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    					| Phosphorus use efficiency and fertilizers: future opportunities for improvements |  
						| Martin BLACKWELL1(  ), Tegan DARCH1, Richard HASLAM2 |  
						| 1. Department of Sustainable Agriculture Sciences, Rothamsted Research, North Wyke, Okehampton, EX20 2SB, UK 2. Department of Plant Sciences, Rothamsted Research, Harpenden, AL5 2JQ, UK
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													    | Abstract The continued supply of phosphate fertilizers that underpin global food production is an imminent crisis. The rock phosphate deposits on which the world depends are not only finite, but some are contaminated, and many are located in geopolitically unstable areas, meaning that fundamental changes will have to take place in order to maintain food production for a growing global population. No single solution exists, but a combination of approaches to phosphorus management is required not only to extend the lifespan of the remaining non-renewable rock phosphate reserves, but to result in a more efficient, sustainable phosphorus cycle. Solutions include improving the efficiency of fertilizer applications to agricultural land, alongside a better understanding of phosphorus cycling in soil-plant systems, and the interactions between soil physics, chemistry and biology, coupled with plant traits. Opportunities exist for the development of plants that can access different forms of soil phosphorus (e.g., organic phosphorus) and that use internal phosphorus more efficiently. The development of different sources of phosphorus fertilizers are inevitably required given the finite nature of the rock phosphate supplies. Clear opportunities exist, and it is now important that a concerted effort to make advances in phosphorus use efficiency is prioritized. |  
															| Keywords 
																																																				organic phosphorus  
																		  																																				phosphorus fertilizer  
																		  																																				phosphorus use efficiency  
																		  																																				rock phosphate |  
															| Corresponding Author(s):
																Martin BLACKWELL |  
															| Just Accepted Date: 30 July 2019  
																																														Online First Date: 23 September 2019   
																																														Issue Date: 29 November 2019 |  |  
								            
								                
																																												
															| 1 | U S G Survey. Mineral commodity summaries. Available at USGS website (NMIC, National Minerals Information Center) on February 11, 2019 |  
															| 2 | D Cordell, S White. Peak phosphorus: clarifying the key issues of a vigorous debate about long-term phosphorus security. Sustainability, 2011, 3(10): 2027–2049 https://doi.org/10.3390/su3102027
 |  
															| 3 | AHDB. Review of AHDB-funded research on phosphorus management in arable crops. Research Review No. 93. Available at AHDB (Agriculture and Horticulture Development Board) website on April 26, 2019 |  
															| 4 | D J Conley, H W Paerl, R W Howarth, D F Boesch, S P Seitzinger, K E Havens, C Lancelot, G E Likens. Controlling eutrophication: nitrogen and phosphorus. Science, 2009, 323(5917): 1014–1015 https://doi.org/10.1126/science.1167755
														     															     															     		pmid: 19229022
 |  
															| 5 | S Z Sattari, A F Bouwman, K E Giller, M K van Ittersum. Residual soil phosphorus as the missing piece in the global phosphorus crisis puzzle. Proceedings of the National Academy of Sciences of the United States of America, 2012, 109(16): 6348–6353 https://doi.org/10.1073/pnas.1113675109
														     															     															     		pmid: 22431593
 |  
