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Frontiers of Agricultural Science and Engineering

ISSN 2095-7505

ISSN 2095-977X(Online)

CN 10-1204/S

Postal Subscription Code 80-906

Front. Agr. Sci. Eng.    2019, Vol. 6 Issue (4) : 321-331    https://doi.org/10.15302/J-FASE-2019283
REVIEW
Innovations of phosphorus sustainability: implications for the whole chain
Jianbo SHEN1, Liyang WANG1, Xiaoqiang JIAO1, Fanlei MENG1, Lin ZHANG1, Gu FENG1, Junling ZHANG1, Lixing YUAN1, Lin MA2, Yong HOU1, Tao ZHANG3, Weifeng ZHANG1, Guohua LI1, Kai ZHANG1, Fusuo ZHANG1()
1. National Academy of Agriculture Green Development, Key Laboratory of Plant-Soil Interactions, Ministry of Education, College of Resources and Environmental Sciences, China Agricultural University, Beijing 100193, China
2. Key Laboratory of Agricultural Water Resources, Center for Agricultural Resources Research, Institute of Genetic and Developmental Biology, Chinese Academy of Sciences, Shijiazhuang 050021, China
3. Department of Environmental Science and Engineering, College of Resources and Environmental Sciences, China Agricultural University, Beijing 100193, China
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Abstract

Phosphorus (P) is a non-renewable resource, therefore ensuring global food and environmental security depends upon sustainable P management. To achieve this goal, sustainable P management in the upstream and downstream sectors of agriculture from mineral extraction to food consumption must be addressed systematically. The innovation and feasibility of P sustainability are highlighted from the perspective of the whole P-based chain, including the mining and processing of P rock, production of P fertilizers, soil and rhizosphere processes involving P, absorption and utilization of P by plants, P in livestock production, as well as flow and management of P at the catchment scale. The paper also emphasizes the importance of recycling P and the current challenges of P recovery. Finally, sustainable solutions of holistic P management are proposed from the perspective of technology improvement with policy support.

Keywords P-use efficiency      recycling      sustainable management      the whole P chain     
Corresponding Author(s): Fusuo ZHANG   
Just Accepted Date: 10 October 2019   Online First Date: 07 November 2019    Issue Date: 29 November 2019
 Cite this article:   
Jianbo SHEN,Liyang WANG,Xiaoqiang JIAO, et al. Innovations of phosphorus sustainability: implications for the whole chain[J]. Front. Agr. Sci. Eng. , 2019, 6(4): 321-331.
 URL:  
https://academic.hep.com.cn/fase/EN/10.15302/J-FASE-2019283
https://academic.hep.com.cn/fase/EN/Y2019/V6/I4/321
Fig.1  Conceptual model for a P flow chain, and sustainable use and recycling at different scales. (a) P flow chain; (b) sustainable P use and recycling.
1 R B Chowdhury, G A Moore, A J Weatherley, M Arora. Key sustainability challenges for the global phosphorus resource, their implications for global food security, and options for mitigation. Journal of Cleaner Production, 2017, 140: 945–963
https://doi.org/10.1016/j.jclepro.2016.07.012
2 D Cordell, J O Drangert, S White. The story of phosphorus: global food security and food for thought. Global Environmental Change, 2009, 19(2): 292–305
https://doi.org/10.1016/j.gloenvcha.2008.10.009
3 N Gilbert. Environment: The disappearing nutrient. Nature, 2009, 461(7265): 716–718
https://doi.org/10.1038/461716a pmid: 19812648
4 J Elser, E Bennett. Phosphorus cycle: a broken biogeochemical cycle. Nature, 2011, 478(7367): 29–31
https://doi.org/10.1038/478029a pmid: 21979027
