WALID FEDIALA ABD EL-GLEEL MOSA1, 2*, LIDIA SAS PASZT1, MATEUSZ FRĄC1 and PAWEŁ TRZCIŃSKI1
1Research Institute of Horticulture, Skierniewice, Poland
2Plant Production Department, Faculty of Agriculture, Saba Basha, Alexandria University, Alexandria, Egypt
*Corresponding author: W.F.A.E.-G. Mosa, Research Institute of Horticulture, Skierniewice, Poland and Plant Production Department, Faculty of Agriculture, Saba Basha, Alexandria University, Alexandria, Egypt; e-mail: walidbreeder@yahoo.com.
Submitted 7 August 2014, revised 19 April 2016, accepted 22 April 2016
DOI: 10.5604/17331331.1215599
Abstract
The excessive use of mineral fertilizers causes many negative consequences for the environment as well as potentially dangerous effects of chemical residues in plant tissues on the health of human and animal consumers. Bio-fertilizers are formulations of beneficial microorganisms, which upon application can increase the availability of nutrients by their biological activity and help to improve soil health. Microbes involved in the formulation of bio-fertilizers not only mobilize N and P but mediate the process of producing crops and foods naturally. This method avoids the use of synthetic chemical fertilizers and genetically modified organisms to influence the growth of crops. In addition to their role in enhancing the growth of the plants, biofertilizers can act as biocontrol agents in the rhizosphere at the same time. Biofertilizers are very safe for human, animal and environment. The use of Azotobacter, Azospirillum, Pseudomonas, Acetobacter, Burkholderia, Bacillus, Paenibacillus and some members of the Enterobacteriaceae is gaining worldwide importance and acceptance and appears to be the trend for the future.
Key words: apple productivity, biocontrol, biofertilization, bioproducts
Introduction
Apple (Malus domestica Borkh.) is the 3rd most important fruit crop worldwide, after citrus and banana (FAOSTAT, 2013). In 2013, the total apple production and harvest in the world was estimated at 80.8 million tons and 5.2 million hectares, respectively. Its cropping has expanded into subtropical and tropical zones (Karakurt and Aslantas, 2010) and is one of the most important cropped and consumed fruits in the world (Brown, 2012). Intensive farming practices, that warrant high yield and quality, require the extensive use of chemical fertilizers and pesticides, which are costly and create environmental problems. Hence, there has been a resurgence of interest in environmental friendly, sustainable and eco-friendly agricultural practices (Esitken et al., 2002). One potential way to decrease negative environmental impacts resulting from continued use of chemical fertilizers is inoculation with plant growth promoting rhizobacteria (PGPR). These bacteria improve nutrient (N, P, K, Fe, and Zn) bioavailability (Table I) and exert beneficial effects on plant growth and development, and therefore may be used as biofertilizers for agriculture. The natural role of the PGPR in maintaining soil fertility is more important than in conventional agriculture where higher use of agrochemicals minimizes their significance (Canbolat et al., 2006). Moreover, the applications of biofertilizers containing beneficial microorganisms instead of synthetic chemicals are known to improve fixation of nutrients in the rhizosphere, produce growth stimulants for plants, improve soil stability, provide biological control, biodegrade substances, recycle nutrients, promote mycorrhiza symbiosis, and develop bioremediation processes in soils contaminated with toxic, xenobiotic and recalcitrant substances (Rivera-Cruz et al., 2008). So the use of more sustainable technologies, such as biofertilization, is inevitable for the mitigation of environmental damage (Karakurt and Aslantas, 2010).
