Improvement of growth and yield of maize under water stress by co-inoculating an arbuscular mycorrhizal fungus and a plant growth promoting rhizobacterium together with phosphate fertilizers
Introduction
Drought is one of the main problems worldwide, which limits the production of crops especially in arid and semi-arid areas (Cimmyt, 2011). Maize (Zea mays L.) as a direct staple food for millions of people is considered as a necessary component of global food security (Boomsma and Vyn, 2008). This plant has high irrigation requirements and its morphophysiology at the cellular level and whole-plant level is affected by drought stress (Boomsma and Vyn, 2008). In addition, maize is one of the most important crops in semiarid areas of the world (Cavero et al., 2000). Due to the dominance of calcareous soils and high pH along with dry climate and recent drought conditions, amount of available phosphorus (P) is low in most arid and semi-arid (agricultural) regions of the world. In order to increase the P availability for plants, large amounts of chemical P-fertilizers on a regular basis are required. However, large amounts of P in fertilizers may immediately be converted to insoluble phosphate by reaction with calcium in the soil, which is unavailable to plants (Zaidi et al., 2009). In addition, the immoderate utilization of chemical P-fertilizers has resulted in several environmental problems including surface runoff of P, eutrophication of aquatic ecosystems, reduction in biodiversity, and abnormal changes in the salt concentration and pH of soils (Adesemoye and Kloepper, 2009).
Due to the increase in the price of phosphate fertilizers and their low recovery (10–30%), the use of indigenous reactive ground rock phosphate (RP) as inexpensive alternative source, proposed for sustainability purposes, is increasing in developing countries. Although the indigenous phosphate source is less expensive, the main problem of which (the sparingly soluble form of P) is its low effectiveness, particularly in calcareous soils (Khasawneh and Doll, 1979). Some of these problems can be decreased by using bio-fertilizers (e.g., enhanced fertilizer-use efficiency, improvement of mineral nutrition, and reduced application rates of chemical fertilizers) (Adesemoye and Kloepper, 2009; Etesami and Alikhani, 2016), which are ecologically friendly, natural, and beneficial (Singh, 2013).
Arbuscular mycorrhizal fungi (AMF) and plant growth promoting rhizobacteria (PGPRs) are considered as two potentially important components of bio-fertilizers (Adesemoye and Kloepper, 2009). AMF establish beneficial symbiosis with the root system of nearly 80% of terrestrial plants. These fungi are almost ubiquitous in all of the agricultural soils. It has been found that AMF can increase P nutrition of plants by their high affinity P uptake mechanisms and by scavenging the available P through the large surface area of their hypha (Gyaneshwar et al., 2002). AMF have the ability to change water relation of their host plants and influence metabolism, protective adaptation, and morphology of host plants in water deficit stress conditions or drought stress (Al-Karaki, 2006; Kirono et al., 2011; Mickan et al., 2016). In addition, these fungi can enhance drought tolerance of host plants through mechanisms such as improvement of soil properties in rhizosphere, enlargement of root areas, enhancement of water use efficiency and uptake of P and other nutrient elements, quickly activation of defense system and protection against oxidative damages created by drought (Augé, 2001). Some researchers reported improved water relations of host plants colonized with AMF and with PGPRs (Kaushal and Wani, 2016) under moisture stress conditions (Augé et al., 2015). Because of their ability to consistently enhance mycorrhizal development, some of the P. fluorescens isolates are known to function as mycorrhization helper bacteria (MHB) (Garbaye, 1994). Due to their multifarious bio-fertilizing activities of increasing soil nutrient status, excretion of plant growth regulators and control of soil-borne pathogens, Pseudomonas species have been known as the most important bio-inoculants and the most efficient phosphate solubilizing bacteria (PSB) throughout the world (Vyas and Gulati, 2009). All of the characteristics noted above along with their diversity and tolerance in some environmental stresses such as drought stress (Marulanda et al., 2009) have shown them as a beneficial bio-fertilizer. Use of PSB as bio-inoculants in agriculture may increase the available P in soil, decreases the P-fertilizer application, minimizes environmental pollution, and finally promotes sustainable agriculture (Chen et al., 2006).
The combined use of PGPRs and AMF has been shown a cumulative and synergistic effect. These beneficial microorganisms have performed in a better way in terms of sustainable plant growth on nutrient-deficient sites (Lee et al., 2015; Mohamed et al., 2014; Xun et al., 2015; Zarei et al., 2006). Most combined applications of PGPRs and AMF are used to improve the nutrient efficiency of fertilizers, enhance phytoremediation (Xun et al., 2015), increase the yields of crops (Mäder et al., 2011), enhance fruit quality (Bona et al., 2016; Ordookhani et al., 2010) and allow reduced application of chemical fertilizers (Adesemoye et al., 2009); however the combination has not been much studied under field conditions (Berta et al., 2014; Bona et al., 2016), where inoculant fungi and bacteria must compete with the indigenous fungal and bacterial population. In addition, there is also little knowledge on the effects of the combined use of AMF and PSB on maize productivity under water stress in field conditions.