5 J G Shepherd, R Kleemann, J Bahri-Esfahani, L Hudek, L Suriyagoda, E Vandamme, K C van Dijk. The future of phosphorus in our hands. Nutrient Cycling in Agroecosystems, 2016, 104(3): 281–287
https://doi.org/10.1007/s10705-015-9742-1
6 J Shen, L Yuan, J Zhang, H Li, Z Bai, X Chen, W Zhang, F Zhang. Phosphorus dynamics: from soil to plant. Plant Physiology, 2011, 156(3): 997–1005
https://doi.org/10.1104/pp.111.175232 pmid: 21571668
7 A Leip, G Billen, J Garnier, B Grizzetti, L Lassaletta, S Reis, D Simpson, M A Sutton, W de Vries, F Weiss, H Westhoek. Impacts of European livestock production: nitrogen, sulphur, phosphorus and greenhouse gas emissions, land-use, water eutrophication and biodiversity. Environmental Research Letters, 2015, 10(11): 115004
https://doi.org/10.1088/1748-9326/10/11/115004
8 Y Hou, L Ma, Z L Gao, F H Wang, J T Sims, W Q Ma, F S Zhang. The driving forces for nitrogen and phosphorus flows in the food chain of china, 1980 to 2010. Journal of Environmental Quality, 2013, 42(4): 962–971
https://doi.org/10.2134/jeq2012.0489 pmid: 24216348
9 United States Geological Survey. Mineral commodity summaries. Available at United States Geological Survey website on June 15, 2019
10 Y Li, W Zhang, L Ma, G Huang, O Oenema, F Zhang, Z Dou. An analysis of China’s fertilizer policies: impacts on the industry, food security, and the environment. Journal of Environmental Quality, 2013, 42(4): 972–981
https://doi.org/10.2134/jeq2012.0465 pmid: 24216349
11 G Li, G Huang, H Li, M Van Ittersum, P Leffelaar, F Zhang. Identifying potential strategies in the key sectors of China’s food chain to implement sustainable phosphorus management: a review. Nutrient Cycling in Agroecosystems, 2016, 104(3): 341–359
https://doi.org/10.1007/s10705-015-9736-z
12 J Shen, F Zhang, K H M Siddique. Sustainable resource use in enhancing agricultural development in China. Engineering, 2018, 4(5): 588–589
https://doi.org/10.1016/j.eng.2018.08.007
13 M Zeng, W de Vries, L T C Bonten, Q Zhu, T Hao, X Liu, M Xu, X Shi, F Zhang, J Shen. Model-based analysis of the long-term effects of fertilization management on cropland soil acidification. Environmental Science & Technology, 2017, 51(7): 3843–3851
https://doi.org/10.1021/acs.est.6b05491 pmid: 28264162
14 Ministry of Agriculture and Rural Affairs of People’s Republic of China. Plan of actions aiming for zero growth in synthetic fertilizer use from 2020 onwards (in Chinese, 2015). Available at Ministry of Agriculture and Rural Affairs of the People’s Republic of China website on June 20, 2019
15 R H Bray, L T Kurtz. Determination of total, organic, and available forms of phosphorus in soils. Soil Science, 1945, 59(1): 39–45
https://doi.org/10.1097/00010694-194501000-00006
16 J Shen, R Li, F Zhang, J Fan, C Tang, Z Rengel. Crop yields, soil fertility and phosphorus fractions in response to long-term fertilization under the rice monoculture system on a calcareous soil. Field Crops Research, 2004, 86(2–3): 225–238
https://doi.org/10.1016/j.fcr.2003.08.013
17 I C R Holford. Soil phosphorus: its measurement, and its uptake by plants. Australian Journal of Soil Research, 1997, 35(2): 227–239
https://doi.org/10.1071/S96047
18 E H Oelkers, E Valsami-Jones. Phosphate mineral reactivity and global sustainability. Elements, 2008, 4(2): 83–87
https://doi.org/10.2113/GSELEMENTS.4.2.83
19 P Hinsinger. Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review. Plant and Soil, 2001, 237(2): 173–195
https://doi.org/10.1023/A:1013351617532
20 R Parfitt. Phosphate reactions with natural allophane, ferrihydrite and goethite. Journal of Soil Science, 1989, 40(2): 359–369
https://doi.org/10.1111/j.1365-2389.1989.tb01280.x
