Effect of presowing treatment of spring wheat and barley seeds with bacterial strains on yield and grain quality.
It is well known that reducing the extent of damage to grain crops by root rot causing agents is one of the most effective ways to increase the yield of agricultural grain crops and improve their quality. These diseases are especially harmful for hard wheat, barley, soft spring wheat, and winter rye. Yield losses due to these diseases may reach 19–20% or more for wheat and 25–30% or more for barley. In order to assess the effectiveness of the bacteria isolated from earthworm coprolites as biological control agents, we conducted a series of field tests in Western Siberia from 2011 to 2015. We compared growth and development indicators of spring wheat (Triticum aestivum L., Irgina variety) and barley (Hordeum vulgare L., Acha variety) where seeds were treated with Bacillus cereus and two strains of Pseudomonas. The results showed that the inoculation increased the grain yield by 0.2–1.0 t ha−1 for spring wheat and by 0.3–1.8 t ha−1 for barley. In addition, the prevalence of the disease in spring wheat plants was significantly reduced from 18.1–61.1% in the control plots to 6.4–50.2% in the inoculated plots. Similarly, the index of root rot development decreased from 18.2–23.0% in the control plots to 13.2–15.8% in the inoculated plots. To understand the mechanism that induces the spring wheat resistance to fungal root rots under the influence of rhizobacteria, we investigated the effect on the guaiacol-dependent peroxidase activity. There was an inverse relationship between the peroxidase activity in wheat tissues and damage of plants caused by root rot agents indicating that the response of peroxidase enzymes to plant inoculation is a meaningful indicator that can be used to assess the potential of a particular strain as a biological agent for protecting spring wheat.
- bacteria inoculation
- Bipolaris sorokiniana
- Hordeum vulgare
- root rot
- Triticum aestivum
It is well known that in soil and climatic conditions of the West Siberian region, reducing the extent of damage to grain crops by root rot causing agents is one of the most effective ways to increase the yield of agricultural grain crops and improve their quality. Unstable weather factors, high probability of spring frosts, high humidity, and heavy soil texture create the most favorable conditions for the rapid development of root rots caused by soil phytopathogenic fungi. A review of literature data  and results of annual phytosanitary inspections of grain plantings by responsible federal services indicates that the most destructive diseases of grain crops in the West Siberian region are root rots caused by
The concept of “high farming culture” implies not only scientifically based and environment-friendly application of chemical fertilizers and pesticides, but also their partial replacement with biological preparations with a similar spectrum of action. Therefore, the development and use of biological preparations for plant protection is one of the key priorities of modern agrobiotechnology. Search for new strains of antagonistic bacteria that can be effectively used as biological control agents and research of antifungal mechanisms of the bacteria are both important tasks.
Long-term studies of microbiological aspects of vermiculture demonstrate that the percentage of
Many rhizosphere bacteria are well known to have fungistatic properties, since this feature provides bacteria with a significant trophic advantage when growing on substrates populated with a mixed (bacterial and fungal) flora. There are a number of mechanisms through which bacteria inhibit the growth of lower soil fungi, for example, competition for nutrients and production of siderophores, antibiotics, enzymes, and a number of other compounds [5, 6, 7, 8].
A number of studies also indicate that growth-stimulating and antifungal activities of the bacteria
2. Materials and methods
The main objects of our research were spring wheat (
2.2. Field experiments
Field experiments were conducted on gray podzoliс medium-loamy soil with the following physical and chemical properties: рН—5.0; humus content—4.87%; total absorbed bases—24.9 mg per 100 g of soil on a dry weight basis; and N─NH4, N─NO3, P2O5, and К2О—2.66, 8.48, 236.5, and 99.2 mg/kg dry weight of soil on a dry weight basis, respectively. Each experiment was repeated three times in all years of the tests. The variants were arranged in a systematic way. The total area of the plot was 40 m2. The area of the record plot was 32 m2. In order to optimize the mineral background, mineral fertilizers were applied to the soil at a dose of N45P30K30.