Table I
Plant Growth Promoting Rhizobacterial (PGPR) strains improving nutrient (N, P, K, Fe and Zn) bioavailability
| Bacteria | References |
| N – Nitrogen, P – Phosphorus, K – Potassium, Fe – Iron | |
| Rhizobium leguminosarum | Biswas et al., 2000 |
| Bradyrhizobium japonicum UCM B-6018 | Tytova et al., 2013 |
| N – Nitrogen, P – Phosphorus, Fe – Iron | |
| Pseudomonas aeruginosa BS8 | Goswami et al., 2015 |
| N – Nitrogen, P – Phosphorus | |
| Bacillus megaterium, Bacillus mucilaginosus | Han and Lee, 2005 |
| N – Nitrogen, Fe – Iron | |
| Pseudomonas strain GRP3 | Sharma et al., 2003 |
| Pseudomonas fluorescens C7 | Vansuyt et al., 2007 |
| N – Nitrogen | |
| Azospirillum spp. | Bashan and De-Bashan, 2010 |
| Pseudomonas alcaligens PsA15, Mycobacterium phlei MbP18 | Egamberdiyeva and Höflich, 2004 |
| Azospirillum lipoferum, Azospirillum brasilense | Malik et al., 2002 |
| Klebsiella pneumonia, Pantoea agglomerans | Riggs et al., 2001 |
| Azotobacter spp. | Mrkovacki and Milic, 2001 |
| Azotobacter chroococcum | Wu et al., 2005 |
| P – Phosphorus | |
| Streptomyces spp. | Chang and Yang, 2009 |
| Microccocus spp. | Dastager et al., 2010 |
| Achromobacter spp. | Ma et al., 2009 |
| Bacillus spp., Burkholderia spp. | Tao et al., 2008 |
| Bacillus megaterium | Wu et al., 2005 |
| Pseudomonas alcaligenes | Zhang et al., 2014 |
| Pseudomonas aeruginosa | Yadav et al., 2014 |
| K – Potassium | |
| Bacillus edaphicus | Sheng and He, 2006 |
| Zn – Zinc | |
| Serratia spp. | Abaid-Ullah et al., 2011 |
| Pseudomonas fluorescens | Di Simine et al., 1998 |
| Pseudomonas aeruginosa | Fasim et al., 2002 |
| Flavobacterium spp. | He et al., 2010 |
| Pseudomonas spp. PsM6, P. jessenii PjM15 | Rajkumar and Freitas, 2008 |
| Acetobacter diazotrophicus | Saravanan et al., 2007 |
| Rhizobia spp. | Wani et al., 2008 |
| Pseudomonas sp. Z5 | Yasmin, 2011 |
The influence of biofertilizers in improving apple growth and productivity
Applications of bio-fertilizers containing beneficial microorganisms instead of synthetic chemicals are known to improve plant growth through the supply of plant nutrients and may help to sustain environmental health and soil productivity (O’Connell, 1992). A biofertilizer is a substance which contains living microorganisms which, when applied to seeds, plant surfaces, or soil, colonizes the rhizosphere or the interior of the plant and promotes growth by increasing the supply or availability of primary nutrients to the host plant (Vessey, 2003). Biofertilization is now a very important method for providing the plants with their nutritional requirements without having an undesirable impact on the environment (Abou El-Yazied and Sellim, 2007). Additionally, the use of biofertilizers can improve productivity per unit area in a relatively short time, consume smaller amounts of energy, mitigate contamination of soil and water, increase soil fertility, and promote antagonism and biological control of phytopathogenic organisms (Corpoica et al., 2007). Moreover, biofertilizers are known to improve fixation of nutrients in the rhizosphere, produce growth stimulants for plants, improve soil stability and provide biological control. They also biodegrade substances, recycle nutrients, promote mycorrhiza symbiosis and develop bioremediation processes in soils contaminated with toxic, xenobiotic and recalcitrant substances (Rivera-Cruz et al., 2008). Raghuwanshi (2012) stated that biofertilizers have a great potential as supplementary, renewable and environmental friendly sources of plant nutrients. Furthermore, they are an important component of integrated nutrient management and plant nutrition system. Application of biological potassium fertilizers (BPF), as preparation of silicate bacteria (liquid solution, containing two million bacteria per 1 ml, or packages of 500 g of peat-moss substrate, contains 2 million bacteria) and Azobacterin increased trunk cross-sectional area, mean shoot length, mean leaf area, total leaf area, number of fruits per tree, mean fruit weight and yield of “Charavnitsa” apple variety (Ryabtseva et al., 2005). Von-Bennewitz and Hlusek (2006) reported that biofertilization is