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Phosphorus starvation response dynamics and management in plants for sustainable agriculture

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Abstract

Phosphorus (P) is an essential macronutrient required for the survival and reproduction of all living organisms. Its inorganic form (Pi) is taken up by the roots to support plant growth and development, and its availability directly determines agricultural productivity. The primary source of P replenishment in agriculture is chemical phosphate (Pi) fertilizers. While application of Pi-fertilizers to croplands ensures high yield agriculture, its intensive use leads to several environmental implications, including loss of soil fertility and pollution of water bodies with runoff fertilizer. Global non-renewable P-reserves are finite and would last for only a few hundred years. Therefore, a holistic approach is needed to combine Pi-use efficient germplasm with the targeted fertilization, agronomically superior fertilizer formulations for better P-management. The latest technologies to reclaim Pi from alternative sources need to be explored. In the present review, we first outline the challenges and environmental consequences of Pi-intensive fertilization, followed by plants' response and adaptive strategies to Pi starvation. Next, we discuss the role of microbes and Pi-nanofertilizer to plant Pi nutrition. Finally, a few cutting-edge technologies and innovative solutions available for reclaiming Pi from waste are argued.

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Fig. 1

Source: Data from 1992–2020 was obtained from the Food and Agriculture organization website. b Annual subsidy outgo for P&K fertilizers in India. Source: Government of India Ministry of Chemicals and Fertilizers for a period from 2005 to 2020

Fig. 2

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Abbreviations

ATP:

Adenosine triphosphate

Al:

Aluminum

Ca:

Calcium

CaP:

Calcium phosphate

CSH:

Calcium silicate hydrate

Cd:

Cadmium

DAG:

Diacylglycerol

DGDG:

Digalactosyldiacylglycerol

nDAP:

Diammonium phosphate nanoparticle

DCP:

Dicalcium phosphate

MGDG:

Monogalactosyldiacylglycerol

G3P:

Glycerol-3-phosphate

G3PDH:

Glycerol-3-phosphate dehydrogenase

GDPDs:

Glycerophosphodiester phosphodiesterase

HATs:

High affinity transporters

Fe:

Iron

ITP:

Inositol 1,4,5-triphosphate

LAH:

Lipid acyl hydrolase

Mg:

Magnesium

μM:

Micrometer

N:

Nitrogen

PHTs:

Phosphate transporters

Pi:

Phosphate

PUE:

Pi use efficiency

Phi:

Phosphite

ptxD:

Phosphite oxidoreductase

PAE:

Phosphate acquisition efficiency

PSR:

Phosphate starvation responses

PUE:

Phosphate use efficiency

PAPs:

Purple acid phosphatase

RP:

Rock phosphate

R:

Radium

RSA:

Root system architecture

PHO1:

PHOSPHATE1

Th:

Thorium

U:

Uranium

Zn:

Zinc

References

  • Adamchuk VI, Hummel JW, Morgan MT, Upadhyaya SK (2004) On-the-go soil sensors for precision agriculture. Comput Electron Agric 44:71–91

    Google Scholar 

  • Akash PAP, Srivastava A, Mathur S, Sharma AK, Kumar R (2021) Identification, evolutionary profiling, and expression analysis of F-box superfamily genes under phosphate deficiency in tomato. J Plant Biochem Physiol 162:349–362

    CAS  Google Scholar 

  • Akhtar MS, Oki Y, Adachi T (2008) Intraspecific variations of phosphorus absorption and remobilization, P forms, and their internal buffering in Brassica cultivars exposed to a P-stressed environment. J Integr Plant Biol 50:703–716

    CAS  PubMed  Google Scholar 

  • Alewell C, Ringeval B, Ballabio C, Robinson DA, Panagos P, Borrelli P (2020) Global phosphorous shortage will be aggravated by soil erosion. Nat Commun 11:1–2

    Google Scholar 

  • Altomare C, Norvell W, Björkman T, Harman GE (1999) Solubilization of phosphates and micronutrients by the plant-growth-promoting and biocontrol fungus Trichoderma harzianum Rifai. Am Soc Microbiol 65:2926–2933

    CAS  Google Scholar 

  • Amundson R, Berhe AA, Hopmans JW, Olson C, Sztein AE, Sparks DL (2015) Soil and human security in the 21st century. Sci 348:6235

    Google Scholar 

  • Anderson G (1980) Assessing organic phosphorus in soils. The role of phosphorus in agriculture, pp 411–31

  • Arslanoglu H (2019) Adsorption of micronutrient metal ion onto struvite to prepare slow release multielement fertilizer: copper (II) doped-struvite. Chemosphere 217:393–401

    CAS  PubMed  Google Scholar 

  • Baldwin JC, Karthikeyan AS, Cao A, Raghothama KG (2008) Biochemical and molecular analysis of LePS2;1: a phosphate starvation induced protein phosphatase gene from tomato. Planta 228:273–280

    CAS  PubMed  Google Scholar 

  • Bates TR, Lynch JP (1996) Stimulation of root hair elongation in Arabidopsis thaliana by low phosphorus availability. Plant Cell Environ 19:529–538

    CAS  Google Scholar 

  • Baylis GT (1967) Experiments on the ecological significance of phycomycetous mycorrhizas. New Phytol 66:231–243

    Google Scholar 

  • Beauregard MS, Hamel C, St-Arnaud M (2010) Long-term phosphorus fertilization impacts soil fungal and bacterial diversity but not AM fungal community in alfalfa. Microb Ecol 59:379–389

    CAS  PubMed  Google Scholar 

  • Bhosale R, Giri J, Pandey BK (2018) A mechanistic framework for auxin dependent Arabidopsis root hair elongation to low external phosphate. Nat Commun 9:1409

    PubMed  PubMed Central  Google Scholar 

  • Bieleski RL (1973) Phosphate pools, phosphate transport, and phosphate availability. Annu Rev Plant Physiol 1973:225–252

    Google Scholar 

  • Bindraban PS, Dimkpa CO, Pandey R (2020) Exploring phosphorus fertilizers and fertilization strategies for improved human and environmental health. Biol Fertil Soils 56:293–317

    Google Scholar 

  • Bolan NS, Currie LD, Baskaran S (1996) Assessment of the influence of phosphate fertilizers on the microbial activity of pasture soils. Biol Fertil Soils 21:284–292

    Google Scholar 

  • Bonser AM, Lynch J, Snapp S (1996) Effect of phosphorus deficiency on growth angle of basal roots in Phaseolus vulgaris. New Phytol 132:281–288

