Affiliation
a Кемеровский государственный университет, Кемерово
Copyright ©Faskhutdinova et al. This is an open access article distributed under the terms of the Creative Commons Attribution 4.0. (
http://creativecommons.org/licenses/by/4.0/), allowing third parties to copy and redistribute the material in any medium or format and to remix, transform, and build upon the material for any purpose, even commercially, provided the original work is properly cited and states its license.
Abstract
Increasing the yield of wheat, barley, and oats is a pressing issue. It largely depends on soil fertility. Mineral fertilizers, however, may be ineffective and unsustainable. As a result, microorganisms seem to be a promising alternative. The authors isolated endophytic microorganisms with growth-stimulating properties and assessed their effect on the growth rate of wheat, barley, and oats in laboratory conditions.
The research involved spring soft wheat of the Sibirsky Alyans variety, spring oats of the Maruchak variety, spring barley of the Nikita variety, and standard bacterial strains (Azospirillum brasilense B-11094, Azotobacter chrococcum B-8739). The isolated bacteria were identified using a Vitex 2 Compact automatic microbiological analyzer. The production potential for indole-3-acetic and gibberellic acids was assessed spectrophotometrically. The nitrogen fixation potential was determined using a Rapid N Cube. The phosphate-solubilizing potential was tested on a calcium phosphate medium. The effect of the most promising strains on the growth rate was assessed in laboratory conditions.
Seven isolates of endophytic microorganisms were identified as Pantoea allii Tri, Bacillus subtilis Tri 2, Bacillus subtilis Ave 1, Pantoea allii Ave 2, Bacillus subtilis Hor 1, Bacillus subtilis Hor 2, and Bacillus subtilis Hor 3. The most promising growth promoters ranged as follows. Bacillus subtilis Ave 1 fixed 790 μg/mL nitrogen, solubilized phosphates with index 1.60, and produced 7100 μg/mL indolyl-3-acetic acid and 343 μg/mL gibberellic acid. Bacillus subtilis Hor 1 fixed 760 μg/mL nitrogen, solubilized phosphates with index 1.44, and synthesized 4490 μg/mL indolyl-3-acetic acid and 409 μg/mL gibberellic acid. Bacillus subtilis Ave 1 demonstrated the greatest growth-stimulating activity.
Bacillus subtilis Ave 1 could synthesize phytohormones, fix atmospheric nitrogen, and solubilize phosphates, which indicated good agricultural prospects. The strain increased the length of shoots and roots in wheat and barley, as well as boosted germination and shoot length in oats.
Keywords
Oats,
wheat,
barley,
endophytic microorganisms,
Bacillus,
Pantoea,
Azotobacter,
Azospirillum
REFERENCES
- Kachutova AA. Efficiency of grain production – basis of food safety of the country. Bulletin of NGIEI. 2013;(3):76–88. (In Russ.).