beneficial in stimulating the growth and fruiting of pome and stone fruits. Treatment of ‘Topaz’ and ‘Ariva’ apple trees with the biopreparations: Micosat F, Humus UP, Humus Active + Aktywit PM, BioFeed Amin, Vinassa, Florovit Eko and Florovit Pro Natura produced positive effects on the growth of apple roots and their mycorrhizal frequency, and the size of the populations of microorganisms in the rhizosphere soil (Derkowska et al., 2014). Besides, Rozpara et al. (2014) found also that Biofeed Amin preparation had a positive influence on the growth and development of ‘Ariwa’ apple trees growing. Tree trunk sectional area and yield of “Topaz” apple trees was improved with Florovit Natura and Yeast combined with Pantoea spp., Pseudomonas fluorescens, Klebsiella oxytoca and Rhizobium spp. bacteria species respectively as compared to NPK chemical fertilization (Mosa et al., 2016).
The effect of mycorrhiza on apple growth and yield
Abuscular mycorrhizal (AM) fungi are associated with the roots of over 90% of terrestrial plant species (Gadkar et al., 2001). They are a very important component within the rich biodiversity of microorganisms occurring in the rhizosphere (Turnau and Haselwandter, 2002). Xavier and Boyetchko (2002) have found that mycorrhizal fungi, in particular endomycorrhizal have a beneficial effect on plant growth and development, and that effect can be likened to the effects of biostimulators and biofertilizers on plants. Root inoculation with two biopreparations, Vambac® (VA-mycorrhiza genus Glomus, Gigaspora and the rhizospheric bacteria Agrobacterium radiobacter) and Amalgerol® (composed of vegetative and sea-algae oils and extracts) enhanced the uptake of phosphorus and vegetative growth of two-year-old apple trees cv. “Jonagold” grown on M.9 root stock (Von Bennewitz and Hlusek, 2006). Cavallazzi et al. (2007) stated that apple (Malus prunifolia) Colonization by Glomus etunicatum SCT110, Scutellospora pellucida SCT111, Acaulospora scrobiculata SCT112 and Scutellospora heterogama SCT113 fungal isolates significantly affected plant height, shoot and root dry weights, and root: shoot ratio. Moreover, mycorrhizal inoculation also significantly altered tissue concentrations of P, Zn, Cu, Ca, S, Na, N, K, Fe and Al.
Overall, G. etunicatum and S. pellucida were the most effective isolates to promote plant growth and nutrient uptake. Many investigations shows that AM symbiosis contributes to plant growth, nutrient uptake and improve fruit quality (Miransari, 2010). The positive and beneficial effects of AM fungi such as growth promotion, increased root length, leaf area and stem diameter (Sharma et al., 2011), transplant performance and tolerance to abiotic (water, nutrition) stresses (Göhre and Paszkowski, 2006), could be due to a positive interaction between AM fungi and other associated microorganisms such as Azotobacter chroococcum in a particular edaphic and agro-climatic conditions. Sharma et al. (2012) reported significant improvement in the vegetative growth parameters of ‘Royal Delicious’ apple saplings by using single and/or dual application of soil inoculation of Glomus fasciculatum, Glomus mosseae, and A. chroococcum strains namely, A. chroococcum strain-I (AZ1) and A. chroococcum strain-II (AZ2) at nursery stage under reduced inorganic fertilization. Grzyb et al. (2015) found that Florovit Eko + mycorrhizal fungi improved the tree trunk diameter of maiden trees of apple cv. “Topaz”. Inoculation of three Arbuscular Mycorrhizal Fungi (AMF) species; Glomus versiforme, Claroideoglomus etunicatum and Rhizophagus intraradices could increase apple rootstocks (M.9, M.7 and MM.106) shoot height, stem diameter, leaf area, shoot fresh and dry weight and root fresh and dry weight and the concentration of N, P, Ca, Mg, Zn, and Fe compared to those of non – mycorhizal control plants (Hosseini and Gharaghani, 2015). Mosa et al. (2016) noticed that the combination of mycorrhizal fungi (G. mosseae and Glomus intraradices) and plant growth promoting bacteria (Pantoea sp., P. fluorescens, K. oxytoca and Rhizobium sp) improved the tree trunk, number and weight of fruits per tree of “Topaz” apple cultivar.
