OPPORTUNITIES AND APPROACHES FOR MANIPULATING SOIL-PLANT MICROBIOMES FOR EFFECTIVE CROP NITROGEN USE IN AGROECOSYSTEMS

doi:10.15302/J-FASE-2022450

Front. Agr. Sci. Eng.

2022, Vol. 9

Issue (3) : 333-343 https://doi.org/10.15302/J-FASE-2022450

REVIEW

OPPORTUNITIES AND APPROACHES FOR MANIPULATING SOIL-PLANT MICROBIOMES FOR EFFECTIVE CROP NITROGEN USE IN AGROECOSYSTEMS

Jingjing PENG¹, Olatunde OLADELE¹, Xiaotong SONG², Xiaotang JU³, Zhongjun JIA⁴, Hangwei HU⁵, Xuejun LIU¹, Shuikuan BEI¹, Anhui GE^2,⁶, Limei ZHANG^2,⁶(

), Zhenling CUI¹

¹. College of Resources and Environmental Sciences; National Academy of Agriculture Green Development, Key Laboratory of Plant-Soil Interactions, Ministry of Education, China Agricultural University, Beijing 100193, China
². State Key Laboratory of Urban and Regional Ecology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing 100085, China
³. College of Tropical Crops, Hainan University, Haikou 570228, China
⁴. Key Labortatory of Mollisols Agroecology, Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences, Changchun 130102, China
⁵. Faculty of Veterinary and Agricultural Sciences, The University of Melbourne, Parkville, VIC. 3010, Australia
⁶. University of Chinese Academy of Sciences, Beijing 100049, China

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Abstract

● Matching nitrification inhibitors with soil properties and nitrifiers is vital to achieve a higher NUE.

● Enhancing BNF, DNRA and microbial N immobilization processes via soil amendments can greatly contribute to less chemical N fertilizer input.

● Plant-associated microbiomes are critical for plant nutrient uptake, growth and fitness.

● Coevolutionary trophic relationships among soil biota need to be considered for improving crop NUE.

Soil microbiomes drive the biogeochemical cycling of nitrogen and regulate soil N supply and loss, thus, pivotal nitrogen use efficiency (NUE). Meanwhile, there is an increasing awareness that plant associated microbiomes and soil food web interactions is vital for modulating crop productivity and N uptake. The rapid advances in modern omics-based techniques and biotechnologies make it possible to manipulate soil-plant microbiomes for improving NUE and reducing N environmental impacts. This paper summarizes current progress in research on regulating soil microbial N cycle processes for NUE improvement, plant-microbe interactions benefiting plant N uptake, and the importance of soil microbiomes in promoting soil health and crop productivity. We also proposes a potential holistic (rhizosphere-root-phyllosphere) microbe-based approach to improve NUE and reduce dependence on mineral N fertilizer in agroecosystems, toward nature-based solution for nutrient management in intensive cropping systems.

Keywords nitrogen microbiome NUE rhizosphere phyllosphere soil food web

Corresponding Author(s): Limei ZHANG

About author:

Tongcan Cui and Yizhe Hou contributed equally to this work.

Just Accepted Date: 08 June 2022 Online First Date: 07 July 2022 Issue Date: 09 September 2022

Cite this article:

Jingjing PENG,Olatunde OLADELE,Xiaotong SONG, et al. OPPORTUNITIES AND APPROACHES FOR MANIPULATING SOIL-PLANT MICROBIOMES FOR EFFECTIVE CROP NITROGEN USE IN AGROECOSYSTEMS[J]. Front. Agr. Sci. Eng. , 2022, 9(3): 333-343.

URL:

https://academic.hep.com.cn/fase/EN/10.15302/J-FASE-2022450
https://academic.hep.com.cn/fase/EN/Y2022/V9/I3/333

Fig.1 Schematic overview of soil-plant microbiomes modulating soil N cycle and crop N uptake. The central box (green) depicts soil microbial N cycle processes and N supply and losses. The dotted lines (red) represent N losses from agroecosystems. The box below (orange) shows the regulation of microbial N cycle processes by soil amendments. Two boxes on the right (purple) depict the roles of rhizosphere and phyllosphere microbiomes in coordinating N cycle and plant N uptake. The box on the left (blue) shows the flux of N compound among soil trophic cascades. Anammox, anaerobic ammonium oxidation; and DNRA, dissimilatory nitrate reduction to ammonium.

