Enhancing sugar beet yield and soil microbial activity under water-limited conditions through mycorrhizal and bacterial inoculations

Abstract

Aim of this study is to investigate the effects of mycorrhizal and bacterial inoculations on sugar beet yield and soil microbial activity under varying water stress conditions. The field experiment was conducted over two successive years with three different irrigation levels: 33% (I1), 66% (I2), and 100% (I3). Mycorrhiza (Mikostar BTH-100) containing Glomus intraradices, Glomus mosseae, Glomus fasciculatum, and Glomus etunicatum, along with Bradyrhizobium japonicum bacteria, were applied to seeds during planting. Results showed that both applications significantly improved sugar beet yield and soil microbial activity compared to the control treatment. Mycorrhiza was particularly effective under full irrigation (I3), while bacterial inoculations showed stronger effects under moderate and low irrigation levels (I2 and I1, respectively). The highest yield (10130 kg/da) was observed under full irrigation with mycorrhiza treatment, while the lowest yield (3917.33 kg/da) was recorded in the control group under low irrigation. Soil microbial analyses revealed significant enhancements in CO₂ respiration, dehydrogenase activity (DHA), and microbial biomass carbon (MBC) in treated soils. These findings highlight the potential of mycorrhiza and bacteria to enhance plant performance and soil health under water-limited conditions, contributing to sustainable agricultural practices.

Keywords

• Sugar beet
• Mycorrhizae
• Bacterium
• Water stress

Mikoriza ve bakteri uygulamalarının su stres koşulları altında şekerpancarı verimi ve toprak mikrobiyal aktivitesine etkisi

Öz

Bu çalışmanın amacı, farklı su stres koşulları altında mikoriza ve bakteri uygulamalarının şekerpancarı verimi ve toprak mikrobiyal aktivitesi üzerindeki etkilerini araştırmaktadır. Deneme, iki yıl boyunca arazi koşullarında ve üç farklı sulama düzeyinde (I₁: %33, I₂: %66, I₃: %100) yürütülmüştür. Bradyrhizobium japonicum bakterileri ile birlikte Glomus intraradices, Glomus mosseae, Glomus fasciculatum ve Glomus etunicatum içeren Mycorrhiza (Mikostar BTH-100) ekim sırasında tohumlara uygulandı. Elde edilen sonuçlar, her iki uygulamanın da kontrole kıyasla şeker pancarı verimini ve toprak mikrobiyal aktivitesini önemli ölçüde geliştirdiğini gösterdi. Mikoriza özellikle tam sulama (I3) altında etkili iken, bakteriyel aşılamalar orta ve düşük sulama seviyeleri altında daha güçlü etkiler gösterdi (sırasıyla I2 ve I1). En yüksek verim (10130 kg/da) mikoriza tedavisi ile tam sulama altında gözlenirken, en düşük verim (3917.33 kg/da) düşük sulama altında kontrol grubuna kaydedildi. Toprak mikrobiyal analizleri, işlenmiş topraklarda CO₂ solunum, dehidrojenaz aktivitesi (DHA) ve mikrobiyal biyokütle karbonunda (MBC) önemli gelişmeler ortaya koymuştur. Bu bulgular mikoriza ve bakterilerin su sınırlı koşullar altında bitki performansını ve toprak sağlığını artırma potansiyelini vurgulamakta ve sürdürülebilir tarım uygulamalarına katkıda bulunmaktadır.