The influence of mycorrhiza in alleviating biotic and abiotic stresses in apple orchard
Runjin (1989) mentioned that sterilized soil inoculated with G. versiforme and Glomus macrocarpum improved water status and drought tolerance of the plants. Furthermore, arbscular mycorrhiza colonization in sterilized soils reduced the stomatal resistance and the permanent wilting as well enhanced the rate of recovery of the plant from the water stress. This was probably due to enhancing absorption and translocation of water by the external hyphae. Kaldorf and Ludwig-Müller (2000) observed that mycorrhiza-covered roots were better developed; especially the number of lateral and fine roots was significantly greater. The presence of mycorrhiza in the roots intensifies uptake of water and minerals from the soil by the root system. Al-Karaki (2004) showed that mycorrhizal fungi colonized more readily the roots of plants growing in an area with high water deficiency, and that the use of mycorrhizal inocula in dry areas had a favourable effect on the size and quality of the crop. Hamel (2004) reported that the network of extraradical mycorrhizal hyphae facilitate nutrient acquisition and transport many ions to roots, particularly less mobile ions such as P, N, K, S, Ca and Zn. Arbuscular mycorrhizal fungi (Glomus deserticola) decreased soil EC and organic carbon and increased soil availability of N, P and K as well as leaf nutrient status of “Kinnow” mandarin (Usha et al., 2004). Inoculation of cherry rootstocks, ‘Edabriz’ and ‘Gisela 5’, plantelts with Glomus clarum, Glomus caledonium, G. etunicatum, G. intraradices, G. mosseae and mixture of these species increased Zn and P nutrient uptake than non-mycorrhizal plantlets (Aka-kaçar et al., 2010). It has been found that AM fungi can alleviate the unfavourable effects on plant growth of stresses such as heavy metals, soil compaction, salinity and drought (Miransari, 2010). Yang et al. (2014) studied the influence of G. versiforme on increasing one-year-old “Red Fuji” apple seedlings (Malus hupehensis Rehd. root stock) salt tolerance. They noticed that abuscular mycorrhizal fungi significantly increased the root length colonization of mycorrhizal apple plants under 2‰, and 4‰ salinity stress levels as compared to non-mycorrhizal plants. However, percent root colonization reduced as saline stress increased. Salinity levels were found to negatively correlate with leaf relative turgidity, osmotic potential irrespective of non-mycorrhizal and mycorrhizal apple plants, but the decreased mycorrhizal leaf turgidity maintained relative normal values under 2‰ and 4‰ salt concentrations. Under salt stress condition, Cl− and Na+ concentrations clearly increased and K+ contents obviously decreased in non-mycorrhizal roots in comparison to mycorrhizal plants, this caused mycorrhizal plants to have a relatively higher K+ /Na+ ratio in the root. Ascorbate peroxidase and catalase activities increased in mycorrhizal more than in non-mycorrhizal plants.
