Early selection of bread wheat genotypes using morphological and photosynthetic attributes conferring drought tolerance

Journal of Integrative Agriculture 2019, 18(11): 2483–2491 Available online at www.sciencedirect.com

ScienceDirect

RESEARCH ARTICLE

Early selection of bread wheat genotypes using morphological and photosynthetic attributes conferring drought tolerance Hafiz Ghulam Muhu-Din Ahmed1, Abdus Salam khan1, LI Ming-ju2, Sultan Habibullah Khan3, Muhammad Kashif1 1

Department of Plant Breeding and Genetics, University of Agriculture Faisalabad, Faisalabad 38000, Pakistan Institute of Agricultural Environment and Resources, Yunnan Academy of Agricultural Sciences, Kunming 650205, P.R.China 3 Center of Agricultural Biotechnology and Biochemistry, University of Agriculture Faisalabad, Faisalabad 38000, Pakistan 2

Abstract Genetic diversity is the base of any genetic improvement breeding program aimed at stress breeding. The variability among breeding materials is of primary importance in the achievements of a good crop production. Herein, 105 wheat genotypes were screened against drought stress using factorial completely randomized design at seedling stage to determine the genetic diversity and traits association conferring drought tolerance. Analysis of variances revealed that all the studied parameters differed significantly among all genotypes, indicating the significance genetic variability existed among all genotypes for studied indices. The 10 best performance genotypes G1, G6, G11, G16, G21, G26, G39, G44, G51, and G61 were screened as drought tolerant, while five lowest performance genotypes G3, G77, G91, G98, and G105 were screened as drought susceptible. Root length, chlorophyll a, chlorophyll b, and carotenoid contents were significantly correlated among themselves which exhibited the importance of these indices for rainfed areas in future wheat breeding scheme. Shoot length exhibited non-significant and negative association with other studied traits, and its selection seems not to be a promising criteria for this germplasm for drought stress. Best performance genotypes under drought stress conditions will be useful in future wheat breeding program and early selection will be effective for developing high yielding and drought tolerant wheat varieties. Keywords: drought, photosynthesis, chlorophyll, wheat, seedling, carotenoid

1. Introduction

Received 2 March, 2018 Accepted 25 July, 2018 Correspondence Hafiz Ghulam Muhu-Din Ahmed, E-mail: [email protected]; LI Ming-ju, E-mail: lily69618@163. com © 2019 CAAS. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http:// creativecommons.org/licenses/by-nc-nd/4.0/). doi: 10.1016/S2095-3119(18)62083-0

Crop productivity faced with many challenges, one of the major challenge is drought, which is primarily due to alterations in precipitation pattern and short rain fall (Toker et al. 2007). For breeding water deficit tolerance, it is very important to first know the mechanism and behavior of plant under drought environments. Many reasons contribute concerning the complexity of drought tolerance mechanism like, crop species, intensity, period of stress, and plant growth stage (Mir et al. 2012). Survival of plant under drought can

