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The Effects of Plant Growth Promotion Rhizobacteria on Vegetative Growth and Leaf Nutrient Contents of Hazelnut Seedlings (Turkish hazelnut cv, Tombul and Sivri)



Yasar Erturk, Ramazan Cakmakci, Omur Duyar and Metin Turan
 
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ABSTRACT

The objective of the study was to explore possibilities to reduce fertilizer requirement and to identify bacterial strains that used for organically grown Turkish hazelnut cultivars. Plant growth promoting effects of L. enzymogenes 9/8, B. atrophaeus 55/1, A. agilis 2/3, P. macquariensis 59/8, B. lentus (Pb. validus) 29/6, B. pyrrocinia 13/4, P. agglomerans 5/8, R. radiobacter 42/1, S.s maltophilia 21/1, Acinetobacter calcoaceticus 47/6 and mineral fertilizer were tested on Turkish hazelnut cultivars (Tombul and Sivri) based on seedling length, total branch length, branch number trunk diameter and ionic composition of leaves. The results showed that all of bacterial treatments significantly affected the parameters tested. The highest seedling length, total branch length, branch number and trunk diameter of Tombul and Sivri of Turkish hazelnut cultivars was obtained with A. calcoaceticus 47/6, R. radiobacter 42/1, S. maltophilia 21/1, P.macquariensis 59/8, respectively and increasing ratio of seedling length, total branch length, branch number and trunk diameter of Turkish hazelnut cultivars was 24.49, 31.60, 69.28 and 18.74% for Tombul and 21.72, 68.43, 46.90 and 24.41% for Sivri, respectively compared to control. The concentrations of N, P, K, Ca, Mg, Fe, Cu, Mn, Zn, B and Al of plant tissue nutrients were significantly increased by the bacterial treatments tested. All bacterial treatments had positive effect but treatments 13/4 and 42/1 were the most effective in promoting macro and micro nutrient uptake. These results suggest that plant growth rhizobacteria (PGPR) treatments offer an economic and simple means to increase plant growth in soils with low fertility.

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Yasar Erturk, Ramazan Cakmakci, Omur Duyar and Metin Turan, 2011. The Effects of Plant Growth Promotion Rhizobacteria on Vegetative Growth and Leaf Nutrient Contents of Hazelnut Seedlings (Turkish hazelnut cv, Tombul and Sivri). International Journal of Soil Science, 6: 188-198.

DOI: 10.3923/ijss.2011.188.198

URL: https://scialert.net/abstract/?doi=ijss.2011.188.198
 
Received: December 21, 2010; Accepted: February 23, 2011; Published: March 25, 2011



INTRODUCTION

Turkey is a center of origin for the hazelnut and an important producer of this crop. The black sea region which has suitable soil and ecological factors, is extremely well suited for hazelnut growing in Turkey. In fact, Turkey currently holds around 75% of the world hazelnut production. Hazelnut varieties grown at the east and west black sea regions in Turkey are Coryllus avellana L and Coryyllus maxima Mill and their hybrids. Hazelnut production in Turkey has initiated an increasing interest by farmers grow organic hazelnuts (Bostan, 2001; Ercisli, 2004).

Because of the rapid increase of world population and parallel technological development, people were directed to obtain maximum yield per unit area in agricultural production. But efforts to obtain maximum yield gives rise to economical, social and environmental problems causing deterioration of the natural balance. It has been suggested that intensive farming methods are not the solution to the hunger problem in world. Besides this, intensive agricultural practices and methods leading to that chemical residues in agricultural crops and constitutes a threat human plant and animal health, consequently the costs of crop production have increased in course of time. To minimize these problems, organic agricultural practices started. Therefore, more recently there has been a resurgence of interest in environmental friendly, sustainable and organic agricultural practices. The use of bio-fertilizers containing beneficial microorganisms instead of synthetic chemical fertilizer is known to improve plant growth through the supply of plant nutrients and may help to sustain environmental health and soil productivity (O’Connell, 1992). However, one of the important problems in organic production is the decrease in yield (Lind et al., 2003; Vessey, 2003). Recent studies showed that a number of bacterial species mostly associated with the plant rhizosphere, are found to be beneficial for plant growth, yield and crop quality. They are called plant growth promoting rhizobacteria (PGPR). Known as PGPR, biological fertilizers have contributed to the increase in yield significantly by increasing availability of soil macro-micro nutrient such as P, Ca, Fe, Zn using of renewable sources. PGPR either directly helps to provide nutrient to the host plant, indirectly influence root growth and morphology or aide other beneficial symbiotic relationships (Vessey, 2003; Lucy et al., 2004; Cakmakci et al., 2009).

