AVAILABILITY OF PHOSPHOROUS TO THE SOIL, THEIR SIGNIFICANCE FOR ROOTS OF PLANTS AND ENVIRONMENT.

Authors

  • Rida Fatima
  • Usama Basharat
  • Anila Safdar
  • Irfan Haidri
  • Arooj Fatima
  • Ans Mahmood
  • Qudrat Ullah
  • Khadija Ummer
  • Muhammad Qasim

DOI:

https://doi.org/10.53555/eijaer.v10i1.97

Keywords:

Phosphorus, Plant Growth, Sustainability, Soil Accessibility, Environmental Effects, Microbial Activity Nutrient Supply, Phosphate Ions

Abstract

In addition to being a crucial component of plant growth, phosphorus (P) is also important for preserving the
sustainability of the environment. The accessibility of phosphorus in soil, its vital importance for plant roots, and the
wider environmental effects of managing it are all covered in this abstract. The intricate interaction of multiple elements,
including soil pH, biological material content, and microbial activity, determines the availability of phosphorus in soil. It
is essential to comprehend and maximize phosphorus availability to guarantee a sufficient supply of nutrients to plant
roots. Plants absorb phosphorus mostly in the form of phosphate ions (H2PO4). A deficiency of phosphorus in the soil
can cause stunted growth, lower agricultural yields, and general plant health problems. Plants have developed several
tactics to improve their uptake of phosphorus, such as the exudation of organic acids from their roots and as well as
symbiotic relationships with mycorrhizae fungus. These adaptations demonstrate how important phosphorus is to plant
life and ecological health.

Author Biographies

Rida Fatima

University of Agriculture Faisalabad

Usama Basharat

University of Agriculture Faisalabad

Anila Safdar

PMAS Arid Agriculture University Rawalpindi

Irfan Haidri

Government College University Faisalabad

Arooj Fatima

National University of Sciences and Technology

Ans Mahmood

Government College University Faisalabad

Qudrat Ullah

Government College University Faisalabad

Khadija Ummer

University of Agriculture Faisalabad

Muhammad Qasim

Government College University Faisalabad

References

. Ai, P., Sun, S., Zhao, J., & Xu, G. (2009). Regulation and function of Pht1 family phosphate transporters in rice.

. Alori, E. T., Glick, B. R., & Babalola, O. O. J. F. i. m. (2017). Microbial phosphorus solubilization and its potential

for use in sustainable agriculture. 8, 971.

. Arpat, A. B., Magliano, P., Wege, S., Rouached, H., Stefanovic, A., & Poirier, Y. J. T. P. J. (2012). Functional

expression of PHO1 to the Golgi and trans‐Golgi network and its role in export of inorganic phosphate. 71(3), 479-

. Ayadi, A., David, P., Arrighi, J.-F., Chiarenza, S., Thibaud, M.-C., Nussaume, L., & Marin, E. J. P. P. (2015).

Reducing the genetic redundancy of Arabidopsis PHOSPHATE TRANSPORTER1 transporters to study phosphate

uptake and signaling. 167(4), 1511-1526.

. Balzergue, C., Puech-Pagès, V., Bécard, G., & Rochange, S. F. J. J. o. E. B. (2011). The regulation of arbuscular

mycorrhizal symbiosis by phosphate in pea involves early and systemic signalling events. 62(3), 1049-1060.

. Bates, T., Lynch, J. J. P., cell, & environment. (1996). Stimulation of root hair elongation in Arabidopsis thaliana

by low phosphorus availability. 19(5), 529-538.

. Behera, M., Bhattacharyya, S., Minocha, A., Deoliya, R., Maiti, S. J. C., & materials, b. (2014). Recycled aggregate

from C&D waste & its use in concrete–A breakthrough towards sustainability in construction sector: A review. 68,

-516.

. Bhosale, R., Giri, J., Pandey, B. K., Giehl, R. F., Hartmann, A., Traini, R., . . . Swarup, K. J. N. c. (2018). A

mechanistic framework for auxin dependent Arabidopsis root hair elongation to low external phosphate. 9(1), 1409.