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be adopted more than one tolerance mechanisms at a time of drought. In that regard, there are three fundamental mechanisms which a plant can acclimatize to manage with the water shortfall: (i) Escape, (ii) avoidance or tolerance, and (iii) resistance mechanisms (Waqas et al. 2013: Ahmed et al. 2017). In escape mechanism, plant finalizes its life cycle in advance the water deficit. In tolerant mechanism, plants take paces to get by with water shortage conditions, e.g., closing of stomata, reducing the rate of transpiration in the plant body. In drought resistant mechanism, plant proceeds phases against water deficit condition by the upkeep of the photosynthetic pigments and maintains rootto-shoot ratio for effectively portioned the whole assimilated (Ashfaq et al. 2016). Vigorous seedling is imperative in defining the yield of plant in short period of time (Noorka and Khaliq 2007). A genotype with drought stress tolerance has more impenetrable rooting facilities to boost the preoccupation of soil moisture and reduces the special effects of water shortfalls during development and growth (Zhong and Wang 2012). Root, the prime portion of wheat plant, is influenced primarily by drought. Lengthy roots confirm the accessibility of moisture from the deepness of the soil and assure the adaptation in drought stress environments. Length of root at the primary stages of the plant is important traits for enhancing yield under rain-fed environments (Shabazi et al. 2012). According to these scientists, growth of wheat seedling is affected under water deficiency conditions, but the effect is different from genotype to genotype. Selection of genotypes with better performance during drought stress conditions could rise the production of rainfed areas (Noork and da Sileva 2012; Waqase et al. 2013). Selection of genotypes on the basis of seedling attributes is easy, cheap, and less laborious. Similarly, seedling indices reveal moderate to high variability with additive types of gene action across environments (Waqas et al. 2013; Ahmed et al. 2018), thus have an advantage of effective screening at primary stage. Reduced or unaffected chlorophyll contents under water shortage conditions have been described in various species, provisional on the period and intensity of drought stress. The level of chlorophyll contents alters during drought conditions. The carotenoid play vital roles and benefit for plants to resist water shortage stress (Jaleel et al. 2009). Drought stress prevents the synthesis of chlorophyll a/b and declines the binding proteins, leading to decrease of the light-harvesting pigment protein allied with photosystem II (Anjum et al. 2011). The possessions of drought stress on chlorophyll and carotenoid levels have been examined in various major field crops. The succeeding experiment was directed for screening of 105 miscellaneous wheat accessions for drought tolerance

on the basis of seedling attributes and to define the link of studied seedling indices under normal and water stress environments. This will provide a theoretical basis of drought resistance abilities for dryland farming in the semiarid and rainfed regions.

2. Materials and methods 2.1. Experimental design Experiment was planted using 15 cm×15 cm sand filled polyethylene bags in the screen house of the Plant Breeding and Genetics, University of Agriculture Faisalabad, Pakistan following completely randomized design under factorial with three replications in normal and water stress environments.

2.2. Experimental materials The experimental material consisted of 105 spring wheat genotypes (Appendix A). Two seeds per polyethylene bag were sown and thinned to one seedling per bag after germination. Five bags per genotype were used for each replication. One set of genotypes has been regularly irrigated (100% of field capacity) while the other set of same wheat genotypes was kept under water deficient stress (at 50% field capacity) after application of watering on sowing. The field capacity (FC) of the soil used in the experiments was calculated with pressure membrane chamber apparatus (Gugino et al. 2009).

2.3. Studied parameters Data of the shoot length, root length, chlorophyll a and b, and carotenoid contents were measured from 3-wk-old wheat seedlings from both environments. The chlorophyll a and b were measured by using the following formula (Lichtenthaler 1983; Lohithaswa et al. 2013): Chl a (mg g–1)=[12.7×(OD663)–2.69×(OD645)]×V/1 000×W Chl b (mg g–1)=[22.9×(OD645)–4.68×(OD663)]×V/1 000×W where V, volume of extract; W, weight of fresh leaves; OD, optimal density. The carotenoid content was calculated by using following formula (Robbelen et al. 1957): Carotenoids=Acar/EM×100 where the unit of carotenoids is mg g–1 fresh weight, Acar=[(OD480)+0.114×(OD663)]–0.638×(OD645), Em=2 500.

2.4. Statistical analysis Scored data were exposed to analysis of variance (ANOVA) technique (Steel et al. 1997). Those characters displayed significant differences between studied genotypes were

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further investigated for correlation and analysis (Ogunbayo et al. 2005).

3. Results A total of 105 spring wheat genotypes were screened in the green house using factorial under completely randomized design. Highly significant differences were exhibited among accessions under normal and drought conditions for all studied traits (Table 1). The summary statistics of five seedling traits (Table 2) and means performance of 105 genotypes under both conditions. All the studied characters exhibited fluctuations in mean value under drought conditions for most of the genotypes.

