Salinty N Hypoxia Interaction In Eucalptus

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Different Eucalyptus Species Show Different Mechanisms of Tolerance to Salinity and Salinity × Hypoxia Muhammad Nasim a; Riaz H. Qureshi b; Tariq Aziz a; M. Saqib b; Shafqat Nawaz a; J. Akhtar b; M. A. Haq b; Shahbaz Talib Sahi a a Sub-Campus Depalpur, University of Agriculture, Faisalabad, Depalpur, Pakistan b Saline Agriculture Research Centre, University of Agriculture, Faisalabad, Depalpur, Pakistan Online Publication Date: 01 September 2009

To cite this Article Nasim, Muhammad, Qureshi, Riaz H., Aziz, Tariq, Saqib, M., Nawaz, Shafqat, Akhtar, J., Haq, M. A. and Sahi,

Shahbaz Talib(2009)'Different Eucalyptus Species Show Different Mechanisms of Tolerance to Salinity and Salinity × Hypoxia',Journal of Plant Nutrition,32:9,1427 — 1439 To link to this Article: DOI: 10.1080/01904160903092648 URL: http://dx.doi.org/10.1080/01904160903092648

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Journal of Plant Nutrition, 32: 1427–1439, 2009 Copyright © Taylor & Francis Group, LLC ISSN: 0190-4167 print / 1532-4087 online DOI: 10.1080/01904160903092648

Different Eucalyptus Species Show Different Mechanisms of Tolerance to Salinity and Salinity × Hypoxia Muhammad Nasim,1 Riaz H. Qureshi,2 Tariq Aziz,1 M. Saqib,2 Shafqat Nawaz,1 J. Akhtar,2 M. A. Haq,2 and Shahbaz Talib Sahi1 Downloaded By: [Nasim, Muhammad] At: 06:19 6 August 2009

1

Sub-Campus Depalpur, University of Agriculture, Faisalabad, Depalpur, Pakistan 2 Saline Agriculture Research Centre, University of Agriculture, Faisalabad, Depalpur, Pakistan

ABSTRACT We studied the effect of sodium chloride (NaCl) salinity and oxygen deficiency stress on growth and leaf ionic composition of three Eucalyptus species [E. tereticornis, E. camaldulensis (Silverton), and E. camaldulensis (Local)]. Species were grown with control (no NaCl) and salinity (150 mol m−3 NaCl) under hypoxic and non-hypoxic conditions in nutrient solution with five replications following CRD. Species differed significantly in their response to salinity and hypoxia. Absolute shoot dry matter was significantly better in E. camaldulensis (Silverton) in salinity and in E. camaldulensis (Local) in saline hypoxic treatment. E. tereticornis was the most sensitive species to salinity and salinity × hypoxia in the root environment. Sodium (Na+ ) and chloride (Cl− ) concentrations were significantly lower in E. camaldulensis (Local) in non-hypoxic saline treatment compared to the other two species. E. camaldulensis (Silverton) seems to have better tissue compartmentalization, whereas E. camaldulensis (local) seems to have better exclusion of Na+ at the root level. Keywords: salinity, hypoxia, Eucalyptus, leaf expansion, growth, ionic composition

INTRODUCTION Desertification of arable lands is a serious threat to agriculture around the globe. Salinization is an important factor contributing to the degradation of the arable Received 29 October 2007; accepted 17 July 2008. Address correspondence to Dr. Muhammad Nasim, University of Agriculture, Faisalabad, Sub-Campus Depalpur, Depalpur, Okara, Pakistan. E-mail: mnasimshahid@ yahoo.com 1427

