INTRODUCTION
Currently, many Russian and foreign researchers have noted that microbiological preparations, changing the microbiome of soil and plants, can stimulate the growth of various crops (Berendsen, Pieterse, & Bakker, 2012; De Faria, Costa, Chiaramonte, Bettiol, & Mendes, 2021;
Lim & Kim, 2009; Santoyo, Moreno-Hagelsieb, del Carmen Orozco-Mosqueda, & Glick, 2016; Zavalin, Chebotar‘, Aritkin, & Smetov, 2012), to increase their economic productivity or the quality of the crop (Mameev, Pavlovskaya, Timakov, & Yakovleva, 2019), to protect plants from pathogens (Cao et al., 2011; Minaeva et al., 2019; Titova, Novikova, Boykova, Pavlyushin, & Krasnobaeva, 2019), and to enhance the resistance of plants to stressful conditions (Pishchik et al., 2021; Rashid et al., 2022).
It is achieved by the synthesis of various metabolites or by mobilization of plant nutrition elements.
Among the good bacteria for crop production, many researchers distinguish representatives of the genera Bacillus, Pseudomonas, Azospirillum, Klebsiella, Enterobacter, etc. (De Souza Vandenberghe et al., 2017; Glick, 2012; Kang et al., 2014; Santoyo, del Carmen Orozco-Mosqueda, & Govindappa, 2012).
At the same time, some bacteria representatives can simultaneously perform several of the above functions, making them more promising and, consequently, more interesting for research.
The genus Bacillus has aroused significant scientific and practical interest; its representatives are pretty diverse and include inhabitants of the rhizosphere, phyllosphere, and endophytic representatives. The researchers pay special attention to the species Bacillus subtilis, different strains of which show efficiency when used in crop production. The main mechanisms of action of Bacillus subtilis on plant growth and development involve the mobilization of nutrients, the synthesis of ARTICLE INFO
Keywords:
Grain productivity
Microbiological preparations Morphological indicators OatPhotosynthetic indicators
Article History:
Received: April 13, 2022 Accepted: January 29, 2023
*) Corresponding author:
E-mail: [email protected]
ABSTRACT
The work studies the effect of microbiological preparations based on the culture of B. subtilis and B. megaterium on the growth processes, photosynthetic parameters, and grain productivity of oats. Field tests were conducted in 2019 in the conditions of a micro plot experiment in the North-West of Russia. Microbiological preparations were introduced by soaking seeds and treating plants in the third leaf stage with preparations of 1 ml/l.The research finds that the introduction of microbiological preparations leads to a significant increase in growth. In the tillering stage, the leaf surface area of the experimental plants was higher by up to 40.1%, and plants’ fresh and dry mass increased by 27.8–58.9%.
Introducing microbiological preparations increased the average daily increments and the net productivity of plant photosynthesis by 1.080–
2.801 g/m2. By the time of harvesting, the mass of the experimental plants remained higher by 13.4–23.3%. The studied preparations increased the grain productivity of oats by up to 16.3% compared to the control. The study indicated a positive effect of microbiological preparations based on B. subtilis and B. megaterium strains on oats.
ISSN: 0126-0537Accredited First Grade by Ministry of Research, Technology and Higher Education of The Republic of Indonesia, Decree No: 30/E/KPT/2018
Cite this as: Platonov, A. V., Rassokhina, I. I., Laptev, G. Y., & Bolshakov, V. N. (2023). Preparations use based on bacteria of the genus Bacillus to increase the yield of oats (Avena sativa L.). AGRIVITA Journal of Agricultural Science, 45(1), 48–55. http://doi.org/10.17503/agrivita.v45i1.3757
Preparations Use Based on Bacteria of the Genus Bacillus to Increase the Yield of Oats (Avena sativa L.)
