Introduction

Soil salinity, especially in arid and semi-arid regions that restrict plant growth and production is a worldwide problem [1]. About 20% global croplands have become less productive or uncultivable wastelands caused by soil salinization [2]. Therefore the researchers have given importance to these serious environmental problems in the last decade. Salinity is of concern because of its detrimental effect on plant growth, nutritional balance, and plant and flower marketable quality, including visual injury, flower distortion and reduced stem length [3-5].

The deterious effects of salinity on plant growth are associated with low osmotic potential of soil solution, nutrient disorders, specific ion effects or a combination of all those factors [6, 7]. Due to the increase in green areas in the urban environment, the demand for water supply is increasing [8, 9]. As demand for water continues to rise in agricultural, urban, industrial, environmental and recreational areas, shortages of quality water have become a concern in many regions [5, 10]. Such as recycled water, treated municipal wastewater and brackish groundwater used due to water scarcity alternative water sources generally contain higher levels of salt [11]. Salinity stress in ornamental plant cultivation draws attention worldwide. The salinity tolerance of plants is a polygenic character governed by many genetic factors [12, 13]. The effect of salt on ornamental value is an important criterion when searching for salinity-tolerant species and cultivars [14].

Arbuscular mycorrhizal fungi are common microorganisms that can form a symbiotic relationship with the roots of most terrestrial plants. Root-infected arbuscular mycorrhizal fungi (AMF) improve plant growth through uptake of soil nutrients via extra matrix hyphae. Furthermore, complementary effect of arbuscular mycorrhizal fungi, as an alternative for reducing fertilizer need of major crop species were reported [15]. AMF can form root interrelations in more than 80% of terrestrial plants worldwide [16]. This relationship improves plant growth and resistance to multiple abiotic stressors, including high temperature, cold, drought, and salinity stress [17-22]. Ornamental plants (herbaceous-woody) vary considerably in terms of degree salt tolerance [23]. Mycorrhizal symbiosis has been recognized as a plant biofertilizer and bioprotectant protecting it from environmental stresses such as drought and salinity [24], improving product [25]. The importance of arbuscular mycorrhiza against salinity should be considered in landscape studies [9].

Cut flowers are an important branch of the floriculture industry [26-28]. Narcissus is one of the cut flowers grown worldwide for its medicinal and ornamental values. The Narcissus species are mostly native to the Mediterranean region, although a few species are found from Central Asia to China [29]. Narcissus tazetta (L.) belonging to the Amaryllidaceae family is used as a cut flower in landscaping and cultivation. It has as much economic value as an ornamental bulbous plant.

The aim of this study was to determine the effect of mycorrhiza on the macro and micro nutrient uptakes in the bulbs, roots and leaves of Narcissus tazetta (L.) under saline conditions.

Experimental

The study was conducted with bulbs of Narcissus tazetta (L.) and completely randomized factorial design with three application so that each replication included five pots. In the experiment, different salt concentrations were applied with mycorrhiza (M+) (Glomus intraradices NC Schenck & GS Sm.) and without mycorrhiza (M-) planting soil. G. intraradices mycorrhizal fungus was mixed at 7.7% percentage to experimental soil. Bulbs were planted into 6 cm diameter plastic pots having 3 kg soil after one week following mycorrhizal inoculation. N:P:K: ratio of chemical fertilizers were applied so that 6:12:6 in pots. Soil properties of experimental soil were determined using the standard analyses methods [30]. Some physical and chemical properties of experimental soil were given in Table 1.

Physical and chemical properties of experimental soil had loamy texture, non-saline, slightly alkaline, low in organic matter, insufficient in phosphorus and zinc contents sufficient in calcium, magnesium, manganese and copper contents (Table 1).

Ten days after planting Narcissus tazetta plant was treated with sodium chloride (NaCl) at three different concentrations such as salt-free (S0), 34 mmol (S1) and 68 mmol (S2) in mediums with mycorrhiza (M+) and without mycorrhiza (M-). Because of the development of the bulb root system, until the first leaves emergence (36 days) all pots were left in 10ºC below the temperature of the cold laboratory, and then were taken to a climate chamber at 20-23ºC temperature. The nutrient uptakes were analyzed in dried and grinded leaf, bulb and root samples according to the methods reported by [31]. Na, Fe, Mn, Zn, Cu K, Ca and Mg uptakes were determined by using atomic absorption spectrophotometers. N and P uptakes content were analyzed by using Kjeldahl method and spectrophotometric method respectively. Statistical analyses of the data were done with MINITAB 14 program.

