Please wait a minute...
Journal of Integrative Agriculture
Advanced Online Publication | Current Issue | Archive | Adv Search
Soil nitrogen dynamics regulate differential nitrogen uptake between rice and upland crops

Shending Chen1 ,2, 5, Ahmed S. Elrys1, 3, 4, Siwen Du2, Wenyan Yang1, Zucong Cai2, 4, Jinbo Zhang1, 4#, Lei Meng1#, Christoph Müller4, 5, 6

1 School of Breeding and Multiplication/Sanya Institute of Breeding and Multiplication, Hainan University, Sanya 572025, China

2 School of Geography, Nanjing Normal University, Nanjing 210023, China

3 Soil Science Department, Faculty of Agriculture, Zagazig University, Zagazig 44519, Egypt

4 Liebig Centre for Agroecology and Climate Impact Research, Justus-Liebig University Giessen, Giessen 35392, Germany

5 Institute of Plant Ecology, Justus-Liebig University Giessen, Giessen 35392, Germany

6 School of Biology and Environmental Science and Earth Institute, University College Dublin, Dublin DO4V1W8, Ireland

 Highlights 

l The characteristics of gross N transformations regulate soil N dynamics.

l Soil N dynamics matching with crop N preference affect crop N uptake.

l Heterotrophic nitrification enhances N uptake in upland systems.

l Autotrophic nitrification constrains N uptake in rice systems.

Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
摘要  

水稻氮利用效率普遍低于旱地作物。土壤氮动态和作物氮形态偏好的差异可能是导致这一现象的重要因素。然而,目前对稻田和旱地土壤氮初级转化速率的差异及其对作物氮吸收的影响仍然知之甚少。我们分析了全球136项研究中的2044个农田土壤氮初级转化速率的观测结果,以期阐明全球尺度上稻田和旱地土壤氮动态特点及其对水稻和旱地作物氮吸收的影响。研究结果表明,水稻土氮初级矿化和自养硝化速率明显低于旱地土壤,而硝酸盐异化还原为铵速率高于旱地。长期淹水环境和水稻土全氮含量较低是导致上述差异的主要因素。土壤氮初级矿化和自养硝化速率调控土壤可利用氮供应量以及铵态氮与硝态氮的比例。水稻铵态氮吸收速率明显高于旱地作物,而旱地作物硝态氮吸收速率则超过水稻的两倍。水稻土铵态氮供应能力较低以及自养硝化作用对铵态氮的竞争及硝化-反硝化氮损失是水稻氮利用率低的重要原因。异养硝化作用有利于提升旱地作物氮吸收。这些结果表明,农田土壤氮动态与作物氮吸收偏好的契合程度对于提高作物生产力并减少活性氮污染具有重要意义。



Abstract  

Nitrogen use efficiency in rice is lower than in upland crops, likely due to differences in soil nitrogen dynamics and crop nitrogen preferences. However, the specific nitrogen dynamics in paddy and upland systems and their impact on crop nitrogen uptake remain poorly understood. The N dynamics and impact on crop N uptake determine the downstream environmental pollution from nitrogen fertilizer. To address this poor understanding, we analyzed 2,044 observations of gross nitrogen transformation rates in soils from 136 studies to examine nitrogen dynamics in both systems and their effects on nitrogen uptake in rice and upland crops. Our findings revealed that nitrogen mineralization and autotrophic nitrification rates are lower in paddies than in upland soil, while dissimilatory nitrate reduction to ammonium is higher in paddies, these differences being driven by flooding and lower total nitrogen content in paddies. Rice exhibited higher ammonium uptake, while upland crops had over twice the nitrate uptake. Autotrophic nitrification stimulated by pH reduced rice nitrogen uptake, while heterotrophic nitrification enhanced nitrogen uptake of upland crops. Autotrophic nitrification played a key role in regulating the ammonium-to-nitrate ratio in soils, which further affected the balance of plant nitrogen uptake. These results highlight the need to align soil nitrogen dynamics with crop nitrogen preferences to maximize plant maximize productivity and reduce reactive nitrogen pollution.

