Wheat Responses to Abiotic Stresses and Microbiome Dynamics: A Review

Abstract

Wheat (Triticum aestivum) is renowned as one of the world's most crucial cereal crops. Throughout agricultural production, wheat faces multiple stressors, with numerous researchers investigating both these stress factors and the resultant response mechanisms. The main abiotic stress factors that wheat is exposed to include drought, salinity, and temperature. Drought stress negatively affects plant productivity by reducing photosynthetic capacity and increasing water loss. Salinity stress disrupts ion balance, limiting plant growth and nutrient uptake. Heat stress leads to yield loss through protein denaturation and a decline in photosynthetic activity. The responses of wheat to stress conditions are supported by various physiological and biochemical mechanisms. These include an increase in hormones such as abscisic acid (ABA), stomatal closure, and osmotic adjustment mechanisms. Additionally, microbiome dynamics are among the important factors supporting wheat against these stresses. Researchers have reported that rhizobacteria (PGPR) and mycorrhizal fungi enhance nutrient uptake, thereby improving stress tolerance. In this context, the response mechanisms of wheat to stress conditions and microbiome interactions have played a critical role in agricultural productivity. The use of microbial supplements in agricultural production is believed to have the potential to increase wheat productivity. In our study, the detailed mechanisms of these interactions have been presented and examined from a sustainable perspective.

Keywords

• Wheat
• microbiome
• stress

Buğdayın Abiyotik Streslere ve Mikrobiyom Dinamiklerine Yanıtları: Bir Derleme

Abstract

Buğday (Triticum aestivum), küresel ölçekte gıda güvenliğinin sağlanmasında temel bir stratejik ürün konumundadır. Tarımsal üretim sürecinde, özellikle kuraklık, tuzluluk ve yüksek sıcaklık gibi abiyotik stres faktörleri bitkinin büyüme ve verim potansiyelini önemli ölçüde sınırlandırmaktadır. Kuraklık stresi, fotosentetik etkinliği azaltarak ve transpirasyon yoluyla su kaybını artırarak bitki verimliliğini düşürürken; tuzluluk stresi iyon homeostazını bozarak kök gelişimi ve besin alımını olumsuz etkiler. Yüksek sıcaklıklar ise protein denatürasyonu ve fotosentez kapasitesinde azalma gibi etkilerle önemli ölçüde ürün kaybına neden olur. Bu stres koşullarına karşı buğday, abiyotik stres toleransını artıran bir dizi fizyolojik ve biyokimyasal savunma mekanizmasını devreye alır. Abscisik asit (ABA) düzeyindeki artış, stomatal düzenleme ve osmotik ayarlama süreçleri bu adaptif tepkilerin başlıca bileşenlerini oluşturur. Bununla birlikte, bitki kök mikrobiyomu da stres toleransının güçlendirilmesinde tamamlayıcı bir rol üstlenmektedir. Bitki gelişimini destekleyen rizobakteriler (PGPR) ve arbusküler mikorizal mantarlar, su ve besin alımını iyileştirerek bitkinin stres koşullarına daha dayanıklı hale gelmesini sağlar. Mikrobiyal etkileşimlerin tarımsal üretim sistemlerine entegre edilmesi, hem kimyasal girdi bağımlılığının azaltılmasına hem de üretim istikrarının artırılmasına katkı sunabilecek önemli bir strateji olarak değerlendirilmektedir. Bu bağlamda, mikrobiyom temelli yaklaşımlar, buğday üretiminde stres toleransını güçlendiren sürdürülebilir uygulamalar için güçlü bir potansiyel taşımaktadır.