Fig.2 Bibliometric analysis of research on soil-plant microbiomes modulating crop N uptake based on Web of Science Core Collection from January 2010 to August 2021. The co-occurrence pattern among keywords was constructed using the full counting method and visualized by bibliometric software VOSviewer (version 1.6.17)^[⁷^]. The keywords with over 200 occurrences were selected, with synonymous keywords (such as, N₂O and nitrous oxide, corn and maize, or bacterial community and bacterial communities) merged. The final network contains 127 keywords (nodes), the node color represents different cluster modules and the node size is proportional to the link strength.

1	D E, Canfield A N, Glazer P G Falkowski. The evolution and future of Earth’s nitrogen cycle. Science , 2010, 330( 6001): 192–196 https://doi.org/10.1126/science.1186120 pmid: 20929768
2	L, Philippot J M, Raaijmakers P, Lemanceau der Putten W H van. Going back to the roots: the microbial ecology of the rhizosphere. Nature Reviews: Microbiology , 2013, 11( 11): 789–799 https://doi.org/10.1038/nrmicro3109 pmid: 24056930
3	M M M, Kuypers H K, Marchant B Kartal. The microbial nitrogen-cycling network. Nature Reviews: Microbiology , 2018, 16( 5): 263–276 https://doi.org/10.1038/nrmicro.2018.9 pmid: 29398704
4	Z, Cui H, Zhang X, Chen C, Zhang W, Ma C, Huang W, Zhang G, Mi Y, Miao X, Li Q, Gao J, Yang Z, Wang Y, Ye S, Guo J, Lu J, Huang S, Lv Y, Sun Y, Liu X, Peng J, Ren S, Li X, Deng X, Shi Q, Zhang Z, Yang L, Tang C, Wei L, Jia J, Zhang M, He Y, Tong Q, Tang X, Zhong Z, Liu N, Cao C, Kou H, Ying Y, Yin X, Jiao Q, Zhang M, Fan R, Jiang F, Zhang Z Dou. Pursuing sustainable productivity with millions of smallholder farmers. Nature , 2018, 555( 7696): 363–366 https://doi.org/10.1038/nature25785 pmid: 29513654
5	L, Liu W, Xu X, Lu B, Zhong Y, Guo X, Lu Y, Zhao W, He S, Wang X, Zhang X, Liu P Vitousek. Exploring global changes in agricultural ammonia emissions and their contribution to nitrogen deposition since 1980. Proceedings of the National Academy of Sciences of the United States of America , 2022, 119( 14): e2121998119 https://doi.org/10.1073/pnas.2121998119 pmid: 35344440
6	F M, Martin S, Uroz D G Barker. Ancestral alliances: plant mutualistic symbioses with fungi and bacteria. Science , 2017, 356( 6340): eaad4501 https://doi.org/10.1126/science.aad4501 pmid: 28546156
7	Eck N J, van L Waltman. Software survey: VOSviewer, a computer program for bibliometric mapping. Scientometrics , 2010, 84( 2): 523–538 https://doi.org/10.1007/s11192-009-0146-3 pmid: 20585380
8	D, Coskun D T, Britto W, Shi H J Kronzucker. Nitrogen transformations in modern agriculture and the role of biological nitrification inhibition. Nature Plants , 2017, 3( 6): 17074 https://doi.org/10.1038/nplants.2017.74 pmid: 28585561
9	N, Wrage G L, Velthof Beusichem M L, van O Oenema. Role of nitrifier denitrification in the production of nitrous oxide. Soil Biology & Biochemistry , 2001, 33( 12-13): 1723–1732 https://doi.org/10.1016/S0038-0717(01)00096-7
10	H, Daims E V, Lebedeva P, Pjevac P, Han C, Herbold M, Albertsen N, Jehmlich M, Palatinszky J, Vierheilig A, Bulaev R H, Kirkegaard Bergen M, von T, Rattei B, Bendinger P H, Nielsen M Wagner. Complete nitrification by Nitrospira bacteria. Nature , 2015, 528( 7583): 504–509 https://doi.org/10.1038/nature16461 pmid: 26610024