    CAS  PubMed  Google Scholar 

  • Borch K, Bouma TJ, Lynch JP, Brown KM (1999) Ethylene: a regulator of root architectural responses to soil phosphorus availability. Plant Cell Environ 22:425–431

    CAS  Google Scholar 

  • De Buck AJ, van Dijk W, van Middelkoop JC (2012) Agricultural scenarios to reduce the national phosphorus surplus in the Netherlands. Ppo Agv https://edepot.wur.nl/247486

  • Buwalda JG, Goh KM (1982) Host-fungus competition for carbon as a cause of growth depressions in vesicular-arbuscular mycorrhizal ryegrass. Soil Biol Biochem 14:103–106

    CAS  Google Scholar 

  • Camacho-Cristóbal JJ, Rexach J, Conéjéro G, Al-Ghazi Y, Nacry P, Doumas P (2008) PRD, an Arabidopsis AINTEGUMENTA-like gene, is involved in root architectural changes in response to phosphate starvation. Planta 228:511–522

    PubMed  Google Scholar 

  • Canarini A, Kaiser C, Merchant A, Richter A, Wanek W (2019) Root exudation of primary metabolites: mechanisms and their roles in plant responses to environmental stimuli. Front Plant Sci 10:157

    PubMed  PubMed Central  Google Scholar 

  • Casacuberta N, Masqué P (2011) Fluxes of 238U decay series radionuclides in a dicalcium phosphate industrial plant. J Hazard Mater 190:245–252

    CAS  PubMed  Google Scholar 

  • Chalasani D, Basu A, Pullabhotla SV, Jorrin B, Neal AL, Poole PS, Podile AR, Tkacz A (2021) Poor competitiveness of Bradyrhizobium in Pigeon pea root colonization in Indian. Soils Mbio 12:e00423-e521

    CAS  Google Scholar 

  • Chen Q, Liu S (2019) Identification and characterization of the phosphate-solubilizing bacterium Pantoea sp. S32 in reclamation soil in Shanxi. China Front Microbiol 10:2171

  • Chen X, Jiang N, Condron LM, Dunfield KE, Chen Z, Wang J, Chen L (2019) Impact of long-term phosphorus fertilizer inputs on bacterial phoD gene community in a maize field. Northeast China Sci Total Environ 669:1011–1018

    CAS  PubMed  Google Scholar 

  • Cheng L, Bucciarelli B, Shen J, Allan D, Vance CP (2011) Update on white lupin cluster root acclimation to phosphorus deficiency update on lupin cluster roots. Plant Physiol 156:1025–1032

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng X, Ruyter-Spira C, Bouwmeester H (2013) The interaction between strigolactones and other plant hormones in the regulation of plant development. Front Plant Sci 4:199

    PubMed  PubMed Central  Google Scholar 

  • Chien PS, Chiang CP, Leong SJ, Chiou TJ (2018) Sensing and signaling of phosphate starvation: from local to long distance. Plant Cell Physiol 59:1714–1722

    CAS  PubMed  Google Scholar 

  • Cho H, Bouain N, Zheng L, Rouached H (2021) Plant resilience to phosphate limitation: current knowledge and future challenges. Crit Rev Biotechnol 41:63–71

    CAS  PubMed  Google Scholar 

  • Ciereszko I, Johansson H, Kleczkowski LA (2005) Interactive effects of phosphate deficiency, sucrose and light/dark conditions on gene expression of UDP-glucose pyrophosphorylase in Arabidopsis. J Plant Physiol 162:343–353

    CAS  PubMed  Google Scholar 

  • Cordell D, Drangert JO, White S (2009) The story of phosphorus: Global food security and food for thought. Glob Environ Change 19:292–305

    Google Scholar 

  • Crombez H, Motte H, Beeckman T (2019) Tackling plant phosphate starvation by the roots. Dev Cell 48:599–615

    CAS  PubMed  Google Scholar 

  • Cruz-Ramírez A, Oropeza-Aburto A, Razo-Hernández F (2006) Phospholipase DZ2 plays an important role in extraplastidic galactolipid biosynthesis and phosphate recycling in Arabidopsis roots. Proc Natl Acad Sci U S A 103:6765–6770

    PubMed  PubMed Central  Google Scholar 

  • Da Conceição FT, Antunes MLP, Durrant SF (2012) Radionuclide concentrations in raw and purified phosphoric acids from Brazil and their processing wastes: implications for radiation exposures. Environ Geochem Health 34:103–111

    PubMed  Google Scholar 

  • De Freitas JR, Banerjee MR, Germida JJ (1997) Phosphate-solubilizing rhizobacteria enhance the growth and yield but not phosphorus uptake of canola (Brassica napus L.). Biol Fert Soils 24:358–364

    Google Scholar 

  • Deguchi S, Uozumi S, Touno E, Kaneko M, Tawaraya K (2012) Arbuscular mycorrhizal colonization increases phosphorus uptake and growth of corn in a white clover living mulch system. Soil Sci Plant Nutr 58:169–172

    CAS  Google Scholar 

  • Del Vecchio HA, Ying S, Park J (2014) The cell wall-targeted purple acid phosphatase AtPAP25 is critical for acclimation of Arabidopsis thaliana to nutritional phosphorus deprivation. Plant J 80:569–581

    PubMed  Google Scholar 

  • 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 Biotech J 7:391–400

    CAS  Google Scholar 

  • Delhaize E, Ma JF, Ryan PR (2012) Transcriptional regulation of aluminium tolerance genes. Trends Plant Sci 17:341–348

    CAS  PubMed  Google Scholar 

  • Deng S, Lu L, Li J (2020) Purple acid phosphatase 10c encodes a major acid phosphatase that regulates plant growth under phosphate-deficient conditions in rice. J EXP Bot 71:4321–4332

    CAS  PubMed  PubMed Central  Google Scholar 

  • Deng S, Caddell DF, Xu G, Dahlen L, Washington L, Yang J, Coleman-Derr D (2021) Genome wide association study reveals plant loci controlling heritability of the rhizosphere microbiome. ISME J 12:1–4

    Google Scholar 

  • Devaiah BN, Karthikeyan AS, Raghothama KG (2007) WRKY75 transcription factor is a modulator of phosphate acquisition and root development in Arabidopsis. Plant Physiol 143:1789–1801

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dinkelaker B, Römheld V, Marschner H (1989) Citric acid excretion and precipitation of calcium citrate in the rhizosphere of white lupin (Lupinus albus L.). Plant Cell Environ 12:285–292

