Multi-Level Assessment of Environmental Effects on Winter Wheat
Keywords:
winter wheat, abiotic stress, miRNAs markers, production, NDVIAbstract
This study aimed to evaluate the variability in agronomic performance and physiological and molecular markers indicative of genomic responses in the winter wheat (Triticum aestivum L.) exposed to a gradient of environmental radiation. Field analyses and plant sampling were conducted at two locations situated 500 m and 1000 m from a nuclear power station (NPS). Parameters assessed included the normalized difference vegetation index (NDVI), plant density, spike number per plant, grain number per spike, thousand grain weight, and overall grain yield. NDVI values exhibited a declining trend from growth stage of Biologische Bundesanstalt, Bundessortenamt und CHemische Industrie (BBCH) 32 to BBCH 51 at both sites. Notably, a marked increase in NDVI was observed at BBCH 59 and the onset of flowering (BBCH 61). Vegetation indices and yield-related traits were consistently higher at the site located further from the radiation source. Genomic analysis of stress-sensitive markers revealed elevated amplification of miR168-based loci during early developmental stages regardless of the distance of the cultivation location. On the other hand, elevated amplification of miR408-based loci was observed during the transition to flowering and flowering stage. This corresponds with observations of agronomic and physiological indicators, as well as background radiation records. Multivariate correlation showed that miR168-based loci of 150 base pairs (bp) or 200 bp, respectively and miR408-based locus of 150 bp have moderate to strong non-linear relationship to developmental stage and growth location. These findings suggest that early growth stages of winter wheat are particularly sensitive to environmental stress, as reflected in both NDVI metrics and microRNA-based (miRNA) markers. The integration of agronomic, physiological and molecular analyses provides a robust framework for assessing crop responses to radiation-induced stress gradients.
References
Agarwal, R., Rane, S. S., & Sainis, J. K. (2008). Effects of 60Co γ radiation on thylakoid membrane functions in Anacystis nidulans. Journal of Photochemistry and Photobiology B: Biology, 91(1), 9–19. https://doi.org/10.1016/j.jphotobiol.2008.01.006
Alikamanoğlu, S., Yaycili, O., & Sen, A. (2011). Effect of gamma radiation on growth factors, biochemical parameters, and accumulation of trace elements in soybean plants (Glycine max L. Merrill). Biological Trace Element Research, 141, 283–293. https://doi.org/10.1007/s12011-010-8709-y
Bej, S., & Basak, J. (2014). MicroRNAs: The potential biomarkers in plant stress response. American Journal of Plant Sciences, 5(6), 748–759. https://doi.org/10.4236/ajps.2014.55089
BPEJ – Bonitated Soil-Ecological Units. (2019). Soil maps. Retrieved February 15, 2026, from http://www.podnemapy.sk/portal/verejnost/bpej/bpej.aspx
Caussade Semences. (2024). Sofolk CS. Retrieved February 15, 2026, from https://caussade-osiva.cz/obilovina/solfolk-cs/
Cuperus, J. T., Fahlgren, N., & Carrington, J. C. (2011). Evolution and functional diversification of MIRNA genes. The Plant Cell, 23(2), 431–442. https://doi.org/10.1105/tpc.110.082784
De Micco, V., Arena, C., Pignalosa, D., & Durante, M. (2011). Effects of sparsely and densely ionizing radiation on plants. Radiation and Environmental Biophysics, 50(1), 1–19. https://doi.org/10.1007/s00411-010-0343-8
Ernst, D., Kolenčík, M., Šebesta, M., Ďurišová, Ľ., Kšiňan, S., Tomovičová, L., Kotlárová, N., Kalúzová, M., Černý, I., Kratošová, G., Žitniak Čurná, V., Ivanič Porhajašová, J., Babošová, M., Dobročka, E., Qian, Y., Swamiappan, S., Illa, R., Gayathri Radhakrishnan, S., Sunil, B. R., & Ducsay, L. (2023). Significance of phosphate nano-fertilizers foliar application: A brief real-field study of quantitative, physiological parameters, and agro-ecological diversity in sunflower. Agronomy, 13(10), Article 2606. https://doi.org/10.3390/agronomy13102606