Andrei V. Platonov1,3*), Irina I. Rassokhina1), Georgii Yu. Laptev2), and Vladislav N. Bolshakov2)
1) Vologda Research Center of the Russian Academy of Sciences, Vologda, Russia
2) JSC “Biotrof+”, St. Petersburg, Russia
3) Vologda Institute of Law and Economics of the Federal Penitentiary Service of Russia, Vologda, Russia
phytohormones, and the expression of antibacterial activity (Liu, Xing, Ma, Du, & Ma, 2013). For example, there is evidence that B. subtilis H-13 enhances the absorption of mineral fertilizers and nutrients from the soil by plant roots, which leads to an increase in yield by 5–10% (Zavalin, Chebotar’, Aritkin, & Smetov, 2012). Chebotar et al. (2016) studied the endophytic strain of B. subtilis HC8, its use significantly increased the yield of radish and lettuce in vegetation experiments by 15.2–42.1%, and the yield of barley grain relative to the control increased by 14.8%. Cao et al. (2011) have noted that colonization of cucumber roots B. subtilis STR 9 reduced wilting of plants sproutings caused by Fusarium oxysporum by 49–61% relative to the control. For representatives of B. subtilis, the ability to synthesize auxins is often noted. For instance, studies by Lim & Kim (2009) have shown the effectiveness of strains of Bacillus subtilis AH18 and Bacillus licheniformis K11, which produced auxins, fungicidal β-glucannase and siderophores, and also mobilized insoluble phosphates, as a result of which the growth processes of pepper and tomato increased by 20%. The effect of Bacillus megatherium on plants is associated with the synthesis of cytokinins which primarily leads to the more active development of the root system of plants, especially the lateral roots (López-Bucio et al., 2007; Ortíz-Castro, Valencia-Cantero, & López- Bucio, 2008). There is evidence that the strain of B. megaterium XTBG34 stimulated plant growth due to the synthesis of 2-pentylfuran (Zou, Li, & Yu, 2010). The ability to positively affect the synthesis of phytohormones of the cytokinin group in plant roots was also noted in B. subtilis. For example, the results of studies by Arkhipova, Veselov, Melentiev, Martynenko, & Kudoyarova (2005) showed a 10- fold increase in zeatin in the roots of experimental plants relative to the control on the second day after inoculation of plants with bacteria. dos Santos et al. (2021) showed an increase in growth rate, shoot diameter, leaf content of N, Fe, and Cu, crude protein, and neutral detergent fiber in Avena sativa L. plants when inoculating their seeds with B.
subtilis and B. megaterium isolates.
Thus, the bacteria B. subtilis and B.
megaterium are promising for studying the possibilities of their use in the agricultural practice of crop production. However, local studies are necessary to assess the effect of a certain bacteria strain on a specific culture in the Russian region.
In this regard, studies have been conducted on the influence of microbiological preparations created based on B. subtilis and B. megaterium strains on morphometric and physiological parameters, as well as the yield of oat grain (Avena sativa L.) in the Vologda Oblast conditions. Oat is the most important agricultural crop in the Vologda Oblast, and its sown area occupies about 20% of the total area of grain crops in the Oblast.
The research aims to study the morphological and physiological characteristics of oats (Avena sativa L.) of the Yak variety under the action of microbiological preparations on it.
MATERIALS AND METHODS
The test site is the experimental field of the Vologda Research Center of the Russian Academy of Sciences. The test time is the growing season of 2019. The soil in the experimental field is drained sod-podzolic, medium loamy. The results of the chemical analysis of the soil (FSBI State Center of Agrochemical Service „Vologodsky“) show that the content of ammonia nitrogen is 4.2 ± 0.6 mg/
kg, nitrate nitrogen is 38.9 ± 7.8 mg/kg, the mass fraction of mobile potassium is 261.0 ± 39.2 mg/kg, the mass fraction of mobile phosphorus is 260.0 ± 52.0 mg/kg, and the pH of the salt extract is 6.6 ± 0.1. Such a relatively low background of biogenic elements allows evaluation of the effectiveness of microorganisms› action on plants› growth and development.
The object of the study is to select oats (Avena sativa ‘Yak’) as a crop cultivated in the conditions of the North-West of Russia. The article studies Naturost and Naturost-M as microbiological preparations. The drug Naturost represents a culture of Bacillus subtilis (Ehrenberg 1835) Cohn 1872 cells; Naturost-M is Bacillus megaterium de Bary 1884. The preparations are produced by JSC
„Biotrof+“ based on the strains of microorganisms deposited in the own collection. The seeds of experimental plants were soaked in working solutions of preparations for 2 hours, and the seeds of control plants were soaked in water.
The concentration of the working solution is 1 ml of the drug per 1 liter of water. In addition to inoculating seeds, single spraying of plants was carried out after the emergence of the third leaf – the beginning of tillering – with working solutions of the same concentration with a total consumption of 1 l/ha preparation. The drugs were introduced
following the doses and terms recommended by the manufacturer.
In a microplot field experiment, this study used the following options: water treatment (1st variant, control), treatment with Naturost (2nd variant), and Naturost-M (3rd option). The experience repetition is 6th-fold, and the area of the accounting plot is 1 m2. The sowing followed the accepted seeding standards: 5.5 million oat grains per 1 hectare.
The care of the crops was carried out following generally accepted agrotechnical techniques.
Mineral fertilizers, pesticides, and herbicides were not applied.
During the growing season (third leaf stage, tillering stage, booting stage), there were taken into account the morphometric indicators of plants (height, wet and dry mass, leaf surface area, total bushiness), average daily increments, and elements of the crop structure (productive tillering, number of spikelets in a panicle, mass of the first 1,000 panicle grains, grain mass from 1 plant, grain mass from 1 m2). For analysis, there 30 plants were taken from the plot.
