their carotenoids content (r=0.77) as well as the calculated carotenoids/total chlorophyll ratio (r=1) (Figure 1). From another point of view, the recoded decrease in polysaccharides content may be a tolerance feature in terms of its carbohydrate subunits hold back for growth as suggested by Chaves et al. [73].
Table 5 also cleared that drought caused significant increase in glucose content of almost all the studied genotypes except for Gimmaza 9 and Sakha 93 (non-significant and significant decrease, respectively). Drought also increased fructose content of almost all the genotypes except for Sids 12 and Giza 186 (non-significant and significant decrease, respectively). For sucrose content, drought increased it significantly in Masr 1, Gimmaza, Sids and Sakha 94; but decreased it significantly in Masr 2, Sakha 93, Shandawel 1 and Giza 186. For trehalose content, drought increased it significantly in Masr 1, Gimmaza and Sids; but decreased it significantly in the remaining five genotypes. Matching the results recorded herein, several physiological studies documented the accumulation of various sugars in plants under limited water conditions [57,73]. Accumulation of various carbohydrates can be considered as a strategy for drought tolerance. A strong correlation between the accumulation of sugars and osmotic stress resistance had been intensively recorded [74]. Moreover, high concentration of carbohydrates along with its role in lowering water potential contributes in avoiding oxidative breakdown by ROS and preserving the structure of proteins and membranes under drought [75]. In addition, carbohydrates can act as signaling molecules for sugar-responsive genes leading to different physiological responses like defense and turgor-driven cell expansion [76]. Regarding sucrose, it can act for maintaining membrane phospholipids in the liquid-crystalline phase and preventing structural changes in soluble proteins [73]. In addition, glucose participates in cross linking with protein by a complex glycosylation reaction between amino and carbonyl groups [77]. Interestingly, it was assumed that the role of trehalose accumulation in response to water stress was very effective; since it acts as a stabilizer compound which could take part in drought tolerance. In this context, trehalose can stabilize biological structures, proteins and membrane lipids in different plants; and can also protect photosynthetic electron transport chain during water stress [78]. In the current study, a strong correlation was recorded between the drought-induced change in trehalose content of the ten wheat genotypes and that in their total carbohydrates content (r=0.95) (Figure 1).
It seemed very critical to summarize the overall leaf photosynthetic efficiency in relation to its agro-histological features of the surveyed wheat genotypes depending on the obtained data. For that, stress impact coefficient (SIC) and stress impact index (SII) were calculated to indicate the effect of drought on the estimated parameters. Irrespective of genotype, values of SIC showed that drought had general positive effect on both of the photosynthetic pigments (8% impact index) and carbohydrates content (9%). On contrary, drought had general negative effect on leaf agronomic features (-15%), anatomical features (-4%) as well as gas exchange parameters (-23%); with leaf potentiality for gas exchange being affected by drought more vigorously than leaf agronomic traits and finally came the anatomical features with the least affected degree. Regarding the various genotypes addressed herein, values of SII represented in Figure 3 indicated that drought could generally exert the lowest negative effect on leaf agronomic and anatomical features in wheat genotype Giza 186 and on gas exchange in Masr 2 [79-81]. At the same time, drought could exert the highest positive effect on leaf pigments in wheat genotype Shandawel 1; and on carbohydrates contents in Sids 12.
CONCLUSION
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