Results and Discussion

The variance analyses results belong the effects of mycorrhiza applications and salinity on plant nutrient uptakes of bulb, root and leaf are given in Table 2, Table 3, and Table 4.

The salt applications had significant effects on K and Na uptakes of bulbs at 5% and 1% levels respectively. The effects of mycorrhiza applications on macro and micro nutrient uptakes of bulbs were found non-significant statistically. The effects of salt and mycorrhiza interactions on the N uptakes were statistically significant at the 5% level in bulbs (Table 2).

Table 1.

Properties of the experiment soil.

TexturepHSalinityLimeOMPKCaMgFeMnZnCu
µS cm-1%%mg kg-1
Loamy7.81360.73.861.325.5029830344055.5829.840.580.81

The effects of salt applications were found significant at 1% level for all nutrients uptakes of roots except Cu uptake. The Cu uptake means of roots were affected by salt applications at 5% significance level. Mycorrhiza applications had a statistically significant effect on all nutrient uptakes except Na and Mn at the level of 1% and for Mg at the level of 5%.

The effects of salt and mycorrhiza interactions on the Fe uptake was statistically significant at the 1% level and were significant at the 5% level for N and P uptakes of roots (Table 3).

All nutrient uptakes except Na of leaves were significantly affected by salt applications at 1% and Na uptakes were affected at 5% significance level. Mycorrhiza treatments had a statistically significant effect at 1% level on P uptakes and on Cu uptakes at 5% level. The effects of interactions among salt and mycorrhiza were found significant at 5% level for Ca, P and Mn uptakes and at 1% level for Mg, Fe and Cu uptakes statistically (Table 4).

The effects of salt and mycorrhiza applications on nutrient uptakes of Narcissus tazetta’s roots, leaves and bulbs were given in Table 5, Table 6 and Table 7.

The increasing salt doses had not significantly effects on nutrient uptakes of Narcissus tazetta’s bulbs except N, K and Na uptakes. The Na and K uptakes increased by increasing salt doses. The lowest K uptake was obtained in S0 application as 0.052 mg plant-1 and the highest K uptake was obtained in S2 application as 0.074 mg plant-1. The lowest Na uptake was obtained in S0 application as 2.487 mg plant-1, and the highest Na uptake was obtained in S2 application as 3.825 mg plant-1. N uptakes obtained as 0.127% in S0 applications with mycorrhiza were higher than those obtained as 0.080% in salt applications without mycorhiza (Table 5).

The salt applications decreased macro and micro nutrients uptakes of roots. The lowest N, P, K, Ca, Mg, Na, Fe, Mn, Zn and Cu uptakes were determined as 0.003 mg plant-1, 0.043 mg plant-1, 0,008 mg plant-1, 0.008 mg plant-1, 0.002 mg plant-1, 0.718 mg plant-1, 896.443 mg plant-1, 35.813 mg plant-1, 7.695 mg plant-1 and 16.340 mg plant-1 in S2 applications respectively. Mycorrhiza applications increased macro and micro nutrients uptakes of roots. These increases did not significant for Na and Mn uptakes statistically. The interactions between salt and mycorrhiza significantly effected N, P and Fe uptakes of roots. The decreases in N, P and Fe uptakes by 68 mmol NaCl applications were lower in mycorrhiza applications than those in non mycorhizza applications (Table 6).

Table 2.

Variance analysis results for nutrient uptakes in bulbs (F values).

BULB
Variation SourcesdfNPKCaMgNaFeMnZnCu
Salt (NaCl)21.52 ns3.40 ns4.60 *0.20 ns1.02 ns12.81 **0.63 ns0.77 ns0.27 ns0.00 ns
Mycorrhiza11.38 ns0.49 ns1.30 ns1.39 ns0.53 ns2.94 ns1.04 ns0.08 ns1.10 ns0.24 ns
Salt*Mycorrhiza26.24 *3.08 ns0.29 ns1.29 ns0.24 ns0.97 ns2.57 ns0.39 ns2.78 ns2.07 ns

[i] *significant at 0.05, **significant at 0.01, ns not significant

Table 3.

Variance analysis results for nutrient uptakes in roots (F values).

