Replace, reuse, recycle: Improving the sustainable use of phosphorus by plants

Journal of Experimental Botany

Volumn 66, Issue 12, 2015, Pages 3523-3540

  Baker, Alison ^a   Ceasar, S Antony ^a,b   Palmer, Antony J ^a   Paterson, Jaimie B ^a   Qi, Wanjun ^a   Muench, Stephen P ^a   Baldwin, Stephen A ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

^b LOYOLA COLLEGE   (India)

Author keywords

Fertilizers; Membrane transporters; Nutrient recycling; Phosphate; Phosphate signalling; Transcription factors

Indexed keywords

PHOSPHORUS; PLANT PROTEIN;

CROP; ENVIRONMENTAL PROTECTION; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PLANT;

CONSERVATION OF NATURAL RESOURCES; CROPS, AGRICULTURAL; GENE EXPRESSION REGULATION, PLANT; PHOSPHORUS; PLANT PROTEINS; PLANTS;

EID: 84940702965     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/erv210     Document Type: Review

References (179)

1. Abuaku E, Frimpong K, Osei B, Verstraete W. 2006. Bio-recovery of N and P from an anaerobic digester effluent: the potential of duckweed (Lemna minor). West African Journal of Applied Ecology 10, 1-9.
2. Ai P, Sun S, Zhao J, et al. 2009. Two rice phosphate transporters, OsPht1;2 and OsPht1;6, have different functions and kinetic properties in uptake and translocation. The Plant Journal 57, 798-809.
3. Alaerts GJ, Mahbubar R, Kelderman P. 1996. Performance analysis of a full-scale duckweed-covered sewage lagoon. Water Research 30, 843-852.
4. Argus FMB, 2014. Argus FMB Phosphates: weekly phosphate report. 31 July 2014, Argus Media Ltd, London, UK.
5. Arnaud C, Clément M, Thibaud M-C, et al. 2014. Identification of phosphatin, a drug alleviating phosphate starvation responses in Arabidopsis. Plant Physiology 166, 1479-1491.
6. Arpat AB, Magliano P, Wege S, Rouached H, Stefanovic A, Poirier Y. 2012. Functional expression of PHO1 to the Golgi and trans-Golgi network and its role in export of inorganic phosphate. The Plant Journal 71, 479-491.
7. Aung K, Lin SI, Wu CC, Huang YT, Su CL, Chiou TJ. 2006. pho2, a phosphate overaccumulator, is caused by a nonsense mutation in a microRNA399 target gene. Plant Physiology 141, 1000-1011.
8. Bayle V, Arrighi JF, Creff A, Nespoulous C, Vialaret J, Rossignol M, Gonzalez E, Paz-Ares J, Nussaume L. 2011. Arabidopsis thaliana highaffinity phosphate transporters exhibit multiple levels of posttranslational regulation. The Plant Cell 23, 1523-1535.
9. Becquer A, Trap J, Irshad U, Ali MA, Claude P. 2014. From soil to plant, the outward journey of P through trophic relationships and ectomycorrhizal association. Frontiers in Plant Science 5, 548.
10. Bieleski RL. 1973. Phosphate pools, phosphate transport, and phosphate availability. Annual Review of Plant Physiology 24, 225-252.
11. Bonser AM, Lynch J, Snapp S. 1996. Effect of phosphorus deficiency on growth angle of basal roots in Phaseolus vulgaris. New Phytologist 132, 281-288.
12. Bournier M, Tissot N, Mari S, Boucherez J, Lacombe E, Briat JF, Gaymard F. 2013. Arabidopsis ferritin 1 (AtFer1) gene regulation by the phosphate starvation response 1 (AtPHR1) transcription factor reveals a direct molecular link between iron and phosphate homeostasis. Journal of Biological Chemistry 288, 22670-22680.
13. Britton A, Koch FA, Mavinic DS, Adnan A, Oldham WK, Udala B. 2005. Pilot scale struvite recovery from anaerobic digester supernatant at an enhanced biological phosphorus removal wastewater treatment plant. Journal of Environmental Engineering and Science 4, 265-277.
14. Bun-Ya M, Nishimura M, Harashima S, Oshima Y. 1991. The PHO84 gene of Saccharomyces cerevisiae encodes an inorganic phosphate transporter. Molecular and Cellular Biology 11, 3229-3238.
15. Ceasar SA, Hodge A, Baker A, Baldwin SA. 2014. Phosphate concentration and arbuscular mycorrhizal colonisation influence the growth, yield and expression of twelve PHT1 family phosphate transporters in foxtail millet (Setaria italica). PLoS One 9, e108459.
16. Chen A, Gu M, Sun S, Zhu L, Hong S, Xu G. 2011. Identification of two conserved cis-acting elements, MYCS and P1BS, involved in the regulation of mycorrhiza-activated phosphate transporters in eudicot species. New Phytologist 189, 1157-1169.
17. Chen A, Hu J, Sun S, Xu G. 2007. Conservation and divergence of both phosphate- and mycorrhiza-regulated physiological responses and expression patterns of phosphate transporters in solanaceous species. New Phytologist 173, 817-831.
18. Chen J, Liu Y, Ni J, Wang Y, Bai Y, Shi J, Gan J, Wu Z, Wu P. 2011. OsPHF1 regulates the plasma membrane localization of low- and high-affinity inorganic phosphate transporters and determines inorganic phosphate uptake and translocation in rice. Plant Physiology 157, 269-278.