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lands particularly in arid and semi-arid regions (Ashraf, 1994). Approximately 6.3 million hectares of agricultural land in Pakistan is affected by varying degrees of salinity/sodicity (Ghafoor et al., 2004) that adversely affects plant growth and yield in a number of species (Eom et al., 2007). Soil salinity affects plant growth mainly through osmotic effects and specific ion toxicities (Grattan and Grieve, 1999; Munns, 2002; 2005) resulting from accumulation of sodium and chloride in the plant tissues (Saqib et al., 2004a; 2005a; Rezaei et al., 2006). Sodium (Na) concentration in tissues and potassium (K+ ): Na+ ratios are extensively used in screening mass germplasms as selection parameters (Saqib et al., 2004a; Tahir et al., 2006). Salt affected soils (mainly those with high sodium) are generally dispersed soils having low soil permeability, porosity, and hydraulic conductivity (Qadir et al., 2005). Low water infiltration and soil dispersion poses a serious drainage problem and may lead to waterlogging. Plant roots affected by waterlogging are deprived of sufficient oxygen resulting in a change in the mode of respiration from aerobic to an-aerobic and low energy production (Marschner, 1995). Low energy production in roots disturbs the nutrient and water uptake (Jackson, 1979; Morard and Silvestre, 1996). Waterlogging also reduces nutrient uptake that results in nutrient deficiency in shoot leading to reduced shoot growth (Trought and Drew, 1980). Higher abscisic acid production and movement to younger leaves under oxygen (O2 ) deficiency causes stomatal closure in plants (Zhang and Zhang, 1994) affecting photosynthesis and ultimately yield. Waterlogging also affects sodium exclusion from plant roots, which is a major salinity tolerance mechanism in various glycophytes (Barrett-Lennard, 1986; Saqib et al. 2005a). A combined effect of salinity and waterlogging on plant growth is more damaging than caused by salinity and waterlogging alone (Qureshi and Barrett-Lennard, 1998; Saqib et al., 2004a). Although several relatively salt tolerant cultivars of different agronomic crops are available to grow on moderately salt affected soils yet these cultivars fail to produce economical yields on highly degraded salt affected soils. Reclamation of such soils through physical and chemical approaches is also not feasible. Revegetation of these lands with salt tolerant tree species is a viable approach mainly because of low input and increased demand of wood for fuel and furniture. Selection of suitable tree species is a pre-requisite for such biological remediation approach. However, very little work has been reported on this aspect particularly on tree species. The present paper reports the effect of salinity and hypoxia interaction on growth and leaf ionic composition of three Eucalyptus species. MATERIALS AND METHODS Site and Environmental Conditions The experiment was conducted in a rain-protected wire house at the Institute of Soil & Environmental Sciences, University of Agriculture, Faisalabad,

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Pakistan. Faisalabad is situated at 73.4◦ longitude and 31.5◦ latitude. The average day and night temperatures during the study were 32 and 20◦ C, respectively, while the average maximum relative humidity was 70%, and there was 7 h average daily sunshine during the growth period.

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Plant Material and Experimental Details Seeds of three Eucalyptus species [E. tereticornis, E. camaldulensis (Silverton), and E. camaldulensis (Local)] were collected from Australian Revegetation Corporation Limited, Western Australia and Saline Agriculture Research Centre, University of Agriculture, Faisalabad, Pakistan. Fifty seeds of each species were sown in polyethylene lined iron trays containing silica gravel and synthetic vermiculite (mixed in 1:1 ratio). The canal water was used to moisten the seeds for proper germination. Electrical conductivity of canal water was 0.29 d Sm−1 . One week after germination, half strength Hoagland’s nutrient solution (Hoagland and Arnon, 1950) was used for the seedling establishment. Seedlings were grown for three months in these trays. Uniform sized seedlings were then transplanted in foam plugged holes in polystyrene sheets floating on continuously aerated half strength Hoagland’s nutrient solution contained in polyethylene lined iron tubs of 200 L capacity (100 × 100 × 30 cm3 ). The experiment was replicated five times following completely randomized design (CRD). Solution pH was monitored and maintained daily at 6 ± 0.5. There were four treatments viz i) non-saline non-hypoxic (control), ii) saline non-hypoxic, iii) non-saline hypoxic, and iv) saline-hypoxic. Salinity level for saline treatment was 150 mol m−3 sodium chloride (NaCl). The salinity was developed in three equal splits in a week (each of 50 mol m−3 NaCl after 2 d). The hypoxia was imposed by surface sealing of the nutrient solution. Three days after surface sealing, substrate oxygen concentration (measured with O2 electrode) was 3 mg dm−3 . The treatment solutions were replaced thereafter weekly till harvesting and in hypoxic treatments the new solution was flushed with N2 for 15 minutes to remove oxygen. Growth Measurement To study leaf expansion (increase in leaf length) 2-day old leaf of each plant from shoot apex was marked and leaf length was measured at 2 day (d) interval up to 11th day. After 8 weeks of salinity and hypoxia stress plant height was recorded. At this time plants were harvested and their dry weights of shoots and roots were recorded after oven drying the samples at 70◦ C in a vacuum oven for 48 hrs. Leaf Ionic Analysis Plants were harvested after 8 weeks and leaves of plants were divided into top leaves (young leaves) and lower fully expanded leaves (mature leaves). The