3.1. Morphological attributes Recorded data for root length of wheat seedling varied significantly, ranged from 7.22 to 23.00 cm under normal condition while in water stress condition ranged from 5.31 to 17.65 cm as shown in Table 2. The genotypes G11 and G61 had the maximum root length 23.00 and 17.65 cm under normal and drought conditions, respectively, while the lowest root length with the mean values of 7.22 and 5.31 cm observed in G98 and G105 under normal and stress conditions respectively as displayed in Fig. 1. Shoot length of wheat is an important character and is also affected by drought stress. The phenotypic behavior

of any character is due to the environment and genotype (G×E) interaction. Shoot length varied significantly, ranging from 13.16 to 29.17 cm under normal and under drought conditions ranging from 11.00 to 25.19 cm (Table 2). The G105 and G3 had the maximum shoot length 29.17 and 25.19 cm under normal and stress conditions, respectively, while the lowest shoot length with the values of 13.16 and 11.00 cm was observed in G32 and G51 under normal and drought conditions respectively (Fig. 1).

3.2. Photosynthetic attributes All studied wheat genotypes behaved differently in terms of seedling’s photosynthetic pigments against drought conditions. Chlorophyll a for studied genotypes varied significantly ranging from 1.37 to 1.64 mg g–1 under normal condition and under water stress conditions ranged from 1.35 to 1.62 mg g–1 as shown in Table 2. The G21 and G6 had the maximum chlorophyll a with the values of 1.64 and 1.62 mg g –1 under normal and stress conditions, respectively, while the lowest chlorophyll a with the values of 1.37 and 1.35 mg g–1 observed in G91 and G105 under normal and stress conditions, respectively (Fig. 2). Data collected for chlorophyll b for all genotypes (Table 2) varied significantly ranging from 0.46 to 0.64 mg g–1 under normal environments while under drought conditions ranged from 0.39 to 0.57 mg g–1. The genotypes G39 and G26 had the maximum chlorophyll b with the values

Table 1 Analysis of variance (ANOVA) mean square of 105 spring wheat genotypes at seedling stage under normal and drought conditions Trait SoV/df1) Root length Shoot length Carotenoid Chlorophyll a Chlorophyll b

Genotype (G) 104 61.15** 39.51** 0.00669** 0.02483** 0.00701**

Environment (E) 1 1 749.07** 3 792.76** 3 792.76** 0.01939** 0.76442

G×E 104 6.86** 8.55** 8.55 ns 0.00074 ns 0.00007**

Error 420 3.13 2.1 2.1 0.00151 0.0005

Total 629          

1) **

SoV, sources of variation; df, degree of freedom. , significance at P=0.01; ns, non significant.

Table 2 Mean summary statistics of five seedling traits of 105 spring wheat genotypes under normal and drought conditions Trait Root length (cm) Shoot length (cm) Carotenoid (mg g–1 FW) Chlorophyll a (mg g–1 FW) Chlorophyll b (mg g–1 FW)

Environment Normal Drought Normal Drought Normal Drought Normal Drought Normal Drought

Minimum 7.22 5.31 13.16 11.00 0.32 0.24 1.37 1.35 0.46 0.39

Maximum 23.00 17.65 29.17 25.19 0.49 0.41 1.64 1.62 0.64 0.57

Mean 11.66 8.32 22.69 17.79 0.40 0.33 1.48 1.47 0.54 0.47

SD 4.005 2.542 2.965 2.755 0.034 0.034 0.066 0.065 0.034 0.034

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RL-N

RL-D G105 G1 G103 G101 30 G99 G97 25 G95 G93 20 G91 G89

SL-N G3 G5

SL-D G7

G9

G11 G13 G15 G17

15

G87

G19 G21

10

G85 G83

G23

5

G25

0

G27

G81 G79

G29

G77

G31

G75

G33

G73

G35

G71

G37

G69 G67 G65 G63 G61 G59

G57 G55

G53 G51

G49

G39 G41 G43 G45 G47

Fig. 1 Performance of wheat seedling traits of 105 genotypes under normal and drought conditions. RL, root length; SL, shoot length; N, normal; D, drought; G, genotypes.