21 L L Willard. Chemical equilibria in soils. Chichester, UK: John Wiley & Sons, 1979
22 H Li, G Huang, Q Meng, L Ma, L Yuan, F Wang, W Zhang, Z Cui, J Shen, X Chen, R Jiang, F Zhang. Integrated soil and plant phosphorus management for crop and environment in China. A review. Plant and Soil, 2011, 349(1–2): 157–167
https://doi.org/10.1007/s11104-011-0909-5
23 S R Carpenter. Phosphorus control is critical to mitigating eutrophication. Proceedings of the National Academy of Sciences of the United States of America, 2008, 105(32): 11039–11040
https://doi.org/10.1073/pnas.0806112105 pmid: 18685114
24 Z Yuan, S Jiang, H Sheng, X Liu, H Hua, X Liu, Y Zhang. Human perturbation of the global phosphorus cycle: changes and consequences. Environmental Science & Technology, 2018, 52(5): 2438–2450
https://doi.org/10.1021/acs.est.7b03910 pmid: 29402084
25 F Zhang, J Shen, J Zhang, Y Zuo, L Li, X Chen. Rhizosphere processes and management for improving nutrient use efficiency and crop productivity: implications for China. Advances in Agronomy, 2010, 107: 1–32
https://doi.org/10.1016/S0065-2113(10)07001-X
26 J Shen, C Li, G Mi, L Li, L Yuan, R Jiang, F Zhang. Maximizing root/rhizosphere efficiency to improve crop productivity and nutrient use efficiency in intensive agriculture of China. Journal of Experimental Botany, 2013, 64(5): 1181–1192
https://doi.org/10.1093/jxb/ers342 pmid: 23255279
27 L Wang, J Shen. Root/rhizosphere management for improving phosphorus use efficiency and crop productivity. Better Crops with Plant Food, 2019, 103(1): 36–39
https://doi.org/10.24047/BC103136
28 Y Lyu, H Tang, H Li, F Zhang, Z Rengel, W R Whalley, J Shen. Major crop species show differential balance between root morphological and physiological responses to variable phosphorus supply. Frontiers of Plant Science, 2016, 7: 1939
https://doi.org/10.3389/fpls.2016.01939 pmid: 28066491
29 H Marschner. Marschner’s mineral nutrition of higher plants, Ed 3. London, UK: Academic Press, 2011
30 K Jin, J Shen, R W Ashton, I C Dodd, M A J Parry, W R Whalley. How do roots elongate in a structured soil? Journal of Experimental Botany, 2013, 64(15): 4761–4777
https://doi.org/10.1093/jxb/ert286 pmid: 24043852
31 Z Wen, H Li, Q Shen, X Tang, C Xiong, H Li, J Pang, M H Ryan, H Lambers, J Shen. Tradeoffs among root morphology, exudation and mycorrhizal symbioses for phosphorus-acquisition strategies of 16 crop species. New Phytologist, 2019, 223(2): 882–895
https://doi.org/10.1111/nph.15833 pmid: 30932187
32 T Kautz, W Amelung, F Ewert, T Gaiser, R Horn, R Jahn, M Javaux, A Kemna, Y Kuzyakov, J C Munch, S Patzold, S Peth, H W Scherer, M Schloter, H Schneider, J Vanderborght, D Vetterlein, A Walter, G L B Wiesenberg, U Kopke. Nutrient acquisition from arable subsoils in temperate climates: a review. Soil Biology & Biochemistry, 2013, 57: 1003–1022
https://doi.org/10.1016/j.soilbio.2012.09.014
33 S L Bauke, C von Sperber, F Tamburini, M I Gocke, B Honermeier, K Schweitzer, M Baumecker, A Don, A Sandhage-Hofmann, W Amelung. Subsoil phosphorus is affected by fertilization regime in long-term agricultural experimental trials. European Journal of Soil Science, 2018, 69(1): 103–112
https://doi.org/10.1111/ejss.12516
34 D Zhang, C Zhang, X Tang, H Li, F Zhang, Z Rengel, W R Whalley, W J Davies, J Shen. Increased soil phosphorus availability induced by faba bean root exudation stimulates root growth and phosphorus uptake in neighbouring maize. New Phytologist, 2016, 209(2): 823–831
https://doi.org/10.1111/nph.13613 pmid: 26313736
35 B L Wang, X Y Tang, L Y Cheng, A Z Zhang, W H Zhang, F S Zhang, J Q Liu, Y Cao, D L Allan, C P Vance, J B Shen. Nitric oxide is involved in phosphorus deficiency-induced cluster-root development and citrate exudation in white lupin. New Phytologist, 2010, 187(4): 1112–1123