The role of some beneficial bacterial strains in improving nutrient uptake, soil fertility, apple growth and productivity
Use of biofertilizers containing beneficial microorganisms instead of synthetic chemical is known to improve plant growth through supply of plant nutrients and may help to sustain environmental health and soil productivity (O’Connell, 1992). In field trials, preplant inoculation with both G. intraradices and G. mosseae increased rootstock growth and leaf concentrations of P, Mg, Zn and Cu in fumigated plots but not in non-fumigated plots, indicating that colonization by native AM fungi in non-fumigated plots may have been sufficient for adequate nutrient acquisition (Forge et al., 2001). The plant promoting effect of the PGPB is mostly explained by the release of metabolites directly stimulating growth. The mechanisms by which PGPB promote plant growth are not fully understood, but are thought to include: (a) the ability to produce plant hormones, such as gibberellins (Gutierrez-Manero et al., 2001), cytokinins (De Salamone et al., 2001) and auxins (Egamberdiyeva, 2005) and inhibit ethylene production (Glick et al., 1995); (b) asymbiotic N2 fixation (Sahin et al., 2004); (c) solubilization of inorganic phosphate and mineralization of organic phosphate and/ or other nutrients (Jeon et al., 2003). Esitken et al. (2003) found that Bacillus strains; OSU-142 and M-3 stimulated macro and micro-nutrient uptake such as N, P, K, Ca, Mg, Fe, Mn, Zn and Cu in apricot (Prunus armeniaca L. cv. Hacihaliloglu). Tenuta (2003) found that Rhizobium, Bacillus and Pseudomonas improve the uptake of nutrients like nitrogen, phosphorus, potassium, sulphur and iron. Recent studies confirmed 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 have been called ‘Plant Growth Promoting Bacteria (PGPB)’ including the strains in the genera Acinetobacter, Alcaligenes, Arthrobacter, Azospirillium, Azotobacter, Bacillus, Beijerinckia, Burkholdria, Enterobacter, Erwinia, Flavobacterium, Rhizobium and Serratia (Bashan and de-Bashan, 2005). Orhan et al. (2006) reported that Bacillus M3 (N2-fixing and phosphate solubilizing) alone or in combination with Bacillus OSU-142 (N2-fixing) increased the total N, available P, K, Ca, Mg, Fe, Mn, Zn contents in the soil and Fe and Mn contents in the leaves of raspberry cv. “Heritage”. Aslantas et al. (2007) mentioned that floral and foliar applications of Pseudomonas BA-8 and Bacillus OSU-142 alone or in combination have the potential to increase yield, growth and nutrition of apple cultivars “Granny Smith and Stark Spur Golden”. Karlidag et al. (2007) noticed that Bacillus M3, Bacillus OSU-142 and Microbacterium FS01 combinations stimulated plant growth and resulted in significant yield increases in apple cv. “Granny smith” by promoting abilities for auxin and cytokinin production, N2-fixation, phosphate solubilization and antimicrobial substance production. Karakurt and Aslantas (2010) evaluate the effects of four strains of plant growth promoting rhizobacteria (Agrobacterium rubi A-18, Bacillus subtilis OSU-142, Burkholderia gladioli OSU-7 and Pseudomonas putida BA-8) on growth and leaf nutrient content of ‘Starking Delicious’, ‘Granny Smith’, ‘Starkrimson Delicious’, ‘Starkspur Golden Delicious’ and ‘Golden Delicious’ apple cultivars grafted on semi-dwarf rootstock MM-106. They found that bacteria applications showed the desirable effects on plant growth and plant nutrient element contents. Mosa et al. (2016) showed the improvement in the growth, yield and fruit quality of “Topaz” apple trees following the addition of Pantoea sp., P. fluorescens, K. oxytoca and Rhizobium sp. bacteria species to Fertigo, Micosat, Humus UP, BioFeed Quality, BioFeed Amin, Yeast, Vinassa and Florovit Eko as compared to chemical NPK fertilization.