Anahtar Kelimeler

• Şeker pancarı
• Mikoriza
• Bakteri
• Su stresi

References

1. Begum, N., Wang, L., Ahmad, H., Akhtar, K., Roy, R., Khan, M.I., & Zhao, T. (2022). Co-inoculation of arbuscular mycorrhizal fungi and the plant growth-promoting rhizobacteria improve growth and photosynthesis in tobacco under drought stress by up-regulating antioxidant and mineral nutrition metabolism. Microbial Ecology, 1-18. https://doi.org/10.1007/s00248-021-01815-7
2. Behrooz, A., Vahdati, K., Rejali, F., Lotfi, M., Sarikhani, S., & Leslie, C. (2019). Arbuscular mycorrhiza and plant growth-promoting bacteria alleviate drought stress in walnut. HortScience, 54 (6), 1087-1092. https://doi.org/10.21273/HORTSCI13961-19
3. Bender, S.F., Wagg, C., & van der Heijden, M.G. (2016). An underground revolution: biodiversity and soil ecological engineering for agricultural sustainability. Trends in Ecology & Evolution, 31 (6), 440-452. 10.1016/j.tree.2016.02.016
4. Bhattacharyya, P.N., & Jha, D.K. (2012). Plant growth-promoting rhizobacteria (PGPR): Emergence in agriculture. World Journal of Microbiology and Biotechnology, 28, 1327-1350. https://doi.org/10.1007/s11274-011-0979-9
5. Braghiere, R.K., Fisher, J.B., Fisher, R.A., Shi, M., Steidinger, B.S., Sulman, B. N., ... & Phillips, R. P. (2021). Mycorrhizal distributions impact global patterns of carbon and nutrient cycling. Geophysical Research Letters, 48 (19), e2021GL094514. https://doi.org/10.1029/2021GL094514
6. Bogati, K., & Walczak, M. (2022). The impact of drought stress on soil microbial community, enzyme activities and plants. Agronomy, 12 (1), 189. https://doi.org/10.3390/agronomy12010189
7. Bojović, R., Popović, V., Popović, D., Prodanović, R., Đukić, R., Bošković, J., ... & Filipović, V. (2024). Economical sugar beet production: Biotechnological advances to ımprove yield in conditions of abiotic and biotic stress. Sugar Tech, 1-17. https://doi.org/10.1007/s12355-024-01461-6
8. Chang, C., Nasir, F., Ma, L., & Tian, C. (2017). Molecular communication and nutrient transfer of arbuscular mycorrhizal fungi, symbiotic nitrogen-fixing bacteria, and host plant in tripartite symbiosis. Legume Nitrogen Fixation in Soils with Low Phosphorus Availability: Adaptation and Regulatory Implication, 169-183. https://doi.org/10.1007/978-3-319-55729-8_9