Keywords:  Paddy soil       upland soil       plant nitrogen uptake       N mineralization       nitrification       15N tracing study  
Online: 22 March 2025  
Fund: 

This work was funded by the National Key Research and Development Program of China (2024YFD1501602), and the National Natural Science Foundation of China (42407437).

About author:  #Correspondence Jinbo Zhang, Mobile: +86-13805188487, E-mail: zhangjinbo@hainanu.edu.cn; Lei Meng, Mobile: +86-13707546016, E-mail: menglei@hainanu.edu.cn

Cite this article: 

Shending Chen, Ahmed S. Elrys, Siwen Du, Wenyan Yang, Zucong Cai, Jinbo Zhang, Lei Meng, Christoph Müller. 2025. Soil nitrogen dynamics regulate differential nitrogen uptake between rice and upland crops. Journal of Integrative Agriculture, Doi:10.1016/j.jia.2025.03.014

Akiyama H, Yan X Y, Yagi K. 2010. Evaluation of effectiveness of enhanced-efficiency fertilizers as mitigation options for N2O and NO emissions from agricultural soils: Meta-analysis. Global Change Biology, 16, 1837-1846.

Armstrong W, Beckett P M. 1987. Internal aeration and the development of stelar anoxia in submerged roots-a multishelled mathematical-model combining axial diffusion of oxygen in the cortex with radial losses to the stele, the wall layers and the rhizosphere. New Phytologist, 105, 221-245.

Asano M, Wagai R. 2014. Evidence of aggregate hierarchy at micro-to submicron scales in an allophanic Andisol. Geoderma, 216, 62-74.

Bates D, Maechler M, Bolker B M, Walker S C. 2015. Fitting linear mixed-effects models using lme4. Journal of Statistical Software, 67, 1-48.

Bengtsson G, Bengtson P, Månsson K F. 2003. Gross nitrogen mineralization-, immobilization-, and nitrification rates as a function of soil C/N ratio and microbial activity. Soil Biology & Biochemistry, 35, 143-154.

Booth M S, Stark J M, Rastetter E. 2005. Controls on nitrogen cycling in terrestrial ecosystems: A synthetic analysis of literature data. Ecological Monographs, 75, 139-157.

Britto D T, Kronzucker H J. 2002. NH4+ toxicity in higher plants: A critical review. Journal of Plant Physiology, 159, 567-584.

Britto D T, Kronzucker H J. 2013. Ecological significance and complexity of N-source preference in plants. Annals of Botany, 112, 957-963.

Cameron K C, Di H J, Moir J L. 2013. Nitrogen losses from the soil/plant system: A review. Annals of Applied Biology, 162, 145-173.

Chen J T, Li J H, Li W F, Li P, Zhu R, Zhong Y X, Zhang W F, Li T Y. 2024. The optimal ammonia-nitrate ratio for various crops: A Meta-analysis. Field Crops Research, 307, 109240.

Chen M T L, Schievano A, Bosco S, Montero-Castaño A, Tamburini G, Pérez-Soba M, Makowski D. 2023. Evidence map of the benefits of enhanced-efficiency fertilisers for the environment, nutrient use efficiency, soil fertility, and crop production. Environmental Research Letters, 18, 043005.

Chen S, Elrys A S, Yang W, Du S, He M, Cai Z, Zhang J, Müller C. 2024. Soil recalcitrant but not labile organic nitrogen mineralization contributes to microbial nitrogen immobilization and plant nitrogen uptake. Global Change Biology, 30, e17290.

Cheng Y, Elrys A S, Merwad A R M, Zhang H, Chen Z, Zhang J, Cai Z, Müller C. 2022. Global patterns and drivers of soil dissimilatory nitrate reduction to ammonium. Environmental Science & Technology, 56, 3791-3800.