of 0.64 and 0.57 under normal and stress conditions, respectively, while the lowest chlorophyll b with the values of 0.46 and 0.39 observed in G91 and G98 under normal and stress conditions respectively as displayed in Fig. 3. Carotenoid contents for all accessions varied significantly from 0.32 to 0.49 mg g–1 under normal conditions and in drought conditions ranged from 0.24 to 0.41 mg g–1 (Table 2). The G11 and G51 had the maximum carotenoids with the values of 0.49 and 0.41 mg g–1 under normal and stress conditions, respectively, while the lowest carotenoids with the values of 0.32 and 0.24 g observed in G77 under normal and stress conditions (Fig. 3).

4. Discussion All the studied characters exhibited fluctuations in mean value under drought condition for most of the genotypes. Mean values for seedling traits in spring wheat were decreased under drought condition. Similar findings have been reported by Khan et al. (2002). Such kind of information was also observed by Dhanda et al. (2004). Those accessions resist in variation of performance for studied characters under drought environments which were

considered as drought tolerant.

4.1. Morphological attributes Root length is a significant parameter against drought stress; in general, genotypes with greater root length have the potential for drought resistance (Leishman and Westoby 1994). This was further strengthened by present findings that the genotype G61 under drought stress had the maximum root length considered as drought tolerant genotypes. Using root length parameter, the best tolerant genotypes were G61 followed by G11 and G1, while drought susceptible genotypes were G105 followed by the genotype G77 (Table 3). It has been proposed that progress in breeding wheat for drought tolerance can be expected from selection for increased root length (Dhanda et al. 2004). The influence of root architecture on yield and other desired characters, especially under drought environments, has been widely reported in all major crops (Tuberosa and Salvi 2006; de Dorlodot et al. 2007). Stimulated root growth of wheat strains under drought stress has also been reported by Chachar et al. (2014). Using shoot length parameter, the best tolerant genotypes were G51 followed by G44, while drought

Hafiz Ghulam Muhu-Din Ahmed et al. Journal of Integrative Agriculture 2019, 18(11): 2483–2491

Chl a-N G105 G1 G103 G101 1.7 G99 G97 G95 1.6 G93 G91 1.5 G89 G87 G85 G83

Chl a-D G3

G5

G7

G9

G11 G13 G15 G17 G19

1.4

G21 G23

1.3

G81

G25 G27

1.2

G79

2487

G29

G77

G31

G75

G33

G73

G35

G71 G69 G67 G65 G63 G61 G59 G57 G55

G37

G53

G39 G41 G43 G45 G47 G51G49

Fig. 2 Performance of wheat seedling traits of 105 genotypes under normal and drought conditions. Chl a, chlorophyll a; N, norma; D, drought; G, genotype.

sensitive genotypes were G3 followed by G98 under drought stress conditions as displayed in Table 3. Those genotypes having the minimum shoot length and the maximum root length under drought stress considered as drought tolerant genotypes. Conclusively, selection based on seedling length combined with extensive root system, could be resulted in better adaptation to dry land environments. Ahmad et al. (2013) and Faisal et al. (2017) also evaluated the decrease in seedling’s growth, including seedling length and seedling weight with an increase in water deficient stress and their results are in line with the present study.

4.2. Photosynthetic attributes Considering chlorophyll a character, the best tolerant genotypes were G6 followed by G11 and G16, while drought sensitive genotypes were G105 followed by G77 under drought stress conditions as mentioned in Table 3. However, the amount of chlorophyll under drought conditions decreased with the increase in the duration of drought stress probably due to the destruction of chloroplast envelope by drought stress. The reduction in chlorophyll content under drought stress has been taken a distinctive symptom of oxidative stress and may be the