https://doi.org/10.1111/j.1469-8137.2010.03323.x pmid: 20553395
36 B L Wang, J B Shen, W H Zhang, F S Zhang, G Neumann. Citrate exudation from white lupin induced by phosphorus deficiency differs from that induced by aluminum. New Phytologist, 2007, 176(3): 581–589
https://doi.org/10.1111/j.1469-8137.2007.02206.x pmid: 17725555
37 X Li, E George, H Marschner. Phosphorus depletion and pH decrease at the root soil and hyphae soil interfaces of VA mycorrhizal white clover fertilized with ammonium. New Phytologist, 1991, 119(3): 397–404
https://doi.org/10.1111/j.1469-8137.1991.tb00039.x
38 F Wang, R Jiang, M A Kertesz, F Zhang, G Feng. Arbuscular mycorrhizal fungal hyphae mediating acidification can promote phytate mineralization in the hyphosphere of maize (Zea mays L.). Soil Biology & Biochemistry, 2013, 65: 69–74
https://doi.org/10.1016/j.soilbio.2013.05.010
39 E Tisserant, M Malbreil, A Kuo, A Kohler, A Symeonidi, R Balestrini, P Charron, N Duensing, N Frei dit Frey, V Gianinazzi-Pearson, L B Gilbert, Y Handa, J R Herr, M Hijri, R Koul, M Kawaguchi, F Krajinski, P J Lammers, F G Masclaux, C Murat, E Morin, S Ndikumana, M Pagni, D Petitpierre, N Requena, P Rosikiewicz, R Riley, K Saito, H San Clemente, H Shapiro, D van Tuinen, G Bécard, P Bonfante, U Paszkowski, Y Y Shachar-Hill, G A Tuskan, J P Young, I R Sanders, B Henrissat, S A Rensing, I V Grigoriev, N Corradi, C Roux, F Martin. Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis. Proceedings of the National Academy of Sciences of the United States of America, 2013, 110(50): 20117–20122
https://doi.org/10.1073/pnas.1313452110 pmid: 24277808
40 L Zhang, J Fan, X Ding, X He, F Zhang, G Feng. Hyphosphere interactions between an arbuscular mycorrhizal fungus and a phosphate solubilizing bacterium promote phytate mineralization in soil. Soil Biology & Biochemistry, 2014, 74: 177–183
https://doi.org/10.1016/j.soilbio.2014.03.004
41 J F Toljander, V Artursson, L R Paul, J K Jansson, R D Finlay. Attachment of different soil bacteria to arbuscular mycorrhizal fungal extraradical hyphae is determined by hyphal vitality and fungal species. FEMS Microbiology Letters, 2006, 254(1): 34–40
https://doi.org/10.1111/j.1574-6968.2005.00003.x pmid: 16451176
42 T R Scheublin, I R Sanders, C Keel, J R van der Meer. Characterisation of microbial communities colonising the hyphal surfaces of arbuscular mycorrhizal fungi. ISME Journal, 2010, 4(6): 752–763
https://doi.org/10.1038/ismej.2010.5 pmid: 20147983
43 L Zhang, G Feng, S Declerck. Signal beyond nutrient, fructose, exuded by an arbuscular mycorrhizal fungus triggers phytate mineralization by a phosphate solubilizing bacterium. ISME Journal, 2018, 12(10): 2339–2351
https://doi.org/10.1038/s41396-018-0171-4 pmid: 29899507
44 L Zhang, X Ding, Y Peng, T S George, G Feng. Closing the loop on phosphorus loss from intensive agricultural soil: a microbial immobilization solution? Frontiers in Microbiology, 2018, 9: 104
https://doi.org/10.3389/fmicb.2018.00104 pmid: 29467734
45 L Zhang, M Xu, Y Liu, F Zhang, A Hodge, G Feng. Carbon and phosphorus exchange may enable cooperation between an arbuscular mycorrhizal fungus and a phosphate-solubilizing bacterium. New Phytologist, 2016, 210(3): 1022–1032
https://doi.org/10.1111/nph.13838 pmid: 27074400
46 L Zhang, N Shi, J Fan, F Wang, T S George, G Feng. Arbuscular mycorrhizal fungi stimulate organic phosphate mobilization associated with changing bacterial community structure under field conditions. Environmental Microbiology, 2018, 20(7): 2639–2651