19. Chen ZH, Nimmo GA, Jenkins GI, Nimmo HG. 2007. BHLH32 modulates several biochemical and morphological processes that respond to Pi starvation in Arabidopsis. Biochemical Journal 405, 191-198.
20. Chin JH, Lu X, Haefele SM, Gamuyao R, Ismail A, Wissuwa M, Heuer S. 2010. Development and application of gene-based markers for the major rice QTL Phosphorus uptake 1. Theoretical and Applied Genetics 120, 1073-1086.
21. Chiou TJ, Lin SI. 2011. Signaling network in sensing phosphate availability in plants. Annual Review of Plant Biology 62, 185-206.
22. Chopin T, Cooper JA, Reid G, Cross S, Moore C. 2012. Open-water integrated multi-trophic aquaculture: environmental biomitigation and economic diversification of fed aquaculture by extractive aquaculture. Reviews in Aquaculture 4, 209-220.
23. Cooper J, Carliell-Marquet C. 2013. A substance flow analysis of phosphorus in the UK food production and consumption system. Resources, Conservation and Recycling 74, 82-100.
24. Cordell D, Drangert JO, White S. 2009. The story of phosphorus: global food security and food for thought. Global Environmental Change-Human and Policy Dimensions 19, 292-305.
25. Dai X, Wang Y, Yang A, Zhang WH. 2012. OsMYB2P-1, an R2R3 MYB transcription factor, is involved in the regulation of phosphate-starvation responses and root architecture in rice. Plant Physiology 159, 169-183.
26. David FG, Brett FC,. 2003. Role of the genotype in tolerance to acidity and aluminum toxicity. In: Rengel Z (ed.) Hand book of soil acidity. New York: Marcel Dekker, 387-406.
27. de-Bashan LE, Bashan Y. 2004. Recent advances in removing phosphorus from wastewater and its future use as fertilizer (1997-2003). Water Research 38, 4222-4246.
28. Delhaize E, Taylor P, Hocking PJ, Simpson RJ, Ryan PR, Richardson AE. 2009. Transgenic barley (Hordeum vulgare L.) expressing the wheat aluminium resistance gene (TaALMT1) shows enhanced phosphorus nutrition and grain production when grown on an acid soil. Plant Biotechnology Journal 7, 391-400.
29. Devaiah BN, Karthikeyan AS, Raghothama KG. 2007a. WRKY75 transcription factor is a modulator of phosphate acquisition and root development in Arabidopsis. Plant Physiology 143, 1789-1801.
30. Devaiah BN, Nagarajan VK, Raghothama KG. 2007b. Phosphate homeostasis and root development in Arabidopsis are synchronized by the zinc finger transcription factor ZAT6. Plant Physiology 145, 147-159.
31. Ding, Z. J., Yan, J. Y., Xu, X. Y., Li, G. X. and Zheng, S. J. 2013. WRKY46 functions as a transcriptional repressor of ALMT1, regulating aluminuminduced malate secretion in Arabidopsis. The Plant Journal 76, 825-835.
32. Dreyer I, Gomez-Porras JL, Riano-Pachon DM, Hedrich R, Geiger D. 2012. molecular evolution of slow and quick anion channels (SLACs and QUACs/ALMTs). Frontiers in Plant Science 3, 263.
33. Duan K, Yi K, Dang L, Huang H, Wu W, Wu P. 2008. Characterization of a sub-family of Arabidopsis genes with the SPX domain reveals their diverse functions in plant tolerance to phosphorus starvation. The Plant Journal 54, 965-975.
34. Elser J, Bennett E. 2011. Phosphorus cycle: a broken biogeochemical cycle. Nature 478, 29-31.
35. Fan C, Wang X, Hu R, Wang Y, Xiao C, Jiang Y, Zhang X, Zheng C, Fu YF. 2013. The pattern of Phosphate transporter 1 genes evolutionary divergence in Glycine max L. BMC Plant Biology 13, 48.
36. Farchy J. 2013. Aluminium prices slide to four-year low. 27 November 2013, Financial Times, UK.
37. Farrell JB. Duckweed uptake of phosphorus and five pharmaceuticals: microcosm and wastewater lagoon studies. MSc thesis, Utah State University, UT, USA.
38. Fedler CB, Duan R. 2011. Biomass production for bioenergy using recycled wastewater in a natural waste treatment system. Resources, Conservation and Recycling 55, 793-800.
39. Fujita M, Mori K, Kodera T. 1999. Nutrient removal and starch production through cultivation of Wolffia arrhiza. Journal of Bioscience and Bioengineering 87, 194-198.
40. Furukawa J, Yamaji N, Wang H, Mitani N, Murata Y, Sato K, Katsuhara M, Takeda K, Ma JF. 2007. An aluminum-activated citrate transporter in barley. Plant and Cell Physiology 48, 1081-1091.
41. Gamuyao R, Chin JH, Pariasca-Tanaka J, Pesaresi P, Catausan S, Dalid C, Slamet-Loedin I, Tecson-Mendoza EM, Wissuwa M, Heuer S. 2012. The protein kinase Pstol1 from traditional rice confers tolerance of phosphorus deficiency. Nature 488, 535-539.
42. Giovannini D, Touhami J, Charnet P, Sitbon M, Battini JL. 2013. Inorganic phosphate export by the retrovirus receptor XPR1 in metazoans. Cell Reports 3, 1866-1873.
43. Glassop D, Godwin RM, Smith SE, Smith FW. 2007. Rice phosphate transporters associated with phosphate uptake in rice roots colonised with arbuscular mycorrhizal fungi. Canadian Journal of Botany-Revue Canadienne De Botanique 85, 644-651.