The net productivity of photosynthesis was determined by A.A. Nichiporovich (Vorob’yev, Nevmerzhitskaya, Khusnetdinova, & Yakushenkova, 2013) (1).
...(1) Where: NPP = net photosynthetic productivity; В1 and В2 = dry biomass at the beginning and end of the accounting period (g); В2 – В1 = dry mass gain for the accounting period (g); (S1 + S2) × 0.5 = the average working area of leaves for this period (m2);
n = number of days of the accounting period.
The NPP shows the specific productivity of the assimilation apparatus; it means the accumulation of biomass by a unit of leaf area per unit of time and characterizes not photosynthesis in its pure form but the daily difference between photosynthesis and respiration of the whole plant attributed to a unit of leaf area.
Chlorophylls were taken by extraction with 85% acetone from plant leaves (Vorob’yev, Nevmerzhitskaya, Khusnetdinova, & Yakushenkova, 2013). The pigment content was determined using an SF-2000 spectrophotometer (LOMO, Russia), the pigments were extracted by triple extraction with 85% acetone, and the chlorophyll content was calculated using the Rebbelen equations (2).
C chl.a = 10.3 D663 – 0.918 D644; С chl.b = 19.7 D644 – 3.87 D663;
C chl.а + chl.b = 6.4 D663 + 18.8 D664; ...(2) Statistical data processing was done according to standard methods using the MS Excel 2010 data analysis package. The tables present the average values of the indicators (M) and the values of their standard deviations (± SD). The reliability of the difference in the sample means was evaluated at a confidence probability value of 0.95.
RESULTS AND DISCUSSION
The data in Table 1 indicate that after the introduction of drugs, at the third leaf stage, there is a tendency to increase the morphometric indicators of experimental plants relative to the control, although the difference is unreliable. It can be assumed that the drought after sowing seeds significantly limited the plants‘ growth and negatively affected the viability and activity of microorganisms of microbiological preparations. This assumption is explained by the significant differences between the experimental and control plants observed during the tillering stage, i.e., after repeated application of microbiological preparations by spraying. Given that the size of plants in the third leaf stage is insignificant, the bacteria of the drug could quickly get to the soil and then reach the rhizosphere of plants.
During the tillering stage, the growth indicators of the experimental plants significantly increased. For example, the indicators of the fresh and dry mass of plants, treated with the microbiological preparation Naturost, increased by 32.4% and 58.9%, respectively, and the leaf surface area by 40.1% compared to the control (Table 1).
The drug Naturost-M had a slightly smaller effect, the fresh mass of plants increased by 31.2%, the dry mass by 27.8%, and the leaf surface area by 33.4%. The difference between the experimental and control plants was even more significant during the booting stage. For instance, the fresh mass of oat plants during treatment with the studied preparations significantly increased by 46.5–51.9%
and the dry mass by 45.8–58.1%. At the same time, the indicators of tillering and the number of leaves in control and experimental oat plants are not significantly different, which is explained by the conservatism of these signs.
Table 1. Morphometric parameters of oats (Avena sativa’ Yak’) in a field microplot experiment with microbiological preparations
Indicator Control Naturost Naturost-М
Third leaf stage
Fresh mass of a plant (g) 0.176±0.014 0.197±0.013 0.190±0.031
Dry mass of a plant (g) 0.034±0.003 0.037±0.003 0.037±0.004
Number of leaves 2.0±0.1 2.0±0.1 2.0±0.1
Average leaf area (cm2) 1.94±0.17 2.15±0.13 2.19±0.26
Leaf surface area of a plant (cm2) 3.86±0.64 4.31±0.57 4.44±0.50
Stage of the beginning of tillering
Fresh mass of a plant (g) 0.788±0.125 1.043±0.114* 1.034±0.116*
Dry mass of a plant (g) 0.158±0.021 0.251±0.047* 0.202±0.017*
Tillering, units 1.4±0.3 1.6±0.3 1.8±0.2
Number of leaves 5.2±1.0 5.9±0.8 5.9±0.5
Average leaf area (cm2) 2.61±0.25 3.24±0.34* 2.94±0.35
Leaf surface area of a plant (cm2) 12.03±1.59 16.86±0.72* 16.05±1.74*
Stage of the beginning of booting
Fresh mass of a plant (g) 5.537±1.102 8.110±1.030* 8.412±1.284*
Dry mass of a plant (g) 1.536±0.208 2.240±0.201* 2.429±0.272*
Tillering, units 3.5±1.6 3.6±1.0 4.2±2.0
Number of leaves 14.9±4.6 11.7±2.9 16.0±7.0
Remarks: * = the difference compared to the control is statistically significant when р < 0.05.
