EurAsian Journal of Biosciences Eurasia J Biosci 6, 47-59 (2012) DOI:10.5053/ejobios.2012.6.0.6

Selection of a salt tolerant Tunisian cultivar of chili pepper {Capsicum frutescens)

Kaouther Zhani1*, Mohamed Aymen Elouer1, Hassan Aloui2, Cherif Hannachi1

1 Department of Horticulture and Landscape, University, High Institute of Agronomy, 4042 Chott Mariem,

2Carthage University, Faculty of Science, Jarzouna 7021, , Tunisia Corresponding author: [email protected]

Abstract Background: Salinity affects germination and seedling growth and yield of several crop species, such as pepper. That is why this study was carried to evaluate the effects of NaCI on seed Li- germination, seedling growth and ionic balance of three Tunisian chili pepper {Capsicum frutescens) cv: , Korba and Awlad . Materials and Methods: The percentage of germination, the growth and the mineral contents were measured in the three Tunisian chili pepper cv watered with water containing 0, 2, 4, 6 or 8 g L1 NaCI. Results: Results showed that different salinity stress levels had significant effect on germination percentage and germination time. In pot experiment, increasing NaCI concentration, for all cv, induced a significant decrease on plant height, root length, leaves number, leaf area and chlorophyll amount. The fresh and dry weights are also affected. In addition, salinity increased Na+ and CI" levels but decreased K+ level in roots and shoots. Conclusions: Awlad Haffouz cv had the highest K7Na+ ratio compared to cv Korba and Tebourba and it has showed the best response under salt stress during germination and growth stage which lets it to be the most tolerant cv. Keywords: Capsicum frutescens, germination, mineral nutrition, salinity, shoot.

Zhani K, Elouer MA, Aloui H, Hannachi C (2012) Selection of a salt tolerant Tunisian cultivar of chili pepper {Capsicum frutescens). Eurasia J Biosci 6: 47-59.

DOI:10.5053/ejobios.2012.6.0.6 ©EurAsian Journal of Biosciences

regulate its accumulation (Munns and Tester 2008). INTRODUCTION Pepper is widely cultivated for its fruits which Salinity is one of the most important abiotic have a recognized nutritional value. In fact, they are stresses limiting crop production in arid and an excellent source of various antioxidant semiarid regions, where soil salt content is high and compounds like flavonoids, carotenoids and vitamin precipitation is low (Neumann 1995). Transpiration C (Chuah et al. 2008). This later protects human body and evaporation from the soil surface, salt load in against oxidative damage and prevents various irrigation water, over use of fertilizers and lack of diseases such as cancer and cardiovascular diseases proper drainage can be the main factors that (Oboth and Rocha 2007). In Tunisia, Pepper is the contribute to this problem. Around 930 million ha of major cultivated plant and its fruits are mainly land world-wide, 20% of total agricultural land, are consumed either fresh or dry. It is cultivated on open affected by salinity (Munns 2002). Salinity limits air and under greenhouse. However, pepper is crops production, especially the sensitive ones exposed to many biotic (virus, fungi) and abiotic (Zadeh and Naeini 2007) and reduces the yield of stress, especially salinity, which has a negative effect major crops by more than 50% (Bray et al. 2000). It on pepper growth and yield (Ibn Maaouia-Houimli et affects morphological, physiological and al. 2011). biochemical processes, including seed germination, The objective of this research was to study the plant growth and water and nutrient uptake effect of salt stress on some characteristics of three (Willenborg et al. 2004). These effects can be due to Tunisian chili pepper cv: Tebourba, Korba and Awlad low osmotic potential of soil solution, specific ion Haffouz by measuring seed germination, seedling effects, nutritional imbalance or a combined effect of all these factors (Marschner 1995). NaCl is the Received: April 2012 predominant salt causing salinization and it is Accepted: April 2012 expected that plants have involved mechanisms to Printed: June 2012