ROOT
Variation SourcesdfNPKCaMgNaFeMnZnCu
Salt (NaCl)2140.29 **74.86 **16.77 **15.02 **13.11 **16.58 **11.91 **8.73 **27.82 **5.35 *
Mycorrhiza115.33 **21.35 **12.20 **14.40 **4.78 *1.20 ns23.25 **4.70 ns12.62 **24.88 **
Salt*Mycorrhiza24.44 *6.15 *2.11 ns0.32 ns0.20 ns2.46 ns7.46 **0.34 ns1.40 ns1.07 ns

[i] *significant at 0.05, **significant at 0.01, ns not significant

Table 4.

Variance analysis results for nutrient uptakes in leaf (F values).

LEAF
Variation SourcesdfNPKCaMgNaFeMnZnCu
Salt (NaCl)246.63 **37.58 **34.86 **12.29 **52.70 **5.61*45.90 **22.16 **37.41 **20.23 **
Mycorrhiza12.09 ns11.53 **0.58 ns0.53 ns0.01 ns0.16 ns1.30 ns0.28 ns0.81 ns7.47 *
Salt*Mycorrhiza23.29 ns5.09 *3.76 ns4.52 *8.96 **1.93 ns7.48 **5.89 *2.54 ns14.79 **

[i] *significant at 0.05, **significant at 0.01, ns not significant

The macro and micro nutrient uptakes of leaves decreased by increasing salt doses. The lowest N, P, K, Ca, Mg, Na, Fe, Mn, Zn and Cu uptakes were determined as 0.058 mg plant-1, 0.597 mg plant-1, 0.072 mg plant-1, 0.028 mg plant-1, 0.008 mg plant-1, 2.613 mg plant-1, 261.422 mg plant-1, 48.177 mg plant-1, 105.540 mg plant-1 and 55.037 mg plant-1 in S2 applications respectively. The highest nutrient uptake means of leaves were obtained in control.

Mycorrhiza applications significantly increased P uptake of leaves. The P uptake means were determined as 1.422 mg plant-1 and 1.007 mg plant-1 in mycorrhiza and non mycorrhiza applications respectively. The effects of interactions were found significant for P, Mg, Fe, Mn, Ca and Cu uptakes of leaves. The decreases in P, Mg, Fe, Mn and Cu by 68 mmol NaCl applications were lower in mycorrhiza applications than those in non mycorhizza applications (Table 7).

According to the results, increasing doses of sodium chloride had negative effects on nutrient uptakes of different organs except Na and K uptakes of bulbs. [5] reported that salinity have negative effects on plant growth and nutritional balance of ornamental plants. Salt stress affects all the major processes, such as growth, photosynthesis, protein synthesis, and energy and lipid metabolisms [32-34]. [3] reported that excessive concentration of ions, especially Na+ and Cl- may limit the uptake of other ions. [35] in carnation (Dianthus caryophyllus L.) and gerbera (Gerbera jamesonii L.), [36] in Limonium species determined that increased level of salinity inhibits water uptake and crop nutritional elements from soil via roots. The most common consequences of salinity stress on plants are the reduction of nutrient ions, especially potassium content [37]. In this study, the K uptake of roots, and leaves decreased significantly while K uptake increased significantly in bulbs by increasing NaCl doses. It was reported that salinity has also different effects on plant organs. Plants are affected in a different way by amount and kind of salt depending on their growth and development stage. For example, plant leaves against salinity more sensitive than plant roots [38]. Similarly in this study Na and K uptakes of bulbs increased by increasing salt doses. The decreases in the K+ concentrations of the roots and shoots by the increase in salinity stress were reported by [39]. They declared that The K+ concentration in the roots and shoots significantly decreased depending on the increase in salinity stress in Tagetes erecta L. ‘Sumo orange’.

Several researchers have reported that Na and Cl can affect the uptake of nutrients by competing with nutrients or by affecting the ion permeability of the membrane. Increasing salinity can lead a decrease in N, P, K and Ca uptakes in most plants [40-42]. [39] declared that decreases in the concentration of Cu and Zn in the roots and Mn and Fe in the shoots were significant depend on salinity degree.

Mycorrhiza applications generally increased nutrient uptakes of daffodil’s roots. These increases were significant for P, K, Ca, Mg, Fe and Zn. P uptake of leaves also increased significantly with mycorrhiza applications. Several researchers reported that root colonization with arbuscular mycorrhizal fungi (AMF) have enhanced the uptake of especially P, N, and other nutrients [16, 43, 44, 45].