result of photo-oxidation of photosynthetic pigments (Anjum et al. 2011). Using chlorophyll b attribute, the best tolerant genotypes were G26 followed by G39 and G21, while drought susceptible genotypes were G98 followed by G91 (Table 3). In plant cells, photosynthesis is a key process which regulates in water culture medium under low concentration. If chlorophyll pigments concentration increases, photosynthesis system will be more efficient. Chlorophyll contents caused more reduction in all wheat genotypes with the increment in levels of water stress because thylakoid membranes disintegrate upon dehydration of cells (Kalaji et al. 2016). Previous studies also highlighted the reduction in chlorophyll under water deficit conditions (Farshadfar and Amiri 2105; Seher et al. 2015) while tolerant genotypes maintained better amount of these pigments under drought stress (Zeng et al. 2016; Pour-Aboughadareh et al. 2017). Considering carotenoid trait, the best tolerant genotypes were G51 followed by G6 and G1, while drought susceptible genotypes were G77 followed by G98 under drought stress conditions as discussed in Table 3. Carotenoids are responsible for scavenging of singlet oxygen and hence their comparative levels in a genotype will determine its relative

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CTD-N

CTD-D

Chl b-N

G105 G1 G103 G101 0.7 G99 G97 0.6 G95

G93 G91

G3 G5

0.5

G87

G9

G11 G13 G15 G17

0.4

G89

G7

Chl b-D

G19

0.3

G85

G21

0.2

G83 G81 G79

G23

0.1

G25

0

G27 G29

G77

G31

G75

G33

G73

G35

G71

G37

G69 G67 G65 G63 G61 G59

G57 G55

G53

G39 G41 G43 G45 G47 G51 G49

Fig. 3 Performance of wheat seedling traits of 105 genotypes under normal and drought conditions. CTD, carotenoid; Chl b, chlorophyll b; N, normal; D, drought; G, genotype.

Table 3 Performance of studied wheat genotypes under drought stress Trait Root length Shoot length Chlorophyll a Chlorophyll b Carotenoid

Best tolerant genotype G61 followed by G11 and G1 G51 followed by G44 G6 followed by G11 and G16 G26 followed by G39 and G21 G51 followed by G6 and G1

tolerance. Higher chlorophyll and carotenoid contents in tolerant genotypes have also been reported in earlier findings of Lichtenthaler and Wellburn (1983), Livingston et al. (2009), and Lohithaswa et al. (2013). Photosynthetic pigments (Chl a and b and carotenoid) were reduced with increase in water scarcity and those genotypes exhibited better chlorophyll contents under drought stress were categorized as drought tolerant. Photosynthetic pigment contents of wheat genotypes were affected by drought (Farshadfar and Amiri 2015).

4.3. Correlation among wheat seedling traits Correlation coefficient describes the degree of association between two variables. It is useful in plant breeding because

Susceptible genotype G105 followed by G77 G3 followed by G98 G105 followed by G77 G98 followed by G91 G77 followed by G98

it can indicate a predictive link that can be exploited in practice and provides the information about the association among various desired characters. In the current study, information about the association of seedling traits under normal and drought conditions may further help to develop the strategies for indirect selection (Table 4). Simple correlation coefficients of root length exhibited positively strong association with carotenoid and chlorophyll a while negatively correlated with shoot length. The same results were reported by Ahmad et al. (2006). Shoot length negatively correlated with all studied traits, but with chlorophyll a showed non-significant association. Findings of Khan et al. (2013) were not similar with these findings which observed that root length positively was correlated with shoot length. This indicated that the underground

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Table 4 Correlation matrix among wheat seedling traits under normal and drought conditions Trait Shoot length Carotenoid Chlorophyll a Chlorophyll b *

Environment Normal

Root length 0.11 ns

Shoot length

Drought

–0.33**

Normal

0.46**

–0.04 ns

Drought

–0.47**

0.15 ns

Normal

0.42**

0.07 ns

0.68**

Drought

0.44

*

0.01 ns

0.65*

Normal

0.51

*

Drought

0.48**

–0.24

*

0.02 ns

Carotenoid

Chlorophyll a

0.58**

0.48*

0.62**

0.82**

**

and , significant at P=0.05 and P=0.01, respectively; ns, non significant.