47 EurAsian Journal of BioSciences 6: 47-59 (2012) Zhani et al. growth and ionic balance at various concentrations according to Arnon (1949) method. Samples of fresh of NaCl (0, 2, 4, 6 and 8 g L-1) in order to select salt leaves (0.1 g) were ground with sand and 10 mL of tolerant cultivars. acetone in a mortar. The absorbance of the extracts was measured by spectrophotometry at 645 and 663 nm. MATERIALS AND METHODS The chl amounts were calculated according to the Seed germination assay following equations: Seeds of three chili pepper cv (Tebourba, Korba Chl a (ug g-1 F.W.): 12.7 (OD 663) - 2.63 (OD 645) and Awlad Haffouz) were collected from plants Chl b (ug g-1 F.W.): 22.9 (OD 645) - 4.86 (OD 663) cultivated one year ago in the experimental station Chl (a+b) (ug g-1 F.W.): 8.02 (OD 663) - 20.2 (OD of Agronomic High Institute of Chott Mariem. The 645) seeds were sterilized for 20 min in sodium hypo¬ K+, Na+ and Cl- root and shoot content were chloride (5%) and then they were rinsed 3 times with analyzed by flame spectrophotometer. Pots were distilled water for 2 min. After sterilization, under disturbed in completely randomized design with 3 laminar flow, 10 seeds of each cv were transferred replications. into sterile Petri dishes (100x100 mm dimensions) Data analysis between two layers Watman filter paper and then All data were analyzed by "SPSS software 13.00" wetted with 10 mL distilled water (control) or saline and Duncan's multiple range tests were used to solution containing 2, 4, 6 and 8 g L-1 NaCl and left to determine significance between variables (P<0.05). germinate at 25°C. Germinated seeds were recorded during 20 days. RESULTS AND DISCUSSION Germination (%)= n/N x 100 n: number of germinated seeds on the nth day Seed germination percentage and germination N: total number of seeds time Treatments were assessed in factorial Effect of NaCl concentration on the percentage experimental based on a completely randomized of germination in the three cv during 20 days is design at 3 replications. Each replication includes shown in Figs. 1-3. In control treatment, seeds one Petri dish (ten seeds per Petri dish). germinated after two (Korba cv) or three days Growth assay (Tebourba and Awlad Haffouz cv) and total Seeds were sterilized for 20 min in sodium hypo¬ germination ended after 13 (Korba and Awlad chloride solution (5%) and then rinsed 3 times with Haffouz cv) or 14 days (Tebourba cv). Salt stress distilled water. Five seeds from each cv were sowed modified germination process by increasing in plastic pot (12 cm diameter and 22 cm height) germination time and decreasing germination containing gravel and fertilized peat (1/4: 3/4) at 1 percentage. Under the highest concentration of cm depth. Pots were put in greenhouse under NaCl, seeds germinated after six (Korba cv) to ten 25°/18°C day/night temperature and natural light. days (Tebourba cv). The maximum germination After emergence, one seedling per pot was percentage was observed in Korba cv (50%) and the conserved. For 60 days, plants were watered with lowest one in Tebourba cv (10%). Zhani (2009) had water (control) or a saline solution containing 2, 4, 6 obtained similar results in other Tunisian pepper cv and 8 g L-1 NaCl. The plant height (cm), root length where NaCl decreased germination percentage to (cm), leaves number per plant, leaf area (cm2), fresh 70 and 20% respectively in Starter and Chergui cv at weight for both shoot and root were measured. Dry 6 g L-1 NaCl. Keshavarzi (2011) and Keshavarzi et al. weights were measured after drying into oven at (2011) have found the same result respectively on 80°C for 48 h. some savory and spinach cv. Leaf area was measured by planimeter (Area NaCl affected seed germination by creating Meter 3100). Chl (a and b) were determined external osmotic potential which causes difficulties