Enhancement of plant P uptake by AMF has been reported [46-50] and has been recognized as one of the main reasons for the improvement of growth in salt-affected plants colonized by AMF [51]. [52] declared that hydrolysis of organic P as a result of secretion of alkaline phosphate compounds by arbuscular mycorrhizal fungi leads to higher plant productivity under P-deficient conditions. [53] reported that mycorrhizal association enhances plant growth and productivity by increasing nutrient element uptake. Arbuscular mycorrhizal fungi are common microorganisms that can form a symbiotic relationship with the roots of most terrestrial plants. Root-infected arbuscular mycorrhizal fungi (AMF) improve plant growth through uptake of soil nutrients via extra matrix hyphae [15, 54]. These extra-radical hyphae act as absorbent structures for mineral elements and water. Since radical hyphae can extend several centimes from the roots can effectively bridge over the nutrient depletion zone around roots and can absorb inert elements from the bulk soil [15, 55]. Arbuscules are the structures, where metabolites exchanges take place between the fungus and host cytoplasm [56-62].

Table 5.

Effects of salt and mycorrhiza applications on nutrient uptakes of Narcissus tazetta’s bulbs and Duncan differentiation groups among means.

BULB
NutrientMycorrhizaSalinity
S0 (control)S1 (34 mmol NaCl)S2 (68 mmol NaCl)Mean
N (mg plant-1)+M0.127 a*0.117 ab0.110 ab0.118
-M0.080 b0.120 ab0.126 a0.109
Mean0.1040.1180.118
P (mg plant-1)+M1.9301.5202.5632.004
- M1.4772.0802.0331.863
Mean1.7031.8002.298
K (mg plant-1)+M0.0580.0630.0780.067
- M0.0470.0630.0700.060
Mean0.052 b0.063 ab0.074 a*
Ca (mg plant-1)+M0.0510.0460.0460.048
- M0.0360.0420.0490.042
Mean0.0440.0440.047
Mg (mg plant-1)+M0.0150.0120.0140.014
- M0.0120.0110.0140.012
Mean0.0140.0110.014
Na (mg plant-1)+M2.5132.7873.5502.950
- M2.4603.4034.1003.321
Mean2.487 c**3.095 b3.825 a
Fe (mg plant-1)+M152.720127.943138.900139.854
- M117.253182.223171.720157.066
Mean134.987155.083155.310
Mn (mg plant-1)+M72.50366.61776.68271.934
- M63.37070.73776.34770.151
Mean67.93768.67776.514
Zn (mg plant-1)+M183.400193.867242.613206.627
- M235.293231.843205.183224.107
Mean209.347212.855223.898
Cu (mg plant-1)+M69.67085.29080.58378.514
- M90.06074.27380.60081.644
Mean79.86579.78280.592

[i] *,**Means followed by different capital letters, in columns, and followed by different small letters, in lines, differ statistically at 0.05 and 0.01

The interactions between salt and mycorrhiza were significant for N in bulbs, for P and Fe in roots and for P, Ca, Mg, Fe, Mn and Cu in leaves. The decreases in these nutrients uptakes by 68 mmol NaCl applications were lower in mycorrhiza applications than those in non mycorrhiza applications.

It was reported that under salinity stress conditions, AMF inoculated plants can improve adverse effects by increasing regulation on ion homeostasis, osmotic balance and antioxidant enzyme activity [63,64]. In addition AMF inoculated plants can ameliorate negative effects caused by salinity on photosynthetic activity, nutrient acquisition, and water uptake [65-68]. The results of this study are in agreement with referred similar studies results and literature knowledge.

Table 6.

Effects of salt and mycorrhiza applications on nutrient uptakes of Narcissus tazetta’s roots and Duncan differentiation groups among means.