11	Kessel M A H J, van D R, Speth M, Albertsen P H, Nielsen den Camp H J M, Op B, Kartal M S M, Jetten S Lücker. Complete nitrification by a single microorganism. Nature , 2015, 528( 7583): 555–559 https://doi.org/10.1038/nature16459 pmid: 26610025
12	T, Shen M, Stieglmeier J, Dai T, Urich C Schleper. Responses of the terrestrial ammonia-oxidizing archaeon Ca. Nitrososphaera viennensis and the ammonia-oxidizing bacterium Nitrosospira multiformis to nitrification inhibitors. FEMS Microbiology Letters , 2013, 344( 2): 121–129 https://doi.org/10.1111/1574-6968.12164 pmid: 23617238
13	K, Fan M, Delgado-Baquerizo X, Guo D, Wang Y, Wu M, Zhu W, Yu H, Yao Y G, Zhu H Chu. Suppressed N fixation and diazotrophs after four decades of fertilization. Microbiome , 2019, 7( 1): 143 https://doi.org/10.1186/s40168-019-0757-8 pmid: 31672173
14	X, Shi H, Hu J, Wang J, He C, Zheng X, Wan Z Huang. Niche separation of comammox Nitrospira and canonical ammonia oxidizers in an acidic subtropical forest soil under long-term nitrogen deposition. Soil Biology & Biochemistry , 2018, 126 : 114–122 https://doi.org/10.1016/j.soilbio.2018.09.004
15	G, Zhu X, Ju J, Zhang C, Müller R M, Rees R E, Thorman R Sylvester-Bradley. Effects of the nitrification inhibitor DMPP (3,4-dimethylpyrazole phosphate) on gross N transformation rates and N2O emissions. Biology and Fertility of Soils , 2019, 55( 6): 603–615 https://doi.org/10.1007/s00374-019-01375-6
16	J, Friedl C, Scheer D W, Rowlings M T, Mumford P R Grace. The nitrification inhibitor DMPP (3,4-dimethylpyrazole phosphate) reduces N2 emissions from intensively managed pastures in subtropical Australia. Soil Biology & Biochemistry , 2017, 108 : 55–64 https://doi.org/10.1016/j.soilbio.2017.01.016
17	W, Xia C, Zhang X, Zeng Y, Feng J, Weng X, Lin J, Zhu Z, Xiong J, Xu Z, Cai Z Jia. Autotrophic growth of nitrifying community in an agricultural soil. ISME Journal , 2011, 5( 7): 1226–1236 https://doi.org/10.1038/ismej.2011.5 pmid: 21326337
18	L M, Zhang H W, Hu J P, Shen J Z He. Ammonia-oxidizing archaea have more important role than ammonia-oxidizing bacteria in ammonia oxidation of strongly acidic soils. ISME Journal , 2012, 6( 5): 1032–1045 https://doi.org/10.1038/ismej.2011.168 pmid: 22134644
19	L M, Zhang P R, Offre J Z, He D T, Verhamme G W, Nicol J I Prosser. Autotrophic ammonia oxidation by soil thaumarchaea. Proceedings of the National Academy of Sciences of the United States of America , 2010, 107( 40): 17240–17245 https://doi.org/10.1073/pnas.1004947107 pmid: 20855593
20	J, Harter H M, Krause S, Schuettler R, Ruser M, Fromme T, Scholten A, Kappler S Behrens. Linking N2O emissions from biochar-amended soil to the structure and function of the N-cycling microbial community. ISME Journal , 2014, 8( 3): 660–674 https://doi.org/10.1038/ismej.2013.160 pmid: 24067258
21	H J, Xu X H, Wang H, Li H Y, Yao J Q, Su Y G Zhu. Biochar impacts soil microbial community composition and nitrogen cycling in an acidic soil planted with rape. Environmental Science & Technology , 2014, 48( 16): 9391–9399 https://doi.org/10.1021/es5021058 pmid: 25054835
22	Y, Zhong J, Hu Q, Xia S, Zhang X, Li X, Pan R, Zhao R, Wang W, Yan Z, Shangguan F, Hu C, Yang W Wang. Soil microbial mechanisms promoting ultrahigh rice yield. Soil Biology & Biochemistry , 2020, 143 : 107741 https://doi.org/10.1016/j.soilbio.2020.107741