Investigating the beneficial effects of microorganisms on water stress affected-plants under field conditions gives us the opportunity to study the real detrimental effects of water stress and the real beneficial effects of inoculated microorganisms for any length of time (Marulanda et al., 2009). Although several bacterial and fungal formulations are currently available as commercial products for agricultural production, their efficiency in open field conditions depends greatly on the viability and survival of the inoculated fungi and bacteria, compatibility of these microorganisms with their host and with each other, and activity of which along the root systems (Bever et al., 2009; Gamalero et al., 2005; Rodriguez and Sanders, 2015).
Keeping in view the above details, the aim of this research was to evaluate the effect of application of AM fungus F. mosseae (formerly known as Glomus mosseae) and plant growth promoting (PGP) bacterium P. fluorescens along with using balanced application of mineral P-fertilizers on the vegetative and reproductive characteristics of maize, nutrient (P and N) contents in the plant tissue, the percentage of root colonization, and finally yield of this plant to achieve the sustainable management of agro-ecological systems through integrated plant nutrition under water deficit stress in field conditions.
Section snippets
Experimental site and climatic conditions
The study was carried out at the research farm of University College of Agriculture and Natural Resources, University of Tehran, Karaj, Iran (latitude: 35°48′N, longitude: 51°10′E, elevation of 1312 m). The growing season was from May to August. No rainfall was received throughout the season. The mean annual rainfall in the area was below 250 mm, and more than 70% falls in February and March. Fresh water is used for irrigation in this area. The mean annual air temperature and the average
Interaction effects of P-fertilizers and microbial inoculants on the measured traits
Analysis of variances indicated that the effect of P-fertilizers and microbial inoculants, and the interaction between the two factors were significant (Table 1). As shown in Table 1, microbial inoculants and P-fertilizers caused a significant increase in leaf dry weight, leaf area, tassel length, and P content compared to control treatments (Fig. 2A–D). The bio-inoculants were effective both at TSP fertilization level and at RP fertilization level. Co-inoculation of P. fluorescens and F.
Conclusions
In conclusion, this study revealed that RP and TSP along with microbial inoculants (single inoculation and co-inoculation) can be used as crude P-fertilizers (sparingly soluble natural phosphates) by direct application to field soil. Double application of P. fluorescens and F. mosseae improved the P and N contents and growth and yield of maize plants fertilized with RP and TSP under water stress conditions and in the presence of native bacteria and AMF, which make the co‐inoculation technique
Acknowledgment
We are grateful to University of Tehran for providing the necessary facilities and funding for doing this study.
References (111)
Nursery inoculation of tomato with arbuscular mycorrhizal fungi and subsequent performance under irrigation with saline water
Sci. Hort.
(2006)- et al.
Biofertilizers improve plant growth fruit yield, nutrition, metabolism and rhizosphere enzyme activities of pomegranate (Punica granatum L.) in Indian Thar Desert
Sci. Hort.
(2008) - et al.
The status of soil phosphate fractions and the ability of fungi to dissolve hardly soluble phosphates
Appl. Soil Ecol.
(2005) - et al.
Interaction between Glomus mosseae and soil yeasts on growth and nutrition of cowpea
Microbiol. Res.
(2008) - et al.
Mycorrhizal colonization improves onion (Allium cepa L.) yield and water use efficiency under water deficit condition
Sci. Hort.
(2007) - et al.
Maize drought tolerance: potential improvements through arbuscular mycorrhizal symbiosis?
Field Crops Res.
(2008) - et al.
Survival of inocula and native AM fungi species associated with shrubs in a degraded Mediterranean ecosystem
Soil Biol. Biochem.
(2005) - et al.
Phosphate solubilizing bacteria from subtropical soil and their tricalcium phosphate solubilizing abilities
Appl. Soil Ecol.
(2006) - et al.
Arbuscular mycorrhizal hyphae in grassland select for a diverse and abundant hyphospheric bacterial community involved in sulfonate desulfurization
Appl. Soil Ecol.
(2015) - et al.
Responses of legumes to rhizobia and arbuscular mycorrhizal fungi: a meta-analysis of potential photosynthate limitation of symbioses
Soil Biol. Biochem.
(2010)
Screening of Brazilian cacti rhizobacteria for plant growth promotion under drought
Microbiol. Res.
The use of phosphate rock for direct application to soils
Adv. Agron.
Characteristics of Australian droughts under enhanced greenhouse conditions: results from 14 global climate models
J. Arid Environ.
Inoculation of root microorganisms for sustainable wheat–rice and wheat–black gram rotations in India
Soil Biol. Biochem.