. Bicharanloo, B., Salomon, M. J., Cavagnaro, T. R., Keitel, C., Brien, C., Jewell, N., . . . Soil. (2023). Arbuscular

mycorrhizae are important for phosphorus uptake and root biomass, and exudation for nitrogen uptake in tomato

plants grown under variable water conditions. 1-18.

. Brown, L., George, T., Thompson, J., Wright, G., Lyon, J., Dupuy, L., . . . White, P. J. A. o. B. (2012). What are

the implications of variation in root hair length on tolerance to phosphorus deficiency in combination with water

stress in barley (Hordeum vulgare)? , 110(2), 319-328.

. Brown, L. K., George, T. S., Barrett, G. E., Hubbard, S. F., White, P. J. J. P., & Soil. (2013). Interactions between

root hair length and arbuscular mycorrhizal colonisation in phosphorus deficient barley (Hordeum vulgare). 372,

-205.29

. Burak, E., Quinton, J. N., & Dodd, I. C. J. A. o. B. (2021). Root hairs are the most important root trait for

rhizosheath formation of barley (Hordeum vulgare), maize (Zea mays) and Lotus japonicus (Gifu). 128(1), 45-57.

. Calderón-Vázquez, C., Alatorre-Cobos, F., Simpson-Williamson, J., & Herrera-Estrella, L. J. H. o. m. I. b. (2009).

Maize under phosphate limitation. 381-404.

. Carminati, A., Passioura, J. B., Zarebanadkouki, M., Ahmed, M. A., Ryan, P. R., Watt, M., & Delhaize, E. J. N. P.

(2017). Root hairs enable high transpiration rates in drying soils. 216(3), 771-781.

. Cheng, L., Bucciarelli, B., Liu, J., Zinn, K., Miller, S., Patton-Vogt, J., . . . Vance, C. P. J. P. p. (2011). White lupin

cluster root acclimation to phosphorus deficiency and root hair development involve unique glycerophosphodiester

phosphodiesterases. 156(3), 1131-1148.

. Chiou, T. J., Liu, H., & Harrison, M. J. J. T. P. J. (2001). The spatial expression patterns of a phosphate transporter

(MtPT1) from Medicago truncatula indicate a role in phosphate transport at the root/soil interface. 25(3), 281-293.

. De Bauw, P., Mai, T. H., Schnepf, A., Merckx, R., Smolders, E., & Vanderborght, J. J. A. o. b. (2020). A

functional–structural model of upland rice root systems reveals the importance of laterals and growing root tips for

phosphate uptake from wet and dry soils. 126(4), 789-806.

. Dissanayaka, D., Plaxton, W. C., Lambers, H., Siebers, M., Marambe, B., Wasaki, J. J. P., Cell, & Environment.

(2018). Molecular mechanisms underpinning phosphorus‐use efficiency in rice. 41(7), 1483-1496.

. Eriksson, A. K., Hesterberg, D., Klysubun, W., & Gustafsson, J. P. J. S. o. t. T. E. (2016). Phosphorus dynamics

in Swedish agricultural soils as influenced by fertilization and mineralogical properties: Insights gained from batch

experiments and XANES spectroscopy. 566, 1410-1419.

. Fageria, N., Santos, A., Reis Jr, R. J. C. i. s. s., & analysis, p. (2014). Agronomic evaluation of phosphorus sources

in lowland rice production. 45(15), 2067-2091.

. Fageria, N. K. (2013). Mineral nutrition of rice: CRC press.

. Fan, X.-D., Wang, J.-Q., Yang, N., Dong, Y.-Y., Liu, L., Wang, F.-W., . . . Sun, Y.-P. J. G. (2013). Gene expression

profiling of soybean leaves and roots under salt, saline–alkali and drought stress by high-throughput Illumina

sequencing. 512(2), 392-402.

. Föhse, D., Claassen, N., Jungk, A. J. P., & Soil. (1991). Phosphorus efficiency of plants: II. Significance of root

radius, root hairs and cation-anion balance for phosphorus influx in seven plant species. 132, 261-272.

. Franco‐Zorrilla, J. M., Martin, A. C., Solano, R., Rubio, V., Leyva, A., & Paz‐Ares, J. J. T. P. J. (2002). Mutations

at CRE1 impair cytokinin‐induced repression of phosphate starvation responses in Arabidopsis. 32(3), 353-360.