Table 2. Physiological parameters of oats (Avena sativa ‘Yak’) in a field microplot experiment with microbiological preparations
Indicator Control Naturost Naturost-М
Third leaf stage – tillering stage
Fresh mass gain (mg/day) 46.78±6.67 68.88±13.73* 66.25±13.47
Dry mass gain (mg/day) 10.00±2.30 17.79±5.48* 14.44±1.67*
Net photosynthetic productivity (g/m2 of leaf surface per day) 11.417±0.460 12.550±0.380* 14.218±0.608*
Chlorophyll a (mg/g of dry mass) 5.05±0.78 3.92±0.43 4.25±0.03
Chlorophyll b (mg/g of dry mass) 6.61±1.66 6.19±0.59 6.30±0.32
Amount of chlorophylls of a and b (mg/g of dry mass) 9.02±2.48 8.36±1.04 8.37±0.34 Tillering stage – stage of the beginning of booting
Fresh mass gain (mg/day) 163.23±6.38 292.95±26.34* 266.31±14.43*
Dry mass gain (mg/day) 49.36±6.80 77.80±2.85* 66.62±6.39*
Chlorophyll a (mg/g of dry mass) 2.00±0.01 2.00±0.02 1.97±0.03
Chlorophyll b (mg/g of dry mass) 4.09±0.40 3.43±0.21* 4.54±0.01*
Amount of chlorophylls of a and b (mg/g of dry mass) 6.09±0.39 5.43±0.19* 6.52±0.03*
Remarks: * = the difference compared to the control is statistically significant when р < 0.05.
An increase in the leaf surface area of experimental plants relative to the control causes a rise in the average daily increments (Table 2).
First of all, this situation may be associated with the intensification of photosynthesis and activation of the pigment apparatus, which is confirmed in several works (Mishina, Belopukhov, & Prusakova, 2010;
Sinegovskaya, Xiaomei, & Sukhorukov, 2009). For example, in the period between the stages of the third leaf and tillering, the average daily increments of experimental plants in the raw mass increased by 41.6–47.2%, in the dry mass by 44.4–77.9%, this pattern persisted in the period between the stages of tillering and the beginning of booting.
The rate of plant biomass accumulation consists of two components: the growth rate of plant mass per unit area of leaf surface per unit time (net photosynthesis productivity), as well as the ratio of leaf area to plant biomass (specific leaf surface). In this study, the NPP of plants treated with Naturost was higher than the control ones by 1.080 g/m2 and those treated with Naturost-M by 2.801 g/m2. The specific leaf surface in the variant with the introduction of preparation based on Bacillus megaterium was higher by 3.31 cm2/g compared to the control. In contrast, the microbiological preparation based on Bacillus subtilis caused a slight decrease in this indicator. Thus, in experimental plants, with an increase in the leaf surface area, the efficiency of the unit of the leaf area and the accumulation of dry matter increased.
Some researchers note that the positive effect of physiologically active substances, including those released by microorganisms, on the photosynthesis process can be viewed from two sides. Firstly, this leads to an increase in the leaf surface and, secondly, to a more extended
period of leaf vegetation (Mishina, Belopukhov, &
Prusakova, 2010; Samaniego-Gámez et al., 2016;
Seregina et al., 2018; Shi, Lou, & Li, 2010; Stefan, Munteanu, Stoleru, Mihasan, & Hritcu, 2013; Zhang et al., 2008). At the same time, the average daily growth, the number of leaves, the leaf surface area, the intensity of photosynthesis, and the content of chlorophyll, all these indicators allow judging the productivity of plant photosynthesis in specific agro-climatic conditions (Mameev, Pavlovskaya, Timakov, & Yakovleva, 2019; Mishina, Belopukhov,
& Prusakova, 2010). In our study, the increase in the leaf surface of plants, the average daily mass gains, and the net productivity of oat photosynthesis, in general, is obvious, which indicates an increase in the efficiency of photosynthetic activity under the influence of microbiological preparations. Similar results were obtained in experiments aimed at studying microbial preparations’ effect on barley growth processes (Rassokhina, Platonov, Laptev, &
Bolshakov, 2020).
Determining the chlorophyll content in the biomaterial has shown ambiguous results (Table 2).
For example, this study has not revealed significant differences during the tillering stage; there is a slight tendency to decrease the chlorophyll content in the plants of the experimental variants. In the setting of the beginning of booting, plants treated with the microbiological preparation Naturost showed a slight decrease in the content of photosynthetic pigments, which can be associated with the effect of the dilution of chlorophyll. Perhaps, against the background of an increase in the leaf surface, the chlorophyll synthesis did not keep up with the growth of plants. When treated with the microbiological preparation Naturost-M, the number of chlorophylls increased (due to an increase in chlorophyll b).