9. Cao, M.A., Wang, P., Hashem, A., Wirth, S., Abd_Allah, E.F., & Wu, Q.S. (2021). Field inoculation of arbuscular mycorrhizal fungi improves fruit quality and root physiological activity of citrus. Agriculture, 11 (12), 1297. https://doi.org/10.3390/agriculture11121297
10. Çağlar, K.Ö. (1949). Toprak bilgisi. A.Ü. Zir. Fak. Yayınları:10, s 230.
11. Dinç, U., Şenol, S., Sayın, M., Kapur, S., Güzel, N., Derici, R., … Kara, E.E. (1988). Güneydoğu Anadolu Bölgesi Toprakları. (GAT): I. Harran Ovası. TÜBİTAK Tarım ve Ormancılık Araştırma Grubu Güdümlü Araştırma Projesi Kesin Raporu. Proje No: TOAG-534, Adana.
12. Drigo, B., Kowalchuk, G.A., & Van Veen, J.A. (2008). Climate change goes underground: effects of elevated atmospheric CO 2 on microbial community structure and activities in the rhizosphere. Biology and Fertility of Soils, 44, 667-679. https://doi.org/10.1007/s00374-008-0277-3
13. Ermiş, O. (1998). Bazı şeker pancarı (Beta vulgaris L.) çeşitlerinde seyreltme ve sıra üzerine mesafelerin verim ve kaliteye etkisi, Doktora Tezi, Yüzüncü Yıl Üniversitesi, Fen Bilimleri Enstitüsü, Van, 21-22.
14. Farooq, M., Hussain, M., Ul-Allah, S., & Siddique, K.H. (2019). Physiological and agronomic approaches for improving water-use efficiency in crop plants. Agricultural Water Management, 219, 95-108. https://doi.org/10.1016/j.agwat.2019.04.010Get rights and content
15. Ghimire, R., Thapa, V.R., Acosta-Martinez, V., Schipanski, M., Slaughter, L.C., Fonte, S.J., ... & Noble Strohm, T. (2023). Soil health assessment and management framework for water-limited environments: examples from the Great Plains of the USA. Soil Systems, 7 (1), 22. https://doi.org/10.3390/soilsystems7010022
16. Hartmann, M., Frey, B., Mayer, J., Mäder, P., & Widmer, F. (2015). Distinct soil microbial diversity under long-term organic and conventional farming. The ISME Journal, 9 (5), 1177-1194. https://doi.org/10.1038/ismej.2014.210
17. Hektaş Tarım (2023). Türkiye’de Şeker Pancarı Hangi Bölgede Yetişir?. Erişim adresi: https://hektas.com.tr/blog/turkiye-de-seker-pancari-hangi-bolgede-yetisir
18. Hu, Y., Chen, J., Olesen, J.E., van Groenigen, K.J., Hui, D., He, X., ... & Deng, Q. (2024). Mycorrhizal association controls soil carbon-degrading enzyme activities and soil carbon dynamics under nitrogen addition: A systematic review. Science of the Total Environment, 175008. https://doi.org/10.1016/j.scitotenv.2024.175008
19. Isermayer, H. (1952). Eine einfache Methode zur Bestimmung der Bodenatmung und der Karbonate im Böden. Z. Pflanzenaehr. Bodenkd, 5, 56-60. https://doi.org/10.1002/jpln.19520560107
20. James, D.W., Hanks, R.J., & Jurınak., J.J. (1982). Modern irrigated soils. Published by John Wiley and Sons Inc. New York USA.
21. Jia, X., Zhong, Y., Liu, J., Zhu, G., Shangguan, Z., & Yan, W. (2020). Effects of nitrogen enrichment on soil microbial characteristics: From biomass to enzyme activities. Geoderma, 366, 114256. https://doi.org/10.1016/j.geoderma.2020.114256
22. Koch, K. (2004). Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development. Current Opinion in Plant Biology, 7 (3), 235-246. https://doi.org/10.1016/j.pbi.2004.03.014
23. Kuzyakov, Y., & Blagodatskaya, E. (2015). Microbial hotspots and hot moments in soil: concept & review. Soil Biology and Biochemistry, 83, 184-199. https://doi.org/10.1016/j.soilbio.2015.01.025
24. Laranjeira, S., Fernandes-Silva, A., Reis, S., Torcato, C., Raimundo, F., Ferreira, L., ... & Marques, G. (2021). Inoculation of plant growth promoting bacteria and arbuscular mycorrhizal fungi improve chickpea performance under water deficit conditions. Applied Soil Ecology, 164, 103927. https://doi.org/10.1016/j.apsoil.2021.103927