PGPR are groups of bacteria that can actively colonize plant roots and increase plant growth. These can stimulate plant growth, increase yield, reduce pathogen infection, as well as reduce biotic or abiotic plant stress, without conferring pathogenity (Compant et al., 2010). The PGPR strains include Acinotobacter, Algaligenes, Arthrobacter, Azospirillium, Azotobacter, Bacillus, Beijerinckia, Burkholdria, Enterobacter, Erwinia, Flavobacterium, Rhizobium and Serrotia genera (Bashan and de-Bashan, 2005; Han and Lee, 2005). Plant Growth Promoting Rhizobacteria (PGPR) have been considered as a possible alternative to inorganic fertilizer. These PGPR strains may affect plant growth directly by synthesis of phytohormones and vitamins, through N fixation, by resistance, or by the solubilization of organic phosphate (Dobbeleare et al., 2002).

Many studies have been done on the mechanisms and principles of the PGPR-plant relationship, which were accepted widely as rhizosphere effect (Glick, 1995; Zhuang et al., 2007). Several studies found that PGPR can stimulate growth and increase yield in apple (Amarente et al., 2002; Aslantas et al., 2007; Karlidag et al., 2007; Pirlak et al., 2007), mulberry (Sudhakar et al., 2000), apricot (Esitken et al., 2003), raspberry (Orhan et al., 2006), sweet cherry (Esitken et al., 2006; Akca and Ercisli, 2010), highbush berry (Da Silva et al., 2000), strawberry (Esitken et al., 2010), tea (Erturk et al., 2008; Cakmakci et al., 2009; Cakmakci et al., 2010), kiwi (Erturk et al., 2010) and banana (Kavino et al., 2010; Mia et al., 2010).

This study was conducted to investigate the possibility of reducing fertilizer requirement by using PGPR and to identify bacterial strains that can be used for organically grown plants. This is the first study investigating the effects of PGPR on hazelnut seedling grown organically.

MATERIALS AND METHODS

Growth conditions and plant materials: The study was conducted in the greenhouse of Hazelnut Reseach Institue in Giresun, Turkey in 2008 and 2009. Turkish hazelnut cultivars, Tombul and Sivri seedlings plants were maintained under natural light conditions, including day/night temperature of 31/22°C and 60-75% relative humidity during the span of the experiment. Cold-stored bare rooted strawberry plants with one well-developed crown of diameter 8-10 mm were planted in the soil. Soil samples were air-dried, crushed and passed through a 2 mm sieve prior to chemical analysis. The Kjeldahl method and a Vapodest 10 Rapid Kjeldahl Distillation Unit (Gerhardt, Konigswinter, Germany) were used to determine total N (Bremner, 1996). Plant-available P was determined by the sodium bicarbonate method of Olsen et al. (1954). Soil pH was determined in 1:2 extracts according to McLean (1982). Soil organic matter was determined by Smith-Weldon method according to Nelson and Sommers (1982). Ammonium acetate buffered at pH 7 (Thomas, 1982) was used to determine exchangeable (K, Ca, Mg, Na) cations. Microelements in the soils were determined by Diethylene Triamine Pentaacetic Acid (DTPA) extraction methods (Lindsay and Norwell, 1978). The analysis results of soil are given in Table 1. Macro (P, K, Ca Mg and Na) and micro-elements (Fe, Mn, Zn , Al, B and Cu) content of plants were determined after wet digestion of dried and ground sub-samples using a HNO3-H2O2 acid mixture (2:3 v/v) with three steps (first step; 145°C, 75% RF, 5 min; second step; 180°C, 90% RF, 10 min and third step; 100°C, 40% RF, 10 min) in a microwave oven (Bergof Speedwave Microwave Digestion Equipment MWS-2) (Mertens, 2005a). Tissue P, K, Ca, Mg, Na, Fe, Mn, Zn, Al, B and Cu were determined using an Inductively Couple Plasma spectrometer (Perkin-Elmer, Optima 2100 DV, ICP/OES, Shelton, CT 06484-4794, USA) (Mertens, 2005b). ICP/OES was also used to determine P, K, Ca, Mg, Na, Fe, Mn, Zn, Cu, B and Al after extraction. The experiment had a randomized complete design with 8 N2 fixing and P-solubilizing PGPR strain [(Lysobacter enzymogenes 9/8), (Bacillus atrophaeus 55/1), (Arthrobacter agilis 2/3), (Paenibacillus macquariensis 59/8), (Bacillus lentus (Pb. validus) 29/6, (Burkholderia pyrrocinia 13/4), (Pantoea agglomerans 5/8), (Rhizobium radiobacter 42/1), (Stenotrophomonas maltophilia 21/1), (Acinetobacter calcoaceticus 47/6)], N fertilizer applications (600 kg ha-1 Ammonium sulphate, 21% N) and NP fertilizer application 600 kg ha-1 (Amonium sulphate, 21% N + 300 kg ha-1 Triple Super Phosphate, 42% P2O5) and the control treatment (without mineral and PGPR application) with 3 replicates per treatment and 6 plants per replicates.