- Albahri G, Alyamani AA, Badran A, Hijazi A, Nasser M, Maresca M, et al. Enhancing essential grains yield for sustainable food security and bio-safe agriculture through latest innovative approaches. Agronomy. 2023;13(7):1709. https:// doi.org/10.3390/agronomy13071709
- Serazetdinova Y, Borodina E, Kolpakova D, Frolova A, Fotina N, Tikhonov S, et al. The biopotential of extremophilic microorganisms isolated from Kuzbass for protection and growth stimulation of oat (Avena sativa L.). BIO Web of Conferences. 2024;82:03009. https://doi.org/10.1051/bioconf/20248203009
- Sullivan P, Arendt E, Gallagher E. The increasing use of barley and barley by-products in the production of healthier baked goods. Trends in Food Science and Technology. 2013;29(2):124–134. https://doi.org/10.1016/j.tifs.2012.10.005
- Langridge P. Economic and academic importance of barley. In: Stein N, Muehlbauer GJ, editors. The Barley Genome. Cham: Springer International Publishing; 2018. pp. 1–10. https://doi.org/10.1007/978-3-319-92528-8_1
- Kolmanič A, Sinkovič L, Nečemer M, Ogrinc N, Meglič V. The effect of cultivation practices on agronomic performance, elemental composition and isotopic signature of spring Oat (Avena sativa L.). Plants. 2022;11(2):169. https://doi.org/ 10.3390/plants11020169
- FAOSTAT [Internet]. [cited 2024 Jun 5]. Available from: http://www.fao.org/faostat/en/#data/QCL
- Daniel AI, Fadaka AO, Gokul A, Bakare OO, Aina O, Fisher S, et al. Biofertilizer: The future of food security and food safety. Microorganisms. 2022;10(6):1220. https://doi.org/10.3390/microorganisms10061220
- Prosekov AYu. Modern aspects of food production. Kemerovo: Kemerovo Technological Institute of Food Industry, 2005. 380 p. (In Russ.). https://elibrary.ru/ZRZGCT
- Abebe TG, Tamtam MR, Abebe AA, Abtemariam KA, Shigut TG, Dejen YA, et al. Growing use and impacts of chemical fertilizers and assessing alternative organic fertilizer sources in Ethiopia. Applied and Environmental Soil Science. 2022;2022(1):1–14. https://doi.org/10.1155/2022/4738416
- Yurina TA, Tkalenko AE. Review of innovative drugs for biologization of agricultural production. AgroForum. 2020;(1):51–53. (In Russ.).https://elibrary.ru/WLIKOC
- Kumar R, Kumawat N, Sahu YK. Role of biofertilizers in agriculture. Popular Kheti. 2017;5(4):63–66.
- Mahmud AA, Upadhyay SK, Srivastava AK, Bhojiya AA. Biofertilizers: A nexus between soil fertility and crop productivity under abiotic stress. Current Research in Environmental Sustainability. 2021;3:100063. https://doi.org/10.1016/ j.crsust.2021.100063
- Chaudhary P, Agri U, Chaudhary A, Kumar A, Kumar G. Endophytes and their potential in biotic stress management and crop production. Frontiers in Microbiology. 2022;13:933017. https://doi.org/10.3389/fmicb.2022.933017
- Liu H, Carvalhais LC, Crawford M, Singh E, Dennis PG, Pieterse CMJ, et al. Inner plant values: diversity, colonization and benefits from endophytic bacteria. Frontiers in Microbiology. 2017;8:2552. https://doi.org/10.3389/fmicb.2017.02552
- Milentyeva IS, Fotina NV, Zharko MYu, Proskuryakova LA. Microbial treatment and oxidative stress in agricultural plants. Food Processing: Techniques and Technology. 2022;52(4):750–61. https://doi.org/10.21603/2074-9414-2022-4-2403
- Asyakina LK, Vorob’eva EE, Proskuryakova LA, Zharko MYu. Evaluating extremophilic microorganisms in industrial regions. Foods and Raw Materials. 2023:11(1)162–71. https://doi.org/10.21603/2308-4057-2023-1-556
- Backer R, Rokem JS, Ilangumaran G, Lamont J, Praslickova D, Ricci E, et al. Plant growth-promoting rhizobacteria: context, mechanisms of action, and roadmap to commercialization of biostimulants for sustainable agriculture. Frontiers in Plant Science. 2018;9:1473. https://doi.org/10.3389/fpls.2018.01473
- Mahanty T, Bhattacharjee S, Goswami M, Bhattacharyya P, Das B, Ghosh A, et al. Biofertilizers: a potential approach for sustainable agriculture development. Environmental Science and Pollution Research. 2017;24:3315–3335. https:// doi.org/10.1007/s11356-016-8104-0