44. Glassop D, Smith SE, Smith FW. 2005. Cereal phosphate transporters associated with the mycorrhizal pathway of phosphate uptake into roots. Planta 222, 688-698.
45. Gonzalez E, Solano R, Rubio V, Leyva A, Paz-Ares J. 2005. PHOSPHATE TRANSPORTER TRAFFIC FACILITATOR1 is a plant-specific SEC12-related protein that enables the endoplasmic reticulum exit of a high-affinity phosphate transporter in Arabidopsis. The Plant Cell 17, 3500-3512.
46. Goopy JP, Murray PJ. 2003. A Review on the Role of Duckweed in Nutrient Reclamation and as a Source of Animal Feed. Asian-Australasian Journal of Animal Science 16, 297-305.
47. Guimil S, Chang HS, Zhu T, Sesma A, Osbourn A, Roux C, Ioannidis V, Oakeley EJ, Docquier M, Descombes P, Briggs SP, Paszkowski U. 2005. Comparative transcriptomics of rice reveals an ancient pattern of response to microbial colonization. Proceedings of the National Academy of Sciences, USA 102, 8066-8070.
48. Hamburger D, Rezzonico E, MacDonald-Comber Petetot J, Somerville C, Poirier Y. 2002. Identification and characterization of the Arabidopsis PHO1 gene involved in phosphate loading to the xylem. The Plant Cell 14, 889-902.
49. Hammond JP, White PJ. 2008. Sucrose transport in the phloem: integrating root responses to phosphorus starvation. Journal of Experimental Botany 59, 93-109.
50. Harrison MJ, Dewbre GR, Liu JY. 2002. A phosphate transporter from Medicago truncatula involved in the acquisition of phosphate released by arbuscular mycorrhizal fungi. The Plant Cell 14, 2413-2429.
51. Hernandez G, Valdes-Lopez O, Ramirez M, et al. 2009. Global changes in the transcript and metabolic profiles during symbiotic nitrogen fixation in phosphorus-stressed common bean plants. Plant Physiology 151, 1221-1238.
52. Hong JJ, Park YS, Bravo A, Bhattarai KK, Daniels DA, Harrison MJ. 2012. Diversity of morphology and function in arbuscular mycorrhizal symbioses in Brachypodium distachyon. Planta 236, 851-865.
53. Hsieh LC, Lin SI, Shih AC, Chen JW, Lin WY, Tseng CY, Li WH, Chiou TJ. 2009. Uncovering small RNA-mediated responses to phosphate deficiency in Arabidopsis by deep sequencing. Plant Physiology 151, 2120-2132.
54. Hu B, Zhu C, Li F, Tang J, Wang Y, Lin A, Liu L, Che R, Chu C. 2011. LEAF TIP NECROSIS1 plays a pivotal role in the regulation of multiple phosphate starvation responses in rice. Plant Physiology 156, 1101-1115.
55. Huang CY, Shirley N, Genc Y, Shi BJ, Langridge P. 2011. phosphate utilization efficiency correlates with expression of low-affinity phosphate transporters and noncoding RNA, IPS1, in barley. Plant Physiology 156, 1217-1229.
56. Huang TK, Han CL, Lin SI, et al. 2013. Identification of downstream components of ubiquitin-conjugating enzyme PHOSPHATE2 by quantitative membrane proteomics in Arabidopsis roots. The Plant Cell 25, 4044-4060.
57. Javot H, Penmetsa RV, Terzaghi N, Cook DR, Harrison MJ. 2007. A Medicago truncatula phosphate transporter indispensable for the arbuscular mycorrhizal symbiosis. Proceedings of the National Academy of Sciences, USA 104, 1720-1725.
58. Jia H, Ren H, Gu M, Zhao J, Sun S, Zhang X, Chen J, Wu P, Xu G. 2011. The phosphate transporter gene OsPht1;8 is involved in phosphate homeostasis in rice. Plant Physiology 156, 1164-1175.
59. Kant S, Peng M, Rothstein SJ. 2011. Genetic regulation by NLA and microRNA827 for maintaining nitrate-dependent phosphate homeostasis in Arabidopsis. PLoS Genetics 7, e1002021.
60. Karandashov V, Bucher M. 2005. Symbiotic phosphate transport in arbuscular mycorrhizas. Trends in Plant Science 10, 22-29.
61. Karthikeyan AS, Varadarajan DK, Jain A, Held MA, Carpita NC, Raghothama KG. 2007. Phosphate starvation responses are mediated by sugar signaling in Arabidopsis. Planta 225, 907-918.
62. Karthikeyan AS, Varadarajan DK, Mukatira UT, D'Urzo MP, Damsz B, Raghothama KG. 2002. Regulated expression of Arabidopsis phosphate transporters. Plant Physiology 130, 221-233.
63. Kato F, Takaoka M, Oshita K, Takeda N. 2007. Present state of phosphorus recovery from wastewater treatment. Doboku Gakkai Ronbunshuu G63, 413-424.
64. Khan GA, Bouraine S, Wege S, Li Y, de Carbonnel M, Berthomieu P, Poirier Y, Rouached H. 2014. Coordination between zinc and phosphate homeostasis involves the transcription factor PHR1, the phosphate exporter PHO1, and its homologue PHO1;H3 in Arabidopsis. Journal of Experimental Botany 65, 871-884.
65. Kochian LV. 1995. Cellular Mechanisms of Aluminum Toxicity and Resistance in Plants. Annual Review of Plant Physiology and Plant Molecular Biology 46, 237-260.