Table 3. Economic productivity of oats (Avena sativa ‘Yak’) when treated with microbiological preparations
Indicator Control Naturost Naturost-М
Mass of 1 plant (g) 5.24±0.83 5.94±0.74 6.46±1.01
Mass of the plant straw (g) 2.96±0.50 3.32±0.39 3.83±0.82
Mass of grain from plant (g) 2.27±0.22 2.61±0.32 2.64±0.18
Productive tillering, units 3.5±0.6 3.7±0.5 3.4±0.5
Number of spikelets in the panicle 22.3±2.7 24.2±2.1 25.4±1.9
Mass of the first 1,000 grains of panicle (g) 46.37±2.45 45.87±1.71 45.56±1.73
Grain mass per 1 m2 (g) 250.64±17.60 300.07±14.97* 313.11±16.58*
Remarks: * = the difference compared to the control is statistically significant when р < 0.05.
Considering that the plants achieved impressive morphometric indicators and average daily gains when treated with Naturost, their chlorophyll concentration was lower than in the control. It can be assumed that their pigment units worked more efficiently. Thus, an increase in the leaf surface area in experimental plants was accompanied by an increase in the productivity of photosynthesis both due to the rise in the content of pigments (Naturost-M) and the activation of the work of pigment units (Naturost). Several studies have shown an increase in the intensity of photosynthesis and the content of photosynthetic pigments due to the interaction of plants with the bacteria B. subtilis and B. Megaterium (Efthimiadou et al., 2020; Katsenios et al., 2021).
Stimulating the growth processes in oat plants under the influence of microbiological preparations may be associated with the synthesis of phytohormonal substances by microorganisms, antifungal and antibacterial effects, and mobilization of mineral nutrition elements from the soil. It has been shown that some bacteria of the genus Bacillus belong to the so-called PGPR (plant growth-promoting rhizobacteria) group. They can contribute to the intensification of plant growth by synthesizing phytohormones, such as auxins (indole-3-acetic acid), which have a beneficial effect on plant nutrition by solubilizing phosphate and chelating iron with siderophores (Raddadi, Cherif, Boudabous, & Daffonchio, 2008; Raddadi et al., 2009). In the laboratory for molecular genetic analysis of JSC “Biotrof+,” it is found that the genome B. subtilis has several clusters of genes associated with siderophore synthesis and phosphorus assimilation, and almost all the genes necessary for the iron-binding process with the participation of bacillibactin were also found (Dunyashev et al., 2021; 2022). There is evidence that some bacteria can inhibit phytopathogenic microorganisms due to the production of siderophores and successful competition for iron ions present in the soil (Rout et al., 2013).
Changes in growth processes at the early stages of ontogenesis could not affect oats’ final productivity, which is consistent with several works (Long, Marshall-Colon, & Zhu, 2015; Mameev, Pavlovskaya, Timakov, & Yakovleva, 2019;
Pryadkina, 2018). In the final productivity analysis of oats (Table 3), it is possible to note a decrease in the difference in the biomass of experimental
and control plants compared with the indicators of earlier phases of ontogenesis. In general, the grain productivity of plants when treated with microbiological preparations increased by 15.0–
16.3%, and the grain mass per m2 increased by 19.8–24.9%. This was due to a certain increase in the number of grains in the panicle and the completeness of the grain. At the same time, the mass of the first grains of the ear and the productive tillering of oat plants did not significantly change. It can assume that the treatment with microbiological preparations accelerates the ontogenesis of plants to a greater extent. Some authors note that the acceleration of plant ontogenesis contributes to faster organogenesis (new leaves are formed, and the leaf surface area of experimental plants is larger than the control ones), which contributes to the accumulation of dry matter and, as a result, increases the grain productivity of plants (Mameev, Pavlovskaya, Timakov, & Yakovleva, 2019;
Pryadkina, 2018).
CONCLUSION
The study indicated a positive effect of microbiological preparations created based on Bacillus subtilis and Bacillus megaterium strains on oats (Avena sativa ‘Yak’). Soaking seeds and spraying plants in the third leaf stage with microbiological preparations contributed to accelerated growth.
They led to faster organogenesis, an increase in the leaf surface of plants, and, ultimately, grain productivity. For instance, grain productivity from 1 m2 increased by 19.7% when treated with Naturost and 24.9% when treated with Naturost-M. The action of the microbiological preparations may be associated with synthesizing phytohormonal substances by microorganisms, antifungal and antibacterial effects, and mobilization of mineral nutrition elements from the soil. Currently, industrial tests of the effectiveness of the studied microbiological preparations are continuing on grain and feed crops.