Cheng Y, Wang J, Wang J Y, Chang S X, Wang S Q. 2017. The quality and quantity of exogenous organic carbon input control microbial NO3- immobilization: A meta-analysis. Soil Biology & Biochemistry, 115, 357-363.

Choi W J, Ro H M. 2003. Differences in isotopic fractionation of nitrogen in water-saturated and unsaturated soils. Soil Biology & Biochemistry, 35, 483-486.

Coskun D, Britto D T, Shi W, Kronzucker H J. 2017. Nitrogen transformations in modern agriculture and the role of biological nitrification inhibition. Nature Plants, 3, 17074.

Elrys A S, Abo El-Maati M F, Dan X, Wen Y, Mou J, Abdelghany A E, Uwiragiye Y, Shuirong T, Yanzheng W, Meng L, Zhang J, Müller C. 2023a. Aridity creates global thresholds in soil nitrogen retention and availability. Global Change Biology, e17003.

Elrys A S, Ali A, Zhang H, Cheng Y, Zhang J, Cai Z, Müller C, Chang S X. 2021a. Patterns and drivers of global gross nitrogen mineralization in soils. Global Change Biology, 27, 5950-5962.

Elrys A S, Uwiragiye Y, Zhang Y, Abdel-Fattah M K, Chen Z, Zhang H, Meng L, Wang J, Zhu T, Cheng Y, Zhang J, Cai Z, Chang S X, Müller C. 2023b. Expanding agroforestry can increase nitrate retention and mitigate the global impact of a leaky nitrogen cycle in croplands. Nature Food, 4, 109-121.

Elrys A S, Wang J, Meng L, Zhu Q, El-Sawy M M, Chen Z, Tu X, El-Saadony M T, Zhang Y, Zhang J, Cai Z, Müller C, Cheng Y. 2023c. Integrative knowledge-based nitrogen management practices can provide positive effects on ecosystem nitrogen retention. Nature Food, 4, 1075-1089.

Elrys A S, Wang J, Metwally M A S, Cheng Y, Zhang J, Cai Z, Chang S X, Müller C. 2021b. Global gross nitrification rates are dominantly driven by soil carbon-to-nitrogen stoichiometry and total nitrogen. Global Change Biology, 27, 6512-6524.

Falkengren-Grerup U, Lakkenborg-Kristensen H. 1994. Importance of ammonium and nitrate to the performance of herb-layer species from deciduous forests in Southern Sweden. Environmental and Experimental Botany, 34, 31-38.

FAO (Food and Agriculture Organization of the United Nations). 2022. FAOSTAT production data. [2024-10-2]. https://www.fao.org/faostat/en/#data

Gao W, Fan C, Zhang W, Li N, Liu H, Chen M. 2023. Heterotrophic nitrification of organic nitrogen in soils: Process, regulation, and ecological significance. Biology and Fertility of Soils, 59, 261-274.

Geisseler D, Horwath W R, Joergensen R G, Ludwig B. 2010. Pathways of nitrogen utilization by soil microorganisms-A review. Soil Biology & Biochemistry, 42, 2058-2067.

Gigon A, Rorison I H. 1972. The response of some ecologically distinct plant species to nitrate- and to ammonium-nitrogen. Journal of Ecology, 60, 93-102.

Gu B J, Zhang X M, Lam S K, Yu Y L, van Grinsven H J M, Zhang S H, Wang X X, Bodirsky B L, Wang S T, Duan J K, Ren C C, Bouwman L, de Vries W, Xu J M, Sutton M A, Chen D L. 2023. Cost-effective mitigation of nitrogen pollution from global croplands. Nature, 613, 77-84.

He M Q, Chen S D, Yang W Y, Dai S Y, Zhu Q Y, Wang W J, Du S W, Meng L, Cai Z C, Zhang J B, Müller C. 2024a. Priming effects of maize growth and photosynthetic substrate supply on soil N mineralization-immobilization turnover. Plant and Soil, doi: 10.1007/s11104-024-06815-3.