66. Kota J, Ljungdahl PO. 2005. Specialized membrane-localized chaperones prevent aggregation of polytopic proteins in the ER. Journal of Cell Biology 168, 79-88.
67. Larsdotter K. 2006. Microalgae for Phosphorus Removal from Wastewater in a Nordic Climate. Royal Institute of Technology, School of Biotechnology, Stockholm, Seden.
68. Leggewie G, Willmitzer L, Riesmeier JW. 1997. Two cDNAs from potato are able to complement a phosphate uptake-deficient yeast mutant: identification of phosphate transporters from higher plants. The Plant Cell 9, 381-392.
69. Li Z, Gao Q, Liu Y, He C, Zhang X, Zhang J. 2011. Overexpression of transcription factor ZmPTF1 improves low phosphate tolerance of maize by regulating carbon metabolism and root growth. Planta 233, 1129-1143.
70. Liao H, Rubio G, Yan X, Cao A, Brown KM, Lynch JP. 2001. Effect of phosphorus availability on basal root shallowness in common bean. Plant and Soil 232, 69-79.
71. Lin SI, Chiang SF, Lin WY, Chen JW, Tseng CY, Wu PC, Chiou TJ. 2008. Regulatory network of microRNA399 and PHO2 by systemic signaling. Plant Physiology 147, 732-746.
72. Lin SI, Santi C, Jobet E, et al. 2010. Complex regulation of two target genes encoding SPX-MFS proteins by rice miR827 in response to phosphate starvation. Plant and Cell Physiology 51, 2119-2131.
73. Lin WY, Huang TK, Chiou TJ. 2013. Nitrogen limitation adaptation, a target of microRNA827, mediates degradation of plasma membranelocalized phosphate transporters to maintain phosphate homeostasis in Arabidopsis. The Plant Cell 25, 4061-4074.
74. Lin WY, Huang TK, Leong SJ, Chiou TJ. 2014. Long-distance call from phosphate: systemic regulation of phosphate starvation responses. Journal of Experimental Botany 65, 1817-1827.
75. Liu C, Muchhal US, Uthappa M, Kononowicz AK, Raghothama KG. 1998a. Tomato phosphate transporter genes are differentially regulated in plant tissues by phosphorus. Plant Physiology 116, 91-99.
76. Liu H, Trieu AT, Blaylock LA, Harrison MJ. 1998b. Cloning and characterization of two phosphate transporters from Medicago truncatula roots: regulation in response to phosphate and to colonization by arbuscular mycorrhizal (AM) fungi. Molecular Plant-Microbe Interactions 11, 14-22.
77. Liu J, Samac DA, Bucciarelli B, Allan DL, Vance CP. 2005. Signaling of phosphorus deficiency-induced gene expression in white lupin requires sugar and phloem transport. The Plant Journal 41, 257-268.
78. Liu J, Vance CP. 2010. Crucial roles of sucrose and microRNA399 in systemic signaling of P deficiency: a tale of two team players? Plant Signaling and Behaviour 5, 1556-1560.
79. Liu JQ, Allan DL, Vance CP. 2010. Systemic signaling and local sensing of phosphate in common bean: cross-talk between photosynthate and microRNA399. Molecular Plant 3, 428-437.
80. Liu TY, Huang TK, Tseng CY, Lai YS, Lin SI, Lin WY, Chen JW, Chiou TJ. 2012. PHO2-dependent degradation of PHO1 modulates phosphate homeostasis in Arabidopsis. The Plant Cell 24, 2168-2183.
81. Lopez-Arredondo DL, Leyva-Gonzalez MA, Gonzalez-Morales SI, Lopez-Bucio J, Herrera-Estrella L. 2014. Phosphate nutrition: improving low-phosphate tolerance in crops. Annual Reviews in Plant Biology 65, 95-123.
82. Loth-Pereda V, Orsini E, Courty PE, et al. 2011. Structure and expression profile of the phosphate Pht1 transporter gene family in mycorrhizal Populus trichocarpa. Plant Physiology 156, 2141-2154.
83. Lundh F, Mouillon JM, Samyn D, Stadler K, Popova Y, Lagerstedt JO, Thevelein JM, Persson BL. 2009. Molecular mechanisms controlling phosphate-induced downregulation of the yeast Pho84 phosphate transporter. Biochemistry 48, 4497-4505.
84. Lv Q, Zhong Y, Wang Y, Wang Z, Zhang L, Shi J, Wu Z, Liu Y, Mao C, Yi K, Wu P. 2014. SPX4 negatively regulates phosphate signaling and homeostasis through its interaction with PHR2 in rice. The Plant Cell 26, 1586-1597.
85. Lynch J, Ho MD. 2005. Rhizoeconomics: carbon costs of phosphorus acquisition. Plant and Soil 269, 45-56.
86. Lynch JP. 2007. Turner Review No. 14. Roots of the Second Green Revolution. Australian Journal of Botany 55, 493-512.
87. Maeda D, Ashida K, Iguchi K, Chechetka SA, Hijikata A, Okusako Y, Deguchi Y, Izui K, Hata S. 2006. Knockdown of an arbuscular mycorrhiza-inducible phosphate transporter gene of Lotus japonicus suppresses mutualistic symbiosis. Plant and Cell Physiology 47, 807-817.
88. Magalhaes JV, Liu J, Guimaraes CT, et al. 2007. A gene in the multidrug and toxic compound extrusion (MATE) family confers aluminum tolerance in sorghum. Nature Genetics 39, 1156-1161.