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separated leaves were immediately washed with distilled water and blotted dry with tissue paper. The samples were then dried at 70◦ C in a forced air driven oven for 48 h. The oven dried plant samples were fine ground in a wily mill to pass through 1 mm sieve. The fine ground plant samples (1 g) were digested in tri-acid mixture (sulfuric acid, nitric acid, and perchloric acid) (Miller, 1998). Potassium and Na+ were determined on a flame photometer (Jenway PFP7, Bibby Scientific LTD., Essex England). For chloride determination, plant samples were extracted with HNO3 and chloride was determined from this extract using chloride analyzer (Corning Chloride Analyzer 926, Corning Inc., Corning, NY, USA).

Statistical Analysis The data were analyzed statistically following the methods of Gomez and Gomez (1984) using MSTAT-C (Russell and Eisensmith, 1983). The significance of differences among the means was compared using standard error √ computed as s/ n, where s is the standard deviation and n shows the number of observations. RESULTS Shoot and Root Growth Salinity significantly reduced shoot dry matter of all the species at both nonhypoxic and hypoxic conditions (Figure 1). E. camaldulensis (Silverton) produced the maximum absolute and relative shoot dry matter (36%) under nonhypoxic salinity followed by E. camaldulensis (Local) and E. tereticornis. However, under hypoxic salinity treatment E. camaldulensis (Local) performed best followed by E. camaldulensis (Silverton) and E. tereticornis, in absolute as well as relative terms. Hypoxia alone reduced the shoot and root dry matter of E. tereticornis only. Root dry matter (RDM) of Eucalyptus species was also significantly reduced by salinity in hypoxic conditions (Figure 2). E. camaldulensis (Local) and E. tereticornis produced respectively, the maximum and minimum root dry matter in this treatment. However, in non-hypoxic salinity treatment E. camaldulensis (Silverten) and E. camaldulensis (Local) differed non-significantly. Root: shoot ratio (RSR) of Eucalyptus species was increased significantly under saline conditions both in hypoxic and non-hypoxic treatments, whereas hypoxia alone did not affect it significantly (data not shown). Salinity also significantly reduced leaf expansion of E. tereticornis and E. camaldulensis (Local) under non-hypoxic as well as hypoxic conditions (Figure 3). Plant height of all the species was also reduced significantly by salinity and salinity × hypoxia (data not shown).

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Figure 1. Shoot dry matter (g/plant) of Eucalyptus species grown with salinity and hypoxia. The columns show mean of 5 replications and bars show standard error. Salinity level for saline treatment was 150 mol m−3 NaCl. Plants were grown for 8 weeks in the treatment solutions.

Figure 2. Root dry matter (g/plant) of Eucalyptus species grown with salinity and hypoxia. The columns show mean of 5 replications and bars show standard error. Salinity level for saline treatment was 150 mol m−3 NaCl. Plants were grown for 8 weeks in the treatment solutions.

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Figure 3. Leaf expansion (cm/d) of Eucalyptus species grown with salinity and hypoxia. The columns show mean of 5 replications and bars show standard error. Salinity level for saline treatment was 150 mol m−3 NaCl. Plants were grown for 8 weeks in the treatment solutions.