23	D, Abalos Z, Liang P, Dörsch L Elsgaard. Trade-offs in greenhouse gas emissions across a liming-induced gradient of soil pH: role of microbial structure and functioning. Soil Biology & Biochemistry , 2020, 150 : 108006 https://doi.org/10.1016/j.soilbio.2020.108006
24	M, Zhang R J E, Alves D, Zhang L, Han J, He L Zhang. Time-dependent shifts in populations and activity of bacterial and archaeal ammonia oxidizers in response to liming in acidic soils. Soil Biology & Biochemistry , 2017, 112 : 77–89 https://doi.org/10.1016/j.soilbio.2017.05.001
25	T, Huang H, Yang C, Huang X Ju. Effect of fertilizer N rates and straw management on yield-scaled nitrous oxide emissions in a maize-wheat double cropping system. Field Crops Research , 2017, 204 : 1–11 https://doi.org/10.1016/j.fcr.2017.01.004
26	C, Xu X, Han S, Ru L, Cárdenas R M, Rees D, Wu W, Wu F Meng. Crop straw incorporation interacts with N fertilizer on N2O emissions in an intensively cropped farmland. Geoderma , 2019, 341 : 129–137 https://doi.org/10.1016/j.geoderma.2019.01.014
27	L, Xia S K, Lam B, Wolf R, Kiese D, Chen K Butterbach-Bahl. Trade-offs between soil carbon sequestration and reactive nitrogen losses under straw return in global agroecosystems. Global Change Biology , 2018, 24( 12): 5919–5932 https://doi.org/10.1111/gcb.14466 pmid: 30295405
28	Y Q, Wang R, Bai H J, Di L Y, Mo B, Han L M, Zhang J Z He. Differentiated mechanisms of biochar mitigating straw-induced greenhouse gas emissions in two contrasting paddy Soils. Frontiers in Microbiology , 2018, 9 : 2566 https://doi.org/10.3389/fmicb.2018.02566 pmid: 30483220
29	Y, Cheng A S, Elrys A M, Merwad H, Zhang Z, Chen J, Zhang Z, Cai C Müller. Global patterns and drivers of soil dissimilatory nitrate reduction to ammonium. Environmental Science & Technology , 2022, 56( 6): 3791–3800 https://doi.org/10.1021/acs.est.1c07997 pmid: 35226464
30	L, Lassaletta G, Billen B, Grizzetti J, Anglade J Garnier. 50 year trends in nitrogen use efficiency of world cropping systems: the relationship between yield and nitrogen input to cropland. Environmental Research Letters , 2014, 9( 10): 105011 https://doi.org/10.1088/1748-9326/9/10/105011
31	Y, Wang C, Li Y, Kou J, Wang B, Tu H, Li X, Li C, Wang M Yao. Soil pH is a major driver of soil diazotrophic community assembly in Qinghai-Tibet alpine meadows. Soil Biology & Biochemistry , 2017, 115 : 547–555 https://doi.org/10.1016/j.soilbio.2017.09.024
32	W, Shi H, Zhao Y, Chen J, Wang B, Han C, Li J, Lu L Zhang. Organic manure rather than phosphorus fertilization primarily determined asymbiotic nitrogen fixation rate and the stability of diazotrophic community in an upland red soil. Agriculture, Ecosystems & Environment , 2021, 319 : 107535 https://doi.org/10.1016/j.agee.2021.107535
33	X, Wu Y, Liu Y, Shang D, Liu W, Liesack Z, Cui J, Peng F Zhang. Peat-vermiculite alters microbiota composition towards increased soil fertility and crop productivity. Plant and Soil , 2022, 470( 1−2): 21–34 https://doi.org/10.1007/s11104-021-04851-x
34	X, Wu J, Peng P, Liu Q, Bei C, Rensing Y, Li H, Yuan W, Liesack F, Zhang Z Cui. Metagenomic insights into nitrogen and phosphorus cycling at the soil aggregate scale driven by organic material amendments. Science of the Total Environment , 2021, 785 : 147329 https://doi.org/10.1016/j.scitotenv.2021.147329 pmid: 33940418