The effectiveness of bacterial application was assessed in terms of field germination, some morphometric parameters of plants (height and green mass of plants), content of photosynthetic pigments in leaves, the extent of damage caused by root rot causing agents, as well as grain yield, yield structure, and grain quality. Morphometric parameters of the plants were taken into account in the flowering stage, and the extent of disease damage in the tillering and early flowering stage. The total protein content in the grain was determined with an Infrared FT-10 IR spectrometer. In order to determine the content of photosynthetic pigments in the leaves in the flowering stage, we analyzed alcohol extracts from the leaves with a UV-1601 SHIMADZU spectrophotometer at wavelengths of 665, 649, and 440.5 nm, and then made calculations using the Vernon formula . The statistical validity of the estimated effects was tested by the Student’s test and the nonparametric Mann-Whitney test using Statistica 10.0 for Windows.
2.3. Weather and soil conditions
Throughout the field test period, there were significant fluctuations in temperature and precipitation. While the growing season of 2011 could be described as moderately warm and humid, the season of 2012 in the south of Western Siberia was characterized by extremely unfavorable weather conditions: June was abnormally hot, with precipitation of 48% below normal. The average monthly air temperature was 5.3°С above normal. The topsoil under spring grain crops was insufficiently moistened (5–22 mm). High temperatures and lack of moisture caused the accelerated development of grain crops at different stages. The weather conditions in the growing season of 2013 were not sufficiently favorable for the growth and development of crops as well. The beginning and end of the growing season were characterized by low temperatures with frequent and heavy precipitation, while late July and early August were hot and dry. The early growing season both in 2013 and 2014 was characterized by unfavorable weather conditions for field work, growth, and development of crops: cold May and early June with frequent and heavy precipitation. The weather conditions of the entire growing period of 2015 were relatively favorable, with high total precipitation between April and September, above-normal precipitation in May, July, August, and September, and a short dry period in June.
2.4. Inoculation study in model experiments
The model experiments were based on a liquid 24-hour culture of the bacteria grown in 250 ml flasks with 100 ml of GRM broth at +28…+29°C to a titer of 1–9 × 109 cells/ml. The experiments were carried out in laboratory conditions. We studied the effect of seed inoculation on the peroxidase activity in the presence of phytopathogen using a model of the simplest terrestrial ecosystem consisting of four links: sand-host plant-bacterial strain-phytopathogenic fungus . Seeds pretreated for 3 min with 70% ethanol were washed with sterile water and germinated in a wet chamber at +18… +20°C. After the appearance of a germ (1 mm), the seeds were inoculated with suspensions of the experimental strains for 20 min at the rate of 104 cells per seed. In the control variant, the seeds were soaked in distilled water. After treatment, the seeds were placed in plastic containers (1200 ml, 45 seeds per container) filled with coarse sterile river sand (800 ml), and evenly moistened with a sterile Knop’s solution for hydroponic and sandy cultures: Ca(NO3)2—1.0 g/l, KH2PO4—0.25 g/l, MgSO4 × 7H2O—0.125 g/l, KNO3—0.25 g/l, FeCl3—0.012 g/l.
In order to create infection background, we used agar strips with a 6-day mycelium of
2.5. Model experiment in growth chamber
The plants were grown in an environmental chamber (Growth Chamber GLK-300, Korea) under fluorescent lamps with an illumination intensity of 12 klux (200 μmol quanta/m2 × sec, PAR) with a 16-hour photoperiod at +18… +20°С (daytime temperature), +14… +16°С (night-time temperature), and 75% humidity. The total duration of the experiments was 12 days. At the end of the experiment, the germination capacity, plant length, peroxidase activity in the leaves and roots of the plants, as well as the prevalence of the disease and index of root rot development (disease index) were determined .
The guaiacol-dependent peroxidase activity was determined spectrophotometrically in the total protein extract (centrifugate) produced from wheat leaves and roots (concentration in the hydrogen peroxide reaction mixture—7.35 mM and guaiacol—0.672 mM). The enzyme activity was calculated by the Boyarkin’s method , taking into account the molar extinction coefficient of tetraguaiacol and expressed in mM of guaiacol/(min × g of fresh weight).
3. Results and discussion
3.1. Effects on morphology of plants
The results of field experiments for different years show that the inoculation usually stimulates the growth of wheat and barley plants, which is expressed in the accelerated development at main plant development stages and a statistically significant increase in the basic morphometric parameters of plants, such as height, the number of productive stems, the number of leaves, as well as the dry green mass compared to the control variant (non-inoculated plants treated with water before planting).