REFERENCES
Arkhipova, T. N., Veselov, S. U., Melentiev, A. I., Martynenko, E. V., & Kudoyarova, G. R.
(2005). Ability of bacterium Bacillus subtilis to produce cytokinins and to influence the growth and endogenous hormone content of lettuce plants. Plant and Soil, 272, 201–209. https://doi.
org/10.1007/s11104-004-5047-x
Berendsen, R. L., Pieterse, C. M. J., & Bakker, P. A. H. M.
(2012). The rhizosphere microbiome and plant health. Trends in Plant Science, 17(8), 478–486.
https://doi.org/10.1016/j.tplants.2012.04.001 Cao, Y., Zhang, Z., Ling, N., Yuan, Y., Zheng, X., Shen, B.,
& Shen, Q. (2011). Bacillus subtilis SQR 9 can control Fusarium wilt in cucumber by colonizing plant roots. Biology and Fertility of Soils, 47, 495–506. https://doi.org/10.1007/s00374-011- 0556-2
Chebotar’, V. K., Zaplatkin, A. N., Shcherbakov, A. V., Mal’fanova, N. V., Startseva, A. A., & Kostin, Ya.
V. (2016). Microbial preparations on the basis of endophytic and rhizobacteria to increase the productivity in vegetable crops and spring barley (Hordeum vulgare L.), and the mineral fertilizer use efficiency. Agricultural Biology, 51(3), 335–342. https://doi.org/10.15389/
agrobiology.2016.3.335eng
De Faria, M. R., Costa, L. S. A. S., Chiaramonte, J.
B., Bettiol, W., & Mendes, R. (2021). The rhizosphere microbiome: functions, dynamics, and role in plant protection. Tropical Plant Pathology, 46, 13–25. https://doi.org/10.1007/
s40858-020-00390-5
De Souza Vandenberghe, L. P., Garcia, L. M. B., Rodrigues, C., Camara, M. C., de Melo Pereira, G. V., de Oliveira, J., & Soccol, C. R.
(2017). Potential applications of plant probiotic microorganisms in agriculture and forestry. AIMS Microbiology, 3(3), 629-648. https://doi.
org/10.3934/microbiol.2017.3.629
dos Santos, A. F., Corrêa, B. O., Klein, J., Bono, J. A.
M., Pereira, L. C., Guimarães, V. F., & Ferreira, M. B. (2021). Biometrics and nutritional status of white oat (Avena sativa L.) culture under Bacillus subtilis and B. megaterium inoculation.
Research, Society and Development, 10(5), e53410515270. https://doi.org/10.33448/rsd- v10i5.15270
Dunyashev, T. P., Laptev, G. Yu., Yildirim, E. A., Ilina, L.
A., Filippova, V. A., Tiurina, D. G., … Platonov, A. V. (2021). Identification of genes associated with the synthesis of siderophores by the Bacillus subtilis. Journal of Livestock Science, 12(4), 287–291. https://doi.org/10.33259/
JLivestSci.2021.287-291
Dunyashev, T., Laptev, G., Yildirim, E., Ilina, L., Filippova, V., Tiurina, D., … Platonov, A. (2022). Analysis of the potential associated with the siderophores synthesis in the Bacillus subtilis strain using whole genome sequencing. In A. Muratov, &
S. Ignateva (Eds.), Fundamental and Applied
Scientific Research in the Development of Agriculture in the Far East (AFE-2021). Lecture Notes in Networks and Systems, 354, 663-669.
Cham: Springer. https://doi.org/10.1007/978-3- 030-91405-9_73
Efthimiadou, A., Katsenios, N., Chanioti, S., Giannoglou, M., Djordjevic, N., & Katsaros, G. (2020). Effect of foliar and soil application of plant growth promoting bacteria on growth, physiology, yield and seed quality of maize under Mediterranean conditions. Scientific Reports, 10, 21060. https://
doi.org/10.1038/s41598-020-78034-6
Glick, B. R. (2012). Plant growth-promoting bacteria:
mechanisms and applications. Scientifica, 2012, 963401. https://doi.org/10.6064/2012/963401 Kang, S.-M., Radhakrishnan, R., You, Y.-H., Joo, G.-J., Lee,
I.-J., Lee, K.-E., & Kim, J.-H. (2014). Phosphate solubilizing Bacillus megaterium mj1212 regulates endogenous plant carbohydrates and amino acids contents to promote mustard plant growth. Indian Journal of Microbiology, 54, 427–
433. https://doi.org/10.1007/s12088-014-0476-6 Katsenios, N., Andreou, V., Sparangis, P., Djordjevic, N.,
Giannoglou, M., Chanioti, S., … Efthimiadou, A. (2021). Evaluation of plant growth promoting bacteria strains on growth, yield and quality of industrial tomato. Microorganisms, 9(10), 2099.
https://doi.org/10.3390/microorganisms9102099 Lim, J.-H., & Kim, S.-D. (2009). Synergistic plant growth
promotion by the indigenous auxins-producing PGPR Bacillus subtilis AH18 and Bacillus licheniforims K11. Journal of the Korean Society for Applied Biological Chemistry, 52, 531–538.
https://doi.org/10.3839/jksabc.2009.090
Liu, F., Xing, S., Ma, H., Du, Z., & Ma, B. (2013).