89. Manske GGB, Ortiz-Monasterio JI, Van Ginkel M, González RM, Rajaram S, Molina E, Vlek PLG. 2000. Traits associated with improved P-uptake efficiency in CIMMYT's semidwarf spring bread wheat grown on an acid Andisol in Mexico. Plant and Soil 221, 189-204.
90. Michels MH, Vaskoska M, Vermue MH, Wijffels RH. 2014. Growth of Tetraselmis suecica in a tubular photobioreactor on wastewater from a fish farm. Water Research 65, 290-296.
91. Misson J, Thibaud MC, Bechtold N, Raghothama K, Nussaume L. 2004. Transcriptional regulation and functional properties of Arabidopsis Pht1;4, a high affinity transporter contributing greatly to phosphate uptake in phosphate deprived plants. Plant Molecular Biology 55, 727-741.
92. Mitsukawa N, Okumura S, Shirano Y, Sato S, Kato T, Harashima S, Shibata D. 1997. Overexpression of an Arabidopsis thaliana high-affinity phosphate transporter gene in tobacco cultured cells enhances cell growth under phosphate-limited conditions. Proceedings of the National Academy of Sciences, USA 94, 7098-7102.
93. Miura K, Rus A, Sharkhuu A, et al. 2005. The Arabidopsis SUMO E3 ligase SIZ1 controls phosphate deficiency responses. Proceedings of the National Academy of Sciences, USA 102, 7760-7765.
94. Moseley JL, Gonzalez-Ballester D, Pootakham W, Bailey S, Grossman AR. 2009. Genetic interactions between regulators of Chlamydomonas phosphorus and sulfur deprivation responses. Genetics 181, 889-905.
95. Motoda H, Sasaki T, Kano Y, Ryan PR, Delhaize E, Matsumoto H, Yamamoto Y. 2007. The membrane topology of ALMT1, an aluminumactivated malate transport protein in wheat (Triticum aestivum). Plant Signaling and Behaviour 2, 467-472.
96. Muchhal US, Pardo JM, Raghothama KG. 1996. Phosphate transporters from the higher plant Arabidopsis thaliana. Proceedings of the National Academy of Sciences, USA 93, 10519-10523.
97. Mudge SR, Rae AL, Diatloff E, Smith FW. 2002. Expression analysis suggests novel roles for members of the Pht1 family of phosphate transporters in Arabidopsis. The Plant Journal 31, 341-353.
98. Muñoz R, Guieysse B. 2006. Algal-bacterial processes for the treatment of hazardous contaminants: a review. Water Research 40, 2799-2815.
99. Nagarajan VK, Jain A, Poling MD, Lewis AJ, Raghothama KG, Smith AP. 2011. Arabidopsis Pht1;5 mobilizes phosphate between source and sink organs and influences the interaction between phosphate homeostasis and ethylene signaling. Plant Physiology 156, 1149-1163.
100. Nagy R, Karandashov V, Chague W, Kalinkevich K, Tamasloukht M, Xu GH, Jakobsen I, Levy AA, Amrhein N, Bucher M. 2005. The characterization of novel mycorrhiza-specific phosphate transporters from Lycopersicon esculentum and Solanum tuberosum uncovers functional redundancy in symbiotic phosphate transport in solanaceous species. The Plant Journal 42, 236-250.
101. Nagy R, Vasconcelos MJV, Zhao S, McElver J, Bruce W, Amrhein N, Raghothama KG, Bucher M. 2006. Differential regulation of five Pht1 phosphate transporters from maize (Zea mays L.). Plant Biology 8, 186-197.
102. Nakamura Y. 2013. Phosphate starvation and membrane lipid remodeling in seed plants. Progress in Lipid Research 52, 43-50.
103. Nilsson L, Muller R, Nielsen TH. 2007. Increased expression of the MYB-related transcription factor, PHR1, leads to enhanced phosphate uptake in Arabidopsis thaliana. Plant, Cell & Environment 30, 1499-1512.
104. Nussaume L, Kanno S, Javot H, Marin E, Pochon N, Ayadi A, Nakanishi TM, Thibaud MC. 2011. Phosphate import in plants: focus on the PHT1 transporters. Frontiers in Plant Science 2, 1-8.
105. Pant BD, Buhtz A, Kehr J, Scheible WR. 2008. MicroRNA399 is a longdistance signal for the regulation of plant phosphate homeostasis. The Plant Journal 53, 731-738.
106. Paszkowski U, Kroken S, Roux C, Briggs SP. 2002. Rice phosphate transporters include an evolutionarily divergent gene specifically activated in arbuscular mycorrhizal symbiosis. Proceedings of the National Academy of Sciences, USA 99, 13324-13329.
107. Pedersen BP, Kumar H, Waight AB, et al. 2013. Crystal structure of a eukaryotic phosphate transporter. Nature 496, 533-536.
108. Peng M, Hannam C, Gu H, Bi YM, Rothstein SJ. 2007. A mutation in NLA, which encodes a RING-type ubiquitin ligase, disrupts the adaptability of Arabidopsis to nitrogen limitation. The Plant Journal 50, 320-337.
109. Poirier Y, Thoma S, Somerville C, Schiefelbein J. 1991. Mutant of Arabidopsis deficient in xylem loading of phosphate. Plant Physiology 97, 1087-1093.
110. Preuss CP, Huang CY, Tyerman SD. 2011. Proton-coupled high-affinity phosphate transport revealed from heterologous characterization in Xenopus of barley-root plasma membrane transporter, HvPHT1;1. Plant, Cell and Environment 34, 681-689.