Some beneficial roles of bacterial strains in apple trees pest management
Biological control is considered a promising strategy for the management of fire blight and several biological control agents are now commercially available, including P. fluorescens A506 (Wilson and Lindow, 1993), Pantoea agglomerans E325 (Pusey, 1999), B. subtilis QST713 (Aldwinckle et al., 2002), P. agglomerans P10c (Vanneste et al., 2002) and B. subtilis BD170 (Broggini-Schärer et al., 2005) and Pantoea vagans C9-1 (Smits et al., 2010). In vitro – bacterized plantlets not only grew faster than nonbacterized controls but also were sturdier, with a better-developed root system and significantly greater capacities for withstanding biotic (Barka et al., 2000) and abiotic (Bensalim et al., 1998) stresses. Ramamoorthy et al. (2001) showed that some plant growth-promoting rhizobacteria (PGPR) induce systemic resistance by strengthening the physical and mechanical strength of the cell wall, as well as altering the biochemical and physiological reaction of the host plant that leads to the synthesis of chemical defense against the pathogen. Plant growth-promoting rhizobacteria can disrupt phytopathogen organization (Barka et al., 2002), stimulate developmental changes in host plants, induce systemic resistance to pathogens, affect phytohormone production, and improve nutrient and water management (Compant et al., 2005). Pseudomonas strains MRS23 and CRP55b inhibited the growth of pathogenic fungi, i.e. Aspergillus sp., Fusarium oxysporum f. sp. ciceri and Rhizoctonia solani under culture condition (Goel et al., 2002). Commercial formulations combining bacteria antagonistic to plant pathogenic microbes with ice nucleation-active bacteria have been utilized as an environmentally safe method to manage biotic and abiotic stress in plants (Lindow and Leveau, 2002). In addition, some of these bacteria, such as epiphytic or endophytic plant growth-promoting rhizobacteria, enhance plant growth while improving their resistance to stress (Dobbelaere et al., 2003). Pseudomonas, Bacillus, Burkholderia, Agrobacterium and Streptomyces suppress plant disease by production of antibiotics, siderophores, or by induction of systemic resistance or any other mechanism (Tenuta, 2003). The plant promoting effect of the PGPB are thought to do antagonism against phytopathogenic microorganisms by production of siderophores, the synthesis of antibiotics, enzymes and/or fungicidal compounds and competition with detrimental microorganisms (Lucy et al., 2004). Lactic acid – (LAB) active against Erwinia amylovora could be a novel approach for fire blight control, because they have been reported in the field of food technology as biopreservatives (Vermeirem et al., 2004), including fermented vegetables or fruit juices (Gomez et al., 2002). The capacities of certain species of LAB isolated from fresh plant products to control food-borne human pathogenic bacteria and postharvest fungi have been studied (Trias et al., 2008a; 2008b; 2008c). Also, strains of LAB have been reported as antagonistic to the plant pathogenic bacteria Pectobacterium carotovorum, Xanthomonas campestris and Pseudomonas syringae (Trias et al., 2008c). This antagonistic and bioprotective capacity is mainly due to a wide diversity of mechanisms of action including not only antibiosis (Cleveland et al., 2001), but also pre-emptive colonization of wounds and cuts (Trias et al., 2008a). In addition, LAB are not perceived as environmental and health hazards, because they have been considered with the status of “generally recognized as safe” (GRAS) by the Food and Drug Administration (FDA, USA) and with the “qualified presumption of safety” (QPS) status by the European Food Safety Agency (EFSA). Ongena et al. (2005) showed the ability of B. subtilis strain M4, an important producer of a wide variety of fengycin-type lipopeptides, to protect wounded apple fruits against mold disease caused by Botrytis cinerea. The resistance of plants to root diseases as well as efficient nutrient assimilation is profoundly influenced by the presence and activity of beneficial microorganisms in the soil (Picardi et al., 2005). Orchard application of biological potassium fertilizers (BPF) increased the resistance of “Charavnitsa” apple trees to viral and bacterial diseases and