48 EurAsian Journal of BioSciences 6: 47-59 (2012) Zhani et al.

Day s after sowing

Fig. 2. Effect of NaCl (0, 2, 4, 6 or 8 g L-1) on the percentage of germination of Korba ch ili pepper cultivar. in absorption of the necessary water quantities for and Korba cv decreased significantly at NaCl 8 g L1 the germination process (Abdelly 1992). Guerrier respectively to 37, 57 and 58%. The same result was (1984) reported that salt stress causes also specific obtained in canola (Bybordi 2010) where the height toxicity by higher accumulation of Na+ and Cl- ions in of plants declines from 56.25 cm in control to 28.19 the embryo in addition to a mineral imbalance. In cm at NaCl 6 g L1. extreme case, death of embryo can take place due to Root length an inhibition of metabolic process (Bliss et al. 1986). Mean of root length was between 15.7 (control) Plant height and 7.4 cm (8 g L1 NaCl). As expected, control The mean of plant height varied between 36.5 condition and the highest NaCl level (8 g L1) induced (control) to 17.9 cm (8 g L-1 NaCl) (Table 1). The the longest and the shortest root length longest plant height was observed in the control of respectively (Table 1). Generally, root length Tebourba cv (38.2 cm). When NaCl concentration decreased as salt stress increased. In the control, it increased, plant height of Awlad Haffouz, Tebourba varied from 14.1 (Korba cv) to 18.8 cm (Awlad

49 EurAsian Journal of BioSciences 6: 47-59 (2012) Zhani et al.

sowing

Fig. 3. Effect of NaCl (0, 2, 4, 6 or 8 g L-1) on the percentage of germination of Awlad Haffouz chili pepper cultivar.

Table 1. Plant height (cm) and root length (cm) of three chili pepper cultivars watered during 60 days with water containing NaCl 0, 2, 4, 6 or 8 g L-1.

NaCl (g L"1) Cultivar 0 2 4 6 8 Tebourba 38.2a 31.0a 30.5a 18.0° 16.1c Plant height Korba 36.4a 30.0b 28.4b 17.3cd 15.2d Awled HaFFouz 35.6a 31.3a 30.9ab 25.8b 22.4b

8 a DC C Tebourba 14.2 13.4 93 8.7 7.0° Root lenght Korba 14.1ab 12.6b 11.3b 8.8C 5.9d Awled HaFFouz 18.8a 14.1b 11.8C 9.5d 9.3d

Means followed by the same letter(s) are not significantly different at P= 0.05 according to Duncan test.

Haffouz cv). At the highest stress level, Korba and According to Fig. 5, when NaCl increased, leaf Awlad Haffouz cv showed a respective decrease of area decreased to 78% for Awlad Haffouz cv with 58 and 50% where root length was 7.02 and 9.3 cm NaCl 8 g L-1. Studies done on five cultivars of canola respectively. Kerkeni (2002) obtained a similar result (Bybordi 2010) gave similar results, leaf area of in potato. canola decreased from 256.25 cm2 in control to Leaf characteristics 107.31cm2 with NaCl 6 g L1. Mean number of leaves per plant (Fig. 4) showed Chl a, b and a+b amounts in leaves were the a decrease with the increase of salt stress in all chili highest in control (Figs. 6-8). Tebourba cv leaves pepper cv. At highest NaCl concentration (8 g L1), were the richest (2.875 ug g-1 F.W.) whereas Awlad pepper plant didn't produce more than 9 leaves Haffouz cv leaves were the poorest (2.282 ug g-1 (Korba cv) which correspond to 81% decrease F.W.). NaCl decreased chl (a+b) synthesis in the three compared to control (47 leaves per plant). The result chili pepper cv and this decrease was the most agrees with the report of Mensah et al. (2006) in important at the highest NaCl concentration (8 g L-1); groundnut where it was observed that salinity at 17 chl a+b decrease was 55% in Tebourba cv and 66% in mS/cm enhanced the production of leaves in RMP91 Awlad Haffouz cv. The same trend was obtained for cv from 42.7 (control) to 19.3 leaves. chl a and chl b amounts but the response of the cv

50 EurAsian Journal of BioSciences 6: 47-59 (2012) Zhani et al.

60 i

0 2 4 6 8

NaCl(g/L)