111. Puga MI, Mateos I, Charukesi R, et al.. 2014. SPX1 is a phosphatedependent inhibitor of PHOSPHATE STARVATION RESPONSE 1 in Arabidopsis. Proceedings of the National Academy of Sciences, USA 111, 14947-14952.
112. Pumplin N, Zhang X, Noar RD, Harrison MJ. 2012. Polar localization of a symbiosis-specific phosphate transporter is mediated by a transient reorientation of secretion. Proceedings of the National Academy of Sciences, USA 109, E665-E672.
113. Rae AL, Cybinski DH, Jarmey JM, Smith FW. 2003. Characterization of two phosphate transporters from barley; evidence for diverse function and kinetic properties among members of the Pht1 family. Plant Molecular Biology 53, 27-36.
114. Raghothama KG. 1999. Phosphate acquisition. Annual Review of Plant Physiology and Plant Molecular Biology 50, 665-693.
115. Raghothama KG, Karthikeyan AS. 2005. Phosphate acquisition. Plant and Soil 274, 37-49.
116. Rausch C, Daram P, Brunner S, Jansa J, Laloi M, Leggewie G, Amrhein N, Bucher M. 2001. A phosphate transporter expressed in arbuscule-containing cells in potato. Nature 414, 462-470.
117. Remy E, Cabrito TR, Batista RA, Teixeira MC, Sa-Correia I, Duque P. 2012. The Pht1;9 and Pht1;8 transporters mediate inorganic phosphate acquisition by the Arabidopsis thaliana root during phosphorus starvation. New Phytologist 195, 356-371.
118. Ren F, Guo QQ, Chang LL, Chen L, Zhao CZ, Zhong H, Li XB. 2012. Brassica napus PHR1 gene encoding a MYB-like protein functions in response to phosphate starvation. PLoS One 7, e44005.
119. Ren F, Zhao C-Z, Liu C-S, Huang K-L, Guo Q-Q, Chang L-L, Xiong H, Li X-B. 2014. A Brassica napus PHT1 phosphate transporter, BnPht1;4, promotes phosphate uptake and affects roots architecture of transgenic Arabidopsis. Plant Molecular Biology 86, 595-607.
120. Ribot C, Zimmerli C, Farmer EE, Reymond P, Poirier Y. 2008. Induction of the Arabidopsis PHO1;H10 gene by 12-oxo-phytodienoic acid but not jasmonic acid via a CORONATINE INSENSITIVE1-dependent pathway. Plant Physiology 147, 696-706.
121. Richardson A, Lynch J, Ryan P, et al. 2011. Plant and microbial strategies to improve the phosphorus efficiency of agriculture. Plant and Soil 349, 121-156.
122. Rosemarin A, Schröder J, Dagerskog L, Cordell D, Smit B. 2011. Future supply of phosphorus in agriculture and the need to maximise efficiency of use and reuse. Proceedings 685, International Fertiliser Society, Leek, UK.
123. Rouached H, Arpat AB, Poirier Y. 2010. Regulation of phosphate starvation responses in plants: signaling players and cross-talks. Molecular Plant 3, 288-299.
124. Rouached H, Secco D, Arpat B, Poirier Y. 2011b. The transcription factor PHR1 plays a key role in the regulation of sulfate shoot-to-root flux upon phosphate starvation in Arabidopsis. BMC Plant Biology 11, 19.
125. Rouached H, Stefanovic A, Secco D, Bulak Arpat A, Gout E, Bligny R, Poirier Y. 2011a. Uncoupling phosphate deficiency from its major effects on growth and transcriptome via PHO1 expression in Arabidopsis. The Plant Journal 65, 557-570.
126. Rubio V, Linhares F, Solano R, Martin AC, Iglesias J, Leyva A, Paz-Ares J. 2001. A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae. Genes & Development 15, 2122-2133.
127. Ryan P, Delhaize E, Jones D. 2001. Function and mechanism of organic anion exudation from plant roots. Annual Review of Plant Physiology and Plant Molecular Biology 52, 527-560.
128. Ryan PR, Tyerman SD, Sasaki T, Furuichi T, Yamamoto Y, Zhang WH, Delhaize E. 2011. The identification of aluminium-resistance genes provides opportunities for enhancing crop production on acid soils. Journal of Experimental Botany 62, 9-20.
129. Sas L, Rengel Z, Tang C. 2001. Excess cation uptake, and extrusion of protons and organic acid anions by Lupinus albus under phosphorus deficiency. Plant Science 160, 1191-1198.
130. Sasaki T, Tsuchiya Y, Ariyoshi M, Ryan PR, Furuichi T, Yamamoto Y. 2014. A domain-based approach for analyzing the function of aluminumactivated malate transporters from wheat (Triticum aestivum) and Arabidopsis thaliana in Xenopus oocytes. Plant and Cell Physiology 55, 2126-2138.
131. Sawaki Y, Iuchi S, Kobayashi Y, et al. 2009 STOP1 regulates multiple genes that protect Arabidopsis from proton and aluminum toxicities. Plant Physiology 150, 281-294.
132. Schachtman DP, Reid RJ, Ayling SM. 1998. Phosphorus uptake by plants: from soil to cell. Plant Physiology 116, 447-453.
133. Schunmann PHD, Richardson AE, Vickers CE, Delhaize E. 2004. Promoter analysis of the barley Pht1;1 phosphate transporter gene identifies regions controlling root expression and responsiveness to phosphate deprivation. Plant Physiology 136, 4205-4214.