He M Q, Dai S Y, Zhu Q Y, Wang W J, Chen S D, Meng L, Dan X Q, Huang X Q, Cai Z C, Zhang J B, Müller C. 2024b. Understanding the stimulation of microbial oxidation of organic N to nitrate in plant soil systems. Soil Biology & Biochemistry, 190, 109312.

He X, Chi Q, Cai Z, Cheng Y, Zhang J, Müller C. 2020. 15N tracing studies including plant N uptake processes provide new insights on gross N transformations in soil-plant systems. Soil Biology & Biochemistry, 141, 107666.

He X, Chi Q, Meng L, Zhao C, He M, Dan X, Huang X, Zhao J, Cai Z, Zhang J, Müller C. 2022. Plants with nitrate preference can regulate nitrification to meet their nitrate demand. Soil Biology & Biochemistry, 165, 108516.

Houlton B Z, Sigman D M, Schuur E A G, Hedin L O. 2007. A climate-driven switch in plant nitrogen acquisition within tropical forest communities. Proceedings of the National Academy of Sciences of the United States of America, 104, 8902-8906.  

Hu Y, Schraml M, von Tucher S, Li F, Schmidhalter U. 2014. Influence of nitrification inhibitors on yields of arable crops: A meta-analysis of recent studies in Germany. International Journal of Plant Production, 8, 33-50.

Huygens D, Boeckx P, Templer P H, Paulino L, Van Cleemput O, Oyarzun C, Müller C, Godoy R. 2008. Mechanisms for retention of bioavailable nitrogen in volcanic rainforest soils. Nature Geoscience, 1, 543-548.

Ishii S, Ikeda S, Minamisawa K, Senoo K. 2011. Nitrogen cycling in rice paddy environments: Past achievements and future challenges. Microbes and Environments, 26, 282-292.

Jackson L E, Burger M, Cavagnaro T R. 2008. Roots nitrogen transformations, and ecosystem services. Annual Review of Plant Biology, 59, 341-363.

Jiao S, Chen W, Wang J, Du N, Li Q, Wei G. 2018. Soil microbiomes with distinct assemblies through vertical soil profiles drive the cycling of multiple nutrients in reforested ecosystems. Microbiome, 6, 146.

Kirk G J D, Kronzucker H J. 2005. The potential for nitrification and nitrate uptake in the rhizosphere of wetland plants: A modelling study. Annals of Botany, 96, 639-646.

Kögel-Knabner I, Amelung W, Cao Z, Fiedler S, Frenzel P, Jahn R, Kalbitz K, Koelbl A, Schloter M. 2010. Biogeochemistry of paddy soils. Geoderma, 157, 1-14.

Kuznetsova A, Brockhoff P B, Christensen R H B. 2017. lmerTest package: Tests in linear mixed effects models. Journal of Statistical Software, 82, 1-26.

Lai C, Hu Q, Sun J, Li C, Chen X, Chen B, Xue X, Chen J, Hou F, Xu G, Du W, Stevens C, Peng F, Zhou J. 2024. Varying soil moisture and pH with alpine meadow degradation affect nitrogen preference of dominant species. Biology and Fertility of Soils, 60, 1041-1053.

Lam P, Kuypers M M M. 2011. Microbial nitrogen cycling processes in oxygen minimum zones. In: Carlson C A, Giovannoni S J eds., Annual Review of Marine Science, 3, 317-345.

Leifeld J, von Luetzow M. 2014. Chemical and microbial activation energies of soil organic matter decomposition. Biology and Fertility of Soils, 50, 147-153.

Li Y L, Fan X R, Shen Q R. 2008. The relationship between rhizosphere nitrification and nitrogen-use efficiency in rice plants. Plant Cell and Environment, 31, 73-85.