35	R, Bai Y, Fang L, Mo J, Shen L, Song Y, Wang L, Zhang J He. Greater promotion of DNRA rates and nrfA gene transcriptional activity by straw incorporation in alkaline than in acidic paddy soils. Soil Ecology Letters , 2020, 2( 4): 255–267 https://doi.org/10.1007/s42832-020-0050-6
36	R, Cavicchioli W J, Ripple K N, Timmis F, Azam L R, Bakken M, Baylis M J, Behrenfeld A, Boetius P W, Boyd A T, Classen T W, Crowther R, Danovaro C M, Foreman J, Huisman D A, Hutchins J K, Jansson D M, Karl B, Koskella Welch D B, Mark J B H, Martiny M A, Moran V J, Orphan D S, Reay J V, Remais V I, Rich B K, Singh L Y, Stein F J, Stewart M B, Sullivan Oppen M J H, van S C, Weaver E A, Webb N S Webster. Scientists’ warning to humanity: microorganisms and climate change. Nature Reviews: Microbiology , 2019, 17( 9): 569–586 https://doi.org/10.1038/s41579-019-0222-5 pmid: 31213707
37	G E D Oldroyd. Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nature Reviews: Microbiology , 2013, 11( 4): 252–263 https://doi.org/10.1038/nrmicro2990 pmid: 23493145
38	B, Li Y Y, Li H M, Wu F F, Zhang C J, Li X X, Li H, Lambers L Li. Root exudates drive interspecific facilitation by enhancing nodulation and N2 fixation. Proceedings of the National Academy of Sciences of the United States of America , 2016, 113( 23): 6496–6501 https://doi.org/10.1073/pnas.1523580113 pmid: 27217575
39	B, Sun Y, Gao X, Wu H, Ma C, Zheng X, Wang H, Zhang Z, Li H Yang. The relative contributions of pH, organic anions, and phosphatase to rhizosphere soil phosphorus mobilization and crop phosphorus uptake in maize/alfalfa polyculture. Plant and Soil , 2020, 447( 1−2): 117–133 https://doi.org/10.1007/s11104-019-04110-0
40	H A K M, Zakir G V, Subbarao S J, Pearse S, Gopalakrishnan O, Ito T, Ishikawa N, Kawano K, Nakahara T, Yoshihashi H, Ono M Yoshida. Detection, isolation and characterization of a root-exuded compound, methyl 3-(4-hydroxyphenyl) propionate, responsible for biological nitrification inhibition by sorghum (Sorghum bicolor). New Phytologist , 2008, 180( 2): 442–451 https://doi.org/10.1111/j.1469-8137.2008.02576.x pmid: 18657214
41	G V, Subbarao K, Nakahara M P, Hurtado H, Ono D E, Moreta A F, Salcedo A T, Yoshihashi T, Ishikawa M, Ishitani M, Ohnishi-Kameyama M, Yoshida M, Rondon I M, Rao C E, Lascano W L, Berry O Ito. Evidence for biological nitrification inhibition in Brachiaria pastures. Proceedings of the National Academy of Sciences of the United States of America , 2009, 106( 41): 17302–17307 https://doi.org/10.1073/pnas.0903694106 pmid: 19805171
42	L, Sun Y, Lu F, Yu H J, Kronzucker W Shi. Biological nitrification inhibition by rice root exudates and its relationship with nitrogen-use efficiency. New Phytologist , 2016, 212( 3): 646–656 https://doi.org/10.1111/nph.14057 pmid: 27292630
43	C A, O′Sullivan I R P, Fillery M M, Roper R A Richards. Identification of several wheat landraces with biological nitrification inhibition capacity. Plant and Soil , 2016, 404( 1−2): 61–74 https://doi.org/10.1007/s11104-016-2822-4
44	J, Otaka G V, Subbarao H, Ono T Yoshihashi. Biological nitrification inhibition in maize—isolation and identification of hydrophobic inhibitors from root exudates. Biology and Fertility of Soils , 2022, 58( 3): 251–264 https://doi.org/10.1007/s00374-021-01577-x