    CAS  Google Scholar 

  • Dinkelaker B, Hengeler C, Marschner H (1995) Distribution and function of proteoid roots and other root clusters. Botanica Acta 108:183–200

    Google Scholar 

  • Dissanayaka DM, Ghahremani M, Siebers M, Wasaki J, Plaxton WC (2021) Recent insights into the metabolic adaptations of phosphorus-deprived plants. J Exp Bot 72:199–223

    CAS  PubMed  Google Scholar 

  • Egle L, Rechberger H, Krampe J (2016) Phosphorus recovery from municipal wastewater: an integrated comparative technological, environmental and economic assessment of P recovery. Sci Total Environ 571:522–542

    CAS  PubMed  Google Scholar 

  • Elser J, Bennett E (2011) A broken biogeochemical cycle: excess phosphorus is polluting our environment while, ironically, mineable resources of this essential nutrient are limited. James Elser and elena bennett argue that recycling programmes are urgently needed. Nature 478:29–32

    CAS  PubMed  Google Scholar 

  • Fenice M, Selbman L, Federici F (2000) Application of encapsulated Penicillium variabile P16 in solubilization of rock phosphate. Bioresource Technol 73:157–162

    CAS  Google Scholar 

  • Furihata T, Suzuki M (1992) Kinetic Characterization of Two Phosphate Uptake Systems with Different Affinities in Suspension-Cultured Catharanthus roseus Protoplasts. Plant Cell Physiol 33:1151–1157

    CAS  Google Scholar 

  • Ganie AH, Ahmad A, Pandey R (2015) Metabolite profiling of low-p tolerant and Low-P sensitive maize genotypes under phosphorus starvation and restoration conditions. Plos One 10:e0129520

  • Gao W, Lu L, Qiu W (2017) OsPAP26 encodes a major purple acid phosphatase and regulates phosphate remobilization in rice. Plant Cell Physiol 58:885–892

    CAS  PubMed  Google Scholar 

  • Gardner WK, Barber DA, Parbery DG (1983) The acquisition of phosphorus by Lupinus albus L. Plant Soil 70:107–124

    CAS  Google Scholar 

  • Gilbert N (2009) Environment: the disappearing nutrient. Nature 461:716–718

    CAS  PubMed  Google Scholar 

  • Giri J, Bhosale R, Huang G (2018) Rice auxin influx carrier OsAUX1 facilitates root hair elongation in response to low external phosphate. Nat Commun 9:1408

    PubMed  PubMed Central  Google Scholar 

  • Gu M, Chen A, Sun S, Xu G (2016) Complex regulation of plant phosphate transporters and the gap between molecular mechanisms and practical application: what is missing? Mol Plant 9:396–416

    CAS  PubMed  Google Scholar 

  • Guan Z, Zhang Q, Zhang Z, Savarin J, Zuo J, Chen J, Broger L, Cheng P, Wang Q, Pei K, Zhang D (2021) Mechanistic insights into the regulation of plant phosphate homeostasis by the rice SPX2–PHR2 complex. Nat Portfolio. Doi:https://doi.org/10.21203/rs.3.rs-653544/v1

  • Gyaneshwar P, Kumar G, Parekh L (2002) Role of soil microorganisms in improving P nutrition of plants. Plant Soil 245:83–93

    CAS  Google Scholar 

  • Ham BK, Chen J, Yan Y, Lucas WJ (2018) Insights into plant phosphate sensing and signaling. Curr Opin Biotechnol 49:1–9

    CAS  PubMed  Google Scholar 

  • Hamburger D, Rezzonico E, MacDonald-Comber Petétot J, Somerville C, Poirier Y (2002) Identification and characterization of the Arabidopsis PHO1 gene involved in phosphate loading to the xylem. Plant Cell 14:889–902

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hammond JP, White PJ (2008) Sucrose transport in the phloem: integrating root responses to phosphorus starvation. J Exp Bot 59:93–109

    CAS  PubMed  Google Scholar 

  • Havlin J, Beaton J, Tisdale S, Nelson W (2005) Soil fertility and fertilizers: An introduction to nutrient management. Pearson Education, Inc. Pearson Prentice Hall. Upper Saddle River, NJ 07458 515:97–141

  • Haynes RJ (1982) Effects of liming on phosphate availability in acid soils. Plant Soil 68:289–308

    CAS  Google Scholar 

  • Hedley M, McLaughlin M (2005) Reactions of phosphate fertilizers and by-products in soils. Phosphorus Agric Ecosyst Environ 46:181–252

    CAS  Google Scholar 

  • Herrera-Estrella L, López-Arredondo D (2016) Phosphorus: the underrated element for feeding the world. Trends Plant Sci 21:461–463

    CAS  PubMed  Google Scholar 

  • Heuer S, Gaxiola R, Schilling R, Herrera-Estrella L, López-Arredondo D, Wissuwa M, Delhaize E, Rouached H (2017) Improving phosphorus use efficiency: a complex trait with emerging opportunities. The Plant J 90:868–885

    CAS  PubMed  Google Scholar 

  • Hinsinger P (2001) Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review. Plant Soil 237:173–195

    CAS  Google Scholar 

  • Hodge A, Berta G, Doussan C et al (2009) Plant root growth, architecture and function. Plant Soil 321:153–187

    CAS  Google Scholar 

  • Holme IB, Dionisio G, Madsen CK, Brinch-Pedersen H (2017) Barley HvPAPhy_a as transgene provides high and stable phytase activities in mature barley straw and in grains. Plant Biotech J 15:415–422

    CAS  Google Scholar 

  • Hopkins B, Ellsworth J (2005) Phosphorus availability with alkaline/calcareous soil. In western nutrient management conference vol 6, pp 88–93

  • Huang B, Kuo S, Bembenek R (2004) Availability of cadmium in some phosphorus fertilizers to field-grown lettuce. Water Air Soil Pollut 158:37–51

    CAS  Google Scholar 

  • Hwang W, Park S, Shin D (2015) Enhanced organic phosphate utilization by over-expression of OsACP1 and OsPAP1 genes in rice (Oryza sativa L.). Philipp J Crop Sci 40:17–23

    Google Scholar 

  • Jacobs H, Boswell G (2002) Solubilization of calcium phosphate as a consequence of carbon translocation by Rhizoctonia solani. FEMS Microbiol Ecol 40:65–71