															| 6 | M I Stutter, C A Shand, T S George, M S A Blackwell, R Bol, R L Mackay, A E Richardson, L M Condron, B L Turner, P M Haygarth. Recovering phosphorus from soil: a root solution? Environmental Science & Technology, 2012, 46(4): 1977–1978 https://doi.org/10.1021/es2044745
														     															     															     		pmid: 22280364
 |  
															| 7 | D Menezes-Blackburn, C Giles, T Darch, T S George, M Blackwell, M Stutter, C Shand, D Lumsdon, P Cooper, R Wendler, L Brown, D S Almeida, C Wearing, H Zhang, P M Haygarth. Opportunities for mobilizing recalcitrant phosphorus from agricultural soils: a review. Plant and Soil, 2018, 427(1–2): 5–16 https://doi.org/10.1007/s11104-017-3362-2
														     															     															     		pmid: 30996482
 |  
															| 8 | A Sinclair, B Crooks, T Edwards, M Coull. Technical Note TN 668. Available at FAS (Farm Advisory Servixe) website on July 15, 2019 |  
															| 9 | L Jordan-Meille, G H Rubaek, P A I Ehlert, V Genot, G Hofman, K Goulding, J Recknagel, G Provolo, P Barraclough. An overview of fertilizer-P recommendations in Europe: soil testing, calibration and fertilizer recommendations. Soil Use and Management, 2012, 28(4): 419–435 https://doi.org/10.1111/j.1475-2743.2012.00453.x
 |  
															| 10 | J Hislop, I J Cooke. Anion exchange resin as a means of assessing soil phosphate status—a laboratory technique. Soil Science, 1968, 105(1): 8–11 https://doi.org/10.1097/00010694-196801000-00003
 |  
															| 11 | H Zhang, W Davison, R Gadi, T Kobayashi. In situ measurement of dissolved phosphorus in natural waters using DGT. Analytica Chimica Acta, 1998, 370(1): 29–38 https://doi.org/10.1016/S0003-2670(98)00250-5
														     															     															     		pmid: 21168548
 |  
															| 12 | I C R Holford. Evaluation of soil phosphate buffering indexes. Australian Journal of Soil Research, 1979, 17(3): 495–504 https://doi.org/10.1071/SR9790495
 |  
															| 13 | AHDB. RB209 Section 3: grass and forage crops. Available at AHDB (Agriculture and Horticulture Development Board) website on February 20, 2019 |  
															| 14 | D Menezes-Blackburn, C Paredes, H Zhang, C D Giles, T Darch, M Stutter, T S George, C Shand, D Lumsdon, P Cooper, R Wendler, L Brown, M Blackwell, C Wearing, P M Haygarth. Organic acids regulation of chemical-microbial phosphorus transformations in soils. Environmental Science & Technology, 2016, 50(21): 11521–11531 https://doi.org/10.1021/acs.est.6b03017
														     															     															     		pmid: 27700099
 |  
															| 15 | S Nawara, T Van Dael, R Merckx, F Amery, A Elsen, W Odeurs, H Vandendriessche, S McGrath, C Roisin, C Jouany, S Pellerin, P Denoroy, B Eichler-Lobermann, G Borjesson, P Goos, W Akkermans, E Smolders. A comparison of soil tests for available phosphorus in long-term field experiments in Europe. European Journal of Soil Science, 2017, 68(6): 873–885 https://doi.org/10.1111/ejss.12486
 |  
															| 16 | S Mason, A McNeill, M J McLaughlin, H Zhang. Prediction of wheat response to an application of phosphorus under field conditions using diffusive gradients in thin-films (DGT) and extraction methods. Plant and Soil, 2010, 337(1–2): 243–258 https://doi.org/10.1007/s11104-010-0521-0
 |  
															| 17 | S D Speirs, B J Scott, P W Moody, S D Mason. Soil phosphorus tests II: a comparison of soil test-crop response relationships for different soil tests and wheat. Crop & Pasture Science, 2013, 64(5): 469–479 https://doi.org/10.1071/CP13111
 |  
															| 18 | R Recena, I Diaz-de la Torre, A M Garcia-Lopez, A Delgado. The determination of total phosphorus improves the accuracy of the bicarbonate extraction as an availability index. Soil Use and Management, 2019, 35(2): 346–354 https://doi.org/10.1111/sum.12498
 |  
															| 19 | R Recena, I Diaz, A Delgado. Estimation of total plant available phosphorus in representative soils from Mediterranean areas. Geoderma, 2017, 297: 10–18 https://doi.org/10.1016/j.geoderma.2017.02.016