Leaf Ionic Composition Leaf ionic composition of young as well as mature leaves was significantly affected by salinity under non-hypoxic as well as hypoxic conditions with a similar trend in both types of the leaves (Figures 4–6; data shown only for the young leaves). Salinity caused a significant increase in Na+ and Cl− concentrations in both type of the leaves irrespective of the hypoxic treatment (Figures 4 and 5). Sodium concentration in young leaves of plants grown with salinity was 3.5 folds and 4.5 folds higher than those grown without salinity under non-hypoxic and hypoxic conditions, respectively. E. tereticornis and E. camaldulensis (Silverton) accumulated the maximum Na+ under non-hypoxic saline treatment and differed non-significantly. E. camaldulensis (Local) accumulated the minimum leaf Na+ in both the saline treatments. Leaf Na+ was also significantly higher in the leaves of all the species under hypoxic salinity treatment than under non-hypoxic salinity treatment. The maximum chloride (Cl− ) concentration was observed in the leaves of E. camaldulensis (Silverton) under non-hypoxic salinity and in the leaves of E. tereticornis under hypoxic salinity treatment. E. camaldulensis (Local) differed non-significantly with E. camaldulensis (Silverton) under hypoxic saline conditions and with E. tereticornis under non-hypoxic saline conditions. Potassium sodium ratio (K+ : Na+ ratio) was significantly decreased due to salinity stress in the root environment

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Figure 4. Sodium concentration (mmoles kg−1 ) in young leaves of Eucalyptus species grown with salinity and hypoxia. The columns show means of 5 replications and bars show standard error. Salinity level for saline treatment was 150 mol m−3 NaCl. Plants were grown for 8 weeks in the treatment solutions.

Figure 5. Chloride concentration (mmoles kg−1 ) in young leaves of Eucalyptus species grown with salinity and hypoxia. The columns show means of 5 replications and bars show standard error. Salinity level for saline treatment was 150 mol m−3 NaCl. Plants were grown for 8 weeks in the treatment solutions.

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Figure 6. K:Na in young Leaves of Eucalyptus species grown with salinity and hypoxia. The columns show means of 5 replications and bars show standard error. Salinity level for saline treatment was 150 mol m−3 NaCl. Plants were grown for 8 weeks in the treatment solutions.

under hypoxic as well as non-hypoxic conditions (Figure 6). The maximum K+ : Na+ ratio was observed in E. camaldulensis (Local) followed by E. camaldulensis (Silverton) under both non-hypoxic and hypoxic salinity treatments. Salinity under hypoxic conditions also have a significantly higher effect than under non-hypoxic conditions whereas hypoxia alone significantly decreased the leaf K+ : Na+ of E. tereticornis only.

DISCUSSION Sodium chloride salinity in the nutrient solution significantly reduced tree growth in terms of plant height, leaf expansion, shoot dry matter, and root dry matter in all the species (Figures 1–3) and there was a negative significant correlation between growth performance and leaf Na+ and Cl− concentrations (Table 1). Water stress, ion imbalance and ion toxicity are considered the common causes of growth reduction due to salinity (Munns, 2002; 2005; Zhu, 2003). Genotypic differences for different growth parameters were significant among the three species in non-hypoxic saline treatment. In this treatment, E. camaldulensis (Silverton) and E. camaldulensis (Local) produced higher shoot and root dry matter than E. tereticornis but differed non-significantly with one

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Table 1 Relationship between different growth parameters and ionic composition of young and mature leaves of Eucalyptus species

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Na+ in young leaves K+ in young leaves K+ :Na+ in young leaves Cl− in young leaves

Shoot dry matter

Root dry matter

Leaf expansion

−0.71∗∗ 0.51∗ 0.82∗∗ −0.69∗

−0.60∗ 0.72∗ 0.79∗∗ −0.63∗

−0.39NS 0.47∗ 0.61∗ −0.47∗

another. The poor growth performance of E. tereticornis may be due to higher Na+ and Cl− uptake, lower K+ uptake (Table 2) and resultantly low K+ : Na+ ratio in its leaves. The leaf Na+ concentration of E. camaldulensis (Silverton) was statistically similar to E. tereticornis but its better growth shows better compartmentalization of Na+ and Cl− into the vacuoles by this species. The higher K+ : Na+ ratio also supports its higher growth performance (Rezaei et al., 2006). Saqib et al. (2005b) reported that better compartmentalization of Na+ into the vacuoles is an important determinant for salt tolerance in wheat. Lower Na+ and Cl− accumulation by E. Camaldulensis (Local) shows better exclusion in this species at the root level (Table 2; Na+ and Cl− uptake per g root dry matter) that enabled its better growth (Saqib et al., 2004a). A number of Table 2 Sodium and chloride uptake (mg per g root dry matter) by different Eucalyptus species under saline and saline hypoxic conditions