https://doi.org/10.1111/1462-2920.14289 pmid: 29901256
47 F Wang, M A Kertesz, G Feng. Phosphorus forms affect the hyphosphere bacterial community involved in soil organic phosphorus turnover. Mycorrhiza, 2019, 29(4): 351–362
https://doi.org/10.1007/s00572-019-00896-0 pmid: 31044298
48 J D Bever. Preferential allocation, physio-evolutionary feedbacks, and the stability and environmental patterns of mutualism between plants and their root symbionts. New Phytologist, 2015, 205(4): 1503–1514
https://doi.org/10.1111/nph.13239 pmid: 25561086
49 J D Bever, I A Dickie, E Facelli, J M Facelli, J Klironomos, M Moora, M C Rillig, W D Stock, M Tibbett, M Zobel. Rooting theories of plant community ecology in microbial interactions. Trends in Ecology & Evolution, 2010, 25(8): 468–478
https://doi.org/10.1016/j.tree.2010.05.004 pmid: 20557974
50 R L Berendsen, C M J Pieterse, P A H M Bakker. The rhizosphere microbiome and plant health. Trends in Plant Science, 2012, 17(8): 478–486
https://doi.org/10.1016/j.tplants.2012.04.001 pmid: 22564542
51 N Dombrowski, K Schlaeppi, M T Agler, S Hacquard, E Kemen, R Garrido-Oter, J Wunder, G Coupland, P Schulze-Lefert. Root microbiota dynamics of perennial Arabis alpina are dependent on soil residence time but independent of flowering time. ISME Journal, 2017, 11(1): 43–55
https://doi.org/10.1038/ismej.2016.109 pmid: 27482927
52 K Hartman, M G A van der Heijden, V Roussely-Provent, J C Walser, K Schlaeppi. Deciphering composition and function of the root microbiome of a legume plant. Microbiome, 2017, 5(1): 2
https://doi.org/10.1186/s40168-016-0220-z pmid: 28095877
53 W H van der Putten, R D Bardgett, J D Bever, T M Bezemer, B B Casper, T Fukami, P Kardol, J N Klironomos, A Kulmatiski, J A Schweitzer, K N Suding, T F J Van de Voorde, D A Wardle. Plant-soil feedbacks: the past, the present and future challenges. Journal of Ecology, 2013, 101(2): 265–276
https://doi.org/10.1111/1365-2745.12054
54 K M Crawford, J T Bauer, L S Comita, M B Eppinga, D J Johnson, S A Mangan, S A Queenborough, A E Strand, K N Suding, J Umbanhowar, J D Bever. When and where plant-soil feedback may promote plant coexistence: a meta-analysis. Ecology Letters, 2019, 22(8): 1274–1284
https://doi.org/10.1111/ele.13278 pmid: 31149765
55 W H van der Putten, M A Bradford, E P Brinkman, T F J van de Voorde, G F Veen. Where, when and how plant-soil feedback matters in a changing world. Functional Ecology, 2016, 30(7): 1109–1121
https://doi.org/10.1111/1365-2435.12657
56 A E Richardson, R J Simpson. Soil microorganisms mediating phosphorus availability update on microbial phosphorus. Plant Physiology, 2011, 156(3): 989–996
https://doi.org/10.1104/pp.111.175448 pmid: 21606316
57 C Mander, S Wakelin, S Young, L Condron, M O’Callaghan. Incidence and diversity of phosphate-solubilising bacteria are linked to phosphorus status in grassland soils. Soil Biology & Biochemistry, 2012, 44(1): 93–101
https://doi.org/10.1016/j.soilbio.2011.09.009
58 D Revillini, C A Gehring, N C Johnson. The role of locally adapted mycorrhizas and rhizobacteria in plant-soil feedback systems. Functional Ecology, 2016, 30(7): 1086–1098
https://doi.org/10.1111/1365-2435.12668
59 C Baxendale, K H Orwin, F Poly, T Pommier, R D Bardgett. Are plant-soil feedback responses explained by plant traits? New Phytologist, 2014, 204(2): 408–423
https://doi.org/10.1111/nph.12915 pmid: 24995955
60 E Laliberté, H Lambers, T I Burgess, S J Wright. Phosphorus limitation, soil-borne pathogens and the coexistence of plant species in hyperdiverse forests and shrublands. New Phytologist, 2015, 206(2): 507–521
https://doi.org/10.1111/nph.13203 pmid: 25494682