Li Z, Tian D, Wang B, Wang J, Wang S, Chen H Y H, Xu X, Wang C, He N, Niu S. 2019. Microbes drive global soil nitrogen mineralization and availability. Global Change Biology, 25, 1078-1088.

Li Z L, Zeng Z Q, Tian D S, Wang J S, Fu Z, Zhang F Y, Zhang R Y, Chen W N, Luo Y Q, Niu S L. 2020. Global patterns and controlling factors of soil nitrification rate. Global Change Biology, 26, 4147-4157.

Li Z X, Peng Y Z J, Gao H. 2020. Enhanced long-term advanced denitrogenation from nitrate wastewater by anammox consortia: Dissimilatory nitrate reduction to ammonium (DNRA) coupling with anammox in an upflow biofilter reactor equipped with EDTA-2Na/Fe(II) ratio and pH control. Bioresource Technology, 305, 123083.

Liesack W, Schnell S, Revsbech N P. 2000. Microbiology of flooded rice paddies. Fems Microbiology Reviews, 24, 625-645.

Lim S S, Kwak J H, Lee K S, Chang S X, Yoon K S, Kim H Y, Choi W J. 2015. Soil and plant nitrogen pools in paddy and upland ecosystems have contrasting δ15N. Biology and Fertility of Soils, 51, 231-239.

Linquist B A, Adviento-Borbe M A, Pittelkow C M, van Kessel C, van Groenigen K J. 2012. Fertilizer management practices and greenhouse gas emissions from rice systems: A quantitative review and analysis. Field Crops Research, 135, 10-21.

Linquist B A, Liu L, van Kessel C, van Groenigen K J. 2013. Enhanced efficiency nitrogen fertilizers for rice systems: Meta-analysis of yield and nitrogen uptake. Field Crops Research, 154, 246-254.

Liu S, Chi Q, Cheng Y, Zhu B, Li W, Zhang X, Huang Y, Müller C, Cai Z, Zhang J. 2019. Importance of matching soil N transformations, crop N form preference, and climate to enhance crop yield and reducing N loss. Science of the Total Environment, 657, 1265-1273.

Rabot E, Wiesmeier M, Schlueter S, Vogel H J. 2018. Soil structure as an indicator of soil functions: A review. Geoderma, 314, 122-137.

Rice K C, Herman J S. 2012. Acidification of Earth: An assessment across mechanisms and scales. Applied Geochemistry, 27, 1-14.

Shan J, Zhao X, Sheng R, Xia Y, Ti C, Quan X, Wang S, Wei W, Yan X. 2016. Dissimilatory nitrate reduction processes in typical chinese paddy soils: Rates, relative contributions, and influencing factors. Environmental Science & Technology, 50, 9972-9980.

Song L, Li Z L, Niu S L. 2021. Global soil gross nitrogen transformation under increasing nitrogen deposition. Global Biogeochemical Cycles, 35, e2020GB006711.

Subbarao G V, Kishii M, Bozal-Leorri A, Ortiz-Monasterio I, Gao X, Ibba M I, Karwat H, Gonzalez-Moro M B, Gonzalez-Murua C, Yoshihashi T, Tobita S, Kommerell V, Braun H J, Iwanaga M. 2021. Enlisting wild grass genes to combat nitrification in wheat farming: A nature-based solution. Proceedings of the National Academy of Sciences of the United States of America, 118, e2106595118.

Sun L, Lu Y, Yu F, Kronzucker H J, Shi W. 2016. Biological nitrification inhibition by rice root exudates and its relationship with nitrogen-use efficiency. New Phytologist, 212, 646-656.

Tang Q, Wang J, Cao M M, Chen Z X, Tu X S, Elrys A S, Jing H, Wang X Z, Cai Z C, Mueller C, Daniell T J, Yan X Y, Cheng Y. 2024. Awakening soil microbial utilization of nitrate by carbon regulation to lower nitrogen pollution. Agriculture Ecosystems & Environment, 362, 108848.