ROOT
NutrientMycorrhizaSalinity
S0 (control)S1 (34 mmol NaCl)S2 (68 mmol NaCl)Mean
N (mg plant-1)+M0.014 a*0.007 c0.004 d0.008 a**
- M0.011 b0.007 c0.002 d0.006 b
Mean0.012 a**0.007 b0.003 c
P (mg plant-1)+M0.187 a*0.097 bc0.063 cd0.115 a**
- M0.123 b0.097 bc0.023 cd0.081 b
Mean0.155 a**0.097 b0.043 c
K (mg plant-1)+M0.0290.0200.0130.021 a**
- M0.0170.0190.0040.013 b
Mean0.023 a**0.020 a0.008 b
Ca (mg plant-1)+M0.0210.0220.0110.018 a**
- M0.0120.0160.0040.011 b
Mean0.017 a**0.019 a0.008 b
Mg (mg plant-1)+M0.0040.0060.0030.005 a*
- M0.0030.0060.0020.003 b
Mean0.003 b**0.006 a0.002 b
Na (mg plant-1)+M1.8101.4130.9201.381
- M1.4471.7070.5171.223
Mean1.628 a**1.560 a0.718 b
Fe (mg plant-1)+M1754.493 a*1170.247 a1376.010 a1433.583 a**
- M1248.280 a1169.730 a416.877 b944.962 b
Mean1501.387 a**1169.988 b896.443 c
Mn (mg plant-1)+M120.403113.88350.20794.831
- M72.33395.26021.42063.004
Mean96.368 a**104.572 a35.813 b
Zn (mg plant-1)+M28.33318.69311.20719.411 a**
- M18.92016.3704.18313.158 b
Mean23.627 a**17.532 b7.695 c
Cu (mg plant-1)+M36.18034.14326.00332.109 a**
- M15.36024.3706.67715.469 b
Mean25.770 a*29.257 a16.340 b

[i] *,**Means followed by different capital letters, in columns, and followed by different small letters, in lines, differ statistically at 0.05 and 0.01

Table 7.

Effects of salt and mycorrhiza applications on nutrient uptakes of Narcissus tazetta’s leaves and Duncan differentiation groups among means.

LEAF
NutrientMycorrhizaSalinity
S0 (control)S1 (34 mmol NaCl)S2 (68 mmol NaCl)Mean
N (mg plant-1)+M0.2200.1310.0870.146
- M0.1990.1540.0290.127
Mean0.210 a**0.142 b0.058 c
P (mg plant-1)+M2.233 a*1.087 b0.947 bc1.422 a*
- M1.550 ab1.223 b0.247 c1.007 b
Mean1.892 a**1.155 b0.597 c
K (mg plant-1)+M0.2680.1510.1060.175
- M0.2430.2030.0390.161
Mean0.256 a**0.177 b0.072 c
Ca (mg plant-1)+M0.069 a0.057 ab0.042 ab0.056
- M0.080 a0.094 a0.013 b0.062
Mean0.074 a**0.075 a0.028 b
Mg (mg plant-1)+M0.030 a0.015 b0.011 bc0.019
- M0.028 a0.025 a0.004 c0.019
Mean0.028 a**0.020 b0.008 c
Na (mg plant-1)+M7.3274.5303.6335.163
- M5.7536.9171.5934.754
Mean6.540 a*5.723 a2.613 b
Fe (mg plant-1)+M753.020 ab428.717 c408.950 c530.229
- M811.300 a512.227 bc113.893 d479.140
Mean782.160 a**470.472 b261.422 c
Mn (mg plant-1)+M120.957 ab98.760 ab72.843 bc97.520
- M153.627 a133.850 ab23.510 c103.662
Mean137.292 a116.305 a48.177 b
Zn (mg plant-1)+M324.053211.657146.887227.532
- M324.057238.53764.193208.929
Mean324.055 a**225.097 b105.540 c
Cu (mg plant-1)+M105.647 bc**100.840 bc88.793 bc98.427 b
- M240.320 a159.437 ab21.280 c140.346 a**
Mean172.983 a**130.138 b55.037 c

[i] *,**Means followed by different capital letters, in columns, and followed by different small letters, in lines, differ statistically at 0.05 and 0.01

Today, there are many studies [69-81] that reveal the effects of biological fertilization, bacterial and fungal inoculations that positively encourage development and growth, such as plant resistance, yield and quality parameters and uptake of nutrients, instead of chemical fertilizers against stress conditions.

In addition to these studies, this study, which determined the effect of mycorrhiza on the nutrient uptake of Narcissus plant in saline growing conditions, provided additional information to the literature.

Conclusions

In this study increasing doses of sodium chloride had negative effects on nutrient uptakes of different organs except Na and K uptakes of bulbs. Mycorrhiza pplications generally increased nutrient uptakes of daffodil’s roots and leaves under salinity conditions. The interactions between salt and mycorrhiza were significant for N in bulbs, for N, P and Fe in roots and for P, Ca, Mg, Fe, Mn and Cu in leaves. The decreases in these nutrients uptakes by 68 mmol NaCl applications were lower in mycorrhiza applications than those in non mycorrhiza applications. According to results of this study it was thought that mycorrhiza applications can be improve adverse effects of salinity on nutrient uptakes in Narcissus tazetta. Mychorrhiza applications can be useful for growing bulbous ornamental plants under salinity conditions.