Ferrante, A., Cartelle, J., Savin, R., & Slafer, G. A. (2017). Yield determination, interplay between major components and yield stability in a traditional and a contemporary wheat across a wide range of environments. Field Crops Research, 203, 114–127. https://doi.org/10.1016/j.fcr.2016.12.028
Fu, D., Ma, B., Mason, A. S., et al. (2013). MicroRNA-based molecular markers: A novel PCR-based genotyping technique in Brassica species. Plant Breeding, 132(4), 375–381. https://doi.org/10.1111/pbr.12069
Gudkov, S. V., Grinberg, M., Sukhov, V. S., & Vodeneev, V. (2019). Effect of ionizing radiation on physiological and molecular processes in plants. Journal of Environmental Radioactivity, 202, 8–24. https://doi.org/10.1016/j.jenvrad.2019.02.001
Hajyzadeh, M., Turktas, M., Khawar, K. M., & Unver, T. (2015). miR408 overexpression causes increased drought tolerance in chickpea. Gene, 555(2), 186–193. https://doi.org/10.1016/j.gene.2014.11.002
Han, B., Gu, J., Zhao, L., Guo, H., Xie, Y., Zhao, S., Song, X., Han, L., & Liu, L. (2016). Factors affecting the radiosensitivity of hexaploid wheat to γ-irradiation. PLOS ONE, 11(8), Article e0161700. https://doi.org/10.1371/journal.pone.0161700
Hasanuzzaman, M., Nahar, K., & Hossain, M. A. (Eds.). (2019). Wheat production in changing environments: Responses, adaptation and tolerance. Springer. https://doi.org/10.1007/978-981-13-6883-7
Igrejas, G., & Branlard, G. (2020). The importance of wheat. In G. Igrejas, T. M. Ikeda, & C. Guzmán (Eds.), Wheat quality for improving processing and human health (pp. 1–7). Springer. https://doi.org/10.1007/978-3-030-34163-3_1
Jones, H. G., Serraj, R., Loveys, B. R., Xiong, L., Wheaton, A., & Price, A. H. (2009). Thermal infrared imaging of crop canopies for the remote diagnosis and quantification of plant responses to water stress in the field. Functional Plant Biology, 36(11), 978–989. https://doi.org/10.1071/FP09123
Kantar, M., Lucas, S. J., & Budak, H. (2010). Regulation of barley miRNAs upon dehydration stress correlated with target gene expression. Functional & Integrative Genomics, 10(4), 493–507. https://doi.org/10.1007/s10142-010-0181-4
Kim, J.-H., Moon, Y. R., Lee, M. H., Kim, J. H., Wi, S. G., Park, B.-J., Kim, C. S., & Chung, B. Y. (2011). Photosynthetic capacity of Arabidopsis plants at the reproductive stage tolerates γ irradiation. Journal of Radiation Research, 52(4), 441–449. https://doi.org/10.1269/jrr.10157
Klubicová, K., Danchenko, M., Skultéty, Ľ., Berezhna, V. V., Uvačková, Ľ., Rashydov, N. M., & Hajduch, M. (2012). Soybeans grown in the Chernobyl area produce fertile seeds that have increased heavy metal resistance and modified carbon metabolism. PLOS ONE, 7(10), Article e48169. https://doi.org/10.1371/journal.pone.0048169
Kruszka, K., Pieczyński, M., Windels, D., Bielewicz, D., Jarmołowski, A., & Szweykowska-Kulińska, Z. (2012). Role of microRNAs and other sRNAs of plants in their changing environments. Journal of Plant Physiology, 169(16), 1664–1672. https://doi.org/10.1016/j.jplph.2012.03.009
Mathur, S., Raikalal, P., & Jajoo, A. (2019). Physiological responses of wheat to environmental stresses. In M. Hasanuzzaman, K. Nahar, & M. A. Hossain (Eds.), Wheat production in changing environments: Responses, adaptation and tolerance (pp. 31–61). Springer. https://doi.org/10.1007/978-981-13-6883-7_2
Meier, U. (Ed.). (2001). Growth stages of mono- and dicotyledonous plants: BBCH monograph (2nd ed.). Federal Biological Research Centre for Agriculture and Forestry.
