Soil moisture modulates biological nitrification inhibitors release in sorghum plants

Plant Soil https://doi.org/10.1007/s11104-023-05913-y RESEARCH ARTICLE Soil moisture modulates biological nitrification inhibitors release in sorghum plants Adrián Bozal‑Leorri · Luis Miguel Arregui · Fernando Torralbo Mª Begoña González‑Moro · Carmen González‑Murua · Pedro Aparicio‑Tejo · Received: 28 September 2022 / Accepted: 30 January 2023 © The Author(s) 2023 Abstract Background and aims Sorghum (Sorghum bicolor) is able to exude allelochemicals with biological nitrification inhibition (BNI) capacity. Therefore, sorghum might be an option as cover crop since its BNI ability may reduce N pollution in the following crop due to a decreased nitrification. However, BNI exudation is related to the physiological state and development of the plant, so abiotic stresses such as drought might modify the rate of BNI exudation. Hence, the objective was to determine the effect of drought stress on sorghum plants’ BNI release. Methods The residual effects of sorghum crops over ammonia-oxidizing bacteria (AOB) were monitored in a 3-year field experiment. In a controlled-conditions experiment, sorghum plants were grown under Responsible Editor: Elizabeth M Baggs. Supplementary information The online version contains supplementary material available at https://doi. org/10.1007/s11104-023-05913-y. A. Bozal‑Leorri (*) · M. B. González‑Moro · C. González‑Murua Department of Plant Biology and Ecology, Faculty of Science and Technology, University of the Basque Country (UPV/EHU), Apdo. 644, Bilbao E‑48080, Spain e-mail: L. M. Arregui Institute for Innovation and Sustainable Development in Food Chain (ISFOOD), Public University of Navarre, Pamplona, Spain Watered (60% WFPS) or Moderate drought (30% WFPS) conditions, and fertilized with ammonium sulphate (A), ammonium sulphate + DMPP (A+D), or potassium nitrate (KNO3−). Soil mineral N was determined, and AOB populations were quantified. Additionally, plant biomass, isotopic discrimination of N and C, and photosynthetic parameters were measured in sorghum plants. Results In the driest year, sorghum was able to reduce the AOB relative abundance by 50% at field conditions. In the plant-soil microcosm, drought stress reduced leaf photosynthetic parameters, which had an impact on plant biomass. Under these conditions, sorghum plants exposed to Moderate drought reduced the AOB abundance of A treatment by 25% compared to Watered treatment. Conclusion The release of BNI by sorghum under limited water conditions might ensure high soil NH4+-N pool for crop uptake due to a reduction of nitrifying microorganisms. F. Torralbo Department of Botany, Ecology, and Vegetal Physiology, University of Córdoba, Severo Ochoa Building, Córdoba, Spain P. Aparicio‑Tejo Institute for Multidisciplinary Research in Applied Biology (IMAB), Public University of Navarre, Pamplona, Spain Vol.: (0123456789) 13 Plant Soil Keywords Ammonium · Cover crops · Drought stress · Nitrate · Soil mineral nitrogen Abbreviations AOB Ammonia-oxidizing bacteria BNI Biological nitrification inhibition BNIs Biological nitrification inhibitors DMPP 3,4-dimethylpyrazole phosphate SNIs Synthetic nitrification inhibitors WFPS Water filled pore space Introduction The availability of nitrogen (N) is the major limiting nutrient for crop growth (LeBauer and Treseder 2008). Although agriculture relies on the intensive use of N fertilizers to maximize crop yields, a great amount is lost as reactive N since crops cannot take the entire N applied and it cannot be retained by soils (Lassaletta et al. 2014). The main pathways for N losses that cause a negative environmental impact are through nitrate ( NO3−) leaching, ammonia ( NH3) volatilization, and emissions of nitrogenous gases such as nitric oxide (NO) and nitrous oxide (N2O) (Coskun et al. 2017). Nitrous oxide, one of the main greenhouse gasses (GHG) generated in upland agriculture (Syakila and Kroeze 2011) with a global warming potential (GWP) between 265 and 298 times higher than that of C O2 in a 100-year time horizon (IPCC 2014), is mainly generated by microbial nitrification and denitrification processes (Li et al. 2016). There are several approaches to reduce N losses derived from fertilization, e.g., the use of synthetic nitrification inhibitors (SNIs), such as 3,4-dimethylpyrazole phosphate (DMPP), when applying ammoniumbased fertilizers (Huérfano et al. 2015, 2018). Unfortunately, the use of SNIs is not widely adopted by farmers due to having some disadvantages such as additional product and field application costs and low cost-effectiveness for farmers (Subbarao et al. 2006, 2013a, 2017). Notwithstanding these drawbacks, the use of crops with the capability of producing biological nitrification inhibitions (BNIs) has become in a promising option to alleviate N losses derived from nitrification. The biological nitrification inhibition (BNI) was firstly described in 1966 in Hyparrhenia filipendula, but it was not termed as BNI until 2003 when Vol:. (1234567890) 13 Ishikawa et al. (2003) tried to describe the capacity of Brachiaria humidicola to inhibit the ammonium (NH4+) oxidation to NO3−. Moreover, the opportunity to exploit this strategy in agricultural systems to minimize the problem of N losses has gone unnoticed until recently (Subbarao and Searchinger 2021). This ability to produce BNIs is highlighted in the framework of sustainable agriculture based on the use of environmentally friendly agronomic practices to decrease pollution derived from the use of fertilizers (Subbarao et al. 2013a; Zhang et al. 2015). Therefore, the use of cover crops capable of producing BNIs represents another promising strategy to control nitrification and, thus, to increase the availability of N in the soil for the next crop while reducing N losses from the agrosystem (Karwat et al. 2019; Momesso et al. 2019). The ability to exude BNIs seems to be related to plants’ adaptability to low N environments (Subbarao et al. 2015). Regarding field crops, unlike crops adapted to high N input environments such as wheat (Triticum aestivum) and maize (Zea mays), the strongest BNI capacity is found in sorghum (Sorghum bicolor) since it is adapted to low N environments (Subbarao et al. 2007). Sorghum roots release two categories of BNIs, hydrophilic and hydrophobic, which may have complementary roles. The hydrophobic BNIs may remain close to the root systems, as they are strongly absorbed by soil mineral or organic particles, which may further increase their persistence (Dayan et al. 2010; Subbarao et al. 2013b). In contrast, hydrophilic BNIs are more likely to move out of the rhizosphere, which may enhance their capacity to suppress nitrification in bulk soil (Nardi et al. 2013; Subbarao et al. 2013b). In addition, BNIs from sorghum can be released until close to the physiological maturity of the crop (Sarr et al. 2021), which would ensure the availability of N during all the stages of crop development. Increasing efforts are taken to identif (...truncated)