Environmental and Experimental Botany 42 (1999) 85 – 94 www.elsevier.com/locate/envexpbot
Phenotypic flexibility as marker of sodium chloride tolerance in sunflower genotypes Abdul Wahid *, Iffat Masood, Intshar-ul-Haq Javed, Ejaz Rasul Department of Botany, Uni6ersity of Agriculture, Faisalabad-38040, Pakistan Received 16 August 1998; received in revised form 20 April 1999; accepted 20 April 1999
Abstract Phenotypic flexibility in three high yielding sunflower genotypes (FS1, FS2 and FS5) was taken as marker to determine NaCl tolerance at germination, 20, 35 and 50 days after emergence (DAE) and maturity (70 DAE) stages of growth. Genotypes displayed a substantial variability for salinity tolerance at all growth stages. FS2 exhibited tolerance at germination and 20 DAE, whereas the most tolerant stages of FS5 were 35, 50 DAE and maturity. At germination enhanced salt tolerance was expressed by higher germination percentage, greater elongation and dry weight of embryonic tissues and at subsequent stages by reduced tip burning and lack of chlorosis of young leaves, greater stem chlorosis, higher number, area and dry weight of green leaves. Salt-tolerant genotypes showed reductions of relative growth rate (RGR), net assimilation rate (NAR) and relative leaf growth rate (RLGR) and an increase of leaf area ratio (LAR) at 35 DAE, although these trends were reversed at 50 DAE. A positive relationship of RGR and NAR with RLGR revealed that increased leaf growth plays a crucial role in sustaining plant growth that results in higher yield under salinity. Hence, increased RLGR can be regarded as a reliable indicator of salinity tolerance. To conclude, FS5 showed some important features of salt tolerance that can be successfully exploited in saline lands. The problem of reduced germination can be overcome by enhancing seed rate to achieve an optimum plant population. © 1999 Elsevier Science B.V. All rights reserved. Keywords: Chlorosis; Genotypes; Growth; Helianthus annuus; Phenotypic flexibility; RLGR; Selection traits
1. Introduction Salinization of soils limits plant growth by inducing numerous physiological and biochemical changes in cells. These changes are ultimately displayed by reduced growth and other signs of salt damage. Major harmful effects of salinity * Corresponding author. E-mail address:
[email protected] (A. Wahid)
may be reduced germination, seedling emergence and establishment (Stumpf et al., 1986; Wahid et al., 1999), visible signs of leaf chlorosis (Wahid et al., 1997a) and senescence (Lutts et al., 1996), reduced absolute and relative growth (Curtis and La¨uchli, 1986; Garcia et al., 1995), and decreased final yield (Francois, 1994; Isla et al., 1998). Salttolerant plants display inherent features which are expressed under saline conditions and may not be apparent otherwise (Wahid et al., 1997a; Shabala
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et al., 1998). This, however, depends upon the stage of growth and plant/variety used. Sunflower, as an important source of oil production, is moderately responsive to salinity, showing a 5% decrease in yield per unit increase in salinity, above 4.8 dS m − 1 (Francois, 1996). In Pakistan, it has suffered a decline in productivity over the past many years (Anonymous, 1996), which may be partly related to the increased salinization of soil. As an open-pollinated species, sunflower exhibits great genetic diversity, which can be exploited for the selection of salt-tolerant materials based on a set of specific phenotypic markers. This hypothesis was tested, in this 2-year study, to identify certain qualitative and quantitative features, as indicators of salinity tolerance, in newly bred promising sunflower genotypes. In addition to visible growth and other symptoms, germination, dry matter, seed and oil yield and physiological growth parameters have been taken as indicators to determine variability for salt tolerance.