Cytokinin-producing, plant growth-promoting rhizobacteria that confer resistance to drought stress in Platycladus orientalis container seedlings. Applied Microbiology and Biotechnology, 97, 9155–9164. https://doi.
org/10.1007/s00253-013-5193-2
Long, S. P., Marshall-Colon, A., & Zhu, X.-G. (2015).
Meeting the global food demand of the future by engineering crop photosynthesis and yield potential. Cell, 161(1), 56–66. https://doi.
org/10.1016/j.cell.2015.03.019
López-Bucio, J., Campos-Cuevas, J. C., Hernández- Calderón, E., Velásquez-Becerra, C., Farías- Rodríguez, R., Macías-Rodríguez, L. I.,
& Valencia-Cantero, E. (2007). Bacillus megaterium rhizobacteria promote growth and alter root-system architecture through an auxin-
and ethylene-independent signaling mechanism in Arabidopsis thaliana. Molecular Plant-Microbe Interactions, 20(2), 207–217. https://doi.
org/10.1094/MPMI-20-2-0207
Mameev, V. V., Pavlovskaya, N. E., Timakov, A. G.,
& Yakovleva, I. V. (2019). The study of the effectiveness of the use of biological products for photosynthetic activity and the harvest of spring barley. Vestnik Irgsha, 90, 44–55 (in Russian).
Retrieved from https://www.elibrary.ru/item.
asp?id=37012762
Minaeva, O. M., Akimova, E. E., Tereshchenko, N. N., Kravets, A. V., Zyubanova, T. I., & Apenysheva, M. V. (2019). Pseudomonads associated with soil lumbricides as promising agents in root rot biocontrol for spring grain crops. Agricultural Biology, 54(1), 91–100. https://doi.org/10.15389/
agrobiology.2019.1.91eng
Mishina, O. S., Belopukhov, S. L., & Prusakova, L. D.
(2010). Physiological bases for the application of zircon and carvitol growth regulators to increase the productivity of buckwheat. Agrokhimiya, 1, 42–54 (in Russian). Retrieved from https://www.
elibrary.ru/item.asp?id=14343686
Ortíz-Castro, R., Valencia-Cantero, E., & López-Bucio, J. (2008). Plant growth promotion by Bacillus megaterium involves cytokinin signaling. Plant Signaling & Behavior, 3(4), 263–265. https://doi.
org/10.4161/psb.3.4.5204
Pishchik, V. N., Filippova, P. S., Mirskaya, G. V., Khomyakov, Y. V., Vertebny, V. E., Dubovitskaya, V. I., … Chebotar, V. K. (2021). Epiphytic PGPB Bacillus megaterium AFI1 and Paenibacillus nicotianae AFI2 improve wheat growth and antioxidant status under Ni stress. Plants, 10(11), 2334. https://doi.org/10.3390/plants10112334 Pryadkina, G. A. (2018). Pigments, photosynthesis
efficiency and wheat productivity. Plant Varieties Studying and Protection, 14(1), 97–108 (in Russian). https://doi.org/10.21498/2518- 1017.14.1.2018.126524
Raddadi, N., Belaouis, A., Tamagnini, I., Hansen, B. M., Hendriksen, N. B., Boudabous, A., … Daffonchio, D. (2009). Characterization of polyvalent and safe Bacillus thuringiensis strains with potential use for biocontrol. Journal of Basic Microbiology, 49(3), 293–303. https://doi.org/10.1002/
jobm.200800182
Raddadi, N., Cherif, A., Boudabous, A., & Daffonchio, D.
(2008). Screening of plant growth promoting traits of Bacillus thuringiensis. Annals of Microbiology,
58, 47–52. https://doi.org/10.1007/BF03179444 Rashid, U., Yasmin, H., Hassan, M. N., Naz, R., Nosheen,
A., Sajjad, M., … Ahmad, P. (2022). Drought- tolerant Bacillus megaterium isolated from semi-arid conditions induces systemic tolerance of wheat under drought conditions. Plant Cell Reports, 41, 549–569. https://doi.org/10.1007/
s00299-020-02640-x
Rassokhina, I. I., Platonov, A. V., Laptev, G. Y., &
Bolshakov, V. N. (2020). Morphophysical reaction of Hordeum vulgare to the influence of microbial preparations. Regulatory Mechanisms in Biosystems, 11(2), 220–225. https://doi.
org/10.15421/022032
Rout, M. E., Chrzanowski, T. H., Westlie, T. K., DeLuca, T. H., Callaway, R. M., & Holben, W. E. (2013).