    CAS  PubMed  Google Scholar 

  • Jakobsen I, Chen B, Munkvold L, Lundsgaard T, Zhu YG (2005) Contrasting phosphate acquisition of mycorrhizal fungi with that of root hairs using the root hairless barley mutant. Plant Cell Environ 28:928–938

    CAS  Google Scholar 

  • Jasinski SM (2011) Phosphate rock. Mineral commodity summaries, pp 122–123

  • Johnson NC (1993) Can fertilization of soil select less mutualistic mycorrhizae? Ecol Appl 3:749–757

    PubMed  Google Scholar 

  • Jones JL, Yingling YG, Reaney IM, Westerhoff P (2020) Materials matter in phosphorus sustainability. MRS Bull 45:7–10

    Google Scholar 

  • Kah M, Kookana R, Gogos A (2018) A critical evaluation of nanopesticides and nanofertilizers against their conventional analogues. Nature Nano 13:677–684

    CAS  Google Scholar 

  • Kalmykova Y, Strömvall AM (2012) Risk assessment of contaminants leaching to groundwater in an infrastructure project. Urban Dev pp 413–423

  • Kaminsky LM, Trexler RV, Malik RJ, Hockett KL, Bell TH (2019) The inherent conflicts in developing soil microbial inoculants. Trends Biotechnol 37:140–151

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Khan MS, Zaidi A, Ahemad M (2010) Plant growth promotion by phosphate solubilizing fungi: current perspective. Arch Agron Soil Sci 56:73–98

    CAS  Google Scholar 

  • Khurana A, Akash, Roychowdhury A (2021) Identification of phosphorus starvation inducible SnRK genes in tomato (Solanum lycopersicum L.). J Plant Biochem Biotechnol

  • Kim HJ, Lynch JP, Brown KM (2008) Ethylene insensitivity impedes a subset of responses to phosphorus deficiency in tomato and petunia. Plant Cell Environ 31:1744–1755

    CAS  PubMed  Google Scholar 

  • Kirk GJ, Santos EE, Findenegg GR (1999) Phosphate solubilization by organic anion excretion from rice (Oryza sativa L.) growing in aerobic soil. Plant Soil 211:11–18

    CAS  Google Scholar 

  • Kobae Y (2019) Dynamic phosphate uptake in arbuscular mycorrhizal roots under field conditions. Front Environ Sci 6:159

    Google Scholar 

  • Kochian LV, Hoekenga OA, Piñeros MA (2004) How do crop plants tolerate acid soils? mechanisms of aluminum tolerance and phosphorous efficiency. Annu Rev Plant Biol 55:459–493

    CAS  PubMed  Google Scholar 

  • Kong Y, Li X, Ma J (2014) GmPAP4, a novel purple acid phosphatase gene isolated from soybean (Glycine max), enhanced extracellular phytate utilization in Arabidopsis thaliana. Plant Cell Rep 33:655–667

    CAS  PubMed  Google Scholar 

  • Kong Y, Li X, Wang B (2018) The soybean purple acid phosphatase GmPAP14 predominantly enhances external phytate utilization in plants. Front Plant Sci 9:292

    PubMed  PubMed Central  Google Scholar 

  • Kottegoda N, Sandaruwan C, Priyadarshana G (2017) Urea-Hydroxyapatite Nanohybrids for Slow Release of Nitrogen. ACS Nano 11:1214–1221

    CAS  PubMed  Google Scholar 

  • Kouas S, Labidi N (2005) Effect of P on nodule formation and N fixation in bean. Agron Sustain Dev 25:389–393

    CAS  Google Scholar 

  • Kucey RMN (1983) Phosphate-solubilizing bacteria and fungi in various cultivated and virgin alberta soils. Can J Soil Sci 63:671–678

    CAS  Google Scholar 

  • Kumar A, Prakash A, Johri BN (2011) Bacillus as PGPR in crop ecosystem. In Bacteria in agrobiology: crop ecosystems, 37–59. Doi:https://doi.org/10.1007/978-3-642-18357-7_2

  • Lambers H, Ahmedi I, Berkowitz O, Dunne C, Finnegan PM, Hardy GE, Jost R, Laliberté E, Pearse SJ, Teste FP (2013) Phosphorus nutrition of phosphorus-sensitive Australian native plants: threats to plant communities in a global biodiversity hotspot. Conserv Physiol 1:cot010

  • Lambers H, Finnegan P (2011) Phosphorus nutrition of Proteaceae in severely phosphorus-impoverished soils: are there lessons to be learned for future crops? Plant Physiol 156:1058–1066

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li WYF, Shao G, Lam HM (2008) Ectopic expression of GmPAP3 alleviates oxidative damage caused by salinity and osmotic stresses. New Phytol 178:80–91

    CAS  PubMed  Google Scholar 

  • Li C, Li C, Zhang H (2016) The purple acid phosphatase GmPAP21 enhances internal\nphosphorus utilization and possibly plays a role in symbiosis\nwith rhizobia in soybean. Physiol Plant 159:215–227

    PubMed  Google Scholar 

  • Li C, Zhou J, Wang X, Liao H (2019) A purple acid phosphatase, GmPAP33, participates in arbuscule degeneration during arbuscular mycorrhizal symbiosis in soybean. Plant Cell Environ 42:2015–2027

    CAS  PubMed  Google Scholar 

  • Liang C, Sun L, Yao Z (2012) Comparative analysis of PvPAP gene family and their functions in response to phosphorus deficiency in common bean. PLoS One 7:e38106

  • Liu J, Yang L, Luan M, Wang Y, Zhang C, Zhang B, Shi J, Zhao FG, Lan W, Luan S (2015) A vacuolar phosphate transporter essential for phosphate homeostasis in Arabidopsis. Proc Natl Acad Sci 112:E6571–E6578

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liu TY, Huang TK, Yang SY (2016) Identification of plant vacuolar transporters mediating phosphate storage. Nat Commun 7:1–11

    CAS  Google Scholar 

  • Liu L, Li J, Yue F, Yan X, Wang F, Bloszies S, Wang Y (2018a) Effects of arbuscular mycorrhizal inoculation and biochar amendment on maize growth, cadmium uptake and soil cadmium speciation in Cd-contaminated soil. Chemosphere 194:495–503

    CAS  PubMed  Google Scholar 

  • Liu P, Cai Z, Chen Z (2018b) A root-associated purple acid phosphatase, SgPAP23, mediates extracellular phytate-P utilization in Stylosanthes guianensis. Plant Cell Environ 41:2821–2834