Table 1: Some chemical and physical properties of studied soil (n = 10)
Image for - The Effects of Plant Growth Promotion Rhizobacteria on Vegetative Growth and Leaf Nutrient Contents of Hazelnut Seedlings (Turkish hazelnut cv, Tombul and Sivri)
Values are Mean±SD

Hazelnut seedlings plants were planted into the pots sterilized with 20% sodium hypochlorite solution, filled with 5 kg soil. Bacterial applications were performed using a dipping method in which plant roots were inoculated with the bacterial suspensions at a concentration of 109 CFU mL-1 in sterile water about 30 min prior to planting. The control plants were dipped into sterile water.

Bacterial strains, isolation and identification of bacteria: The bacterial strains L. enzymogenes 9/8, B. atrophaeus 55/1, A. agilis 2/3, P. macquariensis 59/8, B. lentus (Pb. validus) 29/6, B. pyrrocinia 13/4, P. agglomerans 5/8, R. radiobacter 42/1, S.s maltophilia 21/1, Acinetobacter calcoaceticus 47/6 were initially isolated from the rhizosphere of tea plants in the eastern black sea region (Rize and Trabzon province) of Turkey. The soils of the sampled sites had pH values ranging from 3.4 to 5.8. The bacteria were identified based on their whole-cell fatty acid methyl ester (FAMEs) analysis using the Microbial Identification System (MIDI).

Bacteria were grown on Nutrient Agar (NA) for routine use, and maintained in Nutrient Broth (NB) with 15% glycerol at -80°C for long-term storage. For each experiment, a single colony was transferred to 500 mL flasks containing NB and grown aerobically in flasks on a rotating shaker (150 rpm) for 48 h at 27°C (Merck KGaA, Germany). The bacterial suspension was then diluted in sterile distilled water to a final concentration of 109 CFU•mL-1 and the resulting suspensions were used to treat one year old hazelnut seedlings.

Acetylene reduction assay (ARA): Nitrogen fixation of the isolates was determined in a nitrogen-free medium by the acetylene reduction assay. Cultures for the acetylene reduction assay were prepared and incubated at 30°C for 24 and 48 h without agitation (Cakmakci et al., 2001).

Quantification of Indolylacetic acid (IAA) production and phosphate-solubilizing capacity: The bacteria were also tested for auxin production (IAA-like substances) using the method of Bent et al. (2001) and phosphate solubilization capacity (Cakmakci et al., 2001). The flasks were incubated for 18 h at 27°C with 100 rpm rotary shaking. Following this, 125 mL flasks containing 40 mL half-strength tryptic soy broth (TSB), supplemented with 0, 0.1 and 25 mg tryptophan mL–1 were each inoculated with 1mL of each strain. After incubation for 48, 72 and 168 h, the density of each culture was measured with a spectrophotometer (Shimadzu UV-1208) at 600 nm and then the bacterial cells were removed from the culture medium by centrifugation. The level of indoles present in the culture fluid was estimated calorimetrically. The concentration of IAA in the bacterial elutes was measured by using Salkowski’s reagent (50 mL 35% HClO4 +1 mL FeCL3). Each reaction mixture was centrifuged. The absorbance at 530 nm was measured with a spectrophotometer. Bacterial cells were separated from the supernatant by centrifugation at 10,000 rpm for 30 min. The concentration of IAA in each culture medium was determined by comparison with a standard curve. The IAA produced by each strain was measured in triplicate. In addition, after 48, 72 and 168 h of growth, samples were taken to determine IAA content with thin-layer chromatography (TLC) and high performance liquid chromatography-mass spectrometry (HPLC-MS) analysis. Separation of indole acetic acid in ethyl-acetate fraction was carried out in chloroform-ethyl acetate-formic acid.