2. Materials and methods The seeds of sunflower (Helianthus annuus L.) genotypes, viz. FS1, FS2 and FS5 were obtained from Ayub Agricultural Research Institute, Faisalabad. For germination studies, selected healthy seeds were surface sterilized with 0.1% (w/v) HgCl2 for 3 min, followed by repeated washing with water, and sown in petri dishes lined with double layer of Whatman No. 2 filter paper. The experimental design was completely randomized with three replications. Salinity (NaCl) levels, i.e. 20 (control), 40, 80, 120 and 160 mmol NaCl l − 1 (corresponding to 2 (control), 4, 8, 12 and 16 dS m − 1) were added to petri dishes before placing 25 seeds in each dish. The seed were germinated at 25°C in 12-h light/ dark cycle. After 12 days, germination percentage, elongation and dry matter yield of radicle and plumule were determined. For determination of salt tolerance by applying salinity at 20, 35, 50 days after emergence (DAE) of seedlings and maturity (70 DAE) stages of growth, the plants were raised in pots
containing 10 kg of loam soil and two plants were maintained per pot. The pots (three replicates per treatment) were placed in a wire house in complete randomization, where the ambient temperature for both the study years ranged between 209 4 and 389 5°C, relative humidity between 509 8 and 709 6% and rainfall was 68–85 mm. The above NaCl levels were gradually developed based upon full saturation percentage of soil. Physico-chemical characteristics of the soil were; organic matter, 1.73%; pH 7.4; electrical conductivity (ECe), 2.0 dS m − 1; cation exchange capacity, 14.7 meq l − 1; sodium adsorption ratio, 0.08 meq l − 1; Na + , 4.45 meq l − 1; Cl − , 7.53 meq l − 1; SO24 − , 1.73 meq l − 1; and Ca+ Mg, 14.5 meq l − 1. Original ECe of the soil (equivalent to 20 mmol NaCl l − 1) was accounted for while developing salt levels. Salinity levels were raised daily with the addition of 20 mmol NaCl l − 1 per pot, until required levels of 40, 80, 120 and 160 mmol NaCl l − 1 were achieved. At each growth stage, leaf tip burning, chlorosis and signs of salt injury on leaf or stem were visually noted. The plants were harvested 16 days after the onset of salinity at each growth stage. The data were recorded for shoot and root length, number and area of green leaves, dry weight of leaf, stem, root, and their total at initial stages, while head size, 100 seed weight, seed yield per plant and oil percentage were determined at the end. Salt-tolerance limits, i.e. EC50 values (salt levels in mmol NaCl l − 1 at which growth and yield is reduced to 50%) were computed up to 160 mmol NaCl − 1 at the individual growth stages and their average by the method described elsewhere (Wahid et al., 1997a). Physiological growth parameters including relative growth rate (RGR) (using total plant dry weight), leaf area ratio (LAR) and net assimilation rate (NAR) were calculated as described by Hunt (1982), using the data of non-salinized plants at the onset of each growth stage as a baseline information. To calculate relative leaf growth rate (RLGR), the formula of RGR was used based on dry weight of photosynthetic leaves. Oil content of oven dried seeds was esti-
A. Wahid et al. / En6ironmental and Experimental Botany 42 (1999) 85–94
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Table 1 Changes in some germination characteristics of sunflower genotypes under sodium chloride salinity at 12 days after sowing Genotypes
Salt levels (mmol NaCl l−1)
Germimation (%)
Elongation (mm) Radicle Plumule
Dry weight (g/100 plant) Radicle Plumule
FS1
Control 40 80 120
86.5 77.4 69.5 54.5
2.82 2.77 1.47 1.42
3.83 2.89 2.25 1.70
4.31 3.15 2.81 1.95
2.65 2.01 1.66 1.43
FS2
Control 40 80 120
87.0 86.4 81.5 72.4
3.70 3.61 2.44 2.13
4.57 4.45 2.59 2.58
3.95 3.10 2.65 2.28
2.78 2.15 2.06 1.98
FS5
Control 40 80 120
84.6 82.5 73.5 61.6
4.65 3.88 2.78 2.64
4.78 4.10 3.40 2.34
3.98 3.13 2.51 2.01
2.88 2.44 2.10 1.82
** ** **
** ** **
** ** **
* ** **
** ** n.s.
Summary of significance of variance sources Genotypes (G) 2 Salinity (S) 3 GxS 6 * Significant at PB0.05. ** Significant at PB0.01; n.s., non-significant.
mated by Soxhlet extraction method, using hexane as solvent (AOAC, 1970). The data collected for various germination, growth and yield characteristics were analyzed statistically using Minitab program (Minitab, 1989).