    CAS  PubMed  Google Scholar 

  • Loera-Quezada MM, Leyva-González MA, Velázquez-Juárez G (2016) A novel genetic engineering platform for the effective management of biological contaminants for the production of microalgae. Plant Biotechnol J 14:2066–2076

    CAS  PubMed  PubMed Central  Google Scholar 

  • López-Arredondo DL, Herrera-Estrella L (2012) Engineering phosphorus metabolism in plants to produce a dual fertilization and weed control system. Nat Biotechnol 30:889–893

    PubMed  Google Scholar 

  • Lu L, Qiu W, Gao W (2016) OsPAP10c, a novel secreted acid phosphatase in rice, plays an important role in the utilization of external organic phosphorus. Plant Cell Environ 39:2247–2259

    CAS  PubMed  Google Scholar 

  • Lynch JP (2007) Roots of the second green revolution. Aust J Bot 55:493–512

    Google Scholar 

  • Lynch JP (2011) Root phenes for enhanced soil exploration and phosphorus acquisition: tools for future crops. Plant Physiol 156:1041–1049

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lynch JM, Whipps JM (1990) Substrate flow in the rhizosphere. Plant Soil 129:1

    CAS  Google Scholar 

  • Lyu Y, Tang H, Li H, Zhang F, Rengel Z, Whalley WR, Shen J (2016) Major crop species show differential balance between root morphological and physiological responses to variable phosphorus supply. Front Plant Sci 7:1939

    PubMed  PubMed Central  Google Scholar 

  • Lόpez-Bucio J, de la Vega OM, Guevara-Garcia A, Herrera-Estrella L (2000) Enhanced phosphorus uptake in transgenic tobacco plants that overproduce citrate. Nat Biotechnol 18:450–453

    Google Scholar 

  • Ma Z, Bielenberg DG, Brown KM, Lynch JP (2001) Regulation of root hair density by phosphorus availability in Arabidopsis thaliana. Plant Cell Environ 24:459–467

    CAS  Google Scholar 

  • Ma XF, Tudor S, Butler T (2012) Transgenic expression of phytase and acid phosphatase genes in alfalfa (Medicago sativa) leads to improved phosphate uptake in natural soils. Mol Breed 30:377–391

    CAS  PubMed  Google Scholar 

  • MacDonald GK, Bennett EM, Potter PA, Ramankutty N (2011) Agronomic phosphorus imbalances across the world’s croplands. Proc Nat Acad Sci 108:3086–3091

    CAS  PubMed  PubMed Central  Google Scholar 

  • Manna M, Achary VM, Islam T, Agrawal PK, Reddy MK (2016) The development of a phosphite-mediated fertilization and weed control system for rice. Sci Rep 6:1–2

    Google Scholar 

  • Mardamootoo T, Du Preez CC, Barnard JH (2021) Phosphorus management issues for crop production: A review. Afr J Agric Res 17:939–952

    Google Scholar 

  • McLaughlin MJ, McBeath TM, Smernik R, Stacey SP, Ajiboye B, Guppy C (2011) The chemical nature of P accumulation in agricultural soils—implications for fertiliser management and design: an Australian perspective. Plant Soil 349:69–87

    CAS  Google Scholar 

  • Mehra P, Pandey BK, Giri J (2017) Improvement in phosphate acquisition and utilization by a secretory purple acid phosphatase (OsPAP21b) in rice. Plant Biotechnol J 15:1054–1067

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mikula K, Izydorczyk G, Skrzypczak D, Mironiuk M, Moustakas K, Witek-Krowiak A, Chojnacka K (2020) Controlled release micronutrient fertilizers for precision agriculture: a review. Sci Total Environ 712:136365

    CAS  PubMed  Google Scholar 

  • Miller CR, Ochoa I, Nielsen KL, Beck D, Lynch JP (2003) Genetic variation for adventitious rooting in response to low phosphorus availability: potential utility for phosphorus acquisition from stratified soils. Funct Plant Biol 30:973–985

    CAS  PubMed  Google Scholar 

  • Mogollón JM, Beusen AH, Van Grinsven HJ, Westhoek H, Bouwman AF (2018) Future agricultural phosphorus demand according to the shared socioeconomic pathways. Glob Environ Change 50:149–163

    Google Scholar 

  • Mora-Macías J, Ojeda-Rivera J.O, Gutiérrez-Alanís D, Yong-Villalobos L, Oropeza-Aburto A, Raya-González, J, Jiménez-Domínguez G, Chávez-Calvillo G, Rellán-Álvarez R, Herrera-Estrella L (2017) Malate-dependent Fe accumulation is a critical checkpoint in the root developmental response to low phosphate. Proc Natl Acad Sci 114:E3563–E3572

  • Mortvedt J (1996) Heavy metal contaminants in inorganic and organic fertilizers. Fertiliz Environ. https://doi.org/10.1007/978-94-009-1586-2_2

    Article  Google Scholar 

  • Mosse B, Hayman DS, Arnold DJ (1973) Plant growth responses to vesicular-arbuscular mycorrhiza v. phosphate uptake by three plant species from P-deficient soils labelled with 32P. New Phytol 72:809–815

    CAS  Google Scholar 

  • Nakamura Y (2013) Phosphate starvation and membrane lipid remodeling in seed plants. Prog Lipid Res 52:43–50

    CAS  PubMed  Google Scholar 

  • Nguyen C (2003) Rhizodeposition of organic C by plants: mechanisms and controls. Agronomie 23:375–396

    CAS  Google Scholar 

  • Niu YF, Chai RS, Jin GL (2013) Responses of root architecture development to low phosphorus availability: a review. Ann Bot 112:391–408

    CAS  PubMed  Google Scholar 

  • Nussaume L (2011) Phosphate import in plants: focus on the PHT1 transporters. Front Plant Sci 2:83

    PubMed  PubMed Central  Google Scholar 

  • Ockenden MC, Hollaway MJ, Beven KJ, Collins AL, Evans R, Falloon PD, Forber KJ, Hiscock KM, Kahana R, Macleod CJ, Tych W (2017) Major agricultural changes required to mitigate phosphorus losses under climate change. Nat Commun 8:1–9

    CAS  Google Scholar 

  • Okazaki Y, Otsuki H, Narisawa T (2013) A new class of plant lipid is essential for protection against phosphorus depletion. Nat Commun 4:1510

    PubMed  Google Scholar 

  • Othman I (2007) Impact of phosphate industry on the environment: a case study. Appl Radiat Isot 65:131–141