Bacterial endophytes enhance competition by invasive plants. American Journal of Botany, 100(9), 1726–1737. https://doi.org/10.3732/
ajb.1200577
Samaniego-Gámez, B. Y., Garruña, R., Tun-Suárez, J. M., Kantun-Can, J., Reyes-Ramírez, A.,
& Cervantes-Díaz, L. (2016). Bacillus spp.
inoculation improves photosystem II efficiency and enhances photosynthesis in pepper plants.
Chilean Journal of Agricultural Research, 76(4), 409-416. https://doi.org/10.4067/S0718- 58392016000400003
Santoyo, G., del Carmen Orozco-Mosqueda, C., &
Govindappa, M. (2012). Mechanisms of biocontrol and plant growth-promoting activity in soil bacterial species of Bacillus and Pseudomonas: a review. Biocontrol Science and Technology, 22(8), 855–872. https://doi.org/10.1 080/09583157.2012.694413
Santoyo, G., Moreno-Hagelsieb, G., del Carmen Orozco-Mosqueda, M., & Glick, B. R. (2016).
Plant growth-promoting bacterial endophytes.
Microbiological Research, 183, 92-99. https://
doi.org/10.1016/j.micres.2015.11.008
Seregina, I. I., Shumilin, A. O., Vigilyansky, Yu M., Belopukhov, S. L., Grishina, Ye A., Tsygutkin, A.
S., … Litvinskiy, V. A. (2018). The formation of grain yield and quality indicators of white lupine (Lupinus albus L.) when using sodium selenite.
Agrokhimiya, 7, 73–80 (in Russian). https://doi.
org/10.1134/S0002188118070128
Shi, Y., Lou, K., & Li, C. (2010). Growth and photosynthetic efficiency promotion of sugar beet (Beta vulgaris L.) by endophytic bacteria. Photosynthesis Research, 105, 5–13. https://doi.org/10.1007/
s11120-010-9547-7
Sinegovskaya, V. T., Xiaomei, J., & Sukhorukov, V. P.
(2009). Photosynthesis activation and soybean yield with the integrated use of sodium humate.
Bulletin of Altai State Agrarian University, 10(60), 31–35 (in Russian). Retrieved from https://www.
elibrary.ru/item.asp?id=12864716
Stefan, M., Munteanu, N., Stoleru, V., Mihasan, M., &
Hritcu, L. (2013). Seed inoculation with plant growth promoting rhizobacteria enhances photosynthesis and yield of runner bean (Phaseolus coccineus L.). Scientia Horticulturae, 151, 22–29. https://doi.org/10.1016/j.
scienta.2012.12.006
Titova, J. A., Novikova, I. I., Boykova, I. V., Pavlyushin, V. A., & Krasnobaeva, I. L. (2019). Novel solid- phase multibiorecycled biologics based on Bacillus subtilis and Trichoderma asperellum as effective potato protectants against Phytophthora disease. Agricultural Biology, 54(5), 1002–1013. https://doi.org/10.15389/
agrobiology.2019.5.1002eng
Vorob’yev, V. N., Nevmerzhitskaya, U. U., Khusnetdinova, L. Z., & Yakushenkova, T. P. (2013). Workshop
on plant physiology: teaching aid. Kazan: Kazan University (in Russian). Retrieved from https://
kpfu.ru/portal/docs/F1311509096/Praktikum.
po.fiziologii.rastenij.pdf
Zavalin, A. A., Chebotar‘, V. K., Aritkin, A. G., & Smetov, D. B. (2012). Biologization of mineral fertilizers as a way to increase the efficiency of their use.
Dostizheniye nauki i tekhniki APK, 8, 45–47 (in Russian). Retrieved from http://bisolbiplus.ru/
docs/34.pdf
Zhang, H., Xie, X., Kim, M.‐S., Kornyeyev, D. A., Holaday, S., & Paré, P. W. (2008). Soil bacteria augment Arabidopsis photosynthesis by decreasing glucose sensing and abscisic acid levels in planta. The Plant Journal, 56(2), 264–273 https://
doi.org/10.1111/j.1365-313X.2008.03593.x Zou, C., Li, Z., & Yu, D. (2010). Bacillus megaterium strain
XTBG34 promotes plant growth by producing 2-pentylfuran. The Journal of Microbiology, 48, 460–466. https://doi.org/10.1007/s12275-010- 0068-z