In different years, the height of wheat and barley plants increased, respectively, by 8–14% and 6–40% under the influence of bacteria monocultures and by 6–16% and 5–20%, respectively, under the influence of complex inoculation. On average over all years, the flag leaf area of wheat increased by 5–6%, while the sub-flag leaf area of barley increased by 5–15%. On average over all years, the dry mass of wheat and barley plants increased, respectively, by 10–40% and 15–73%, for monoculture variants, and by 7–54% and 23–63% for the variants with complex inoculation. In general, the plants responded to the inoculation by increasing not so much their length as their green mass, which contributed to an increase in the stem thickness and, therefore, indicated an increased lodging resistance of the plants.
The analysis of the moisture content in the green mass of wheat and barley shows that the water content of the inoculated plants tends to be higher compared to the control plants, which suggests a positive effect of the bacteria on the development of the root system. Rhizobacteria are known to be capable of controlling parameters of the root system by producing a wide range of hormone-like metabolites. Therefore, they contribute to an increase in length of both main and lateral roots, thereby increasing the catchment area .
These physiological effects are especially important in the context of the recent climate changes that increase the risk of extreme weather events (sudden changes in air temperature and humidity, increased dry periods during vegetation, etc.). It was no coincidence that the positive effects from the inoculation of spring grain crops were most noticeable in 2012—the year marked by an extremely dry summer period. The moisture content in the inoculated wheat plants was significantly (8–10%) higher than that of the control plants. Notably, the differences with the control variant are most noticeable at the flowering and tillering stages where the need of spring wheat for soil moisture is maximal and the water consumption makes up 50–60% of the total water consumption for the entire growing season.
For barley, the differences with the control variant are also most noticeable at the tillering (booting) stage when this crop has the maximum need for soil moisture. The root system of the inoculated barley plants absorbed 18.5–28.4% more moisture compared to the control plants. Lack of soil moisture in this period is known to lead to an increased number of sterile spikelets in a barley ear, thereby significantly reducing its yield. The more noticeable response of barley to the inoculation, compared to spring wheat, may be attributed to a less developed root system of barley and, therefore, to a larger “compensatory effect” of inoculation.
3.2. Effects on physiology and productivity of plants
Stimulation of the root system with the bacteria increased the feeding area and, therefore, the total content of nitrogen and phosphorus in the green mass of both tested crops. Improvement of nitrogen and phosphorus nutrition of the plants under the influence of inoculation is noted by many researchers [17, 18]. In our studies, the complex inoculation of spring wheat increased the total nitrogen content by 10–12% and the total phosphorus content by 50–54% on average over all years. The inoculation of barley contributed to a significant increase in the total nitrogen (24–30%) and phosphorus (11–13%).
Photosynthesis processes, along with mineral nutrition processes, are known to be decisive factors of grain maturing. At the same time, optimization of mineral nutrition is known to have a positive effect on photosynthetic activity of plants . It is probably for this reason that the inoculation has also contributed to a significant increase of photosynthetic pigments in wheat and barley leaves. The inoculation of wheat with the