3. Results Preliminary results revealed that for both study years a few seeds of genotypes germinated at 160 mmol NaCl l − 1. At all other stages, except FS5,
Table 2 Symptoms and degree of salt injury in leaves and stem of sunflower genotypes at 120 mmol NaCl l−1 at different growth stages Sign of salt injury
Tip burning
Plant tissues
(a) Young leaves
(b) Old leaves
Chlorosis
(a) Young leaves
(b) Old leaves
(c) Stem
Degree
Growth stages (DAE) 20 35
50
Low ¡ High Low ¡ High
FS2 FS5 FS1 FS2 FS1 FS5
FS5 FS2 FS1 FS1 FS5 FS2
FS5 FS2 FS1 FS1 FS2 FS5
Low ¡ High Low ¡ High Low ¡ High
FS2 FS5 FS1 FS2 FS5 FS1 FS1 FS5 FS2
FS5 FS2 FS1 FS1 FS5 FS2 FS1 FS2 FS5
FS5 FS2 FS1 FS1 FS2 FS5 FS1 FS2 FS5
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Table 3 Effect of sodium chloride salinity on the growth characteristics of sunflower genotypes after 20, 35 and 50 days of emergence of seedlings Salt applied/genotypes
Salt levels (mmol NaCl l−1)
Shoot length (cm)
Root length (cm)
No. of leaves per plant
Leaf area (cm2) per plant
Dry weight (g) Leaf
Stem
Root
total
11.8 10.2 8.2 6.7
10.9 8.5 7.0 5.9
8.0 7.3 6.0 5.3
50.5 40.6 29.4 18.2
0.21 0.20 0.18 0.17
0.19 0.18 fl0.17 0.15
0.09 0.08 0.06 0.05
0.49 0.46 0.41 0.37
FS2
Control 40 80 120
13.4 12.3 11.0 9.6
13.0 10.9 10.1 9.2
8.0 8.0 7.6 5.7
48.7 46.7 44.5 33.8
0.23 0.22 0.20 0.17
0.22 0.21 0.19 0.18
0.13 0.11 0.06 0.05
0.58 0.54 0.45 0.40
FS5
Control 40 80 120
13.5 13.4 12.6 10.6
14.1 11.9 10.7 8.7
8.6 8.3 7.3 5.6
42.6 35.9 30.5 24.0
0.23 0.22 0.20 0.16
0.23 0.19 0.17 0.12
0.13 0.13 0.12 0.11
0.59 0.54 0.49 0.39
Summary of significance of 6ariance sources Genotypes (G) 2 Salinity (S) 3 GxS 6
** ** **
** ** n.s.
n.s. ** n.s.
** ** **
n.s. ** n.s.
** ** **
** ** **
** ** n.s.
35 days after emergence FS1 Control 40 80 120
25.9 17.2 13.9 12.8
36.6 25.6 23.4 14.4
16.6 14.6 9.6 7.7
186.5 159.3 114.8 48.4
1.79 1.66 1.46 0.90
1.17 1.10 1.00 0.62
0.44 0.32 0.30 0.14
3.40 3.08 2.76 1.66
FS2
Control 40 80 120
23.3 22.3 19.0 13.5
28.0 22.7 16.7 15.6
12.0 10.6 9.6 7.6
118.5 91.6 51.3 48.1
1.81 1.67 1.30 0.80
1.18 0.89 0.69 0.35
0.51 0.47 0.31 0.10
3.50 3.03 2.30 1.25
FS5
Control 40 80 120
29.2 26.1 18.3 16.0
30.8 22.3 15.6 10.5
12.6 11.6 9.6 8.6
143.9 103.5 89.1 62.6
1.93 1.91 1.33 0.98
0.88 0.82 0.76 0.62
0.49 0.40 0.33 0.28
3.30 3.13 2.42 1.73
** ** **
** ** n.s.
** ** **
** ** **
n.s. ** n.s.