Fig. 5. Effect of NaCl (0, 2, 4, 6 or 8 g L1) on leaf area (cm2) of three 60 days old ch ili pepper cultivars. was different. At NaCl 8 g L1, leaves of Tebourba cv amounts were observed in Korba cv (0.38 ug g-1 F.W.) had the highest amounts of both chl a (0.84 ug g1 and Awlad Haffouz cv (0.21 ug g1 F.W.) respectively F.W.) and chl b (0.4 ug g1 F.W.) while the lowest for chl a and chl b. Biricolti and Pucci (1995) observed

51 EurAsian Journal of BioSciences 6: 47-59 (2012) Zhani et al.

2,5 iTebourba

I Korba

I Awlad Haffouz

1,5

0,5

0 8 NaCl{g/L)

Fig. 6. Effect of NaCl (0, 2, 4, 6 or 8 g L1) on the chlorophyll a content (ug/g FW) in three 60 days old chili pepper cultivars.

NaCl{g/L)

Fig. 7. Effect of NaCl (0, 2, 4, 6 or 8 g L-1) on the chlorophyll b content (ug/g FW) in three 60 days old chili pepper cultivars. such result in peach where chl a synthesis was of Mulberry because of total destruction of reduced in "Readheaven" cultivar by salt treatment. chloroplast structure (Blumenthal-Goldschidt and Agastian et al. (2000) reported that at higher salinity Poljakoff-Mayber 1968). (12 mS/cm) chl a was totally eliminated in mesophyll

52 EurAsian Journal of BioSciences 6: 47-59 (2012) Zhani et al.

Fig. 8. Effect of NaCl (0, 2, 4, 6 or 8 g L-1) on the chlorophyll a+b content (ug/g FW) in three 60 days old chili pepper cultivars.

Fresh and dry weights tissue water content resulted in reduction of cellular Fresh and dry weights of aerial parts and roots of growth and development. Therefore, restriction of three chili pepper cv grown in 0 to 8 g L-1. NaCl are water absorption was one of the most important presented in Table 2. The shoot and root fresh and causes of stem and root growth decrease. Farhoudi dry biomass of the three studied cv were and Tafti (2011) reported that root cells have a much significantly reduced with increasing NaCl less turgor threshold pressure than that of stem concentration. At the highest salinity, cv Awlad cells thus root growth was more than stem growth Haffouz had the highest biomass and Tebourba cv under salt and drought stresses. Therefore, root was had the lowest ones. Thus, at the highest salt significantly less affected by salt stress in concentration, the dry weight of Tebourba cv comparison to stem (Sadeghi 2009). decreased till 88 and 92% for root and shoot Mineral analysis respectively. Results in Table 3 show that in aerial parts and Al Thabet et al. (2004) working on canola, Ben roots low concentrations of Na+ and Cl- were Said (2004) on melon, Ibriz et al. (2005) on luzerne observed in control plants. Values for roots were and Singh et al. (2007) on groundnut indicated that lower than those for shoots. Increasing NaCl under salinity stress plant growth was inhibited concentration amplified Na+ and Cl- contents in because salinity exerted low water potential, ion shoots and roots in the three cv and decreased at toxicity and ion imbalance (Greenway and Munns the same time K+ content. The present result was in 1980). In the three chili pepper cv, shoots were more agreement with the work of Mezni et al. (2002) in affected by NaCl than roots. Those results are similar luzene, Kaya et al. (2002) in strawberry, Sahloul to those reported by Hajlaoui (2003) in chick pea, (2002) in tomato, Ben Dkhil and Denden (2010) in Akinci et al. (2004) in eggplant and Saboora et al. okra and Akbarimoghaddam et al. (2011) in wheat, (2006) in wheat plants. However, Bybordi et al. those authors observed that high saline (2010) have showed that root length was the most concentration increased Na+ and Cl- contents and affected in the five studied canola cultivars. decreased K+ content in the affected crops. Bybordi El-Bassiouny and Bekheta (2005) have shown that et al. (2010) showed that potassium content accumulation of ions in wheat plants grown in the decreased due to salinity in sensitive canola cv. It presence of salt (14 dS/cm) environment causes seems that the decrease in potassium content is due osmotic and pseudo-drought stresses leading to to an antagonistic effect between sodium and decrease of water absorption. The decrease of potassium. Greenway and Munns (1980) had

53 EurAsian Journal of BioSciences 6: 47-59 (2012) Zhani et al.

Table 2. Plant biomass of three chili pepper cultivars watered during 60 days with water containing NaCl 0, 2, 4, 6 or 8 g L-1.