The assessment of presowing seed treatment of spring wheat and barley conducted from 2011 to 2015 showed that, with rare exceptions, the inoculation in the climatic conditions of Western Siberia increased the grain yield of spring wheat by 8–37% compared to the control variant. It is equivalent to 0.2–1.0 tonnes per ha. The greatest increase was provided by the inoculation of wheat with a monoculture of
|Variant||Research period, year|
|Grain yield (ton/ha)||Protein content (%)||Grain yield (ton/ha)||Grain yield (ton/ha)||Grain yield (ton/ha)||Protein content (%)||Grain yield (ton/ha)||Protein content (%)|
|Control (water treatment)||2.7 ± 0.1||16.2 ± 1.2||0.9 ± 0.04||2.5 ± 0.1||3.4 ± 0.2||15.3 ± 1.4||2.3 ± 0.1||17.4 ± 1.1|
|Bacterization of ||3.0 ± 0.1||16.5 ± 1.2||1.2 ± 0.1||—||—||—||—||—|
|Bacterization of ||3.7 ± 0.2*||16.6 ± 1.3||1.0 ± 0.1||2.7 ± 0.3||—||—||—||—|
|Bacterization of ||—||—||1.2 ± 0.1||2.8 ± 0.3||3.6 ± 0.1||16.8 ± 0.9||3.3 ± 0.2*||17.5 ± 0.8|
|Complex bacterization (mixed culture)||3.1 ± 0.1*||16.9 ± 1.3||—||3.2 ± 0.2*||3.4 ± 0.03||17.0 ± 1.2||2.5 ± 0.2||17.7 ± 0.9|
|Control (water treatment)||8.1 ± 0.4||8.2 ± 0.5||1.5 ± 0.2||3.9 ± 0.3||7.5 ± 0.2||11.8 ± 1.1||3.9 ± 0.2||12.5 ± 0.7|
|Bacterization of ||9.5 ± 0.3*||9.3 ± 0.3*||2.4 ± 0.3||—||—||—||—||—|
|Bacterization of ||9.7 ± 0.3*||9.1 ± 0.2||2.4 ± 0.2||4.2 ± 0.2||—||—||—||—|
|Bacterization of ||—||—||2.5 ± 0.1||4.3 ± 0.3||7.8 ± 0.3||11.5 ± 1.0||4.4 ± 0.3||12.6 ± 0.6|
|Complex bacterization (mixed culture)||9.9 ± 0.4*||9.4 ± 0.2*||—||4.3 ± 0.1||8.0 ± 0.3*||11.5 ± 1.1||4.9 ± 0.2*||12.7 ± 0.7|
In addition to the increased yield of the grain crops per hectare, the inoculation contributed to improving its quality. For example, in different years, the inoculation of spring wheat contributed to an increase in the protein content in the grain from 15.3–17.4% in the control variant to 16.5–17.7% in the experimental variants (Table 1).
The analysis of the yield structure shows that the bacteria contribute, first of all, to an increase in the productive tillering capacity and grain content. For example, on average over the years, the productive tillering capacity of spring wheat increased from 1.04–1.37 in the control variant to 1.12–1.55 in the inoculated variants. The grain content of spring wheat increased from 23–26 grains per year in the control variant to 24.4–32.4 grains per year in the experimental variants. The inoculation with the monoculture of phosphate-mobilizing strain
3.3. Effects on the resistance of plants to pathogens
One of the most important factors that makes a significant contribution to grain crop yield is the development of diseases on plants, including root rots. Five-year field tests showed that the inoculation enhanced the resistance of spring wheat and barley plants to agents of root rots. Except for the dry year of 2012, the prevalence of the disease in spring wheat plants was significantly reduced—from 18.1–61.1% in the control variant to 6.4–50.2% in the inoculated variants. Severity of the disease was also significantly reduced in most cases. For example, in different years, the index of root rot development decreased from 18.2–23.0% in the control variants to 13.2–15.8% in the inoculated variants (Table 2).
|Variant||Research period, year|
|Prevalence of the disease (%)||Prevalence of the disease (%)||Index of disease development (%)||Prevalence of the disease (%)||Index of disease development (%)||Prevalence of the disease (%)||Index of disease development (%)||Prevalence of the disease (%)||Index of disease development (%)|