All isolates were tested for their phosphate-solubilizing capacities in a sucrose-tricalciumphosphate agar media by inoculating 1 mL of a 6 day-old culture (density 4x109) in 250 mL Erlenmeyer flasks in triplicates containing 500 μg P mL-1 as Rock Phosphate (RP) at 30±1°C. After incubation for 6 days, water-soluble P was determined colorimetrically by the vanadomolybdophosphoric yellow color method (Pikovskaya, 1948).

Statistical analysis: All data were analyzed using Costat software (CoHortSoftware, Montery, USA). Plant nutrient content, some vegetative growth parameters and PGPR treatments were tested using a randomized complete design with tree replications. Mean comparisons were conducted using an ANOVA protected Least Significant Difference (LSD) (p<0.05) test.

RESULTS

Effects of bacterial application on growth parameters of Turkish hazelnut cultivars seedling.

The results of this study showed that some seedling growth parameters of hazelnut plants were significantly affected by bacterial applications (Table 2). Seedling length per plant was 93.7 cm in the control treatment. However, some of bacterial applications significantly increased seedling length per plant compared with the control. The average increase of seedling length was 4.2, 12.9, 14.6, 11.0, 13.7 and 4.2% for tombul cv and 13.7, 1.0, 17.4, 1.0, 2.0 and 21.7%, respectively for sivri cv when L. enzymogenes, B. atrophaeus A. agilis, P. macquariensis, B. lentus (Pb. validus), B. pyrrocinia, P. agglomerans and A. calcoaceticus were applied.

Table 2: Effects of PGPR applications on some vegetative growth parameters of Turkish hazelnut cultivars (Tombul and Sivri) (two years average n = 12)
Image for - The Effects of Plant Growth Promotion Rhizobacteria on Vegetative Growth and Leaf Nutrient Contents of Hazelnut Seedlings (Turkish hazelnut cv, Tombul and Sivri)
*Values in the same column with different letters are significantly different at p<0.05. ** Values in the same column with different letters are significantly different at p<0.01. NS: Not significant, N: Nitrogen fertilizer; NP: Nitrogen±Phosphorus fertilizer

Table 3: Effects o f PGPR applications on plant nutrient element content of leaves in one year old Turkish hazelnut seedling (Tombul and Sivri) (Two years average n = 12)
Image for - The Effects of Plant Growth Promotion Rhizobacteria on Vegetative Growth and Leaf Nutrient Contents of Hazelnut Seedlings (Turkish hazelnut cv, Tombul and Sivri)
*Values in the same column with different letters are significantly different at p<0.05. ** Values in the same column with different letters are significantly different at p<0.01. N: Nitrogen fertilizer; NP: Nitrogen + Phosphorus fertilizer

Similar to seedling length, total branch length, branch number and trunk diameter were also significantly increased by bacterial treatments compared with the control. But some bacterial strains such as R.radiobacter 42/1, S. maltophilia 21/1 and A.calcoaceticus 47/6 decreased seedling length and total branch length compared to the control in Tombul cv and A. agilis 2/3, P. macquariensis 59/8, S. maltophilia 21/1 and A. calcoaceticus 47/6 decreased seedling length and total branch number compared to the control in Sivri cv. The result of the present study suggests that maximal seedling length and trunk diameter were obtained in P. macquariensis 59/8 and maximum brunch number in S. maltophilia 21/1 in Tombul cv. The highest seedling length, total branch length, branch number and trunk diameter of Tombul and Sivri of Turkish hazelnut cultivars was obtained with A. calcoaceticus 47/6, R. radiobacter 42/1, S. maltophilia 21/1, P. macquariensis 59/8, respectively and increasing ratio of seedling length, total branch length, branch number and trunk diameter of Turkish hazelnut cultivars was 24.49, 31.60, 69.28 and18.74% for Tombul and 21.72, 68.43, 46.90 and 24.41% for Sivri, respectively, compared to control (Table 2).