NaCl Shoot dry Roots dry Shoot Fresh Roots Fresh Cultivar (g weight (mg) weight (mg) weight (g) weight (g) 0 8.17a 2.67a 47.32a 10.34a 2 3.02b 0.94b 17.34b 3.58b Tebourba 4 2.40c 0.84b 15.56b 3.22b 6 0.75cd 0.36c 5.06cd 1.88b 8 0.64d 0.32c 3.06d 1.38b 0 5.35a 2.02a 33.17a 7.22s 2 2.17b 1.12b 13.8bc 4.76b Korba 4 2.01b 1.04b 12.18c 4.70b 6 1.03cd 0.45c 5.12d 2.42c 8 0.84d 0.40c 5.02d 2.18C

a a a 0 6.82a 2.01 34.32 6.00 2 3.64b 1.25b 14.94b 5.04a Awled HaFFouz 4 2.27bc 1.17b 12.14bc 4.56bc 6 1.47c 0.69c 9.94c 3.00c 8 1.27c 0.53d 8.16C 2.88c

Means followed by the same letter(s) are not significantly different at P= 0.05 according to Duncan test.

Table 3. Na+, Cl- and K+ concentrations (meq/g DW) in roots and shoots of three chili pepper cultivars watered during 60 days with water containing NaCl 0, 2, 4, 6 or 8 g L-1.

NaCl Shoots Roots Shoots Roots Shoots Roots Cultivar (g Cl cr Na+ Na+ K+ K+ 0 0.40° 0.49c 0.98c 0.73e 1.44a 1.40a 2 1.11cd 0.77c 2.13b 1.20d 1.30a 1.02a Awled HaFFouz 4 1.88bc 1.64b 3.30a 2.53cd 1.08b 0.89b 6 2.49b 2.09b 3.60a 3.83b 0.75bc 0.61b 8 3.53a 5.26a 4.56a 4.23a 0.42c 0.31c 0 0.37° 0.65c 1.36c 0.68e 1.45a 1.42a 2 1.22c 0.71c 2.27b 1.09d 1.07b 0.98b Korba 4 2.17bc 1.30b 3.45ab 2.80c 0.83c 1.13a 6 2.99b 1.65b 3.82a 3.36b 0.48d 0.62b 8 4.20a 4.20a 4.73a 4.13a 0.32d 0.23c 0 0.61° 0.67° 1.43c 0.72e 1.49a 1.35a 2 1.56cd 1.30c 3.00b 1.03d 1.01b 1.30a Tebourba 4 2.83b 1.29c 3.57b 2.06c 0.66c 0.88b 6 3.80b 1.80b 4.15a 2.60b 0.43c 0.44c 8 4.80a 4.36a 4.55a 3.86a 0.26c 0.20c

Means followed by the same letter(s) are not significantly different at P= 0.05 according to Duncan test.

54 EurAsian Journal of BioSciences 6: 47-59 (2012) Zhani et al. highlighted the antagonistic effect between these more K+ accumulation in roots compared with the two elements. two other studied cv. Ashraf and Harris (2004) Na+ content in shoots of Awlad Haffouz cv was reported that Na+ and Cl" accumulation in tolerant cv significantly lower than Na+ content in the other chili was lower than in sensitive cv and K+ concentration pepper cv. According to these results, it was was higher in tolerant cv. Additionally, according to concluded that Awlad Haffouz cultivar was the most results showed in Figs. 9 and 10, K+/Na+ ratio was the salt stress tolerant due to its less Na+ absorption and highest in this cv, especially at the highest salt stress

0,7

O 0,6

nj AWLAD HAFFOUZ + 0,5

KORBA + 0,4 4-> o o 0,3 _c TEBOURBA on 0,2

0,1

0 8

NaCl (g/L)

Fig. 9. Effect of NaCl (0, 2, 4, 6 or 8 g L1) on shoot K+/Na+ ratio in three 60 days old chili pepper cultivars.