|Control (water treatment)||18.1 ± 3.4||53.1 ± 10.7||23.0 ± 3.0||51.7 ± 3.6||19.9 ± 3.8||56.4 ± 10.5||18.2 ± 3.4||61.1 ± 17.4||21.7 ± 7.1|
|Bacterization of ||14.3 ± 1.2||43.3 ± 6.4||21.7 ± 3.9||—||—||—||—||—||—|
|Bacterization of ||6.4 ± 0.8*||45.2 ± 7.1||14.7 ± 2.9*||44.4 ± 2.6*||15.8 ± 3.1*||—||—||—||—|
|Bacterization of ||—||50.2 ± 11.4||21.1 ± 2.1||36.7 ± 5.7*||13.2 ± 2.6*||39.4 ± 12.4||13.9 ± 1.7*||50.0 ± 17.8||15.8 ± 3.3|
|Complex bacterization (mixed culture)||10.0 ± 2.2*||—||—||38.3 ± 6.7*||11.2 ± 0.6*||47.2 ± 9.8||16.0 ± 2.5||26.6 ± 15.8*||9.2 ± 1.7*|
|Control (water treatment)||13.9 ± 1.7||79.2 ± 17.3||45.5 ± 6.1||44.4 ± 2.9||14.7 ± 2.6||87.0 ± 11.3||41.2 ± 9.7||66.7 ± 16.8||28.3 ± 2.7|
|Bacterization of ||5.8 ± 1.3*||71.5 ± 10.7||31.6 ± 2.7*||—||—||—||—||—||—|
|Bacterization of ||11.7 ± 2.7||73.7 ± 11.0||33.7 ± 2.3*||24.4 ± 8.07*||8.3 ± 2.5*||—||—||—||—|
|Bacterization of ||—||61.9 ± 8.8||30.6 ± 1.8*||—||—||73.1 ± 11.6||34.3 ± 5.1*||46.6 ± 7.8*||14.2 ± 2.0*|
|Complex bacterization (mixed culture)||6.5 ± 1.9*||—||—||41.0 ± 7.8||13.3 ± 2.5||71 ± 6.7||30.1 ± 3.4*||57.7 ± 12.6||20.8 ± 3.7*|
The capability of rhizobacteria to increase the resistance of plants to phytopathogens is widely discussed in the scientific literature. However, mechanisms responsible for increasing this resistance remain understudied. Most researchers have come to the conclusion that nonpathogenic rhizobacteria can activate resistance mechanisms of plants in the same way as phytopathogens, in particular through the synthesis of PR proteins, including peroxidase [7, 20, 21].
To clarify the mechanism that induces the spring wheat resistance to the agent of
It was no coincidence that microorganisms of the
Bacteria are known to have a positive effect only if they successfully colonize the rhizosphere [22, 25]. The effectiveness of wheat inoculation in our model experiment was assessed in terms of decreased development and prevalence of root rot agents in variants with and without infection background. The prevalence of the disease in the experimental variant without infection background and inoculation was at the level of 26%. In variants with artificial
3.4. Effects on peroxidase activity in model experiment with an artificial infectious load
According to some authors, the peroxidase activity can be used as a marker of plant resistance to phytopathogens [26, 27]. Since roots (rather than stems and leaves) are the first to contact the phytopathogenic fungus when the plants are infected with root rots, a separate assessment of oxidative stress enzyme activity in roots and aerial parts of plants is a matter of scientific interest.
The results of the peroxidase activity analysis showed that, in general, the inoculation significantly increased the enzyme activity in wheat leaves, both with and without the
In our experiment, wheat plants responded to the infection with
A comparison of the peroxidase activity in leaves and roots of uninfected and infected plants showed that the free peroxidase activity in the plant roots was, respectively, 60 and 23% higher than that in the leaves. At the same time, the response of enzyme systems to the inoculation in the presence of the causing agent was found to be much higher in the roots than the response of free peroxidase in the leaves. For example, the inoculation of wheat seeds with
The correlation analysis of the data obtained in the variants without a causing agent
Thus, the experimental findings suggest that there is an inverse relationship between the peroxidase activity in wheat tissues and damage of plants caused by root rot agents, and that the response of peroxidase enzymes to plant inoculation is a meaningful indicator that can be used to assess the potential of a particular strain as a biological agent for protecting spring wheat.