61 F P Teste, P Kardol, B L Turner, D A Wardle, G Zemunik, M Renton, E Laliberté. Plant-soil feedback and the maintenance of diversity in Mediterranean-climate shrublands. Science, 2017, 355(6321): 173–176
https://doi.org/10.1126/science.aai8291 pmid: 28082588
62 M A Miguel, J A Postma, J P Lynch. Phene synergism between root hair length and basal root growth angle for phosphorus acquisition. Plant Physiology, 2015, 167(4): 1430–1439
https://doi.org/10.1104/pp.15.00145 pmid: 25699587
63 G Mi, F Chen, L Yuan, F Zhang. Ideotype root system architecture for maize to achieve high yield and resource use efficiency in intensive cropping systems. Advances in Agronomy, 2016, 139: 73–97
https://doi.org/10.1016/bs.agron.2016.05.002
64 R Gamuyao, J H Chin, J Pariasca-Tanaka, P Pesaresi, S Catausan, C Dalid, I Slamet-Loedin, E M Tecson-Mendoza, M Wissuwa, S Heuer. The protein kinase PSTOL1 from traditional rice confers tolerance of phosphorus deficiency. Nature, 2012, 488(7412): 535–539
https://doi.org/10.1038/nature11346 pmid: 22914168
65 R Gu, F Chen, L Long, H Cai, Z Liu, J Yang, L Wang, H Li, J Li, W Liu, G Mi, F Zhang, L Yuan. Enhancing phosphorus uptake efficiency through QTL-based selection for root system architecture in maize. Journal of Genetics and Genomics, 2016, 43(11): 663–672
https://doi.org/10.1016/j.jgg.2016.11.002 pmid: 27889500
66 E J Veneklaas, H Lambers, J Bragg, P M Finnegan, C E Lovelock, W C Plaxton, C A Price, W R Scheible, M W Shane, P J White, J A Raven. Opportunities for improving phosphorus-use efficiency in crop plants. New Phytologist, 2012, 195(2): 306–320
https://doi.org/10.1111/j.1469-8137.2012.04190.x pmid: 22691045
67 T Takami, N Ohnishi, Y Kurita, S Iwamura, M Ohnishi, M Kusaba, T Mimura, W Sakamoto. Organelle DNA degradation contributes to the efficient use of phosphate in seed plants. Nature Plants, 2018, 4(12): 1044–1055
https://doi.org/10.1038/s41477-018-0291-x pmid: 30420711
68 N Yamaji, Y Takemoto, T Miyaji, N Mitani-Ueno, K T Yoshida, J F Ma. Reducing phosphorus accumulation in rice grains with an impaired transporter in the node. Nature, 2017, 541(7635): 92–95
https://doi.org/10.1038/nature20610 pmid: 28002408
69 L Xu, H Zhao, R Wan, Y Liu, Z Xu, W Tian, W Ruan, F Wang, M Deng, J Wang, L Dolan, S Luan, S Xue, K Yi. Identification of vacuolar phosphate efflux transporters in land plants. Nature Plants, 2019, 5(1): 84–94
https://doi.org/10.1038/s41477-018-0334-3 pmid: 30626920
70 T J Chiou, S I Lin. Signaling network in sensing phosphate availability in plants. Annual Review of Plant Biology, 2011, 62(1): 185–206
https://doi.org/10.1146/annurev-arplant-042110-103849 pmid: 21370979
71 R Wild, R Gerasimaite, J Y Jung, V Truffault, I Pavlovic, A Schmidt, A Saiardi, H J Jessen, Y Poirier, M Hothorn, A Mayer. Control of eukaryotic phosphate homeostasis by inositol polyphosphate sensor domains. Science, 2016, 352(6288): 986–990
https://doi.org/10.1126/science.aad9858 pmid: 27080106
72 B Hu, Z Jiang, W Wang, Y Qiu, Z Zhang, Y Liu, A Li, X Gao, L Liu, Y Qian, X Huang, F Yu, S Kang, Y Wang, J Xie, S Cao, L Zhang, Y Wang, Q Xie, S Kopriva, C Chu. Nitrate-NRT1.1B-SPX4 cascade integrates nitrogen and phosphorus signalling networks in plants. Nature Plants, 2019, 5(4): 401–413
https://doi.org/10.1038/s41477-019-0384-1 pmid: 30911122
73 National Bureau of Statistics of China. China Statistical Yearbook. Beijing: China Statistics Press,2015 (in Chinese)
74 Z Bai, L Ma, W Ma, W Qin, G Velthof, O Oenema, F Zhang. Changes in phosphorus use and losses in the food chain of China during 1950–2010 and forecasts for 2030. Nutrient Cycling in Agroecosystems, 2016, 104(3): 361–372
https://doi.org/10.1007/s10705-015-9737-y