134. Secco D, Baumann A, Poirier Y. 2010. Characterization of the rice PHO1 gene family reveals a key role for OsPHO1;2 in phosphate homeostasis and the evolution of a distinct clade in dicotyledons. Plant Physiology 152, 1693-1704.
135. Secco D, Jabnoune M, Walker H, Shou H, Wu P, Poirier Y, Whelan J. 2013. Spatio-temporal transcript profiling of rice roots and shoots in response to phosphate starvation and recovery. The Plant Cell 25, 4285-4304.
136. Secco D, Wang C, Arpat BA, Wang Z, Poirier Y, Tyerman SD, Wu P, Shou H, Whelan J. 2012. The emerging importance of the SPX domaincontaining proteins in phosphate homeostasis. New Phytologist 193, 842-851.
137. Seo HM, Jung Y, Song S, et al. 2008. Increased expression of OsPT1, a high-affinity phosphate transporter, enhances phosphate acquisition in rice. Biotechnology Letters 30, 1833-1838.
138. Shin H, Shin H-S, Chen R, Harrison MJ. 2006. Loss of At4 function impacts phosphate distribution between the roots and the shoots during phosphate starvation. The Plant Journal 45, 712-726.
139. Shu B, Xia R-X, Wang P. 2012. Differential regulation of Pht1 phosphate transporters from trifoliate orange (Poncirus trifoliata L. Raf) seedlings. Scientia Horticulturae 146, 115-123.
140. Sisaphaithong T, Kondo D, Matsunaga H, Kobae Y, Hata S. 2012. Expression of plant genes for arbuscular mycorrhiza-inducible phosphate transporters and fungal vesicle formation in sorghum, barley, and wheat roots. Bioscience, Biotechnology, and Biochemistry 76, 2364-2367.
141. Smil V. 2000. Phosphorus in the environment: natural flows and human interferences. Annual Review of Energy and the Environment 25, 53-88.
142. Smith SE, Read DJ. 2008. Mycorrhizal symbiosis, 3rd edn. San Diego, CA: Academic Press.
143. Stefanovic A, Arpat AB, Bligny R, Gout E, Vidoudez C, Bensimon M, Poirier Y. 2011. Over-expression of PHO1 in Arabidopsis leaves reveals its role in mediating phosphate efflux. The Plant Journal 66, 689-699.
144. Stefanovic A, Ribot C, Rouached H, Wang Y, Chong J, Belbahri L, Delessert S, Poirier Y. 2007. Members of the PHO1 gene family show limited functional redundancy in phosphate transfer to the shoot, and are regulated by phosphate deficiency via distinct pathways. The Plant Journal 50, 982-994.
145. Sun S, Gu M, Cao Y, Huang X, Zhang X, Ai P, Zhao J, Fan X, Xu G. 2012. A constitutive expressed phosphate transporter, OsPht1;1, modulates phosphate uptake and translocation in phosphate-replete rice. Plant Physiology 159, 1571-1581.
146. Svistoonoff S, Creff A, Reymond M, Sigoillot-Claude C, Ricaud L, Blanchet A, Nussaume L, Desnos T. 2007. Root tip contact with lowphosphate media reprograms plant root architecture. Nature Genetics 39, 792-796.
147. Tamura Y, Kobae Y, Mizuno T, Hata S. 2012. Identification and expression analysis of arbuscular mycorrhiza-inducible phosphate transporter genes of soybean. Bioscience, Biotechnology, and Biochemistry 76, 309-313.
148. Thibaud M-C, Arrighi J-F, Bayle V, Chiarenza S, Creff A, Bustos R, Paz-Ares J, Poirier Y, Nussaume L. 2010. Dissection of local and systemic transcriptional responses to phosphate starvation in Arabidopsis. The Plant Journal 64, 775-789.
149. Tian J, Venkatachalam P, Liao H, Yan X, Raghothama K. 2007. Molecular cloning and characterization of phosphorus starvation responsive genes in common bean (Phaseolus vulgaris L.). Planta 227, 151-165.
150. Ticconi CA, Delatorre CA, Lahner B, Salt DE, Abel S. 2004. Arabidopsis pdr2 reveals a phosphate-sensitive checkpoint in root development. The Plant Journal 37, 801-814.
151. Ticconi CA, Lucero RD, Sakhonwasee S, Adamson AW, Creff A, Nussaume L, Desnos T, Abel S. 2009. ER-resident proteins PDR2 and LPR1 mediate the developmental response of root meristems to phosphate availability. Proceedings of the National Academy of Sciences, USA 106, 14174-14179.
152. 3 uptake and fusicoccin in root hairs of Limnobium stoloniferum. Plant Physiology 94, 1561-1567.
153. Veneklaas EJ, Lambers H, Bragg J, et al. 2012. Opportunities for improving phosphorus-use efficiency in crop plants. New Phytologist 195, 306-320.
154. Verma R, Suthar S. 2014. Synchronized urban wastewater treatment and biomass production using duckweed Lemna gibba L. Ecological Engineering 64, 337-343.
155. Vermaat JE, Khalid Hanif M. 1998. Performance of common duckweed species (Lemnaceae) and the waterfern Azolla filiculoides on different types of waste water. Water Research 32, 2569-2576.
156. Vidal J. 2008. Soaring fertiliser prices threaten world's poorest farmers. 12 August 2008, Guardian, UK. http://www.guardian.co.uk/environment/2008/aug/12/biofuels.food.
157. von Uexküll HR, Mutert E. 1995. Global extent, development and economic impact of acid soils. Plant and Soil 171, 1-15.
158. Wang C, Ying S, Huang H, Li K, Wu P, Shou H. 2009. Involvement of OsSPX1 in phosphate homeostasis in rice. The Plant Journal 57, 895-904.