45	C, Bardon F, Piola F, Bellvert F E Z, Haichar G, Comte G, Meiffren T, Pommier S, Puijalon N, Tsafack F Poly. Evidence for biological denitrification inhibition (BDI) by plant secondary metabolites. New Phytologist , 2014, 204( 3): 620–630 https://doi.org/10.1111/nph.12944 pmid: 25059468
46	S, Nie H, Li X, Yang Z, Zhang B, Weng F, Huang G B, Zhu Y G Zhu. Nitrogen loss by anaerobic oxidation of ammonium in rice rhizosphere. ISME Journal , 2015, 9( 9): 2059–2067 https://doi.org/10.1038/ismej.2015.25 pmid: 25689022
47	A C, Finzi R Z, Abramoff K S, Spiller E R, Brzostek B A, Darby M A, Kramer R P Phillips. Rhizosphere processes are quantitatively important components of terrestrial carbon and nutrient cycles. Global Change Biology , 2015, 21( 5): 2082–2094 https://doi.org/10.1111/gcb.12816 pmid: 25421798
48	P B L, George D, Lallias S, Creer F M, Seaton J G, Kenny R M, Eccles R I, Griffiths I, Lebron B A, Emmett D A, Robinson D L Jones. Divergent national-scale trends of microbial and animal biodiversity revealed across diverse temperate soil ecosystems. Nature Communications , 2019, 10( 1): 1107 https://doi.org/10.1038/s41467-019-09031-1 pmid: 30846683
49	J, Zhang Y X, Liu N, Zhang B, Hu T, Jin H, Xu Y, Qin P, Yan X, Zhang X, Guo J, Hui S, Cao X, Wang C, Wang H, Wang B, Qu G, Fan L, Yuan R, Garrido-Oter C, Chu Y Bai. NRT1.1B is associated with root microbiota composition and nitrogen use in field-grown rice. Nature Biotechnology , 2019, 37( 6): 676–684 https://doi.org/10.1038/s41587-019-0104-4 pmid: 31036930
50	J P, Lynch C F, Strock H M, Schneider J S, Sidhu I, Ajmera T, Galindo-Castañeda S P, Klein M T Hanlon. Root anatomy and soil resource capture. Plant and Soil , 2021, 466( 1−2): 21–63 https://doi.org/10.1007/s11104-021-05010-y
51	Y G, Zhu C, Xiong Z, Wei Q L, Chen B, Ma S Y, Zhou J, Tan L M, Zhang H L, Cui G L Duan. Impacts of global change on the phyllosphere microbiome. New Phytologist , 2022, 234( 6): 1977–1986 https://doi.org/10.1111/nph.17928 pmid: 34921429
52	M, Madhaiyan T H H, Alex S T, Ngoh B, Prithiviraj L Ji. Leaf-residing Methylobacterium species fix nitrogen and promote biomass and seed production in Jatropha curcas . Biotechnology for Biofuels , 2015, 8(1): 222
53	F, Batool Y, Rehman S Hasnain. Phylloplane associated plant bacteria of commercially superior wheat varieties exhibit superior plant growth promoting abilities. Frontiers in Life Science , 2016, 9( 4): 313–322 https://doi.org/10.1080/21553769.2016.1256842
54	V V S R, Gupta B, Zhang C R, Penton J, Yu J M Tiedje. Diazotroph diversity and nitrogen fixation in summer active perennial grasses in a mediterranean region agricultural soil. Frontiers in Molecular Biosciences , 2019, 6 : 115 https://doi.org/10.3389/fmolb.2019.00115 pmid: 31750314
55	M, Fürnkranz W, Wanek A, Richter G, Abell F, Rasche A Sessitsch. Nitrogen fixation by phyllosphere bacteria associated with higher plants and their colonizing epiphytes of a tropical lowland rainforest of Costa Rica. ISME Journal , 2008, 2( 5): 561–570 https://doi.org/10.1038/ismej.2008.14 pmid: 18273066
56	C, Knief A, Ramette L, Francès C, Alonso-Blanco J A Vorholt. Site and plant species are important determinants of the Methylobacterium community composition in the plant phyllosphere. ISME Journal , 2010, 4( 6): 719–728 https://doi.org/10.1038/ismej.2010.9 pmid: 20164863