25. Mickan, B.S., Abbott, L.K., Solaiman, Z.M., Mathes, F., Siddique, K.H., & Jenkins, S.N. (2019). Soil disturbance and water stress interact to influence arbuscular mycorrhizal fungi, rhizosphere bacteria and potential for N and C cycling in an agricultural soil. Biology and Fertility of Soils, 55, 53-66. https://doi.org/10.1007/s00374-018-1328-z
26. Mickan, B.S., Abbott, L.K., Stefanova, K., & Solaiman, Z.M. (2016). Interactions between biochar and mycorrhizal fungi in a water-stressed agricultural soil. Mycorrhiza, 26 (6), 565-574. https://doi.org/10.1007/s00572-016-0693-4
27. Miransari, M. (2010). Contribution of arbuscular mycorrhizal symbiosis to plant growth under different types of soil stress. Plant Biology, 12 (4), 563-569. https://doi.org/10.1111/j.1438-8677.2009.00308.x
28. Mohamed, H.I., Sofy, M.R., Almoneafy, A.A., Abdelhamid, M.T., Basit, A., Sofy, A.R., ... & Abou-El-Enain, M.M. (2021). Role of microorganisms in managing soil fertility and plant nutrition in sustainable agriculture. Plant Growth-Promoting Microbes for Sustainable Biotic and Abiotic Stress Management, 93-114. https://doi.org/10.1007/978-3-030-66587-6_4
29. Mubarak, M.U., Zahir, M., Ahmad, S., & Wakeel, A. (2016). Sugar beet yield and industrial sugar contents improved by potassium fertilization under scarce and adequate moisture conditions. Journal of Integrative Agriculture, 15 (11), 2620-2626. https://doi.org/10.1016/S2095-3119(15)61252-7
30. Ortiz, N., Armada, E., Duque, E., Roldán, A., & Azcón, R. (2015). Contribution of arbuscular mycorrhizal fungi and/or bacteria to enhancing plant drought tolerance under natural soil conditions: effectiveness of autochthonous or allochthonous strains. Journal of Plant Physiology, 174, 87-96. https://doi.org/10.1016/j.jplph.2014.08.019
31. Öhlinger, R. (1993). Bestimmung des Biomasse-Kohlenstoffs mittels Fumigation-Exstraktion. In:Schinner. F.. Öhlinger. R.. Kandler. E.. Margesin. R. (eds.). Bodenbiologische Arbeits methoden. 2. Auflage. Springer Verlag. Berlin. Heidelberg. https://doi.org/10.1007/978-3-642-77936-7
32. Rahimzadeh, S., & Pirzad, A. (2017). Arbuscular mycorrhizal fungi and Pseudomonas in reduce drought stress damage in flax (Linum usitatissimum L.): A field study. Mycorrhiza, 27, 537-552. https://doi.org/10.1007/s00572-017-0775-y
33. Ranjan, A., Rajput, V.D., Prazdnova, E.V., Gurnani, M., Sharma, S., Bhardwaj, P., ... & Wong, M.H. (2024). Augmenting abiotic stress tolerance and root architecture: The function of phytohormone-producing PGPR and their interaction with nanoparticles. South African Journal of Botany, 167, 612-629. https://doi.org/10.1016/j.sajb.2024.02.041
34. Rawat, P., Shankhdhar, D., & Shankhdhar, S.C. (2020). Plant growth-promoting rhizobacteria: A booster for ameliorating soil health and agriculture production. Soil Health, 47-68. https://doi.org/10.1007/978-3-030-44364-1_3
35. Reinefeld, E., Emmerich, A., Baumgarten, G., Winner, C., & Beiβ, U. (1974). Zur voraussage des melassezuckers aus rübenanalysen. Zucker, 27, 2-15.
36. Rillig, M.C., & Mummey, D.L. (2006). Mycorrhizas and soil structure. New Phytologist, 171 (1), 41-53. https://doi.org/10.1111/j.1469-8137.2006.01750.x
37. Sarma, R.K. (2024). Harnessing the rhizosphere soil microbiome for sustainable agriculture: Recent technological developments and future challenges. In progress in soil microbiome research (pp. 481-500). Cham: Springer Nature Switzerland. https://doi.org/10.1007/978-3-031-71487-0_20
38. Schimel, J. (2023). Modeling ecosystem-scale carbon dynamics in soil: the microbial dimension. Soil Biology and Biochemistry, 178, 108948. https://doi.org/10.1016/j.soilbio.2023.108948
39. Sheteiwy, M.S., Ali, D.F.I., Xiong, Y.C., Brestic, M., Skalicky, M., Hamoud, Y.A., ... & El-Sawah, A.M. (2021). Physiological and biochemical responses of soybean plants inoculated with Arbuscular mycorrhizal fungi and Bradyrhizobium under drought stress. BMC Plant Biology, 21, 1-21. https://doi.org/10.1186/s12870-021-02949-z