** ** **
** ** **
** ** **
Summary of significance of 6ariance sources Genotypes (G) 2 Salinity (S) 3 GxS 6
A. Wahid et al. / En6ironmental and Experimental Botany 42 (1999) 85–94
20 days after emergence FS1 Control 40 80 120
Salt applied/genotypes
Salt levels (mmol NaCl l−1)
50 days after emergence FS1 Control 40 80 120 FS2
Control 40 80 120
FS5
Control 40 80 120 Summary of significance of 6ariance sources Genotypes (G) 2 Salinity (S) 3 GxS 6 ** Significant at PB0.01; n.s., non-significant.
Shoot length (cm)
Root length (cm)
No. of leaves per plant
Leaf area (cm2) per plant
Dry weight (g) Leaf
Stem
Root
total
44.1 37.5 28.5 20.0
36.5 31.1 25.6 18.6
17.6 15.0 13.3 8.7
218.7 197.2 140.6 106.0
2.51 2.01 1.76 1.24
2.15 1.86 1.67 0.72
1.20 1.03 0.43 0.16
5.86 4.90 3.86 2.12
48.3 40.6 32.3 27.0
37.0 29.1 18.3 17.3
18.3 16.3 13.3 9.3
213.4 186.3 170.8 120.1
2.50 2.13 1.88 1.52
2.33 1.95 1.96 1.35
1.20 1.00 0.39 0.33
6.03 5.08 4.23 3.20
52.1 48.0 44.6 33.0
32.6 24.0 21.0 13.3
16.6 14.6 12.3 10.3
250.1 230.1 218.3 171.9
2.91 2.74 1.91 1.79
2.52 2.33 2.20 2.10
1.31 1.10 0.41 0.37
6.74 6.17 4.52 4.17
** ** **
** ** n.s.
n.s. ** n.s.
** ** **
** ** n.s.
** ** n.s.
n.s. ** n.s.
** ** n.s.
A. Wahid et al. / En6ironmental and Experimental Botany 42 (1999) 85–94
Table 3 (Continued)
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90
none of the genotype could survive up to harvest time, hence the data have been presented up to 120 mmol NaCl l − 1 only. The results given here are the average of 2 study years.
young leaves but it was greater on the old leaves and stem.
3.3. Growth and yield characteristics 3.1. Germination studies Table 3 shows that at 20, 35, 50 DAE, applied salinity highly significantly (PB0.01) reduced most of the growth and yield parameters, indicating highly significant (PB0.01) genotypic differences. At 20 DAE, FS2 performed best of all the genotypes and gave greatest root length, number and area of green leaves, while leaf and total dry weight were highest in FS1 and shoot and total dry weight were higher in FS5 over respective controls. At 35, 50 DAE and maturity, FS5 was superior to all other genotypes in giving greater number and area of leaves, dry matter yield of leaf, stem, root and their total as expressed on the basis of controls, while highest shoot and root length were recorded in FS2 at 35 DAE and in FS1 at 50 DAE. At 70 DAE, applied salinity highly significantly reduced (P B0.01) economic yield parameters, with highly significant (PB 0.01) interactions of genotypes and salt levels (Table 4). Greater head
All the genotypes indicated highly significant (PB 0.01) differences with respect to germination and related parameters (Table 1). Under salinity, FS2 had the highest germination percentage, elongation and dry matter yield of radicle and plumule over controls and was thus regarded as highly salt tolerant at this stage followed by FS5.