57	C, Xiong B K, Singh J Z, He Y L, Han P P, Li L H, Wan G Z, Meng S Y, Liu J T, Wang C F, Wu A H, Ge L M Zhang. Plant developmental stage drives the differentiation in ecological role of the maize microbiome. Microbiome , 2021, 9( 1): 171 https://doi.org/10.1186/s40168-021-01118-6 pmid: 34389047
58	S, Bowatte P C D, Newton S, Brock P, Theobald D Luo. Bacteria on leaves: a previously unrecognised source of N2O in grazed pastures. ISME Journal , 2015, 9( 1): 265–267 https://doi.org/10.1038/ismej.2014.118 pmid: 25012902
59	S P, Brown M A, Grillo J C, Podowski K D Heath. Soil origin and plant genotype structure distinct microbiome compartments in the model legume Medicago truncatula . Microbiome , 2020, 8(1): 139
60	A, Abdelfattah M, Wisniewski L, Schena A J M Tack. Experimental evidence of microbial inheritance in plants and transmission routes from seed to phyllosphere and root. Environmental Microbiology , 2021, 23( 4): 2199–2214 https://doi.org/10.1111/1462-2920.15392 pmid: 33427409
61	H J, Di K C, Cameron R G Mclaren. Isotopic dilution methods to determine the gross transformation rates of nitrogen, phosphorus, and sulfur in soil: a review of the theory, methodologies, and limitations. Soil Research , 2000, 38( 1): 213–230 https://doi.org/10.1071/SR99005
62	R Bardgett. The biology of soil: a community and ecosystem approach. Cambridge: Oxford university press, 2005
63	M, Mooshammer W, Wanek I, Hämmerle L, Fuchslueger F, Hofhansl A, Knoltsch J, Schnecker M, Takriti M, Watzka B, Wild K M, Keiblinger S, Zechmeister-Boltenstern A Richter. Adjustment of microbial nitrogen use efficiency to carbon:nitrogen imbalances regulates soil nitrogen cycling. Nature Communications , 2014, 5( 1): 3694 https://doi.org/10.1038/ncomms4694 pmid: 24739236
64	C, Nevison P, Hess C, Goodale Q,Vira J Zhu. Nitrification, denitrification, and competition for soil N: evaluation of two earth system models against observations. Ecological Applications , 2022, e2528
65	S, Guo W, Xiong X, Hang Z, Gao Z, Jiao H, Liu Y, Mo N, Zhang G A, Kowalchuk R, Li Q, Shen S Geisen. Protists as main indicators and determinants of plant performance. Microbiome , 2021, 9( 1): 64 https://doi.org/10.1186/s40168-021-01025-w pmid: 33743825
66	C, Santi D, Bogusz C Franche. Biological nitrogen fixation in non-legume plants. Annals of Botany , 2013, 111( 5): 743–767 https://doi.org/10.1093/aob/mct048 pmid: 23478942
67	O, Coban Deyn G B, De der Ploeg M van. Soil microbiota as game-changers in restoration of degraded lands. Science , 2022, 375( 6584): abe0725 https://doi.org/10.1126/science.abe0725 pmid: 35239372
68	J, Verzeaux B, Hirel F, Dubois P J, Lea T Tétu. Agricultural practices to improve nitrogen use efficiency through the use of arbuscular mycorrhizae: basic and agronomic aspects. Plant Science , 2017, 264 : 48–56 https://doi.org/10.1016/j.plantsci.2017.08.004 pmid: 28969802
69	M Parniske. Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nature Reviews: Microbiology , 2008, 6( 10): 763–775 https://doi.org/10.1038/nrmicro1987 pmid: 18794914
70	F, Lesuffleur F, Paynel M P, Bataillé Deunff E, Le J B Cliquet. Root amino acid exudation: measurement of high efflux rates of glycine and serine from six different plant species. Plant and Soil , 2007, 294( 1−2): 235–246 https://doi.org/10.1007/s11104-007-9249-x