- Steenhoudt O, Vanderleyden J. Azospirillum, a free-living nitrogen-fixing bacterium closely associated with grasses: genetic, biochemical and ecological aspects. FEMS Microbiology Reviews. 2000;24(4):487–506. https://doi.org/10.1111/ j.1574-6976.2000.tb00552.x
- Iqbal R, Valipour M, Ali B, Zulfiqar U, Aziz U, Zaheer MS, et al. Maximizing wheat yield through soil quality enhancement: A combined approach with Azospirillum brasilense and bentonite. Plant Stress. 2024;11:100321. https://doi.org/ 10.1016/j.stress.2023.100321
- Fukami J, Cerezini P, Hungria M. Azospirillum: benefits that go far beyond biological nitrogen fixation. AMB Express. 2018;8:73. https://doi.org/10.1186/s13568-018-0608-1
- Turan M, Gulluce M, Von Wirén N, Sahin F. Yield promotion and phosphorus solubilization by plant growth–promoting rhizobacteria in extensive wheat production in Turkey. Journal of Plant Nutrition and Soil Science. 2012;175(6):818–826. https://doi.org/10.1002/jpln.201200054
- Aroca R. Plant responses to drought stress: from morphological to molecular features. Heidelberg: Springer; 2012. p. 466. https://doi.org/10.1007/978-3-642-32653-0
- Kızılkaya R. Yield response and nitrogen concentrations of spring wheat (Triticum aestivum) inoculated with Azoto- bacter chroococcum strains. Ecological Engineering. 2008;33(2):150–156. https://doi.org/10.1016/j.ecoleng.2008.02.011
- Dal Cortivo C, Ferrari M, Visioli G, Lauro M, Fornasier F, Barion G, et al. Effects of Seed-Applied Biofertilizers on Rhizosphere Biodiversity and Growth of Common Wheat (Triticum aestivum L.) in the Field. Frontiers in Plant Science. 2020; 11:72. https://doi.org/10.3389/fpls.2020.00072
- Mishra P, Dash D. Rejuvenation of biofertilizer for sustainable agriculture and economic development. Consilience: The Journal of Sustainable Development. 2014;11(1):41–61.
- Das HK. Azotobacters as biofertilizer. Advances in Applied Microbiology. 2019;108:1–43. https://doi.org/10.1016/ bs.aambs.2019.07.001
- Harper SHT, Lynch JM. Effects of Azotobacter chroococcum on barley seed germination and seedling development. Journal of General Microbiology. 1979;112(1):45–51. https://doi.org/10.1099/00221287-112-1-45
- Bageshwar UK, Srivastava M, Pardha-Saradhi P, Paul S, Gothandapani S, Jaat RS, et al. An environmentally friendly engineered Azotobacter Strain that replaces a substantial amount of urea fertilizer while sustaining the same wheat yield. Applied and Environmental Microbiology. 2017;83(15):e00590-17. https://doi.org/10.1128/AEM.00590-17
- Kopylov IP, Spyrydonov VH, Patyka VP. Identification of Azospirillum genus bacteria isolated from the spring wheat root zone. Mikrobiolohichnyi Zhurnal. 2009;71:13–19.
- Ayyaz K, Zaheer A, Rasul G, Mirza MS. Isolation and identification by 16S rRNA sequence analysis of plant growth-promoting azospirilla from the rhizosphere of wheat. Brazilian Journal of Microbiology. 2016;47(3):542–550. https:// doi.org/10.1016/j.bjm.2015.11.035
- Camilios-Neto D, Bonato P, Wassem R, Tadra-Sfeir MZ, Brusamarello-Santos LC, Valdameri G, et al. Dual RNA- seq transcriptional analysis of wheat roots colonized by Azospirillum brasilense reveals up-regulation of nutrient acquisition and cell cycle genes. BMC Genomics. 2014;15:378. https://doi.org/10.1186/1471-2164-15-378
- Kumar V, Narula N. Solubilization of inorganic phosphates and growth emergence of wheat as affected by Azotobacter chroococcum mutants. Biology and Fertility of Soils. 1999;28:301–305. https://doi.org/10.1007/s003740050497
- Iqbal Z, Ahmad M, Raza MA, Hilger T, Rasche F. Phosphate-Solubilizing Bacillus sp. Modulate Soil Exoenzyme Activities and Improve Wheat Growth. Microbial Ecology. 2024;87:31. https://doi.org/10.1007/s00248-023-02340-5
- Iqbal Z, Ahmad M, Jamil M, Akhtar MFUZ. Appraising the potential of integrated use of Bacillus strains for improving wheat growth. International Journal of Agriculture and Biology. 2020;24:1439‒1448.