159. Wang J, Sun J, Miao J, Guo J, Shi Z, He M, Chen Y, Zhao X, Li B, Han F, Tong Y, Li Z. 2013. A phosphate starvation response regulator Ta-PHR1 is involved in phosphate signalling and increases grain yield in wheat. Annals of Botany 111, 1139-1153.
160. Wang X, Bai J, Liu H, Sun Y, Shi X, Ren Z. 2013. Overexpression of a maize transcription factor ZmPHR1 improves shoot inorganic phosphate content and growth of Arabidopsis under low-phosphate conditions. Plant Molecular Biology Reporter 31, 665-677.
161. Wang Y, Ribot C, Rezzonico E, Poirier Y. 2004. Structure and expression profile of the Arabidopsis PHO1 gene family indicates a broad role in inorganic phosphate homeostasis. Plant Physiology 135, 400-411.
162. Wang Z, Hu H, Huang H, Duan K, Wu Z, Wu P. 2009. Regulation of OsSPX1 and OsSPX3 on expression of OsSPX domain genes and Pi-starvation signaling in rice. Journal of Integrative Plant Biology 51, 663-674.
163. Wang Z, Ruan W, Shi J, Zhang L, Xiang D, Yang C, Li C, Wu Z, Liu Y, Yu Y, Shou H, Mo X, Mao C, Wu P. 2014. Rice SPX1 and SPX2 inhibit phosphate starvation responses through interacting with PHR2 in a phosphate-dependent manner. Proceedings of the National Academy of Sciences, USA 111, 14953-14958.
164. Wege S, Poirier Y. 2014. Expression of the mammalian Xenotropic Polytropic Virus Receptor 1 (XPR1) in tobacco leaves leads to phosphate export. FEBS Letters 588, 482-489.
165. Wegmuller S, Svistoonoff S, Reinhardt D, Stuurman J, Amrhein N, Bucher M. 2008. A transgenic dTph1 insertional mutagenesis system for forward genetics in mycorrhizal phosphate transport of Petunia. The Plant Journal 54, 1115-1127.
166. Xiao K, Liu J, Dewbre G, Harrison M, Wang ZY. 2006. Isolation and characterization of root-specific phosphate transporter promoters from Medicago truncatula. Plant Biology 8, 439-449.
167. Xie XA, Huang W, Liu FC, Tang NW, Liu Y, Lin H, Zhao B. 2013. Functional analysis of the novel mycorrhiza-specific phosphate transporter AsPT1 and PHT1 family from Astragalus sinicus during the arbuscular mycorrhizal symbiosis. New Phytologist 198, 836-852.
168. Xu GH, Chague V, Melamed-Bessudo C, Kapulnik Y, Jain A, Raghothama KG, Levy AA, Silber A. 2007. Functional characterization of LePT4: a phosphate transporter in tomato with mycorrhiza-enhanced expression. Journal of Experimental Botany 58, 2491-2501.
169. Xu F, Liu Q, Chen L, Kuang J, Walk T, Wang J, Liao H. 2013. Genome-wide identification of soybean microRNAs and their targets reveals their organ-specificity and responses to phosphate starvation. BMC Genomics 14, 66.
170. Yan X, Liao H, Beebe S, Blair M, Lynch J. 2004. QTL mapping of root hair and acid exudation traits and their relationship to phosphorus uptake in common bean. Plant and Soil 265, 17-29.
171. Yang S-Y, Grønlund M, Jakobsen I, Grotemeyer MS, Rentsch D, Miyao A, Hirochika H, Kumar CS, Sundaresan V, Salamin N, Catausan S, Mattes N, Heuer S, Paszkowski U. 2012. Nonredundant regulation of rice arbuscular mycorrhizal symbiosis by two members of the PHOSPHATE TRANSPORTER1 gene family. The Plant Cell 24, 4236-4251.
172. Yi K, Wu Z, Zhou J, Du L, Guo L, Wu Y, Wu P. 2005. OsPTF1, a novel transcription factor involved in tolerance to phosphate starvation in rice. Plant Physiology 138, 2087-2096.
173. Yuan H, Liu D. 2008. Signaling components involved in plant responses to phosphate starvation. Journal of Integrative Plant Biology 50, 849-859.
174. 3+-activated anion channel in transformed tobacco (Nicotiana tabacum L.) cells. Plant and Cell Physiology 49, 1316-1330.
175. Zhang Z, Liao H, Lucas WJ. 2014. Molecular mechanisms underlying phosphate sensing, signaling, and adaptation in plants. Journal of Integrative Plant Biology 56, 192-220.
176. Zhou J, Jiao F, Wu Z, Li Y, Wang X, He X, Zhong W, Wu P. 2008. OsPHR2 is involved in phosphate-starvation signaling and excessive phosphate accumulation in shoots of plants. Plant Physiology 146, 1673-1686.
177. Zhou Y, Ni M. 2010. SHORT HYPOCOTYL UNDER BLUE1 truncations and mutations alter its association with a signaling protein complex in Arabidopsis. The Plant Cell 22, 703-715.
178. Zhu J, Kaeppler S, Lynch J. 2005a. Mapping of QTL controlling root hair length in maize (Zea mays L.) under phosphorus deficiency. Plant and Soil 270, 299-310.
179. Zhu J, Kaeppler S, Lynch J. 2005b. Mapping of QTLs for lateral root branching and length in maize (Zea mays L.) under differential phosphorus supply. Theoretical and Applied Genetics 111, 688-695.