Keywords

• Buğday
• Mikrobiyom
• Stres

References

1. Abid, M., Tian, Z., Ata-Ul-Karim, S. T., Liu, Y., Cui, Y., Zahoor, R., Dai, T. (2016). Improved tolerance to post-anthesis drought stress by pre-drought priming at vegetative stages in drought-tolerant and -sensitive wheat cultivars. Plant Physiology and Biochemistry, 106, 218–227. https://doi.org/10.1016/j.plaphy.2016.04.046
2. Alzahrani, Y., Kuşvuran, A., Alharby, H. F., Kuşvuran, S., Rady, M. M. (2018). The defensive role of silicon in wheat against stress conditions induced by drought, salinity or cadmium. Ecotoxicology and Environmental Safety, 154, 187–196. https://doi.org/10.1016/j.ecoenv.2018.02.002
3. Ashraf, M., & Foolad, M. R. (2007). Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environmental and Experimental Botany, 59(2), 206–216. https://doi.org/10.1016/j.envexpbot.2005.12.006
4. Ashraf, M. & Harris, P. J. C. (2004). Potential biochemical indicators of salinity tolerance in plants. Plant Science, 166(1), 3–16. https://doi.org/10.1016/j.plantsci.2003.10.024
5. Bashan, Y., & de-Bashan, L. E. (2010). How the plant growth-promoting bacterium Azospirillum promotes plant growth—A critical assessment. Advances in Agronomy, 108, 77–136. https://doi.org/10.1016/S0065-2113(10)08002-8
6. Berendsen, R. L., Pieterse, C. M., Bakker, P. A. (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
7. Bharti, N., Barnawal, D., & Kalra, A. (2016). Halophilic bacteria mediate salt stress tolerance in plants: Recent developments. Journal of Plant Growth Regulation, 35(3), 943–960. https://doi.org/10.1007/s00344-016-9599-3
8. Bresson, J., Varoquaux, F., Bontpart, T., Touraine, B., Vile, D. (2013). The PGPR strain Phyllobacterium brassicacearum STM196 induces a reproductive delay and increases drought tolerance in Arabidopsis. New Phytologist, 200(2), 558–569.