- Kaur T, Devi R, Kumar S, Sheikh I, Kour D, Yadav AN. Microbial consortium with nitrogen fixing and mineral solubilizing attributes for growth of barley (Hordeum vulgare L.). Heliyon. 2022;8(4):e09326. https://doi.org/10.1016/ j.heliyon.2022.e09326
- Pang F, Tao A, Ayra-Pardo C, Wang T, Yu Z, Huang S. Plant organ- and growth stage-diversity of endophytic bacteria with potential as biofertilisers isolated from wheat (Triticum aestivum L.). BMC Plant Biology. 2022;22:276. https:// doi.org/10.1186/s12870-022-03615-8
- Da Silva MF, De Souza Antônio C, De Oliveira PJ, Xavier GR, Rumjanek NG, De Barros Soares LH, et al. Survival of endophytic bacteria in polymer-based inoculants and efficiency of their application to sugarcane. Plant Soil. 2012;356:231–243. https://doi.org/10.1007/s11104-012-1242-3
- Cavalcante VA, Dobereiner J. A new acid-tolerant nitrogen-fixing bacterium associated with sugarcane. Plant Soil. 1988;108:23–31. https://doi.org/10.1007/BF02370096
- Tarrand JJ, Krieg NR, Döbereiner J. A taxonomic study of the Spirillum lipoferum group, with descriptions of a new genus, Azospirillum gen. nov. and two species, Azospirillum lipoferum (Beijerinck) comb. nov. and Azospirillum brasilense sp. nov. Canadian Journal of Microbiology. 1978;24:967–980. https://doi.org/10.1139/m78-160
- Wisniewski-Dyé F, Borziak K, Khalsa-Moyers G, Alexandre G, Sukharnikov LO, Wuichet K, et al. Azospirillum Genomes Reveal Transition of Bacteria from Aquatic to Terrestrial Environments. PLoS Genetics. 2011;7(12):e1002430. https:// doi.org/10.1371/journal.pgen.1002430
- Khammas KM, Ageron E, Grimont PAD, Kaiser P. Azospirillum irakense sp. nov., a nitrogen-fixing bacterium associated with rice roots and rhizosphere soil. Research in Microbiology. 1989;140(9):679–693. https://doi.org/10.1016/0923- 2508(89)90199-X
- Baldani VLD, Alvarez MADB, Baldani JI, Döbereiner J. Establishment of inoculated Azospirillum spp. in the rhizosphere and in roots of field grown wheat and sorghum. Plant and Soil. 1986;90:35–46. https://doi.org/10.1007/BF02277385
- Bhatia R, Ruppel S, Narula N. Diversity studies of Azotobacter spp. from cotton‐wheat cropping systems of India. Journal of Basic Microbiology. 2008;48(6):455–463. https://doi.org/10.1002/jobm.200800059
- Kumawat KC, Razdan N, Saharan K. Rhizospheric microbiome: Bio-based emerging strategies for sustainable agriculture development and future perspectives. Microbiological Research. 2022;254:126901. https://doi.org/10.1016/j.micres. 2021.126901
- Li H, Parmar S, Sharma VK, White JF. Seed endophytes and their potential applications. In: Verma SK, White, Jr JF, editors. Seed Endophytes. Cham: Springer International Publishing; 2019. pp. 35–54. https://doi.org/10.1007/978- 3-030-10504-43
- Sa R, He S, Han D, Liu M, Yu Y, Shang R, et al. Isolation and identification of a new biocontrol bacteria against Salvia miltiorrhiza root rot and optimization of culture conditions for antifungal substance production using response surface methodology. BMC Microbiology. 2022;22:231. https://doi.org/10.1186/s12866-022-02628-5
- Amna, Ud Din B, Sarfraz S, Xia Y, Kamran MA, Javed MT, et al. Mechanistic elucidation of germination potential and growth of wheat inoculated with exopolysaccharide and ACC- deaminase producing Bacillus strains under induced salinity stress. Ecotoxicology and Environmental Safety. 2019;183:109466. https://doi.org/10.1016/j.ecoenv.2019.109466