Effect of dual inoculation with arbuscular mycorrhizal fungi and sulphur-oxidising bacteria on onion (Allium cepa L.) and maize (Zea mays L.) grown in sandy soil under green house conditions
Ann. Agric. Sci.
A modified single solution method for the determination of phosphate in natural waters
Anal. Chim. Acta
Hydraulic lift may buffer rhizosphere hyphae against the negative effects of severe soil drying in a California Oak savanna
Soil Biol. Biochem.
Responses of field grown tomato plants to arbuscular mycorrhizal fungal colonization under varying intensities of drought stress
Sci. Hort.
Isolation and screening of bacteria from rhizospheric soils of rice fields in Northwestern Morocco for different plant growth promotion (PGP) activities: an in vitro study
Int. J. Curr. Microbiol. Appl. Sci.
Plant–microbes interactions in enhanced fertilizer-use efficiency
Appl. Microbiol. Biotechnol.
Plant growth-promoting rhizobacteria allow reduced application rates of chemical fertilizers
Microb. Ecol.
Field response of wheat to arbuscular mycorrhizal fungi and drought stress
Mycorrhiza
Growth of mycorrhizal tomato and mineral acquisition under salt stress
Mycorrhiza
Short term effects of Glomus claroideum and Azospirillum brasilense on growth and root acid phosphatase activity of Carica papaya L. under phosphorus stress
Revista Latinoamericana de Microbiología
Effect of two species of arbuscular mycorrhizal fungi on growth, assimilation and leaf water relations in maize (Zea mays)
Aspects Appl. Biol.
Bioprospecção de isolados de Bacillus promotores de crescimento de milho cultivado em solo autoclavado e natural
Ciênc. agrotec (Impr.)
Interactions between arbuscular mycorrhizal fungi and bacteria and their potential for stimulating plant growth
Environ. Microbiol.
The decrease in growth of phosphorus-deficient maize leaves is related to a lower cell production
Plant Cell Environ.
Arbuscular mycorrhizal symbiosis alters stomatal conductance of host plants more under drought than under amply watered conditions: a meta-analysis
Mycorrhiza
Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis
Mycorrhiza
Rock phosphate and vesicular-arbuscular mycorrhiza effects on growth and nutrient uptake of Faidherbia albida (Del.) seedlings in an alkaline sandy soil
Agrofor. Syst.
Breeding for drought and nitrogen stress tolerance in maize: from theory to practice
Cimmyt
Interactions between mycorrhizal fungi and rhizosphere micro2organismswithin the context of sustainable soil2plant systems
The application of isotopic (32P and 15N) dilution techniques to evaluate the interactive effect of phosphate-solubilizing rhizobacteria, mycorrhizal fungi and Rhizobium to improve the agronomic efficiency of rock phosphate for legume crops
Nutr. Cycl. Agroecosyst.
Facilitation of phosphorus uptake in maize plants by mycorrhizosphere bacteria
Sci. Rep.
Symbiotic relationships between soil fungi and plants reduce N 2 O emissions from soil
ISME J.: Multidiscip. J. Microbial. Ecol.
Maize development and grain quality are differentially affected by mycorrhizal fungi and a growth-promoting pseudomonad in the field
Mycorrhiza
Preferential allocation to beneficial symbiont with spatial structure maintains mycorrhizal mutualism
Ecol. Lett.
Interactions among Glomus irregulare, arbuscular mycorrhizal spore-associated bacteria, and plant pathogens under in vitro conditions
Mycorrhiza
Arbuscular mycorrhizal fungi: a specialised niche for rhizospheric and endocellular bacteria
Antonie van Leeuwenhoek
A critical review on the role of mycorrhizal fungi in the uptake of phosphorus by plants
Plant Soil
Arbuscular mycorrhizal fungi and plant growth-promoting pseudomonads improve yield, quality and nutritional value of tomato: a field study
Mycorrhiza
Phosphate solubilizing bacteria efficiency on mycorrhization and growth of peanut in the northwest of Morocco
Am. J. Microbiol. Res.
Nitrogen total
Simulation of maize yield under water stress with the EPICphase and CROPWAT models
Maize: Global Alliance for Improving Food Security and the Livelihoods of the Resource-Poor in the Developing World| CGIAR Fund [WWW Document]
Mineral acquisition by arbuscular mycorrhizal plants
J. Plant Nutr.
Enhancement of nitrogen fixation in lentil, faba bean, and soybean by dual inoculation with Rhizobia and mycorrhizae
Plant Soil
Effect of inoculation with phosphate solubilizing bacteria on the tomato rhizosphere colonization process, plant growth and yield under organic and inorganic fertilization
J. Appl. Sci. Res.
Co-inoculation with endophytic and rhizosphere bacteria allows reduced application rates of N-fertilizer for rice plant
Rhizosphere
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