Totsche K U, Amelung W, Gerzabek M H, Guggenberger G, Klumpp E, Knief C, Lehndorff E, Mikutta R, Peth S, Prechtel A, Ray N, Koegel-Knabner I. 2018. Microaggregates in soils. Journal of Plant Nutrition and Soil Science, 181, 104-136.

Vinutha H P, Poornima B, Sagar B M. 2017. Detection of outliers using interquartile range technique from intrusion dataset. In: 6th International Conference on Frontiers of Intelligent Computing: Theory and Applications (FICTA). Kalinga Institute of Industrial Technology University, School of Computer Applications, Bhubaneswar, India. pp. 511-518.

Wang A, Li X, Hao X, Luo X, Chen W, Huang Q. 2022. Ammonia level influences the assembly of dissimilatory nitrate reduction to ammonia bacterial community in soils under different heavy metal remediation treatments. Science of the Total Environment, 838, 156393.

Wang L, Macko S A. 2011. Constrained preferences in nitrogen uptake across plant species and environments. Plant Cell and Environment, 34, 525-534.

Wei L, Ge T, Zhu Z, Luo Y, Yang Y, Xiao M, Yan Z, Li Y, Wu J, Kuzyakov Y. 2021. Comparing carbon and nitrogen stocks in paddy and upland soils: Accumulation, stabilization mechanisms, and environmental drivers. Geoderma, 398, 115121.

Weil R R, Brady N C. 2017. The Nature and Properties of Soils. 15th ed. Pearson Education, USA.

vonWiren N, Gazzarrini S, Frommer W B. 1997. Regulation of mineral nitrogen uptake in plants. Plant and Soil, 196, 191-199.

Wrage-Mönnig N, Horn M A, Well R, Müller C, Velthof G, Oenema O. 2018. The role of nitrifier denitrification in the production of nitrous oxide revisited. Soil Biology & Biochemistry, 123, A3-A16.

Xu C M, Chen L P, Chen S, Chu G, Wang D Y, Zhang X F. 2020. Rhizosphere aeration improves nitrogen transformation in soil, and nitrogen absorption and accumulation in rice plants. Rice Science, 27, 162-174.

Yang Y J, Zhang J B, Cai Z C. 2016. Nitrification activities and N mineralization in paddy soils are insensitive to oxygen concentration. Acta Agriculturae Scandinavica Section B (Soil and Plant Science), 66, 272-281.

Yue H, Yue W J, Jiao S, Kim H, Lee Y H, Wei G H, Song W N, Shu D T. 2023. Plant domestication shapes rhizosphere microbiome assembly and metabolic functions. Microbiome, 11, 70.

Zhang J, Cai Z, Müller C. 2018. Terrestrial N cycling associated with climate and plant-specific N preferences: A review. European Journal of Soil Science, 69, 488-501.

Zhang J, Wang J, Müller C, Cai Z. 2016. Ecological and practical significances of crop species preferential N uptake matching with soil N dynamics. Soil Biology & Biochemistry, 103, 63-70.

Zhang X, Davidson E A, Mauzerall D L, Searchinger T D, Dumas P, Shen Y. 2015. Managing nitrogen for sustainable development. Nature, 528, 51-59.

Zhao X, Wang Y, Cai S, Ladha J K, Castellano M J, Xia L, Xie Y, Xiong Z, Gu B, Xing G, Yan X. 2024. Legacy nitrogen fertilizer in a rice-wheat cropping system flows to crops more than the environment. Science Bulletin, 69, 1212-1216.

Zimmermann M, Leifeld J, Conen F, Bird M I, Meir P. 2012. Can composition and physical protection of soil organic matter explain soil respiration temperature sensitivity? Biogeochemistry, 107, 423-436. 

No related articles found!
No Suggested Reading articles found!