Effects of bacterial application on plant nutrient element (PNE) contents of leaves: The Plant Nutrient Element (PNE) contents of leaves treated by PGPR strains may provide important information about the effect of bacterial inoculation in PNE uptake. PGPR strains could improve production of plant growth regulators or increase plant nutrient uptake. In this study; we have found that bacterial treatments significantly increased plant nutrient element contents of hazelnut leaves compared with the control (Table 3). Root inoculation with A. agilis 2/3, A. calcoaceticus 47/6, R. radiobacter 42/1 and L. enzymogenes 9/8 strains promoted N, P and K uptake of hazelnut seedlings (Tombul varieties). The highest Fe, Na and Al contents were obtained from R. radiobacter 42/1 and Lysobacter enzymogenes 9/8 applications compared to control. Root inoculation of S. maltophilia 21/1, R. radiobacter 42/1 and P. macquariensis 59/8 applications promoted N, P and K uptake of hazelnut seedling (Sivri cv.). The highest Mg, Mn, Fe content of leaves were obtained from the P. agglomerans 5/8 application compared the control. Inoculation with PGPR strains promoted significantly seedling growth, but the growth responses were strain and variety-specific. For example, A. calcoaceticus 47/6 application significantly increased seedling length in Sivri varieties. In contrast, A. calcoaceticus 47/6 was not significant statistically for the same parameter. The positive effects of A. agilis 2/3, P. agglomerans 5/8, P. macquariensis 59/8, B. pyrrocinia 13/4, S. maltophilia 21/1 and A. calcoaceticus 47/6 on the N contents of the leaves may be related to N fixing capacity of these bacterial strains.

DISCUSSION

Two years of trials under greenhouse conditions showed that inoculations with L. enzymogenes 9/8, B. atrophaeus 55/1, A. agilis 2/3, P. macquariensis 59/8, B. lentus (Pb. validus) 29/6, B. pyrrocinia 13/4, P. agglomerans 5/8, R. radiobacter 42/1, S.s maltophilia 21/1, Acinetobacter calcoaceticus 47/6 significantly enhanced seedling length, total branch length, branch number and trunk diameter and PNE uptake of Turkish hazelnut cultivars seedling. The nutritional status of the medium was important for the plant growth period. This result may be explained by bacterial applications which may have influenced plant cytokinins and IAA hormone contents. These findings supported by PGPR strains tested on chickpea, sugar beet, barley, corn, raspberry and tomatoes in different soil conditions. In fact the positive effects of PGPR on the yield and growth of crops such as chickpea, apple strawberry, spinach, tomatoes, sugar beet, barley and wheat were explained by N2-fixation ability, phosphate solubilizing capacity, indole acetic acid (IAA) and antimicrobial substance production (Cakmakci et al., 2001, 2007a, b; Karlidag et al., 2007; Esitken et al., 2010).

Nutrient (N, P, K, Ca, Mg, Fe, Zn, Al, B, Cu and Mn) contents of leaves were significantly increased by bacterial treatments. Kumawat et al. (2000) and Hoque et al., (1999) studies show that plant N content were higher in bacterial inoculation than that of N and NP applications.

In addition, exogenous IAA is proven to contribute to colonization efficiency and to the growth and survival of PGPR on host plants (Vandeputte et al., 2005). The presence of high numbers of bacteria in the rhizosphere is important in order to convert insoluble forms of organic and inorganic substances into available plant nutrients, which can affect vegetative growth. Therefore, one of the possible mechanisms by which PGPR enhances hazelnut seedlings' growth is the production of plant growth regulators and available nutrients. This assertion is in agreement with the findings reported by Bent et al. (2001), Watanabe et al. (2004), Zhang et al. (2003), Orhan et al. (2006) and Erturk et al. (2010). In addition, bacterial inoculations increased Ca, K, Fe, Cu, Mn and Zn in leaves. This increase may also be explained by organic acids production by plants and bacteria in the rhizosphere, which decrease soil pH and stimulate the availability of Ca, Fe, K, Cu, Mn and Zn. These findings a supported by previous studies (Smith and Read, 1997; Sundara et al., 2002; Shen et al., 2004; Karlidag et al., 2007; Cakmakci et al., 2009).

CONCLUSION

The results of this study clearly indicated that the PGPR root inoculations could reduce the deleterious effects of low nutrient content on hazelnut seedling growth. PGPR root inoculation was shown to increase seedling length, branch length and number of improved hormonal metabolism. Among the various PGPR isolates tested, 59/8, 21/1, 47/6, 42/1 strains was the most effective in promoting growth and growth parameter of hazelnut, but 13/4 and 42/1 were most effective in promoting macro and micro nutrient uptake of Turkish hazelnut cultivars (Tombul and Sivri), therefore reducing the need for chemical fertilizers for hazelnut seedlings. Further studies are needed to determine the effect of PGPR tested at these levels and the efficiency of PGPR under natural field condition and other plant species.

ACKNOWLEDGMENTS

This study was supported financially by a grant (TOVAG; 107 O 360) from the Scientific and Technological Research Council of Turkey (TUBITAK).

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