part of the plant plays an important role under drought stress conditions (Dhanda et al. 2004). Higher chlorophyll and carotenoids contents in tolerant genotypes have also been reported earlier by Livingston et al. (2009) and Lohithaswa et al. (2013). Ul-Allah et al. (2014) conducted an experiment and their findings related to current study in term of that shoot length is negatively correlated with root length. In this experiment, strong association exists of the carotenoid with chlorophyll a and b. Chlorophyll b had negative association with shoot length. Chlorophyll a had non-significant positive correlation with shoot length while the remaining studied traits exhibited the significant positive correlation. Present results supported with the findings of Dhanda et al. (2004). The findings of Kumar et al. (2014) were similar to present results that root length had non-significant relationship with shoot length under drought conditions. Adnan (2013) investigated six wheat genotypes for their capacity to stand under drought conditions. The results of Khan et al. (2002) were similar with this experiment. The relationship between chlorophyll a and b was positive and highly significant while both negatively correlated with carotenoids. The results of Khan et al. (2010) were similar with these findings. Ghafoor et al. (2013) evaluated physiological traits as indicators of drought tolerance in wheat and concluded that those genotypes which possessed higher chlorophyll contents resist more against drought than genotypes which possessed lower chlorophyll contents. Various responses of the trait under different environments for correlation may be due to the different response of genotypes under different environments. The obtained results are in accordance with the findings of Khan et al. (2002) and Dhanda et al. (2004). The parameters that were negatively correlated can affect the performance of other during the selection process. As root length, chlorophyll a, b, and carotenoid were positively correlated among themselves in both environments, therefore, selection of any one of these traits, enhances the

performance of other traits. As the shoot length was non significant and negatively correlated with all other traits, so selection for shoot length seems not to be the promising criterion for this material.

5. Conclusion On the basis of performance, 105 wheat genotypes at the seedling stage of studied traits under normal and drought conditions were classified as drought tolerant and drought susceptible. Those genotypes performed better among 105 spring wheat genotypes were categorized as drought tolerant and those having the lowest performance under both environments were classified as drought susceptible. So using this criterion, 10 genotypes (G1, G6, G11, G16, G21, G26, G39, G44, G51, and G61) were selected as drought tolerant and five genotypes (G3, G77, G91, G98, and G105) as drought susceptible. Strong association amongst the photosynthetic attributes under drought condition indicated the significance of these indices for future wheat breeding programs for rainfed areas. Shoot length was non significant and negatively correlated with all other traits, so adequate attention should be given to the negatively correlated seedling parameters during selection.

Acknowledgements The authors gratefully acknowledge the National Key R&D Program of China (2018YFD0200500) for the financial support. Appendix associated with this paper can be available on http://www.ChinaAgriSci.com/V2/En/appendix.htm

References Adnan M. 2013. Effect of drought stress on the physiology and yield of the Pakistani wheat germplasm. International Journal of Advanced Research and Technology, 2, 419–430.