The results of a series of field tests in the climatic conditions of Western Siberia showed that the inoculation of spring wheat seeds with three bacterial strains isolated from earthworm coprolites increased the grain yield of spring wheat by 0.2–1.0 t ha−1. In different years, the inoculation of barley increased the grain yield by 0.3–1.8 t ha−1. In addition, the inoculation contributed to improving grain quality where the inoculation of spring wheat contributed to an increase in the protein content in the grain from 15.3–17.4% in the control variant to 16.5–17.7% in the variants with bacterization. Besides, field experiments showed that the grain bacteria inoculation enhanced the resistance of spring wheat and barley plants to root rots. For example, the prevalence of the disease in spring wheat plants subjected to bacterization was reduced from 18.1–61.1 to 6.4–50.2%. Severity of the disease was also significantly reduced in most cases where the index of root rot development decreased from 18.2–23.0% in the control variants to 13.2–15.8% in the inoculated variants. The results of model experiment clarified a number of mechanisms for increasing the plants’ resistance to root rots under the influence of rhizobacteria in the presence of artificial infection load (
Kozhemyakov AP, Belobrova SN, Orlova AG. Creating and analyzing a database on the efficiency of microbial preparations of complex action. Sel’skohozyaistvennaya biologiya (Agricultural Biology). 2011; 3:112-115
Chulkina VA, Konyaeva NM, Kuznetsova TT. Bor’ba s boleznyami sel’skokhozyaistvennykh kul’tur v Sibiri. Moscow: Rossel’hozizdat; 1987. p. 252
Toropova EYu, Vorob’eva IG, Chulkina VA, Marmuleva EY. About a role of biological diversity in the phytosanitary optimization of agrarian landscapes. Sel’skohozyaistvennaya biologiya (Agricultural Biology). 2013; 3:12-17
Tereshchenko NN, Kravets AV, Akimova EE, Minayeva OM, Zotikova AP. Effectiveness of applying microorganisms isolated from earthworm coprolites in increasing yielding capacity of grain crops. Siberian Herald of Agricultural Science. 2013; 5:10-17
Compant S, Duffy B, Nowak J, Clement C, Barka EA. Use of plant growth-promoting bacteria for biocontrol of plant diseases: Principles, mechanisms of action, and future prospects. Applied and Environmental Microbiology. 2005; 71(9):4951-4959. DOI: 10.1128/AEM.71.9.4951-4959.2005
Raupach GS, Kloepper JW. Mixtures of plant growth-promoting rhizobacteria enhance biological control of multiple cucumber pathogens. Phytopathology. 1998; 88(11):1158-1164. DOI: 10.1094/PHYTO.1922.214.171.1248
Johnson KB. Pathogen refuge: A key to understanding biological control. Annual Review of Phytopathology. 2010; 48:141-160. DOI: 10.1146/annurev.phyto.112408.132643
Gupta G, Parihar SS, Ahirwar NK, Snehi SK, Singh V. Plant growth promoting rhizobacteria (PGPR): Current and future prospects for development of sustainable agriculture. Journal of Microbial and Biochemical Technology. 2015; 7:096-102. DOI: 10.4172/1948-5948.1000188
Berg G, Fritze A, Roskot N, Smalla K. Evaluation of potential biocontrol rhizobacteria from different host plants of Verticillium dahliaKleb. Journal of Applied Microbiology. 2001; 91:963-971. DOI: 10.1046/j.1365-2672.2001.01462.x
Georgakopoulos DG, Fiddaman P, Leifert C, Malathrakis NE. Biological control of cucumber and sugar beet damping-off caused by Pythium ultimumwith bacterial and fungal antagonists. Journal of Applied Microbiology. 2002; 92:1078-1086. DOI: 10.1046/j.1365-2672.2002.01658.x
Smyth EM, McCarthy J, Nevin R, Khan MR, Dow JM, O'Gara F, et al. In vitro analyses are not reliable predictors of the plant growth promotion capability of bacteria; a Pseudomonas fluorescensstrain that promotes the growth and yield of wheat. Journal of Applied Microbiology. 2011; 111(3):683-692. DOI: 10.1111/j.1365-2672.2011.05079.x
Minaeva OM, Akimova EE. Effectiveness of applying bacteria Pseudomonas sp., strain B-6798, for anti-phytopathogenic protection of crops in Western Siberia. Journal of Biology. Tomsk State University. 2013; 3(23):19-37