    CAS  PubMed  Google Scholar 

  • Pant B, Burgos A (2015) The transcription factor PHR1 regulates lipid remodeling and triacylglycerol accumulation in Arabidopsis thaliana during phosphorus starvation. J Exp Bot 66:1907–1918

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pearse SJ, Veneklaas EJ, Cawthray G (2007) Carboxylate composition of root exudates does not relate consistently to a crop species ability to use phosphorus from aluminium, iron or calcium phosphate sources. New Phytol 173:181–190

    CAS  PubMed  Google Scholar 

  • Peret B, Desnos T, Jost R (2014) Root architecture responses: in search of phosphate. Plant Physiol 166:1713–1723

    PubMed  PubMed Central  Google Scholar 

  • Plaxton WC, Podestá FE (2006) The functional organization and control of plant respiration. Crit Rev Plant Sci 25:159–198

    CAS  Google Scholar 

  • Plaxton WC, Tran HT (2011) Metabolic adaptations of phosphate-starved plants. Plant Physiol 156:1006–1015

    CAS  PubMed  PubMed Central  Google Scholar 

  • Poirier Y, Bucher M (2002) Phosphate transport and homeostasis in Arabidopsis. The Arabidopsis Book. American Society of Plant Biologists pp 1–35. doi: https://doi.org/10.1199/tab.0024

  • Raghothama KG (1999) Phosphate acquisition. Annu Rev Plant Biol 50:665–693

    CAS  Google Scholar 

  • Rath M, Salas J, Parhy B, Norton R, Menakuru H, Sommerhalter M, Hatlstad G, Kwon J, Allan DL, Vance CP, Uhde-Stone C (2010) Identification of genes induced in proteoid roots of white lupin under nitrogen and phosphorus deprivation, with functional characterization of a formamidase. Plant Soil 334:137–150

    CAS  Google Scholar 

  • Ravichandran S, Stone SL, Benkel B (2015) Optimal level of purple acid phosphatase5 is required for maintaining complete resistance to Pseudomonas syringae. Front Plant Sci 6:1–10

    Google Scholar 

  • Rawat P, Shankhdhar D, Shankhdhar SC (2020) Plant growth promoting potential and biocontrol efficiency of phosphate solubilizing bacteria in rice (Oryza sativa L.). Int J Curr Microbiol Appl Sci 9:2145–2152

    CAS  Google Scholar 

  • Raya-González J, Pelagio-Flores R, López-Bucio J (2012) The jasmonate receptor COI1 plays a role in jasmonate-induced lateral root formation and lateral root positioning in Arabidopsis thaliana. J Plant Physiol 169:1348–1358

    PubMed  Google Scholar 

  • Rees RM, Bingham IJ, Baddeley JA, Watson CA (2005) The role of plants and land management in sequestering soil carbon in temperate arable and grassland ecosystems. Geoderma 128:130–154

    CAS  Google Scholar 

  • Reyes I, Bernier L, Antoun H (2002) Rock phosphate solubilization and colonization of maize rhizosphere by wild and genetically modified strains of Penicillium rugulosum. Microb Ecol 44:39–48

    CAS  PubMed  Google Scholar 

  • Richardson AE (2001) Prospects for using soil microorganisms to improve the acquisition of phosphorus by plants. Func Plant Biol 28:897–906

    Google Scholar 

  • Richardson AE, Lynch JP, Ryan PR, Delhaize E, Smith FA, Smith SE, Harvey PR, Ryan MH, Veneklaas EJ, Lambers H, Oberson A (2011) Plant and microbial strategies to improve the phosphorus efficiency of agriculture. Plant Soil 349:121–156

    CAS  Google Scholar 

  • Robinson WD, Carson I, Ying S, Ellis K, Plaxton WC (2012) Eliminating the purple acid phosphatase AtPAP26 in Arabidopsis thaliana delays leaf senescence and impairs phosphorus remobilization. New Phytol 196:1024–1029

    CAS  PubMed  Google Scholar 

  • Rose TJ, Wissuwa M (2012) Rethinking internal phosphorus utilization efficiency: a new approach is needed to improve PUE in grain crops. Adv Agron 116:185–217

    CAS  Google Scholar 

  • Ruzicka K, Ljung K, Vanneste S, Podhorská R, Beeckman T, Friml J, Benková E (2007) Ethylene regulates root growth through effects on auxin biosynthesis and transport-dependent auxin distribution. Plant Cell 19:2197–2212

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rychter AM, Chauveau M, Bomsel JL, Lance C (1992) The effect of phosphate deficiency on mitochondrial activity and adenylate levels in bean roots. Physiol Plant 84:80–86

    CAS  Google Scholar 

  • Sabet MS, Zamani K, Lohrasebi T (2018) Functional assessment of an overexpressed arabidopsis purple acid phosphatase gene (AtPAP26) in tobacco plants. Iran J Biotechnol 16:31–41

    Google Scholar 

  • Sahu S, Ajmal P, Bhangare R (2014) Natural radioactivity assessment of a phosphate fertilizer plant area. J Radiat Res Appl Sci J Radiat Res Appl Sc 7:123–128

    CAS  Google Scholar 

  • Sattari SZ, Bouwman AF, Martinez Rodríguez R (2016) Negative global phosphorus budgets challenge sustainable intensification of grasslands. Nat Commun 7:1–12

    Google Scholar 

  • Sawers RJ, Svane SF, Quan C, Grønlund M, Wozniak B, Gebreselassie MN, González-Muñoz E, Chávez Montes RA, Baxter I, Goudet J, Jakobsen I (2017) Phosphorus acquisition efficiency in arbuscular mycorrhizal maize is correlated with the abundance of root-external hyphae and the accumulation of transcripts encoding PHT1 phosphate transporters. New Phytol 214:632–643

    CAS  PubMed  Google Scholar 

  • Schachtman DP, Reid RJ, Ayling SM (1998) Phosphorus uptake by plants: from soil to cell. Plant Physiol 116:447–453

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schoumans OF, Bouraoui F, Kabbe C, Oenema O, Van Dijk KC (2015) Phosphorus management in Europe in a changing world. Ambio 44(2):180–192

    CAS  PubMed Central  Google Scholar 

  • Shen J, Yuan L, Zhang J (2011) Phosphorus dynamics: from soil to plant. Plant Physiol 156:997–1005

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sieger SM, Kristensen BK, Robson CA (2005) The role of alternative oxidase in modulating carbon use efficiency and growth during macronutrient stress in tobacco cells. J EXP Bot 56:1499–1515