71	H W, Hu J He. Manipulating the soil microbiome for improved nitrogen management. Microbiology Australia , 2018, 39( 1): 24–27 https://doi.org/10.1071/MA18007
72	W W, Xia J, Zhao Y, Zheng H M, Zhang J B, Zhang R R, Chen X G, Lin Z J Jia. Active soil nitrifying communities revealed by in situ transcriptomics and microcosm-based stable-isotope probing. Applied and Environmental Microbiology , 2020, 86( 23): e01807-20 https://doi.org/10.1128/AEM.01807-20 pmid: 32978127
73	Q L, Chen J, Ding Y G, Zhu J Z, He H W Hu. Soil bacterial taxonomic diversity is critical to maintaining the plant productivity. Environment International , 2020, 140 : 105766 https://doi.org/10.1016/j.envint.2020.105766 pmid: 32371308
74	C, Xiong Y G, Zhu J T, Wang B, Singh L L, Han J P, Shen P P, Li G B, Wang C F, Wu A H, Ge L M, Zhang J Z He. Host selection shapes crop microbiome assembly and network complexity. New Phytologist , 2021, 229( 2): 1091–1104 https://doi.org/10.1111/nph.16890 pmid: 32852792
75	Y, Shi M, Delgado-Baquerizo Y, Li Y, Yang Y G, Zhu J, Peñuelas H Chu. Abundance of kinless hubs within soil microbial networks are associated with high functional potential in agricultural ecosystems. Environment International , 2020, 142 : 105869 https://doi.org/10.1016/j.envint.2020.105869 pmid: 32593837
76	Vries F T, de Groenigen J W, van E, Hoffland J Bloem. Nitrogen losses from two grassland soils with different fungal biomass. Soil Biology & Biochemistry , 2011, 43( 5): 997–1005 https://doi.org/10.1016/j.soilbio.2011.01.016
77	Vries F T, de M E, Liiri L, Bjornlund M A, Bowker S, Christensen H M, Setala R D Bardgett. Land use alters the resistance and resilience of soil food webs to drought. Nature Climate Change , 2012, 2( 4): 276–280 https://doi.org/10.1038/nclimate1368
78	L, Su T, Bai X, Qin H, Yu G, Wu Q, Zhao L Tan. Organic manure induced soil food web of microbes and nematodes drive soil organic matter under jackfruit planting. Applied Soil Ecology , 2021, 166 : 103994 https://doi.org/10.1016/j.apsoil.2021.103994
79	B A, Hungate J C, Marks M E, Power E, Schwartz Groenigen K J, van S J, Blazewicz P, Chuckran P, Dijkstra B K, Finley M K, Firestone M, Foley A, Greenlon M, Hayer K S, Hofmockel B J, Koch M C, Mack R L, Mau S N, Miller E M, Morrissey J R, Propster A M, Purcell E, Sieradzki E P, Starr B W G, Stone C, Terrer J Pett-Ridge. The functional significance of bacterial predators. mBio , 2021, 12( 2): e00466-21 https://doi.org/10.1128/mBio.00466-21 pmid: 33906922
80	S J, Leroux D, Hawlena O J Schmitz. Predation risk, stoichiometric plasticity and ecosystem elemental cycling. Proceedings. Biological Sciences , 2012, 279( 1745): 4183–4191 https://doi.org/10.1098/rspb.2012.1315 pmid: 22896643
81	J P, Schimel J Bennett. Nitrogen mineralization: challenges of a changing paradigm. Ecology , 2004, 85( 3): 591–602 https://doi.org/10.1890/03-8002
82	Z B, Zhao J Z, He S, Geisen L L, Han J T, Wang J P, Shen W X, Wei Y T, Fang P P, Li L M Zhang. Protist communities are more sensitive to nitrogen fertilization than other microorganisms in diverse agricultural soils. Microbiome , 2019, 7( 1): 33 https://doi.org/10.1186/s40168-019-0647-0 pmid: 30813951

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