75 Z Bai, W Ma, L Ma, G L Velthof, Z Wei, P Havlík, O Oenema, M R Lee, F. ZhangChina’s livestock transition: driving forces, impacts, and consequences. Science Advances, 2018, 4(7): eaar8534
76 G H Li, M K van Ittersum, P A Leffelaar, S Z Sattari, H Li, G Huang, F Zhang. A multi-level analysis of China’s phosphorus flows to identify options for improved management in agriculture. Agricultural Systems, 2016, 144: 87–100
https://doi.org/10.1016/j.agsy.2016.01.006
77 Z Luo, S Ma, S Hu, D Chen. Towards the sustainable development of the regional phosphorus resources industry in China: a system dynamics approach. Resources, Conservation and Recycling, 2017, 126: 186–197
https://doi.org/10.1016/j.resconrec.2017.07.018
78 W Zhang, W Ma, Y Ji, M Fan, O Oenema, F Zhang. Efficiency, economics, and environmental implications of phosphorus resource use and the fertilizer industry in China. Nutrient Cycling in Agroecosystems, 2008, 80(2): 131–144
https://doi.org/10.1007/s10705-007-9126-2
79 A Sharpley, B Foy, P Withers. Practical and innovative measures for the control of agricultural phosphorus losses to water: an overview. Journal of Environmental Quality, 2000, 29(1): 1–9
https://doi.org/10.2134/jeq2000.00472425002900010001x
80 R McDowell, A Sharpley. Variation of phosphorus leached from Pennsylvanian soils amended with manures, composts or inorganic fertilizer. Agriculture, Ecosystems & Environment, 2004, 102(1): 17–27
https://doi.org/10.1016/j.agee.2003.07.002
81 M S Aulakh, A K Garg, B S Kabba. Phosphorus accumulation, leaching and residual effects on crop yields from long-term applications in the subtropics. Soil Use and Management, 2007, 23(4): 417–427
https://doi.org/10.1111/j.1475-2743.2007.00124.x
82 United States Geological Survey. Mineral commodity summaries. Available at United States Geological Survey website on March 15, 2019
83 B E Rittmann, B Mayer, P Westerhoff, M Edwards. Capturing the lost phosphorus. Chemosphere, 2011, 84(6): 846–853
https://doi.org/10.1016/j.chemosphere.2011.02.001 pmid: 21377188
84 Ministry of Agriculture and Rural Affairs of the People’ Republic of China. The plan for promoting the pilot project of recycling agricultural wastes (in Chinese). Available at Ministry of Agriculture and Rural Affairs of the People’s Republic of China website on April 3, 2019
85 E Desmidt, K Ghyselbrecht, Y Zhang, L Pinoy, B Van der Bruggen, W Verstraete, K Rabaey, B Meesschaert. Global phosphorus scarcity and full-scale P-recovery techniques: a review. Critical Reviews in Environmental Science and Technology, 2015, 45(4): 336–384
https://doi.org/10.1080/10643389.2013.866531
86 M El Wali, S R Golroudbary, A Kraslawski. Impact of recycling improvement on the life cycle of phosphorus. Chinese Journal of Chemical Engineering, 2019, 27(5): 1219–1229
https://doi.org/10.1016/j.cjche.2018.09.004
87 B K Mayer, L A Baker, T H Boyer, P Drechsel, M Gifford, M A Hanjra, P Parameswaran, J Stoltzfus, P Westerhoff, B E Rittmann. Total value of phosphorus recovery. Environmental Science & Technology, 2016, 50(13): 6606–6620
https://doi.org/10.1021/acs.est.6b01239 pmid: 27214029
88 L Ma, J Guo, G L Velthof, Y Li, Q Chen, W Ma, O Oenema, F Zhang. Impacts of urban expansion on nitrogen and phosphorus flows in the food system of Beijing from 1978 to 2008. Global Environmental Change, 2014, 28: 192–204
https://doi.org/10.1016/j.gloenvcha.2014.06.015
89 F Li, S Cheng, H Yu, D Yang. Waste from livestock and poultry breeding and its potential assessment of biogas energy in rural China. Journal of Cleaner Production, 2016, 126: 451–460
https://doi.org/10.1016/j.jclepro.2016.02.104