 |  
															| 20 | T S George, P J Gregory, P Hocking, A E Richardson. Variation in root-associated phosphatase activities in wheat contributes to the utilization of organic P substrates in vitro, but does not explain differences in the P-nutrition of plants when grown in soils. Environmental and Experimental Botany, 2008, 64(3): 239–249 https://doi.org/10.1016/j.envexpbot.2008.05.002
 |  
															| 21 | C D Giles, A E Richardson, B J Cade-Menun, M M Mezeli, L K Brown, D Menezes-Blackburn, T Darch, M S A Blackwell, C A Shand, M I Stutter, R Wendler, P Cooper, D G Lumsdon, C Wearing, H Zhang, P M Haygarth, T S George. Phosphorus acquisition by citrate- and phytase-exuding Nicotiana tabacum plant mixtures depends on soil phosphorus availability and root intermingling. Physiologia Plantarum, 2018, 163(3): 356–371 https://doi.org/10.1111/ppl.12718
														     															     															     		pmid: 29498417
 |  
															| 22 | P J A Withers, R Sylvester-Bradley, D L Jones, J R Healey, P J Talboys. Feed the crop not the soil: rethinking phosphorus management in the food chain. Environmental Science & Technology, 2014, 48(12): 6523–6530 https://doi.org/10.1021/es501670j
														     															     															     		pmid: 24840064
 |  
															| 23 | P J Gregory, S Nortcliff. Soil conditions and plant growth. Chicester: Wiley-Blackwell, 2013 |  
															| 24 | B L Turner, M S A Blackwell. Isolating the influence of pH on the amounts and forms of soil organic phosphorus. European Journal of Soil Science, 2013, 64(2): 249–259 https://doi.org/10.1111/ejss.12026
 |  
															| 25 | T Darch, M S A Blackwell, J M B Hawkins, P M Haygarth, D Chadwick. A meta-analysis of organic and inorganic phosphorus in organic fertilizers, soils, and water: implications for water quality. Critical Reviews in Environmental Science and Technology, 2014, 44(19): 2172–2202 https://doi.org/10.1080/10643389.2013.790752
 |  
															| 26 | A G Nino-Savala, X Zhang, X Ma, A Fangmeier, H Li, A Tang, X J Liu. Cadmium pollution from phosphate fertilizers in arable soils and crops: an overview. Frontiers of Agricultural Science and Engineering, 2019. doi: 10.15302/J-FASE-2019273 |  
															| 27 | R Rietra, M Heinen, C O Dimkpa, P S Bindraban. Effects of nutrient antagonism and synergism on yield and fertilizer use efficiency. Communications in Soil Science and Plant Analysis, 2017, 48(16): 1895–1920 https://doi.org/10.1080/00103624.2017.1407429
 |  
															| 28 | M E Sumner, M P W Farina. Phosphorus interactions with other nutrients and lime in field cropping systems. New York:Springer, 1986, 201–236 |  
															| 29 | V D Fageria. Nutrient interactions in crop plants. Journal of Plant Nutrition, 2001, 24(8): 1269–1290 https://doi.org/10.1081/PLN-100106981
 |  
															| 30 | M Eggersdorfer, K Kraemer, J B Cordaro, J Fanzo, M J Gibney, E T Kennedy, A Labrique, J Steffen. Good nutrition: perspectives for the 21st Century. Basel: Karger, 2016 |  
															| 31 | M A Hossain, T Kamiya, D J Burritt, L S P Tran, T Fujiwara. Plant macronutrient use efficiency: molecular and genomic perspectives in crop plants. Pittsburgh, USA: Academic Press, 2018. doi: 10.1016/C2016-0-03180-7 |  
															| 32 | 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
 |  
															| 33 | D M S B Dissanayaka, W C Plaxton, H Lambers, M Siebers, B Marambe, J Wasaki. Molecular mechanisms underpinning phosphorus-use efficiency in rice. Plant, Cell & Environment, 2018, 41(7): 1483–1496 https://doi.org/10.1111/pce.13191
														     															     															     		pmid: 29520969
 |  
															| 34 | H Lambers, G R Cawthray, P Giavalisco, J Kuo, E Laliberté, S J Pearse, W R Scheible, M Stitt, F Teste, B L Turner. Proteaceae from severely phosphorus-impoverished soils extensively replace phospholipids with galactolipids and sulfolipids during leaf development to achieve a high photosynthetic phosphorus-use-efficiency. New Phytologist, 2012, 196(4): 1098–1108 https://doi.org/10.1111/j.1469-8137.2012.04285.x