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Ahmad H, Mohammad F, Hassan G, Gul R. 2006. Evaluation of the heterotic and heterobeltiotic potential of wheat genotypes for improved yield. Pakistan Journal of Botany, 38, 1159–1167. Ahmad M, Shabbir G, Minhas N M, Shah M K. 2013. Identification of drought tolerant wheat genotypes based on seedling traits. Sarhad Journal of Agriculture, 29, 21–27. Ahmed H G M D, Khan A S, Kashif M, Khan S H. 2018. Genetic analysis of yield and physical traits of spring wheat grain. Journal of the National Science Foundation of Sri Lanka, 46, 23–30. Ahmed H G M D, Khan A S, Khan S H, Kashif M. 2017. Genome wide allelic pattern and genetic diversity of spring wheat genotypes through SSR markers. International Journal of Agriculture and Biology, 19, 1559–1565. Anjum S A, Xie X Y, Wang L C, Saleem M F, Man C, Lei W. 2011. Morphological, physiological and biochemical responses of plants to drought stress. African Journal of Agricultural Research, 6, 2026–2032. Ashfaq W, Ul-Allah S, Kashif M, Sattar A, Nabi H G. 2016. Genetic variability study among wheat genotypes under normal and drought conditions. Journal of Global Innovations in Agricultural and Social Sciences, 4, 111–116. Chachar N A, Chachar M H, Chachar Q I, Chachar Z, Chachar G A, Nadeem F. 2014. Exploration of genetic diversity between six wheat genotypes for drought tolerance. Climate Change Outlook and Adaptation, 2, 27–33. Dhanda S S, Sethi G S, Behl R K. 2004. Indices of drought tolerance in wheat genotypes at early stages of plant growth. Journal of Agronomy and Crop Science, 190, 612–618. de Dorlodot S, Forster B, Pagès L, Price A, Tuberosa R, Draye X. 2007. Root system architecture: Opportunities and constraints for genetic improvement of crops. Trends in Plant Sciences, 12, 474–481. Faisal S, Mujtaba S, Khan M, Mahboob W. 2017. Morphophysiological assessment of wheat (Triticum aestivum L.) genotypes for drought stress tolerance at seedling stage. Pakistan. Journal of Botany, 49, 445–452. Farshadfar E, Amiri R. 2105. Genetic analysis of physiological indicators of drought tolerance in bread wheat using diallel technique. Genetika, 47, 107–118. Ghafoor G, Hassan G, Ahmad I, Khan S N, Suliman S. 2013. Correlation analysis for different parameters of F2 bread wheat population. Pure and Applied Biology, 2, 28–31. Gugino B K, Abawi G S, Idowu O J, Schindelbeck R R, Smith L L, Thies J E, Wolfe D W, Van Es H M. 2009. Cornell soil health assessment training manual. Cornell University College of Agriculture and Life Sciences, USA. Jaleel C A, Manivannan P A, Wahid A, Farooq M, Al-Juburi H J, Somasundaram R A, Panneerselvam R. 2009. Drought stress plants: A review on morphological characteristics and pigments composition. International Journal of Agriculture and Biology, 11, 100–105. Kalaji H M, Jajoo A, Oukarroum A, Brestic M, Zivcak M, Samborska I A, Cetner M D, Łukasik I, Goltsev V, Ladle