- Masi C, Tebiso A, Selva Kumar KV. Isolation and characterization of potential multiple extracellular enzymeproducing bacteria from waste dumping area in Addis Ababa. Heliyon. 2023;9(2):e12645. https://doi.org/10.1016/j.heliyon. 2022.e12645
- Wu SC, Gao J-K, Chang B-S. Isolation of lindane- and endosulfan-degrading bacteria and dominance analysis in the microbial communities by culture-dependent and independent methods. Microbiological Research. 2021;251:126817. https://doi.org/10.1016/j.micres.2021.126817
- Borodina E, Asyakina L, Proskuryakova L, Osintseva M, Milentyeva I, Prosekov A. The potential of using plantgrowth-stimulating bacteria in phytoremediation of coal dumps. BIO Web of Conferences. 2024;82:06011. https://doi.org/10.1051/ bioconf/20248206011
- Medfu Tarekegn M, Zewdu Salilih F, Ishetu AI. Microbes used as a tool for bioremediation of heavy metal from the environment. Cogent Food and Agriculture. 2020;6(1):1783174. https://doi.org/10.1080/23311932.2020.1783174
- Atuchin VV, Asyakina LK, Serazetdinova YuR, Frolova AS, Velichkovich NS, Prosekov AYu. Microorganisms for bioremediation of soils contaminated with heavy metals. Microorganisms. 2023;11(4):864. https://doi.org/10.3390/ microorganisms11040864
- Asyakina LK, Mudgal G, Tikhonov SL, Larichev TA, Fotina NV, Prosekov AYu. Study of the potential of natural microbiota of spring soft wheat to increase yield. Achievements of Science and Technology in Agro-Industrial Complex. 2023;37(11):12–17. (In Russ.). https:// elibrary.ru/HXXGEC
- Serazetdinova YuR, Fotina NV, Asyakina LK, Milentyeva IS. Prosekov AYu. Rhizobacteria for Reducing Biotic Stress in Spring Wheat (Triticum aestivum L.) Caused by Phytopathogenic Fungi. Storage and Processing of Farm Products. 2023;(4):98–113. (In Russ.). https://elibrary.ru/JTKRHL
- Asyakina LK, Isachkova AO, Kolpakova DE, Borodina EE, Boger VYu, Prosekov AYu. The effect of a microbial consortium on spring barley growth and development in the Kemerovo region, Kuzbass. Grain Economy of Russia. 2024; 16(1):104–112. (In Russ.). https://doi.org/10.31367/2079-8725-2024-90-1-104-112
- Fotina NV, Serazetdinova YuR, Kolpakova DE, Asyakina LK, Atuchin VV, Alotaibi KM, et al. Enhancement of wheat growth by plant growth-stimulating bacteria during phytopathogenic inhibition. Biocatalysis and Agricultural Biotechnology. 2024;60:103294. https://doi.org/10.1016/j.bcab.2024.103294
- Faskhutdinova ER, Fotina NV, Neverova OA, Golubtsova YuV, Mudgal G, Asyakina LK, et al. Extremophilic bacteria as biofertilizer for agricultural wheat. Foods and Raw Materials. 2024;12(2):348–360. https://doi.org/10.21603/2308- 4057-2024-2-613
- Albassam M, Aslam M. Testing Internal Quality Control of Clinical Laboratory Data Using Paired t-Test under Uncertainty. BioMed Research International. 2021:5527845. https://doi.org/10.1155%2F2021%2F5527845
- Singh RK, Singh P, Guo D-J, Sharma A, Li D-P, Li X, et al. Root-Derived Endophytic Diazotrophic Bacteria Pantoea cypripedii AF1 and Kosakonia arachidis EF1 Promote Nitrogen Assimilation and Growth in Sugarcane. Frontiers in Microbiology. 2021;12:774707. https://doi.org/10.3389/fmicb.2021.774707