    CAS  PubMed  Google Scholar 

  • Simpson RJ, Oberson A, Culvenor RA, Ryan MH, Veneklaas EJ, Lambers H, Lynch JP, Ryan PR, Delhaize E, Smith FA, Smith SE (2011) Strategies and agronomic interventions to improve the phosphorus-use efficiency of farming systems. Plant Soil 349:89–120

    CAS  Google Scholar 

  • Singh B, Pandey R (2003) Differences in root exudation among phosphorus-starved genotypes of maize and green gram and its relationship with phosphorus uptake. J Plant Nutr 26:2391–2401

    CAS  Google Scholar 

  • Singh NRR, Sarma SS, Rao TN, Pant H, Srikanth VVSS, Kumar R (2021) Cryo-milled nano-DAP for enhanced growth of monocot and dicot plants. Nanoscale Adv 3:4834–4842

    CAS  Google Scholar 

  • Skene KR, James WM (2000) A comparison of the effects of auxin on cluster root initiation and development in Grevillea robusta Cunn. ex R. Br. (Proteaceae) and in the genus Lupinus (Leguminosae). Plant Soil 219:221–229

    CAS  Google Scholar 

  • Song L, Yu H, Dong J, Che X, Jiao Y, Liu D (2016) The molecular mechanism of ethylene-mediated root hair development induced by phosphate starvation. PLoS Genet 12:e1006194

  • Sperber J (1958) The incidence of apatite-solubilizing organisms in the rhizosphere and soil. Aust J Agric Res 9:778–781

    CAS  Google Scholar 

  • Srivastava R, Akash PAP (2020) Identification, structure analysis, and transcript profiling of purple acid phosphatases under Pi deficiency in tomato (Solanum lycopersicum L.) and its wild relatives. Int J Biol Macromol 165:2253–2266

    CAS  PubMed  Google Scholar 

  • Srivastava R, Sirohi P, Chauhan H, Kumar R (2021) The enhanced phosphorus use efficiency in phosphate-deficient and mycorrhiza-inoculated barley seedlings involves activation of different sets of PHT1 transporters in roots. Planta 254:1–7

    Google Scholar 

  • Subba Rao A, Srivastava S, Ganeshamurty AN (2015) Phosphorus supply may dictate food security prospects in India. Curr Sci 108:1253–1261

    Google Scholar 

  • Sulieman S, Tran LS (2017) Legume nitrogen fixation in soils with low phosphorus availability: adaptation and regulatory implication. Springer International Publishing, switzerland

  • Sulpice R, Flis A, Ivakov AA, Apelt F, Krohn N, Encke B, Abel C, Feil R, Lunn JE, Stitt M (2014) Arabidopsis coordinates the diurnal regulation of carbon allocation and growth across a wide range of photoperiods. Mol Plant 7:137–155

    CAS  PubMed  Google Scholar 

  • Sun H, Tao J, Liu S, Huang S, Chen S, Xie X, Yoneyama K, Zhang Y, Xu G (2014) Strigolactones are involved in phosphate-and nitrate-deficiency-induced root development and auxin transport in rice. J Exp Bot 65:6735–6746

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sun T, Li M, Shao Y (2017) Comprehensive genomic identification and expression analysis of the phosphate transporter (PHT) gene family in apple. Front Plant Sci 8:426

    PubMed  PubMed Central  Google Scholar 

  • Svistoonoff S, Creff A, Reymond M, Sigoillot-Claude C, Ricaud L, Blanchet A, Nussaume L, Desnos T (2007) Root tip contact with low-phosphate media reprograms plant root architecture. Nat Genet 39:792–796

    CAS  PubMed  Google Scholar 

  • Syers J, Johnston A, Bulletin DC (2008) Efficiency of soil and fertilizer phosphorus use. FAO Fertiliz Plant Nutrit Bull 18:108

    Google Scholar 

  • Tang H, Li X, Zu C, Zhang F, Shen J (2013) Spatial distribution and expression of intracellular and extracellular acid phosphatases of cluster roots at different developmental stages in white lupin. J Plant Phys 170:1243–1250

    CAS  Google Scholar 

  • Tawaraya K (2003) Arbuscular mycorrhizal dependency of different plant species and cultivars. Soil Sci Plant Nutr 49:655–668

    Google Scholar 

  • Thao HT, Yamakawa T (2019) Phosphite (phosphorous acid): fungicide, fertilizer or bio-stimulator? Soil Sci Plant Nutr 2:228–234

    Google Scholar 

  • Theodorou ME, Plaxton WC (1993) Metabolic adaptations of plant respiration to nutritional phosphate deprivation. Plant Physiol 101:339–344

    CAS  PubMed  PubMed Central  Google Scholar 

  • Thirukkumaran CM, Parkinson D (2002) Microbial activity, nutrient dynamics and litter decomposition in a Canadian Rocky Mountain pine forest as affected by N and P fertilizers. For Ecol Manag 159:187–201

    Google Scholar 

  • Tian J, Wang C, Zhang Q (2012) Overexpression of OsPAP10a, a root-associated acid phosphatase, increased extracellular organic phosphorus utilization in rice. J Integr Plant Biol 54:631–639

    CAS  PubMed  Google Scholar 

  • Tran HT, Hurley BA, Plaxton WC (2010) Feeding hungry plants: the role of purple acid phosphatases in phosphate nutrition. Plant Sci 179:14–27

    CAS  Google Scholar 

  • Ullrich-Eberius CI, Novacky A, van Bel AJE (1984) Phosphate uptake in Lemna gibba G1: energetics and kinetics. Planta 161:46–52

    CAS  PubMed  Google Scholar 

  • Van de Wiel CCM, van der Linden CG, Scholten OE (2016) Improving phosphorus use efficiency in agriculture: opportunities for breeding. Euphytica 207:1–22

    Google Scholar 

  • Van Geel M, De Beenhouwer M, Ceulemans T, Caes K, Ceustermans A, Bylemans D, Gomand A, Lievens B, Honnay O (2016) Application of slow-release phosphorus fertilizers increases arbuscular mycorrhizal fungal diversity in the roots of apple trees. Plant Soil 402:291–301

    Google Scholar 

  • Vazquez P, Holguin G, Puente ME (2000) Phosphate-solubilizing microorganisms associated with the rhizosphere of mangroves in a semiarid coastal lagoon. Biol Fertil Soils 30:460–468

    CAS  Google Scholar 

  • Veneklaas EJ, Lambers H, Bragg J (2012) Opportunities for improving phosphorus-use efficiency in crop plants. New Phytol 195:306–320