Shlyk AA. Opredelenie khlorofillov i karotinoidov v ekstraktakh zelenykh list’ev. Biokhimicheskie metody v fiziologii rasteniy. M.: Nauka; 1971. pp. 154-170
Cooke BM. Disease assessment and yield loss. In: Cooke BM, Jone DG, Kaye B, editors. The Epidemiology of Plant Diseases. 2nd ed. Dorchert: Springer; 2006. pp. 43-80
Boyarkin AN. Bystryjmetodopredeleniyaaktivnostiperoksidazy. Biohimiya (Biochemistry). 1951; 16(4):352
Dodd IC, Zinovkina NY, Safronova VI, Belimov AA. Rhizobacterial mediation of plant hormone status. Annals of Applied Biology. 2010; 157:361-379
Khamova OF, Ledovsky EN, Tukmacheva EV, Shuliko NN. Influence of bacterial fertilizer on the biological activity of leached chernozem and cereal crops productivity. Vestnik Omskogo gosudarstvennogo agrarnogo universiteta (Bulletin of Omsk State Agrarian University). 2016; 3(23):44-48
Vacheron J, Desbrosses G, Bouffaud ML. Prigent-combaret plant growth-promoting rhizobacteria and root system functioning. Frontiers in Plant Science. 2013; 4:356-361
Priadkina GА, Stasik OO, Mikhalskaya LN, Shvartau VV. A relationship between chlorophyll photosynthetic potential and yield in winter wheat ( Triticum aestivumL.) at elevated temperatures. Sel’skohozyaistvennaya biologiya (Agricultural Biology). 2014; 5:88-95
Zaharenko VA. Biopesticidyisredstvazashchityrastenij s nebiocidnojaktivnost'yu v integrirovannomupravleniifitosanitarnymsostoyaniemzernovyhagroehkosistem. Agrohimiya (Agrochemistry). 2015; 6:64-76
Schisler DA, Slininger PJ, Bothast RJ. Effects of antagonist cell concentration and two strain mixtures on biological control of Fusarium dry rot of potatoes. Phytopathology. 1997; 87:177-183. DOI: 10.1094/PHYTO.19126.96.36.199
Choudhary DK, Kasotia A, Jain S, Vaishnav A, Kumari S, Sharma KP, et al. Bacterial-mediated tolerance and resistance to plants under abiotic and biotic stresses. Journal of Plant Growth Regulation. 2016; 35:276-300. DOI: 10.1007/s00344-015-9521-x
Van Loon LC. Plant responses to plant growth-promoting rhizobacteria. European Journal of Plant Pathology. 2007; 119:243-254. DOI: 10.1007/s10658-007-9165-1
Jankiewicz U, Kotonowicz M. The involvement of Pseudomonas bacteria in induced systemic resistance in plants (review). Prikladnayabiohimiyaimikrobiologiya (Applied Biochemistry and Microbiology). 2012; 48(3):276-281
Garcia-Cristobal J, Garcia-Villaraco A, Ramos B, Gutierrez-Manero J, Lucas JA. Priming of pathogenesis related-proteins and enzymes related to oxidative stress by plant growth promoting rhizobacteria on rice plants upon abiotic and biotic stress challenge. Journal of Plant Physiology. 2015; 188:72-79. DOI: 10.1016/j.jplph.2015.09.011
Van Lelyveld LJ, van Vuuren SP. Peroxidase activity as a marker in greening disease of citrus for assessment of tolerance and susceptibility. Journal of Phytopathology. 1988; 121:357-362. DOI: 10.1111/j.1439-0434.1988.tb00979.x
Reuveni R. Biochemical markers for disease resistance. In: Singh RP, Singh US, editors. Molecular Methods in Plant Pathology. Boca Ratton, FL, USA: Lewis Publisher; 1995. pp. 99-114
Manikandan R, Raguchander T. Fusarium oxysporumf. sp. lycopersici retardation through induction of defensive response in tomato plants using a liquid formulation of Pseudomonas fluorescens (Pf1). European Journal of Plant Pathology. 2014; 140:469-480. DOI: 10.1007/s10658-014-0481-y
Pieterse CMJ, Zamioudis C, Berendsen RL, Weller DM, Van Wees SCM, Bakker PAHM. Induced systemic resistance by beneficial microbes. Annual Reviews of Phytopathology. 2014; 52:347-375. DOI: 10.1146/annurev-phyto-082712-102340
Jain A, Das S. Insight into the interaction between plants and associated fluorescent Pseudomonas spp. International Journal of Agronomy. 2016. 4269010, 8 pages 10.1155/2016/4269010
Maksimov IV, Valeev AS, Cherepanova EA, Yarullina LG. Hydrogen peroxide production in wheat leaves infected with the fungus Septoria nodorumBerk. Strains with different virulence. Applied Biochemistry and Microbiology. 2009: 45(4):433-438. DOI: 10.1134/S0003683809040152