3.2. Symptoms of salt injury Genotypes exhibited increased symptoms of salt injury in the form of tip burning and chlorosis of leaves and stem chlorosis with a rise in salinity, but the degree of salt damage was greatly variable in the young and old leaves as well as the stem (Table 2). At 20 DAE, FS2 indicated a low degree of salt damage on young leaves but the injury was higher on stem. In contrast, FS5 at 35 and 50 DAE indicated the lowest effect of salt damage on
Table 4 Effect of sodium chloride salinity on some yield characteristics of sunflower genotypes Genotypes
Salt levels (mmol NaCl l−1)
Head diameter (cm)
Total seed yield per plant
100 seed weight Seed oil content (g) (%)
FS1
Control 40 80 12 Control 40 80 12 Control 40 80 12
8.57 6.90 5.67 4.80 8.17 7.13 6.33 5.77 8.30 7.57 6.43 5.33
4.96 3.95 2.93 0.84 4.09 3.34 1.46 0.96 4.99 3.30 2.46 1.25
3.79 3.00 2.20 1.87 3.80 3.10 2.90 2.10 3.50 3.00 2.40 2.21
33.6 28.5 23.7 19.2 31.9 27.1 23.2 19.1 34.7 28.9 25.1 22.7
** ** **
** ** **
** ** **
** ** **
FS2
FS5
Summary of significance of 6ariance sources Genotypes (G) 2 Salinity (S) 3 GxS 6
** Significant at PB0.01; n.s., non-significant.
A. Wahid et al. / En6ironmental and Experimental Botany 42 (1999) 85–94
diameter was noted in FS2, followed by FS5, while 100 seed weight, total seed yield per plant, and seed oil content were the maximum in FS5 followed by FS2 at the highest level of salinity.
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duced the RGR of FS2, but at 50 DAE RGR highly significantly (PB0.01) increased in FS5 followed by FS2 and decreased in FS1 with enhanced salinity when expressed over control. A highly significant (PB 0.01) difference among the genotypes, salinity levels and their interaction was noted for LAR at 35 DAE, showing a greatly reduced LAR in FS1 followed by FS5 and enhanced in FS2. At 50 DAE, the genotypes differed highly significantly (PB 0.01) for LAR, which increased in FS1 but changed the least in other genotypes with increased salinity. All the genotypes indicated significant (PB 0.05) differences for NAR and showed highly significant (PB 0.01) interaction with salinity levels at both growth stages. At 35 DAE FS2, while at 50 DAE FS5 displayed increased NAR which was decreased in case of FS1. At 35 DAE applied salinity had no influence on the RLGR, however at 50 DAE it was highly significantly (PB 0.01) increased in case of FS5 followed by FS2, but decreased in case of FS1.
3.4. Salt-tolerance limits The salt-tolerance limits (EC50), based on various growth and yield parameters, revealed that the genotypes had relatively greater EC50 at germination and 20 DAE, but it was reduced and variable at the later growth stages (Table 5). On average, FS5 with EC50 of 121 mmol NaCl l − 1 was ranked as highly salt tolerant followed by FS2 and FS1.
3.5. Deri6ed physiological parameters The data regarding the physiological efficiency of the genotypes as affected by salinity have been presented in Table 6 and Fig. 1. At 35 DAE applied salinity significantly (PB 0.05) re-
Table 5 Salt-tolerance limits (EC50) of sunflower genotypes at different growth stages Genotypes
Germination
20 DAE
35 DAE
50 DAE
70 DAE
Average
FS1 FS2 FS5
130a 145 139
123 130 128
85 88 113
82 95 124
75 84 98
99 108 121
a
mmol NaCl l−1 level at which germination, growth and yield is reduced to 50%.
Table 6 Significance of variance sources of some derived physiological parameters of sunflower genotypes as affected by salinity at 35 and 50 DAE Source of variation
Genotypes (G) Salinity (S) GxS a
Degrees of freedom
2 3 6
n.s., non-significant. * Significant at PB0.05. ** Significant at PB0.01.
RGR
LAR
NAR
RLGR
35 DAE
50 DAE
35 DAE
50 DAE
35 DAE
50 DAE
35 DAE
50 DAE
n.s.a * n.s.
** n.s. n.s.
** ** **
** n.s. n.s.
* n.s. **
** n.s. *
n.s. n.s. n.s.