R J. 2016. Chlorophyll a fluorescence as a tool to monitor physiological status of plants under abiotic stress conditions. Acta Physiologiae Plantarum, 38, 102–112. Khan A S, Allah S U, Sadique S A. 2010. Genetic variability and correlation among seedling traits of wheat (Triticum aestivum L.) under water stress. International Journal of Agriculture and Biology, 12, 247–250. Khan M I, Shabbir G, Akram Z, Shah M K, Ansar M, Cheema N M, Iqbal M S. 2013. Character association studies of seedling traits in different wheat genotypes under moisture stress conditions. SABRAO Journal of Breeding and Genetics, 45, 458–467. Khan M Q, Anwar S, Khan M I. 2002. Genetic variability for seedling traits in wheat (Triticum aestivum L.) under moisture stress conditions. Asian Journal of Plant Sciences, 1, 588–590. Kumar N, Markar S, Kumar V. 2014. Studies on heritability and genetic advance estimates in timely sown bread wheat (Triticum aestivum L.). Bioscience Discovery, 5, 64–69. Leishman M R, Westoby M. 1994. The role of seed size in seedling establishment in dry soil conditions-experimental evidence from semi-arid species. Journal of Ecology, 82, 249–258. Lichtenthaler H K, Wellburn A R. 1983. Determination of total carotenoids and chlorophyll a and b of leaf extracts in different solvents. Biochemical Society Transactions, 11, 591–592. Livingston D P, Hincha D K, Heyer A G. 2009. Fructan and its relationship to abiotic stress tolerance in plants. Cellular and Molecular Life Sciences, 66, 2007–2023. Lohithaswa H C, Desai S A, Hanchinal R R, Patil B N, Math K K, Kalappanavar I K, Bandivadder T T, Chandrashekhara C P. 2013. Combining ability in tetraploid wheat for yield, yield attributing traits, quality and rust resistance over environments. Journal of Agricultural Sciences, 26, 190–193. Mir R R, Zaman-Allah M, Sreenivasulu N, Trethowan R, Varshney R K. 2012. Integrated genomics, physiology and breeding approaches for improving drought tolerance in crops. Theoretical and Applied Genetics, 125, 625–645. Noorka I R, Khaliq I. 2007. An efficient technique for screening wheat (Triticum aestivum L.) germplasm for drought tolerance. Pakistan Journal of Botany, 39, 1539–1546. Noorka I R, da Silva J A. 2012. Mechanistic insight of water stress induced aggregation in wheat (Triticum aestivum L.) quality: The protein paradigm shift. Notulae Scientia Biologicae, 4, 32–38. Ogunbayo S A, Ojo D K, Guei R G, Oyelakin O O, Sanni K L. 2005. Phylogenetic diversity and relationship among 40 rice accessions using morphological and RAPDs techniques. African Journal of Biotechnology, 4, 1234–1244. Pour-Aboughadareh A, Ahmadi J, Mehrabi A A, Etminan A, Moghaddam M, Siddique K H. 2017. Physiological responses to drought stress in wild relatives of wheat: implications for wheat improvement. Acta Physiologiae

Hafiz Ghulam Muhu-Din Ahmed et al. Journal of Integrative Agriculture 2019, 18(11): 2483–2491

Plantarum, 39, 106–114. Robbelen G. 1957. Untersuchungen an strahlen-induzierten blattfarbmutanten von Arabidopsis thaliana (L.) Heynh. Z. Induktive Abstammungs-Vererbungslehre, 88, 189–252. Seher G S, Rasheed A, Kazi A G, Mahmood T, Mujeeb-Kazi A B. 2015. Performance of diverse wheat genetic stocks under moisture stress condition. Pakistan Journal of Botany, 4, 21–26. Shahbazi H, Bihamta M R, Taeb M, Darvish F. 2012. Germination characters of wheat under osmotic stress: Heritability and relation with drought tolerance. International Journal of Research and Review, 2, 689–698. Steel R G, Torrie J H, Dickey D A. 1997. Principles and Procedures of Statistics: A Biometrical Approach. McGraw Hill Book Company, New York, USA. Toker C, Canci H, Yildirim T. 2007. Evaluation of perennial wild Cicer species for drought resistance. Genetic Resources and Crop Evolution, 54, 1781–1786. Tuberosa R, Salvi S. 2006. Genomics approaches to improve

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drought tolerance in crops. Trends in Plant Sciences, 11, 405–412. Ul-Allah S, Khan A S, Saeed M F, Ashfaq W, Iqbal M. 2014. Genetic variability and correlation studies for seedling traits of wheat (Triticum aestivum L.) genotypes under normal and water stress conditions. Journal of Agricultural and Crop Research, 2, 173–180. Waqas M, Noorka I R, Khan A S, Tahir M A. 2013. Heritable variations the base of effective selection in wheat (Triticum aestivum L.) to ensure food security. Climate Change Outlook and Adaptation, 1, 14–18. Zeng F, Zhang B, Lu Y. 2016. Morpho-physiological responses of Alphagi sparsifolia SHAP (Leguminosae) seedlings to progressive drought stress. Pakistan Journal of Botany, 48, 429–438. Zhong H, Wang H. 2012. Evaluation of drought tolerance from a wheat recombination inbred line population at the early seedling growth stage. African Journal of Agricultural Research, 7, 6167–6172. Executive Editor-in-Chief LI Shao-kun Managing editor WANG Ning