NaCl (g/L)

Fig. 10. Effect of NaCl (0, 2, 4, 6 or 8 g L-1) on root K+/Na+ ratio in three 60 days old chili pepper cultivars.

55 EurAsian Journal of BioSciences 6: 47-59 (2012) Zhani et al. concentration, which was 0.08 in shoots and 0.07 in CONCLUSION roots. Thus, this result explains the advantage of this cv during its germination and its vegetative growth Results of this study demonstrate that NaCl in the presence of NaCl. Morant-Manceau et al. affects some of the physiological process in pepper. (2004) and Farhoudi and Tafti (2011) found also that The increase of salinity level decreased all studied K+/Na+ ratio was higher in salt tolerant triticale and parameters except Na+ and Cl" concentrations in soybean cv respectively. The results for this tolerant aerial parts and in roots. Awled Haffouz cv had a cv can be explained in the light of early findings of higher tolerance to salinity compared with Korba many scientists that salt tolerant mesophytes and Tebourba cv. It is clear that the main generally excluded either Na+ and Cl" from their mechanisms for the salt tolerance of pepper were shoots (Lauchli et al.1994, Saqib et al. 2005) because exclusion of Na+ and Cl" from shoots, high uptake of Na+ was the primary cause of ion specific damage, K+ and maintening a high K+/Na+ ratio. The 2+ resulting in a range of disorders in enzyme activation measurement of Ca content, organic solutes and protein synthesis (Tester and Davenport 2003). synthesis such as proline, soluble sugars, soluble Therefore, exclusion of Na+ at root level and proteins and free amino"acids would allow to better maintenance of a high K+ content in the shoots were explain the salt tolerance in pepper. Also, efficiency vital for the plants to grow under saline conditions of ion transporters, cellular compartmentation of (Munns et al. 2000). This cv also maintained ions, oxidative stress and synthesis of osmoticums in considerably high K+/Na+ ratio in both shoots and relation with salinity stress are worth studying. roots. This trait has a potential value as selection criterion for salt tolerance (Greenway and Munns 1980).

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Tuza Dayanıklı Tunus Kırmızı Biberinin (Capsicum frutescens) Seçilmesi

Özet

Giriş: Tuzluluk; biber gibi bazı tarım bitkilerinde çimlenmeyi, fide büyümesini ve verimi etkilemektedir. Bu yüzden bu çalışma, üç Tunus biber (Capsicum frutescens) çeşidinde, Tebourba, Korba ve Awlad Haffouz, NaCl'ün tohum çimlenmesi, fide büyümesi ve iyon dengesi üzerindeki etkilerini araştırmak için gerçekleştirildi. Materyal ve Metot: 0, 2, 4, 6 veya 8 g L1 NaCl içeren suyla sulanan üç Tunus kırmızı biber çeşidinde çimlenme yüzdesi, büyüme ve mineral içerikleri ölçüldü. Bulgular: Bulgular, değişik tuz stresi seviyelerinin, çimlenme yüzdesi ve çimlenme zamanı üzerinde önemli etkisinin olduğunu göstermiştir. Saksı deneyinde, artan NaCL konsantrasyonu, bütün çeşitlerde bitki boyu, kök uzunluğu, yaprak sayısı, yaprak alanı ve klorofil miktarında önemli azalmaya sebep oldu. Yaş ve kuru ağırlıklar da etkilendi. Buna ek olarak tuzluluk, kök ve sürgündeki Na+ ve Cl- seviyelerini artırdı, fakat K+ seviyelerini azalttı. Sonuç: Awlad Haffouz çeşidi Korba ve Tebourba çeşitlerine kıyasla, en yüksek K+/Na+ oranına sahipti ve çimlenme esnasındaki en iyi tuz stres tepkisini verdi. Bu durum, bu çeşidin en toleranslı çeşit olduğunu göstermektedir.

Anahtar Kelimeler: Capsicum frutescens, çimlenme, filiz, mineral beslenme, tuzluluk.

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