- Ma Q, He S, Wang X, Rengel Z, Chen L, Wang X, et al. Isolation and characterization of phosphate-solubilizing bacterium Pantoea rhizosphaerae sp. nov. from Acer truncatum rhizosphere soil and its effect on Acer truncatum growth. Frontiers in Plant Science. 2023;14:1218445. https://doi.org/10.3389/fpls.2023.1218445
- Rfaki A, Zennouhi O, Aliyat FZ, Nassiri L, Ibijbijen J. Isolation, selection and characterization of root-associated rock phosphate solubilizing bacteria in moroccan wheat (Triticum aestivum L.). Geomicrobiology Journal. 2020;37(3):230–241. https://doi.org/10.1080/01490451.2019.1694106
- Shao J, Xu Z, Zhang N, Shen Q, Zhang R. Contribution of indole-3-acetic acid in the plant growth promotion by the rhizospheric strain Bacillus amyloliquefaciens SQR9. Biology and Fertility of Soils. 2015;51:321–330. https://doi.org/ 10.1007/s00374-014-0978-8
- Özdal M, Gür Özdal Ö, Sezen A, Algur ÖF. Biosynthesis of indole-3-acetic acid by Bacillus cereus Immobilized Cells. Cumhuriyet Science Journal. 2016;37(3):212. https://doi.org/10.17776/csj.34085
- Lee J-C, Whang K-S. Optimization of Indole-3-acetic Acid (IAA) Production by Bacillus megaterium BM5. Korean Journal of Soil Science and Fertilizer. 2016;49(5):461–468. https://doi.org/10.7745/KJSSF.2016.49.5.461
- Rivera D, Mora V, Lopez G, Rosas S, Spaepen S, Vanderleyden J, et al. New insights into indole-3-acetic acid metabolism in Azospirillum brasilense. Journal of Applied Microbiology. 2018;125(6):1774–1785. https://doi.org/10.1111/ jam.14080
- Shokri D, Emtiazi G. Indole-3-Acetic acid (IAA) production in symbiotic and non-symbiotic nitrogen-fixing bacteria and its optimization by taguchi design. Current Microbiology. 2010;61:217–25. https://doi.org/10.1007/s00284-010-9600-y
- Lv L, Luo J, Ahmed T, Zaki HEM, Tian Y, Shahid MS, et al. Beneficial effect and Potential risk of Pantoea on rice production. Plants. 2022;11(19):2608. https://doi.org/10.3390/plants11192608
- Lenin G, Jayanthi M. Indole Acetic Acid, Gibberellic Acid and Siderophore Production by PGPR Isolates from Rhizospheric Soils of Catharanthus roseus. International Journal of Pharmaceutical and Biological Archives. 2012;3(4):933–938
- Dahiya A, Sharma R, Sindhu S, Sindhu SS. Resource partitioning in the rhizosphere by inoculated Bacillus spp. towards growth stimulation of wheat and suppression of wild oat (Avena fatua L.) weed. Physiology and Molecular Biology of Plants. 2019;25:1483–1495. https://doi.org/10.1007/s12298-019-00710-3
- Platonov AV, Rassokhina II, Laptev GY, Bolshakov VN. Preparations Use Based on Bacteria of the Genus Bacillus to Increase the Yield of Oats (Avena sativa L.). AGRIVITA Journal of Agricultural Science. 2023;45(1):48–55. https:// doi.org/10.17503/agrivita.v45i1.3757
- Mohan V, Devi KS, Anushya A, Revathy G, Viji Kuzhalvaimozhi G, Vijayalakshmi KS. Screening of Salt Tolerant and Growth Promotion Efficacy of Phosphate Solubilizing Bacteria. Journal of Academia and Industrial Research. 2017;5(12):168–172.
- Kumari S, Kumar P, Kiran S, Kumari S, Singh A. Characterization of culture condition dependent, growth responses of phosphate solubilizing bacteria (Bacillus subtilis DR2) on plant growth promotion of Hordeum vulgare. Vegetos. 2023;37:266–276. https://doi.org/10.1007/s42535-023-00589-2