														     															     															     		pmid: 22937909
 |  
															| 35 | B Yu, C Xu, C Benning. Arabidopsis disrupted in SQD2 encoding sulfolipid synthase is impaired in phosphate-limited growth. Proceedings of the National Academy of Sciences of the United States of America, 2002, 99(8): 5732–5737 https://doi.org/10.1073/pnas.082696499
														     															     															     		pmid: 11960029
 |  
															| 36 | J P Hammond, S Mayes, H C Bowen, N S Graham, R M Hayden, C G Love, W P Spracklen, J Wang, S J Welham, P J White, G J King, M R Broadley. Regulatory hotspots are associated with plant gene expression under varying soil phosphorus supply in Brassica rapa. Plant Physiology, 2011, 156(3): 1230–1241 https://doi.org/10.1104/pp.111.175612
														     															     															     		pmid: 21527424
 |  
															| 37 | P Mehra, B K Pandey, J Giri. Comparative morphophysiological analyses and molecular profiling reveal Pi-efficient strategies of a traditional rice genotype. Frontiers of Plant Science, 2016, 6: 1184 https://doi.org/10.3389/fpls.2015.01184
														     															     															     		pmid: 26779218
 |  
															| 38 | J P Hammond, M J Bennett, H C Bowen, M R Broadley, D C Eastwood, S T May, C Rahn, R Swarup, K E Woolaway, P J White. Changes in gene expression in Arabidopsis shoots during phosphate starvation and the potential for developing smart plants. Plant Physiology, 2003, 132(2): 578–596 https://doi.org/10.1104/pp.103.020941
														     															     															     		pmid: 12805589
 |  
															| 39 | P Wu, L Ma, X Hou, M Wang, Y Wu, F Liu, X W Deng. Phosphate starvation triggers distinct alterations of genome expression in Arabidopsis roots and leaves. Plant Physiology, 2003, 132(3): 1260–1271 https://doi.org/10.1104/pp.103.021022
														     															     															     		pmid: 12857808
 |  
															| 40 | J Misson, K G Raghothama, A Jain, J Jouhet, M A Block, R Bligny, P Ortet, A Creff, S Somerville, N Rolland, P Doumas, P Nacry, L Herrerra-Estrella, L Nussaume, M C Thibaud. A genome-wide transcriptional analysis using Arabidopsis thaliana Affymetrix gene chips determined plant responses to phosphate deprivation. Proceedings of the National Academy of Sciences of the United States of America, 2005, 102(33): 11934–11939 https://doi.org/10.1073/pnas.0505266102
														     															     															     		pmid: 16085708
 |  
															| 41 | R Morcuende, R Bari, Y Gibon, W Zheng, B D Pant, O Bläsing, B Usadel, T Czechowski, M K Udvardi, M Stitt, W R Scheible. Genome-wide reprogramming of metabolism and regulatory networks of Arabidopsis in response to phosphorus. Plant, Cell & Environment, 2007, 30(1): 85–112 https://doi.org/10.1111/j.1365-3040.2006.01608.x
														     															     															     		pmid: 17177879
 |  
															| 42 | R W Brooker, A E Bennett, W F Cong, T J Daniell, T S George, P D Hallett, C Hawes, P P Iannetta, H G Jones, A J Karley, L Li, B M McKenzie, R J Pakeman, E Paterson, C Schöb, J Shen, G Squire, C A Watson, C Zhang, F Zhang, J Zhang, P J White. Improving intercropping: a synthesis of research in agronomy, plant physiology and ecology. New Phytologist, 2015, 206(1): 107–117 https://doi.org/10.1111/nph.13132
														     															     															     		pmid: 25866856
 |  
															| 43 | E Betencourt, M Duputel, B Colomb, D Desclaux, P Hinsinger. Intercropping promotes the ability of durum wheat and chickpea to increase rhizosphere phosphorus availability in a low P soil. Soil Biology & Biochemistry, 2012, 46: 181–190 https://doi.org/10.1016/j.soilbio.2011.11.015
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