** * n.s.
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Fig. 1. Changes in derived growth parameters of sunflower genotypes FS1 (), FS2 ( ), FS5 ( ) under sodium chloride salinity at 35 and 50 DAE of seedlings.
A. Wahid et al. / En6ironmental and Experimental Botany 42 (1999) 85–94
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Table 7 Significant correlations between derived physiological parameters of sunflower genotypes under salinity Physiological growth parameters
Correlation co-efficient (r) FS2
FS1
RGR vs. NAR RGR vs. RLGR NAR vs. RLGR
FS5
35 DAE
50 DAE
35 DAE
50 DAE
35 DAE
50 DAE
n.s.a 0.97** n.s.
n.s n.s. n.s.
0.95* n.s. n.s.
n.s. n.s. 0.95
n.s. 0.97* n.s.
0.99** 0.95* 0.99**
a
n.s., non-significant. * Significant at PB0.05. ** Significant at PB0.01.
4. Discussion This study revealed that sunflower genotypes, used here, have a high variability in phenotypic flexibility for salt tolerance. This was determined in terms of (a) signs of salt damage, (b) absolute growth and (c) derived growth parameters. At germination, the success of FS2 in better seedling establishment under salinity rested in higher germination percentage, vigorous emergence and dry weight of embryonic tissues (Table 1). These data confirm the findings of Igartua et al. (1994) for sorghum inbred lines, those of Katerji et al. (1994) for sunflower and maize and Wahid et al. (1997b) for sugarcane lines. Among the genotypes, FS2 at initial stages and FS5 at subsequent stages were rated as the most salt-tolerant one (Table 4). A critical examination of the data revealed that salinity tolerance was based on the qualitative characteristics such as reduced chlorosis and tip burning of young emerging leaves and increased stem chlorosis, and on quantitative parameters such as greater number and area of leaves and higher growth and dry matter yield of aerial parts of tolerant genotypes at any stage. Although the plants were not analyzed for ionic content, a decreased chlorosis and tip burning of young emerging leaves and enhanced chlorosis of stem allude to the exclusion of toxic ions from stem and older tissues of the tolerant line, so avoiding toxicity to the growing tissues. A similar mechanism has been suggested in other genotypes of sunflower (Ashraf and
O’Leary, 1995; Francois, 1996) and other crops (Rawson et al., 1988; Shannon, 1997; Shabala et al., 1998). The physiological efficiency of genotypes expressed in terms of RGR, LAR, NAR and RLGR revealed that a declining trend of these parameters at initial growth stages appeared as a result of greater sensitivity of the genotypes to ionic stress (Curtis and La¨uchli, 1986; Wahid et al., 1997a, 1999), but significant genotypic differences were discernible. However, at later stages, enhanced values of RGR, NAR and RLGR under salinity reflected better efficiency of the tolerant genotypes to photosynthesize at an enhanced rate in giving greater seed and oil yield. A substantive proof of these findings came from significant correlation of RGR and NAR with RLGR of the tolerant genotypes, which was absent in FS1, the salt-sensitive genotype (Table 7). In contrast, LAR was not correlated significantly with the growth of any genotype (data not shown). This indicated that among the derived physiological parameters, increased leaf growth plays a crucial role and may, therefore, be regarded as a reliable indicator of salinity tolerance in sunflower. Likewise, an enhanced NAR coupled with reduced LAR have been reported as growth determinants of salinity grown kenaf (Curtis and La¨uchli, 1986) and maize (Cramer et al., 1994). In conclusion, although sunflower elicited moderate response to salinity, there existed a significant phenotypic flexibility for salt tolerance, as reflected by EC50 values. The authors propose
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that higher germination, vigorous growth of seedlings, sustained photosynthetic area, rare signs of salt damage in the form of tip burning and chlorosis of young leaves, increased stem chlorosis and increased RLGR are useful criteria of selection for salinity tolerance. FS5, a highly salt-tolerant genotype, can be successfully grown in moderately saline areas. The problem of relatively reduced germination can be overcome by achieving optimum plant density with the use of high seed rate.
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