    CAS  PubMed  Google Scholar 

  • Von Uexküll HR, Mutert E (1995) Global extent, development and economic impact of acid soils. Plant Soil 171:1–15

    Google Scholar 

  • Wang L, Nancollas GH (2008) Calcium orthophosphates: crystallization and dissolution. Chem Rev 108:4628–4669

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang X, Wang Y, Tian J (2009) Overexpressing AtPAP15 enhances phosphorus efficiency in soybean. Plant Physiol 151:233–2450

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang X, Yan X, Liao H (2010) Genetic improvement for phosphorus efficiency in soybean: a radical approach. Ann Bot 106:215–222

    PubMed  PubMed Central  Google Scholar 

  • Wang L, Li Z, Qian W, Guo W, Gao X, Huang L, Wang H, Zhu H, Wu JW, Wang D, Liu D (2011) The Arabidopsis purple acid phosphatase AtPAP10 is predominantly associated with the root surface and plays an important role in plant tolerance to phosphate limitation. Plant Physiol 157:1283–1299

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang L, Lu S, Zhang Y (2014) Comparative genetic analysis of Arabidopsis purple acid phosphatases AtPAP10, AtPAP12, and AtPAP26 provides new insights into their roles in plant adaptation to phosphate deprivation. J Integr Plant Biol 56:299–314

    CAS  PubMed  Google Scholar 

  • Wang C, Yue W, Ying Y, Wang S, Secco D, Liu Y, Whelan J, Tyerman SD, Shou H (2015) Rice SPX-Major Facility Superfamily3, a vacuolar phosphate efflux transporter, is involved in maintaining phosphate homeostasis in rice. Plant Physiol 169:2822–2831

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Wang F, Lu H, Liu Y, Mao C (2021a) Phosphate uptake and transport in plants: an elaborate regulatory system. Plant Cell Physiol. https://doi.org/10.1093/pcp/pcab011

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Chen YF, Wu WH (2021b) Potassium and phosphorus transport and signaling in plants. J Integr Plant Biol 63:34–52

    CAS  PubMed  Google Scholar 

  • Wen Z, Li H, Shen Q, Tang X, Xiong C, Li H, Pang J, Ryan MH, Lambers H, Shen J (2019) Tradeoffs among root morphology, exudation and mycorrhizal symbioses for phosphorus-acquisition strategies of 16 crop species. New Phytol 223:882–895

    CAS  PubMed  Google Scholar 

  • White PJ, Veneklaas EJ (2012) Nature and nurture: the importance of seed phosphorus content. Plant Soil 357:1–8

    CAS  Google Scholar 

  • Williamson LC, Ribrioux SP, Fitter AH, Leyser HO (2001) Phosphate availability regulates root system architecture in Arabidopsis. Plant Physiol 126:875–882

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yan X, Liao H, Beebe SE, Blair MW, Lynch JP (2004) QTL mapping of root hair and acid exudation traits and their relationship to phosphorus uptake in common bean. Plant Soil 265:17–29

    CAS  Google Scholar 

  • Yanni YG, Rizk RY, Abd El-Fattah FK, Squartini A, Corich V, Giacomini A, de Bruijn F, Rademaker J, Maya-Flores J, Ostrom P, Vega-Hernandez M (2001) The beneficial plant growth-promoting association of Rhizobium leguminosarum bv. trifolii with rice roots. Funct Plant Biol 28:845–870

    CAS  Google Scholar 

  • Zakhleniuk OV, Raines CA, Lloyd JC (2001) pho3: a phosphorus-deficient mutant of Arabidopsis thaliana (L.) Heynh. Planta 212:529–534

    CAS  PubMed  Google Scholar 

  • Zhang Y, Yu L, Yung KF (2012) Over-expression of AtPAP2 in Camelina sativa leads to faster plant growth and higher seed yield. Biotechnol Biofuels 5:1–10

    Google Scholar 

  • Zhang Y, Sun F, Fettke J (2014a) Heterologous expression of AtPAP2 in transgenic potato influences carbon metabolism and tuber development. FEBS Lett 588:3726–3731

    CAS  PubMed  Google Scholar 

  • Zhang Z, Liao H, Lucas WJ (2014b) Molecular mechanisms underlying phosphate sensing, signaling, and adaptation in plants. J Integrat Plant Biol 56(192):220

    Google Scholar 

  • Zhang JC, Wang XN, Sun W, Wang XF, Tong XS, Ji XL, An JP, Zhao Q, You CX, Hao YJ (2020) Phosphate regulates malate/citrate-mediated iron uptake and transport in apple. Plant Sci 297:110526

  • Zhu X, Lee SY, Yang WT (2019) The Burholderia pyrrocinia purple acid phosphatase Pap9 mediates phosphate acquisition in plants. J Plant Biol 62:342–350

    CAS  Google Scholar 

  • Zoboli O, Laner D, Zessner M, Rechberger H (2016) Added values of time series in material flow analysis: the austrian phosphorus budget from 1990 to 2011. J Ind Ecol 20:1334–1348

    CAS  PubMed  Google Scholar 

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Acknowledgements

This work is supported by grants received from the Science and Engineering Research Board, Govt. of India (CRG/2018/001033), and IoE, MHRD (RC1-20-018) and the Department of Science and Technology (DST), Government of India, Indo-Bulgaria Bilateral Research Cooperation (INT/BLG/P-06/2019). RK thanks the Department of Science and Technology (DST), Government of India, for Funds for Infrastructure in Science and Technology (FIST), Level II, and from the University Grants Commission under Special Assistance Programme (UGC-SAP-DRS-II) for improving the infrastructure in the Department of Plant Sciences, University of Hyderabad (UoH). RK also acknowledges the financial support to the University of Hyderabad-IoE by MHRD (F11/9/2019-U3(A)). RS thanks the Council of Scientific and Industrial Research, Govt. of India, for the JRF and SRF fellowships and UoH BBL for research fellowship.

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  1. Department of Plant Sciences, School of Life Sciences, University of Hyderabad, Hyderabad, Telangana, 500046, India

    Rajat Srivastava, Suvajit Basu & Rahul Kumar

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RK conceived the idea. RK, RS, and SB wrote the original draft. All authors read the final draft and approved it.

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Srivastava, R., Basu, S. & Kumar, R. Phosphorus starvation response dynamics and management in plants for sustainable agriculture. J. Plant Biochem. Biotechnol. 30, 829–847 (2021). https://doi.org/10.1007/s13562-021-00715-8

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