9. Büyük, İ., Soydam-Aydın, S., & Aras, S. (2012). Bitkilerin stres koşullarına verdiği moleküler cevaplar. Turkish Bulletin of Hygiene & Experimental Biology, 69(2). https://doi.org/10.5505/TurkHijyen.2012.44946
10. Chaves, M. M., Flexas, J., Pinheiro, C. (2009). Photosynthesis under drought and salt stress: Regulation from the whole plant to cell. Annals of Botany, 103(4), 551–560. https://doi.org/10.1093/aob/mcn125
11. Chaves, M. M., Maroco, J. P., Pereira, J. S. (2003). Understanding plant responses to drought—From genes to the whole plant. Functional Plant Biology, 30(3), 239–264. https://doi.org/10.1071/FP02076
12. Cohen, A. C., Bottini, R., Piccoli, P. N. (2008). Azospirillum brasilense Sp 245 produces ABA in chemically defined culture medium and increases ABA content in Arabidopsis plants. Plant Growth Regulation, 54(2), 97–103. https://doi.org/10.1007/s10725-007-9232-9
13. Coleman-Derr, D., & Tringe, S. G. (2014). Building the crops of tomorrow: Advantages of symbiont-based approaches to improving abiotic stress tolerance. Frontiers in Microbiology, 5, 283. https://doi.org/10.3389/fmicb.2014.00283
14. Egamberdieva, D., Wirth, S., Bellingrath-Kimura, S. D., Mishra, J., Arora, N. K. (2019). Salt-tolerant plant growth-promoting rhizobacteria for enhancing crop productivity of saline soils. Frontiers in Microbiology, 10, 2791. https://doi.org/10.3389/fmicb.2019.02791
15. Evelin, H., Kapoor, R., Giri, B. (2009). Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Annals of Botany, 104(7), 1263–1280. https://doi.org/10.1093/aob/mcp251
16. Farooq, M., Bramley, H., Palta, J. A., Siddique, K. H. (2011). Heat stress in wheat during reproductive and grain-filling phases. Critical Reviews in Plant Sciences, 30(6), 491–507. https://doi.org/10.1080/07352689.2011.615687
17. Farooq, M., Wahid, A., Kobayashi, N., Fujita, D., Basra, S. M. A. (2009). Plant drought stress: Effects, mechanisms and management. Agronomy for Sustainable Development, 29(1), 185–212. https://doi.org/10.1051/agro:2008021
18. Fitzpatrick, C. R., Salas-González, I., Conway, J. M., Finkel, O. M., Gilbert, S., Russ, D., Teixeira, P. J. P. L., Dangl, J. L., Jones, C. D. (2020). The plant microbiome: From ecology to reductionism and beyond. Annual Review of Microbiology, 74, 81–100. https://doi.org/10.1146/annurev-micro-022620-014327
19. Gill, S. S., & Tuteja, N. (2010). Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiology and Biochemistry, 48(12), 909–930. https://doi.org/10.1016/j.plaphy.2010.08.016
20. Glick, B. R. (2012). Plant growth-promoting bacteria: Mechanisms and applications. Scientifica, 2012, 963401. https://doi.org/10.6064/2012/963401
21. Hasegawa, P. M., Bressan, R. A., Zhu, J. K., Bohnert, H. J. (2000). Cellular and molecular responses of plants to high salinity. Annual Review of Plant Physiology and Plant Molecular Biology, 51, 463–499. https://doi.org/10.1146/annurev.arplant.51.1.463
22. Hasanuzzaman, M., Nahar, K., Alam, M. M., Roychowdhury, R., Fujita, M. (2013). Physiological, biochemical, and molecular mechanisms of heat stress tolerance in plants. International Journal of Molecular Sciences, 14(5), 9643–9684. https://doi.org/10.3390/ijms14059643
23. Hays, D. B., Do, J. H., Mason, R. E., Morgan, G., Finlayson, S. A. (2007). Heat stress induced ethylene production in developing wheat grains induces kernel abortion and increased maturation in a susceptible cultivar. Plant Science, 172(6), 1113–1123. https://doi.org/10.1016/j.plantsci.2007.02.004
24. Joshi, R., Wani, S. H., Singh, B., Bohra, A., Dar, Z. A., Lone, A. A., Singla-Pareek, S. L. (2016). Transcription factors and plants’ response to drought stress: Current understanding and future directions. Frontiers in Plant Science, 7, 1029. https://doi.org/10.3389/fpls.2016.01029
25. Kohler, J., Hernández, J. A., Caravaca, F., Roldán, A. (2008). Plant-growth-promoting rhizobacteria and arbuscular mycorrhizal fungi modify alleviation biochemical mechanisms in water-stressed plants. Functional Plant Biology, 35(2), 141–151. https://doi.org/10.1071/FP07218
26. Kotak, S., Larkindale, J., Lee, U., von Koskull-Döring, P., Vierling, E., Scharf, K. D. (2007). Complexity of the heat stress response in plants. Current Opinion in Plant Biology, 10(3), 310–316. https://doi.org/10.1016/j.pbi.2007.04.011
27. Lynch, J. P. (2013). Steep, cheap and deep: An ideotype to optimize water and N acquisition by maize root systems. Functional Plant Biology, 40(9), 975–982. https://doi.org/10.1071/FP13033
28. Marulanda, A., Barea, J. M., Azcón, R. (2009). Stimulation of plant growth and drought tolerance by native microorganisms (AM fungi and bacteria) from dry environments. Journal of Plant Growth Regulation, 28(2), 115–124. https://doi.org/10.1007/s00344-009-9079-6
29. Mendes, R., Garbeva, P., Raaijmakers, J. M. (2013). The rhizosphere microbiome: Significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms. FEMS Microbiology Reviews, 37(5), 634–663. https://doi.org/10.1111/1574-6976.12028