. Fujita, K., Kai, Y., Takayanagi, M., El-Shemy, H., Adu-Gyamfi, J. J., & Mohapatra, P. K. J. P. S. (2004). Genotypic

variability of pigeonpea in distribution of photosynthetic carbon at low phosphorus level. 166(3), 641-649.

. Gahoonia, T., Nielsen, N. J. P., Cell, & Environment. (2003). Phosphorus (P) uptake and growth of a root hairless

barley mutant (bald root barley, brb) and wild type in low‐and high‐P soils. 26(10), 1759-1766.

. Gaxiola, R. A., Edwards, M., & Elser, J. J. J. C. (2011). A transgenic approach to enhance phosphorus use

efficiency in crops as part of a comprehensive strategy for sustainable agriculture. 84(6), 840-845.

. George, T. S., Brown, L. K., Ramsay, L., White, P. J., Newton, A. C., Bengough, A. G., . . . Thomas, W. T. J. N.

P. (2014). Understanding the genetic control and physiological traits associated with rhizosheath production by

barley (H ordeum vulgare). 203(1), 195-205.

. George, T. S., Fransson, A.-M., Hammond, J. P., & White, P. J. J. P. i. a. b. p. i. s. p. c. (2011). Phosphorus nutrition:

rhizosphere processes, plant response and adaptations. 245-271.

. Gilroy, S., & Jones, D. L. J. T. i. p. s. (2000). Through form to function: root hair development and nutrient uptake.

(2), 56-60.

. Glaser, B., & Lehr, V.-I. J. S. r. (2019). Biochar effects on phosphorus availability in agricultural soils: A metaanalysis. 9(1), 9338.

. Gomez-Ariza, J., Balestrini, R., Novero, M., Bonfante, P. J. B., & Soils, F. o. (2009). Cell-specific gene expression

of phosphate transporters in mycorrhizal tomato roots. 45, 845-853.

. Grossman, J. D., & Rice, K. J. J. E. A. (2012). Evolution of root plasticity responses to variation in soil nutrient

distribution and concentration. 5(8), 850-857.

. Grunwald, U., Guo, W., Fischer, K., Isayenkov, S., Ludwig-Müller, J., Hause, B., . . . Franken, P. J. P. (2009).

Overlapping expression patterns and differential transcript levels of phosphate transporter genes in arbuscular

mycorrhizal, P i-fertilised and phytohormone-treated Medicago truncatula roots. 229, 1023-1034.

. Gu, B.-W., Lee, C.-G., Lee, T.-G., & Park, S.-J. J. S. o. t. T. E. (2017). Evaluation of sediment capping with

activated carbon and nonwoven fabric mat to interrupt nutrient release from lake sediments. 599, 413-421.

. Gu, R., Chen, F., Long, L., Cai, H., Liu, Z., Yang, J., . . . Genomics. (2016). Enhancing phosphorus uptake

efficiency through QTL-based selection for root system architecture in maize. 43(11), 663-672.

. Güimil, S., Chang, H.-S., Zhu, T., Sesma, A., Osbourn, A., Roux, C., . . . Descombes, P. J. P. o. t. N. A. o. S.

(2005). Comparative transcriptomics of rice reveals an ancient pattern of response to microbial colonization.

(22), 8066-8070.

. Guo, W., Zhao, J., Li, X., Qin, L., Yan, X., & Liao, H. J. T. P. J. (2011). A soybean β‐expansin gene GmEXPB2

intrinsically involved in root system architecture responses to abiotic stresses. 66(3), 541-552.

. Gyaneshwar, P., Naresh Kumar, G., Parekh, L., Poole, P. J. P., & soil. (2002). Role of soil microorganisms in

improving P nutrition of plants. 245, 83-93.30

. Haling, R. E., Brown, L. K., Bengough, A. G., Valentine, T. A., White, P. J., Young, I. M., & George, T. S. J. P.

(2014). Root hair length and rhizosheath mass depend on soil porosity, strength and water content in barley

genotypes. 239, 643-651.

. Haling, R. E., Simpson, R. J., Delhaize, E., Hocking, P. J., Richardson, A. E. J. P., & Soil. (2010). Effect of lime

on root growth, morphology and the rhizosheath of cereal seedlings growing in an acid soil. 327, 199-212.

