Background – N fertilization in agriculture, a gift and a curse
Agriculture faces the challenge of increasing yields while using resources more efficiently, in the context of a changing climate, growing world population, declining biodiversity, and governmental regulations. The urgent need to reduce N pollution is a primary goal of the “UN environment programme”.
Excess N is lost to the environment. Data source: West, Gerber, Engstrom, Mueller, Brauman, Carlson, Cassidy, Johnston, MacDonald, Ray & Siebert (2014). Leverage points for improving global food security and the environment. Science. Modified from OurWorldInData.org/fertilizers | CC BY
Many farmers fertilize with urea or ammonium-based fertilizers that are less easily lost to the environment than nitrate-based fertilizers. Nitrifying soil bacteria, however, convert these fertilizers to nitrate usually in less than a month, before the crop has taken them up. Nitrate is prone to leaching and denitrification causing pollution of groundwater and air. Plant roots can exude biological nitrification inhibitors (BNIs), which may increase nitrogen (N) uptake efficiency (N uptake per N input in the field), and at the same time, prevent N-pollution1 from the excess N of fertilizer input that is lost to the environment. The idea is that N is retained in the soil as ammonium when the microbial oxidation of ammonium (NH4+) to nitrate (NO3-) is inhibited.
Biological nitrification inhibition causes ammonium retention in soil, leading to less N loss to the environment, but does it also lead to increased plant N uptake? AI-generated image for illustrative purposes only, items not to scale.
BNI – a hot topic for sustainability
Recently, BNIs were found in main crops (e.g., wheat, maize, and rice), as well as in grasses and trees, but there are genotypic differences in the efficiency of inhibiting nitrification. Not all plants release BNIs; some even promote nitrification2,3. Therefore, breeding for BNI release has been proposed. Reducing N emissions and leaching by BNI is, for example, covered in a TED talk by G.V. Subbarao (2022) and at the United Nations Framework Convention on Climate Change (UNFCCC) in Bonn by Tadashi Yoshihashi (2023) about wheat, both from the Japanese research center JIRCAS. Also, European, British, US, Chinese, and other research groups are working on BNIs4.
We want a mechanistic explanation of the BNI-effect using modeling
BNI molecules are usually successively tested in bioassays3 and soil5 and then confirmed in plant and soil systems6. These studies show the inhibitory potential of root exudates. However, we missed a mechanistic investigation of the relevant rhizosphere processes determining the effectiveness of BNIs to increase N retention and plant nitrogen uptake. We wondered under what conditions BNI exudation might be beneficial and if there are conditions when their utility is reduced or even absent. We lay down fundamental processes and the limits of nitrification inhibition. Our study gives mechanistic insights into the plant-soil-microbe interaction with BNIs by modeling both the ecological aspect of plant and microbe interactions, as well as the functional aspects of N uptake and loss. BNIs are mostly beneficial, but is there a catch? We simulated BNIs, ammonium, nitrate, and the population dynamics of nitrifiers in the rhizosphere over space and time. We studied the influence of different processes on the utility of BNIs with a sensitivity analysis.
A model reveals the relevant processes in the rhizosphere
The governing processes for the usefulness of BNIs to plant N uptake are (1) the utilization of the NH4+ and NO3- uptake systems over time, and (2) the competition for NH4+ between plants and microbes, which is both coupled over (3) the available N (NH4+ and NO3-) concentration over time. With the model at hand, we can now ask what happens when nitrate production is slow (e.g., caused by slower oxidation or smaller nitrifier population over time). What happens when soil conditions change (e.g., sorption rates or initial ammonium concentrations)? Or what happens when uptake kinetics change (e.g., faster nitrate uptake by the plant)? We studied many scenarios addressing the above questions by exploring how sensitive the model results, nitrogen uptake efficiency, and nitrate loss are to changes in the model parameter values. Future experimental studies and eventually breeding crops for BNIs may take our theoretical findings into account.
BNIs are generally beneficial but in some cases BNIs can decrease plant N uptake
It was speculated that plants were selected for BNI activity in low N environments7. However, the simulation showed that in low N environments, where the initial ammonium concentration is also low, there is no need for BNI activity. Low ammonium concentrations self-inhibit the nitrifier activity and thus make BNIs redundant. BNIs benefit the plant above a threshold of initial N, implying fertilization plus BNIs give more uptake. Furthermore, the simulations also showed a beneficial effect of nitrifiers as plants benefit from nitrate uptake. Thus, nitrifiers can be friend or foe.
The results imply that the efficiency of BNIs depend on the specific growth rate of the nitrifying microbial population, their nitrification activity, on soil type. Breeders may select for kinetic traits together with BNIs, since BNI exudation benefits from enhanced ammonium uptake. We conclude that BNIs facilitate soil N retention but not necessarily plant N uptake, and thus, aiming for less environmental impact by increasing the ammonium concentration at the cost of nitrate does not always correlate with increased total N uptake. Inhibition only facilitates N uptake when the inferred lower nitrate production is compensated.
References
Subbarao, G. V. & Searchinger, T. D. A “more ammonium solution” to mitigate nitrogen pollution and boost crop yields. Proceedings of the National Academy of Sciences 118, e2107576118 (2021).
O’Sullivan, C. A., Fillery, I. R. P., Roper, M. M. & Richards, R. A. Identification of several wheat landraces with biological nitrification inhibition capacity. Plant Soil 404, 61–74 (2016).
Sun, L., Lu, Y., Yu, F., Kronzucker, H. J. & Shi, W. Biological nitrification inhibition by rice root exudates and its relationship with nitrogen-use efficiency. New Phytologist 212, 646–656 (2016).
Shi, H., Liu, G. & Chen, Q. Research Hotspots and Trends of Nitrification Inhibitors: A Bibliometric Review from 2004–2023. Sustainability 16, 3906 (2024).
Lu, Y. et al. Effects of the biological nitrification inhibitor 1,9-decanediol on nitrification and ammonia oxidizers in three agricultural soils. Soil Biology and Biochemistry 129, 48–59 (2019).
Chen, S. et al. Rice genotype affects nitrification inhibition in the rhizosphere. Plant Soil 481, 35–48 (2022).
Coskun, D., Britto, D. T., Shi, W. & Kronzucker, H. J. Nitrogen transformations in modern agriculture and the role of biological nitrification inhibition. Nature Plants 3, nplants201774 (2017).