Melnikova, N. V., Dmitriev, A. A., Belenikin, M. S., et al. (2016). Identification, expression analysis, and target prediction of flax genotroph microRNAs under normal and nutrient stress conditions. Frontiers in Plant Science, 7, Article 399. https://doi.org/10.3389/fpls.2016.00399
Melnikova, N. V., Dmitriev, A. A., Belenikin, M. S., Speranskaya, A. S., Krinitsina, A. A., Rachinskaia, O. A., et al. (2015). Excess fertilizer responsive miRNAs revealed in Linum usitatissimum L. Biochimie, 109, 36–41. https://doi.org/10.1016/j.biochi.2014.11.017
Nakanishi, T. M. (2017). Research with radiation and radioisotopes to better understand plant physiology and agricultural consequences of radioactive contamination from the Fukushima Daiichi nuclear accident. Journal of Radioanalytical and Nuclear Chemistry, 311, 947–971. https://doi.org/10.1007/s10967-016-5148-z
Pan, J., Huang, C., Guo, Z., Zhang, H., & Yang, J. (2018). Overexpression of microRNA408 enhances photosynthesis, growth, and seed yield in diverse plants. Journal of Integrative Plant Biology, 60(4), 323–340. https://doi.org/10.1111/jipb.12634
Ražná, K., & Hlavačková, L. (2017). The applicability of genetic markers based on microRNA molecules in agricultural research. Open Access Journal of Agricultural Research, 2(3), Article 000125. https://doi.org/10.23880/OAJAR-16000125
Ražná, K., Khasanova, N., Ivanišová, E., Qahramon, D., & Habán, M. (2018). Antioxidant properties of cumin (Bunium persicum Boiss.) extract and its protective role against ultrasound-induced oxidative stress tested by microRNA-based markers. Potravinárstvo Slovak Journal of Food Sciences, 12(1), 11–19. https://doi.org/10.5219/838
Ražná, K., Žiarovská, J., & Gálová, Z. (2020). MicroRNA-based markers in plant genome response to abiotic stress and their application in plant genotyping. In Non-coding RNAs (pp. 71–81). IntechOpen.
Robles-Zazueta, C. A., Molero, G., Pinto, F., Foulkes, M. J., Reynolds, M. P., & Murchie, E. H. (2021). Field-based remote sensing models predict radiation use efficiency in wheat. Journal of Experimental Botany, 72(10), 3756–3773. https://doi.org/10.1093/jxb/erab115
RWA Slovakia. (2024). Sofolk CS. Retrieved February 15, 2026, from https://www.rwa.sk/pšenica-ozimná+2500++1005243
Satorre, E. H., & Slafer, G. A. (Eds.). (1999). Wheat: Ecology and physiology of yield determination. Food Products Press.
SHMÚ – Slovak Hydrometeorological Institute. (2020). Quantities and units used in radiation protection. https://www.shmu.sk/File/Radioaktivita_1/7_Jednotky_info_web.pdf
SHMÚ – Slovak Hydrometeorological Institute. (2024a). Radioactivity – general information. Retrieved February 15, 2026, from https://www.shmu.sk/sk/?page=240
SHMÚ – Slovak Hydrometeorological Institute. (2024b). Gamma dose equivalent rate – measured quantity. Retrieved February 15, 2026, from https://www.shmu.sk/sk/?page=256
SHMÚ – Slovak Hydrometeorological Institute. (2024c). Hourly averages of the gamma dose equivalent rate in air. Retrieved February 15, 2026, from https://www.shmu.sk/sk/?page=1&id=radioaktivita
Singh, M. (2025). Nuclear and irradiation technology for agriculture sustainability and global food security. Radiation Protection and Environment, 48(2), 63–71. https://doi.org/10.4103/rpe.rpe_7_25
Wu, Y., Chen, Z., Wang, Z., Chen, S., Ge, D., Chen, C., Jia, J., Li, Y., Jin, M., Zhou, T., Wang, F., & Hu, L. (2019). Nuclear safety in the unexpected second nuclear era. Proceedings of the National Academy of Sciences, 116(36), 17673–17682. https://doi.org/10.1073/pnas.1820007116
Xie, Z., Khanna, K., & Ruan, S. (2010). Expression of microRNAs and its regulation in plants. Seminars in Cell & Developmental Biology, 21(8), 790–797. https://doi.org/10.1016/j.semcdb.2010.03.012
Yadav, C., Muthamilarasan, M., Pandey, G., et al. (2014). Development of novel microRNA-based genetic markers in foxtail millet for genotyping applications in related grass species. Molecular Breeding, 34(4), 2219–2224. https://doi.org/10.1007/s11032-014-0137-9
Zhang, B., Pan, X., Cobb, G. P., & Anderson, T. A. (2006). Plant microRNA: A small regulatory molecule with big impact. Developmental Biology, 289(1), 3–16. https://doi.org/10.1016/j.ydbio.2005.10.036
Žiarovská, J., Ražná, K., Urbanová, L., Klongová, L., Kováčik, A., Kučka, M., Harenčár, Ľ., & Zeleňáková, L. (2023). Allergen coding genes and miRNA-based DNA fingerprints in revealing differences among Vaccinium corymbosum L. and Vaccinium myrtillus L. Journal of Central European Agriculture, 24(3), 749–760. https://doi.org/10.5513/JCEA01/24.3.3955
Downloads
Published
Issue
Section
License
Copyright (c) 2026 Katarína Ražná, Dávid Ernst, Dominik Selnekovič, Matúš Kučka, Simona Čerteková, Jit Mukherjee
This work is licensed under a Creative Commons Attribution 4.0 International License.