to the sucking pests (Ryabtseva et al., 2005). Rhizobacteria are soil bacteria that colonize plant roots; they are able to multiply and occupy all the ecological niches found on the roots at all stages of plant growth (Antoun and Prévost, 2006). Such bacteria may negatively interact with plants, directly by competing for nutrients. Alternatively, the relationship between rhizobacteria and the host plant can be positive. For example, the bacteria may compete with pathogens for survival in the rhizosphere or they may promote mutualistic relationships with plants they were associated, allowing nutrient exchange and stimulating antibiotic production against phytopathogenic agents (Siddiki, 2006). Floral and foliar applications of Bacillus OSU-142 and BA-8 and OSU-142 decreased shot-hole disease in “Granny Smith” and “Star Spur Golden” young apple trees (Aslantas et al., 2007). Over 400 species of fungi and more than 90 species of bacteria which infect insects have been described including Bacillus thuringiensis, varieties of which are manufactured and sold throughout the world primarily for the control of caterpillar pests and more recently mosquitoes and black flies. So far, more than 40000 species of B. thuringiensis have been isolated and identified belonging to 39 serotypes. These organisms are active against either Lepidoptera, Diptera or Coleoptera pests (Moazami, 2007). Burkholderia species are able to synthesize a remarkable array of metabolites, including siderophores, antibiotics, and phytohormones (Vial et al., 2007), and many strains belonging to this genus exhibit activities involved in bioremediation or biological control in vitro (Caballero-Mellado et al., 2007). Beneduzi et al. (2012) mentioned that bacteria that colonize plant roots and promote plant growth are referred to as plant growth-promoting rhizobacteria (PGPR). Their effects can occur via local antagonism to soil-borne pathogens or by induction of systemic resistance against pathogens throughout the entire plant.
The effect of biocontrol agents in nematode control
Different fungal strains isolated from nematodes, soil and plants were shown to produce substances that inhibit nematode egg hatch or kill nematodes (Nitao et al., 1999). Khan et al. (2003) showed that the fungus Paecilomyces lilacinus penetrates nematode eggs and cuticles through the production of the lytic enzymes serine protease and chitinase. Pseudomonas aeruginosa (Siddiqui et al., 2000) and Pseudomonas spp. (Ali et al., 2002) have shown good results for the control of Meloidogyne spp. Besides, antagonistic bacteria have been repeatedly shown to be promising microorganisms for the biological control of plant-parasiticnematodes (Giannakou et al., 2004). Furthermore, many attempts have been made to use antagonistic bacteria and fungi to control root-knot nematodes (Khan et al., 2008). The damage caused by root-knot nematodes could be managed by application of microorganisms antagonistic to Meloidogyne spp., or compounds produced by these microbes (Ashraf and Khan, 2010). Mazzola et al. (2009) mentioned that the root-lesion nematode Pratylenchus penetrans is the most important nematode affecting apple production. This lesion may exhibit poor growth of “Gala” young apple trees grown on M26 stock apple, stunting and a gradual decline in yields. Severely infected root systems may lack feeder roots. Moreover, the author stated that this lesion can be controled by MeloCon WG (P. lilacinus strain 251) at 2 to 4 lb/A plus a soil wetting agent to established plants, although it might be better used when applied to plants just before planting.
Conclusions
- Biofertilizers are important components of integrated nutrients management and renewable source of plant nutrients to supplement chemical fertilizers in sustainable agricultural system.
- Biological fertilizers would play key role in productivity and sustainability of soil and also protect the environment as ecofriendly and cost effective inputs for the farmers.
- Beneficial microorganisms can be used as a tool in the apple orchard to improve greatly growth, yield and fruit quality.
- Biological pest mangement can be aim to reduce the usage of insecticides and maintain a clean environment and food safety, and then human health.
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