40. Silva, A.M.M., Feiler, H.P., Qi, X., de Araújo, V.L.V.P., Lacerda-Júnior, G.V., Fernandes-Júnior, P.I., & Cardoso, E.J.B.N. (2023). Impact of water shortage on soil and plant attributes in the presence of arbuscular mycorrhizal fungi from a harsh environment. Microorganisms, 11 (5), 1144. https://doi.org/10.3390/microorganisms11051144
41. Smith, S.E., & Read, D.J. (2010). Mycorrhizal symbiosis. Academic press.
42. Sun, Y., Wang, C., & Ruan, H. (2022). Increased microbial carbon and nitrogen use efficiencies under drought stress in a poplar plantation. Forest Ecology and Management, 519, 120341. https://doi.org/10.1016/j.foreco.2022.120341
43. Tarım ve Orman Bakanlığı (2023). "Tarımsal ekonomi ve politika geliştirme enstitüsü."
44. Thalman, A. (1967). Über die mikrobielle Aktivitaet und ihre Beziehungen zur Fruchtbarkeitsmerkmalen einiger Ackerböden unter besonderer Berücksichtigung der Dehydrogenase aktivitaet (TTC-Reduktion) Diss. Giessen (FRG).
45. Treseder, K.K., & Lennon, J.T. (2015). Fungal traits that drive ecosystem dynamics on land. Microbiology and Molecular Biology Reviews, 79 (2), 243-262. https://doi.org/10.1128/mmbr.00001-15
46. Ullah, N., Ditta, A., Imtiaz, M., Li, X., Jan, A.U., Mehmood, S., ... & Rizwan, M. (2021). Appraisal for organic amendments and plant growth‐promoting rhizobacteria to enhance crop productivity under drought stress: A review. Journal of Agronomy and Crop Science, 207 (5), 783-802. https://doi.org/10.1111/jac.12502
47. U.S. Salinity Laboratory Staff (1954). Diagnosis and Improvement of Saline and Alkaline Soils, USDA No: 6.
48. Vurukonda, S.S.K.P., Vardharajula, S., Shrivastava, M., & SkZ, A. (2016). Enhancement of drought stress tolerance in crops by plant growth promoting rhizobacteria. Microbiological Research, 184, 13-24. https://doi.org/10.1016/j.micres.2015.12.003
49. Medina, A., & Azcón, R. (2010). Effectiveness of the application of arbuscular mycorrhiza fungi and organic amendments to improve soil quality and plant performance under stress conditions. Journal of Soil Science and Plant Nutrition, 10 (3), 354-372. https://doi.org/10.3390/plants12173102
50. Walkley, A., & Black, I.A. (1934). An examination of the Degtjareff method for determining soil organic matter, and a proposed modification of the chromic acid titration method. Soil Science, 37, 29-38.
51. Wang, R., Sun, Q., Wang, Y., Zheng, W., Yao, L., Hu, Y., & Guo, S. (2018). Contrasting responses of soil respiration and temperature sensitivity to land use types: Cropland vs. apple orchard on the Chinese Loess Plateau. Science of the Total Environment, 621, 425-433. https://doi.org/10.1016/j.scitotenv.2017.11.290
52. Wang, Z.G., Bi, Y.L., Jiang, B., Zhakypbek, Y., Peng, S.P., Liu, W.W., & Liu, H. (2016). Arbuscular mycorrhizal fungi enhance soil carbon sequestration in the coalfields, northwest China. Scientific Reports, 6 (1), 34336. https://doi.org/10.1038/srep34336
53. Wu, Q.S., Huang, Y.M., Li, Y., & He, X.H. (2014). Contribution of arbuscular mycorrhizas to glomalin-related soil protein, soil organic carbon and aggregate stability in citrus rhizosphere. International Journal of Agriculture & Biology, 16 (1).
54. Xu, C., Li, Y., Hu, X., Zang, Q., Zhuang, H., & Huang, L. (2022). The influence of organic and conventional cultivation patterns on physicochemical property, enzyme activity and microbial community characteristics of paddy soil. Agriculture, 12 (1), 121. https://doi.org/10.3390/agriculture12010121
55. Yang, H., Schroeder-Moreno, M., Giri, B., & Hu, S. (2018). Arbuscular mycorrhizal fungi and their responses to nutrient enrichment. Root Biology, 429-449. https://doi.org/10.1007/978-3-319-75910-4_17