30. Mittler, R. (2002). Oxidative stress, antioxidants and stress tolerance. Trends in Plant Science, 7(9), 405–410. https://doi.org/10.1016/S1360-1385(02)02312-9
31. Mittova, V., Tal, M., Volokita, M., Guy, M. (2004). Salt stress induces up-regulation of an efficient chloroplast antioxidant system in the salt-tolerant wild tomato species Lycopersicon pennellii. Journal of Experimental Botany, 55(399), 1105–1113. https://doi.org/10.1093/jxb/erh113
32. Munns, R., & Tester, M. (2008). Mechanisms of salinity tolerance. Annual Review of Plant Biology, 59, 651–681. https://doi.org/10.1146/annurev.arplant.59.032607.092911
33. Nakashima, K., & Yamaguchi-Shinozaki, K. (2013). ABA signaling and abiotic stress responses in plants. Journal of Plant Research, 126(5), 613–620. https://doi.org/10.1007/s10265-013-0561-4
34. Ngumbi, E., & Kloepper, J. (2016). Bacterial-mediated drought tolerance: Current and future prospects. Applied Soil Ecology, 105, 109–125. https://doi.org/10.1016/j.apsoil.2016.04.009
35. Nguyen, N. H., Song, I. J., Cheong, J. J., Park, S. H. (2020). Plant growth-promoting rhizobacteria improve salt stress tolerance in plants. Microbiological Research, 235, 126–146. https://doi.org/10.1016/j.micres.2020.126446
36. Sairam, R. K., & Srivastava, G. C. (2001). Water stress tolerance of wheat (Triticum aestivum L.): Variations in hydrogen peroxide accumulation and antioxidant activity. Journal of Agronomy and Crop Science, 186(1), 63–70. https://doi.org/10.1046/j.1439-037x.2001.00461
37. Sandhya, V., Ali, S. Z., Grover, M., Reddy, G., Venkateswarlu, B. (2010). Effect of plant growth promoting Pseudomonas spp. on compatible solutes, antioxidant status and plant growth of maize under drought stress. Plant Growth Regulation, 62(1), 21–30. https://doi.org/10.1007/s10725-010-9479-4
38. Sharma, B., Yadav, L., Shrestha, A., Shrestha, S., Subedi, M., Subedi, S., Shrestha, J. (2022). Drought stress and its management in wheat (Triticum aestivum L.): A review. Agricultural Science & Technology, 14(1), 1–10.
39. Shi, H., Quintero, F. J., Pardo, J. M., Zhu, J. K. (2002). The putative plasma membrane Na⁺/H⁺ antiporter SOS1 controls long-distance Na⁺ transport in plants. The Plant Cell, 14(2), 465–477. https://doi.org/10.1105/tpc.010371
40. Shrivastava, P., & Kumar, R. (2015). Soil salinity: A serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation. Saudi Journal of Biological Sciences, 22(2), 123–131. https://doi.org/10.1016/j.sjbs.2014.12.001
41. Smith, S. E., & Read, D. J. (2008). Mycorrhizal symbiosis (3rd ed.). Academic Press.
42. Trachsel, S., Kaeppler, S. M., Brown, K. M., Lynch, J. P. (2011). Shovelomics: High throughput phenotyping of maize (Zea mays L.) root architecture in the field. Plant and Soil, 341(1), 75–87. https://doi.org/10.1007/s11104-010-0623-8
43. Uga, Y., Sugimoto, K., Ogawa, S., Rane, J., Ishitani, M., Hara, N., Kitomi, Y., Inukai, Y., Ono, K., Kanno, N., Inoue, H., Takehisa, H., Motoyama, R., Nagamura, Y., Wu, J., Matsumoto, T., Takai, T., Okuno, K., Yano, M. (2013). Control of root system architecture by DEEPER ROOTING 1 increases rice yield under drought conditions. Nature Genetics, 45(9), 1097–1102. https://doi.org/10.1038/ng.2725
44. Vierling, E. (1991). The roles of heat shock proteins in plants. Annual Review of Plant Physiology and Plant Molecular Biology, 42(1), 579–620. https://doi.org/10.1146/annurev.pp.42.060191.003051
45. Vishwakarma, K., Kumar, N., Shandilya, C., Mohapatra, S., Bhayana, S., Varma, A. (2020). Revisiting plant–microbe interactions and microbial consortia application for enhancing sustainable agriculture: A review. Frontiers in Microbiology, 11, 560406. https://doi.org/10.3389/fmicb.2020.560406
46. Vurukonda, S. S. K. P., Vardharajula, S., Shrivastava, M., Ali, S. Z. (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
47. Wahid, A., Gelani, S., Ashraf, M., Foolad, M. R. (2007). Heat tolerance in plants: An overview. Environmental and Experimental Botany, 61(3), 199–223. https://doi.org/10.1016/j.envexpbot.2007.05.011
48. Qiao, M. (2024). Physiological and biochemical responses of plants to drought stress: Adaptation mechanisms and management strategies. Plants, 13(13), 1808. https://doi.org/10.3390/plants13131808
49. Yamaguchi-Shinozaki, K., & Shinozaki, K. (2006). Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annual Review of Plant Biology, 57, 781–803. https://doi.org/10.1146/annurev.arplant.57.032905.105444
50. Yasmeen, A., Basra, S., Wahid, A., Farooq, M., Nouman, W., Hussain, N. (2013). Improving drought resistance in wheat (Triticum aestivum) by exogenous application of growth enhancers. International Journal of Agriculture & Biology, 15(6), 1307–1312.
51. Zhu, J.-K. (2021). Abiotic stress signaling and responses in plants. Cell, 184(6), 1525–1539. https://doi.org/10.1016/j.cell.2021.01.029