90 J Némery, J Garnier. Biogeochemistry: the fate of phosphorus. Nature Geoscience, 2016, 9(5): 343–344
https://doi.org/10.1038/ngeo2702
91 R Huang, C Fang, X Lu, R Jiang, Y Tang. Transformation of phosphorus during (hydro)thermal treatments of solid biowastes: reaction mechanisms and implications for P reclamation and recycling. Environmental Science & Technology, 2017, 51(18): 10284–10298
https://doi.org/10.1021/acs.est.7b02011 pmid: 28876917
92 D Montalvo, M J McLaughlin, F Degryse. Efficacy of hydroxyapatite nanoparticles as phosphorus fertilizer in andisols and oxisols. Soil Science Society of America Journal, 2015, 79(2): 551–558
https://doi.org/10.2136/sssaj2014.09.0373
93 M Everaert, F Degryse, M J McLaughlin, D De Vos, E Smolders. Agronomic effectiveness of granulated and powdered P-exchanged Mg-Al LDH relative to struvite and MAP. Journal of Agricultural and Food Chemistry, 2017, 65(32): 6736–6744
https://doi.org/10.1021/acs.jafc.7b01031 pmid: 28731709
94 T I McLaren, R J Smernik, R J Simpson, M J McLaughlin, T M McBeath, C N Guppy, A E Richardson. The chemical nature of organic phosphorus that accumulates in fertilized soils of a temperate pasture as determined by solution 31P NMR spectroscopy. Journal of Plant Nutrition and Soil Science, 2017, 180(1): 27–38
https://doi.org/10.1002/jpln.201600076
95 D F da Cruz, R Bortoletto-Santos, G G F Guimarães, W L Polito, C Ribeiro. Role of polymeric coating on the phosphate availability as a fertilizer: insight from phosphate release by castor polyurethane coatings. Journal of Agricultural and Food Chemistry, 2017, 65(29): 5890–5895
https://doi.org/10.1021/acs.jafc.7b01686 pmid: 28640614
96 X Jiao, Y Lyu, X Wu, H Li, L Cheng, C Zhang, L Yuan, R Jiang, B Jiang, Z Rengel, F Zhang, W J Davies, J Shen. Grain production versus resource and environmental costs: towards increasing sustainability of nutrient use in China. Journal of Experimental Botany, 2016, 67(17): 4935–4949
https://doi.org/10.1093/jxb/erw282 pmid: 27489235
97 T N Nortey, J F Patience, P H Simmins, N L Trottier, R T Zijlstra. Effects of individual or combined xylanase and phytase supplementation on energy, amino acid, and phosphorus digestibility and growth performance of grower pigs fed wheat-based diets containing wheat millrun. Journal of Animal Science, 2007, 85(6): 1432–1443
https://doi.org/10.2527/jas.2006-613 pmid: 17325125
98 W Christel, S Bruun, J Magid, W Kwapinski, L S Jensen. Pig slurry acidification, separation technology and thermal conversion affect phosphorus availability in soil amended with the derived solid fractions, chars or ashes. Plant and Soil, 2016, 401(1–2): 93–107
https://doi.org/10.1007/s11104-015-2519-0
99 P J Talboys, J Heppell, T Roose, J R Healey, D L Jones, P J Withers. Struvite: a slow-release fertiliser for sustainable phosphorus management? Plant and Soil, 2016, 401(1–2): 109–123
https://doi.org/10.1007/s11104-015-2747-3 pmid: 27429478
100 Third Sustainable Phosphorus Summit. Blueprint global phosphorus security. Sydney, Australia: University of Technology Sydney,2012
101 H Rowe, P J A Withers, P Baas, N I Chan, D Doody, J Holiman, B Jacobs, H Li, G K MacDonald, R McDowell, A N Sharpley, J Shen, W Taheri, M Wallenstein, M N Weintraub. Integrating legacy soil phosphorus into sustainable nutrient management strategies for future food, bioenergy and water security. Nutrient Cycling in Agroecosystems, 2016, 104(3): 393–412
https://doi.org/10.1007/s10705-015-9726-1
102 E D Roy. Phosphorus recovery and recycling with ecological engineering: a review. Ecological Engineering, 2017, 98: 213–227
https://doi.org/10.1016/j.ecoleng.2016.10.076
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