Sodium uptake E. tereticornis E. camaldulensis (Silverton) E. camaldulensis (Local) Chloride uptake E. tereticornis E. camaldulensis (Silverton) E. camaldulensis (Local) Potassium uptake E. tereticornis E. camaldulensis (Silverton) E. camaldulensis (Local)

Non-hypoxic saline

Hypoxic saline

3.8 2.9 1.4

3.2 2.8 2.3

1.6 1.3 1.1

2.0 1.4 1.7

0.95 1.0 1.0

0.76 0.69 1.4

The columns show mean of 5 replications and bars show standard error. Salinity level for saline treatment was 150 mol m−3 NaCl. Plants were grown for 8 weeks in the treatment solutions.

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researchers have reported significant variations in the growth and salt tolerance among different species of the woody plants (Bell et al., 1994; Marcar et al., 1995; Rawat and Banerjee, 1998). Many earlier researchers have used Na+ : K+ ratio as an indicator of salinity tolerance (Saqib et al., 2004b; Munns, 2005; Rezaei et al., 2006) as adequate Na+ : K+ ratio in the cytosol is essential for normal cellular functions of plants (Marschner, 1995; Chinnusamy et al., 2005). Higher levels of external Na+ in saline soils interfere with K+ acquisition by plants (Subbarao et al., 1990). The species with ability to maintain K+ uptake or to exclude Na+ can tolerate salinity stress such as E. camaldulensis (local). The lower Na+ uptake and higher K+ uptake at root level, and higher K+ : Na+ ratio in this species is in accordance with its better performance at saline environment (Table 2; Figure 6). Low oxygen supply in hypoxia affects root growth because energy production is decreased (Barret-Lennard, 1986). Under hypoxia, shoot and root growth retardation has also been reported by several researchers (Jackson, 1979; Lizaso et al., 2001). In the present study, hypoxia significantly reduced the shoot and root growth of the salt sensitive species E. tereticornis only (Figures 1-2). Aerenchyma development in the roots is an important mechanism of hypoxia tolerant (Saqib et al., 2005a) that may not have developed considerably in this species. Marcar et al. (1995) also observed large variations among the eucalyptus species for their tolerance to oxygen deficiency (waterlogging). In saline-hypoxic conditions roots are not able to exclude Na+ and Cl− mainly because of low energy production (Qureshi and Barret-Lennard, 1998). This lower ability to exclude toxic elements can further inhibit K+ uptake by plant roots. Saqib et al. (2004a) reported a higher accumulation of Na+ and Cl− and lower K+ in leaf sap under saline waterlogged conditions than under saline conditions. Marcar et al. (1993) and Galloway and Davidson (1993) observed similar depressive effects of salinity × hypoxia interaction on growth of Eucalyptus and Atriplexes. However, in the present study higher reduction in shoot and root growth was observed only in E. camaldulensis (Silverton) in saline hypoxic treatment than in the non-hypoxic saline treatment (Figures 1–2). It may be due to its decreased root ability to develop aerenchyma that resulted in low Na+ exclusion and K+ uptake at the root level (Figure 4; Table 2) as aerenchyma helps in root Na+ exclusion (Saqib et al., 2005b). In this treatment E. camaldulensis (local) performed significantly better than the other species which may be due to its better aerenchyma and nodal root development and hence better salt exclusion at the root level. In conclusion, E. camaldulensis (Silverton) is better tolerant to salinity alone and E. camaldulensis (local) is better tolerant to saline and hypoxic conditions. E. camaldulensis (Silverton) seems to have better tissue compartmentalization whereas E. camaldulensis (local) seems to have better exclusion of Na+ at the root level.

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