. Ham, B.-K., Chen, J., Yan, Y., & Lucas, W. J. J. C. O. i. B. (2018). Insights into plant phosphate sensing and

signaling. 49, 1-9.

. Hammond, J. P., Broadley, M. R., White, P. J., King, G. J., Bowen, H. C., Hayden, R., . . . Spracklen, W. P. J. J.

o. e. b. (2009). Shoot yield drives phosphorus use efficiency in Brassica oleracea and correlates with root

architecture traits. 60(7), 1953-1968.

. Hanlon, M. T., Ray, S., Saengwilai, P., Luthe, D., Lynch, J. P., & Brown, K. M. J. J. o. e. b. (2018). Buffered

delivery of phosphate to Arabidopsis alters responses to low phosphate. 69(5), 1207-1219.

. Hayat, R., Ali, S., Amara, U., Khalid, R., & Ahmed, I. J. A. o. m. (2010). Soil beneficial bacteria and their role in

plant growth promotion: a review. 60, 579-598.

. Hirsch, J., Marin, E., Floriani, M., Chiarenza, S., Richaud, P., Nussaume, L., & Thibaud, M. J. B. (2006). Phosphate

deficiency promotes modification of iron distribution in Arabidopsis plants. 88(11), 1767-1771.

. Ho, M. D., McCannon, B. C., & Lynch, J. P. J. J. o. T. B. (2004). Optimization modeling of plant root architecture

for water and phosphorus acquisition. 226(3), 331-340.

. Holz, M., Zarebanadkouki, M., Kuzyakov, Y., Pausch, J., & Carminati, A. J. A. o. B. (2018). Root hairs increase

rhizosphere extension and carbon input to soil. 121(1), 61-69.

. Huang, W., Liu, J., Wang, Y. P., Zhou, G., Han, T., Li, Y. J. P., & Soil. (2013). Increasing phosphorus limitation

along three successional forests in southern China. 364, 181-191.

. Jain, A., Poling, M. D., Karthikeyan, A. S., Blakeslee, J. J., Peer, W. A., Titapiwatanakun, B., . . . Raghothama, K.

G. J. P. P. (2007). Differential effects of sucrose and auxin on localized phosphate deficiency-induced modulation

of different traits of root system architecture in Arabidopsis. 144(1), 232-247.

. Jia, H., Ren, H., Gu, M., Zhao, J., Sun, S., Zhang, X., . . . Xu, G. J. P. P. (2011). The phosphate transporter gene

OsPht1; 8 is involved in phosphate homeostasis in rice. 156(3), 1164-1175.

. Jing, J., Rui, Y., Zhang, F., Rengel, Z., & Shen, J. J. F. C. R. (2010). Localized application of phosphorus and

ammonium improves growth of maize seedlings by stimulating root proliferation and rhizosphere acidification.

(2-3), 355-364.

. Jones, D. L., & Oburger, E. J. P. i. a. b. p. i. s. p. c. (2011). Solubilization of phosphorus by soil microorganisms.

-198.

. Jungk, A. J. J. o. P. N., & Science, S. (2001). Root hairs and the acquisition of plant nutrients from soil. 164(2),

-129.

. Kabir, Z., Koide, R. J. A., ecosystems, & environment. (2000). The effect of dandelion or a cover crop on

mycorrhiza inoculum potential, soil aggregation and yield of maize. 78(2), 167-174.

. Kang, S.-M., Joo, G.-J., Hamayun, M., Na, C.-I., Shin, D.-H., Kim, H. Y., . . . Lee, I.-J. J. B. l. (2009). Gibberellin

production and phosphate solubilization by newly isolated strain of Acinetobacter calcoaceticus and its effect on

plant growth. 31, 277-281.

. Karthikeyan, A. S., Varadarajan, D. K., Mukatira, U. T., D'Urzo, M. P., Damsz, B., & Raghothama, K. G. J. P. p.

(2002). Regulated expression of Arabidopsis phosphate transporters. 130(1), 221-233.

. Kereszt, A., Li, D., Indrasumunar, A., Nguyen, C. D., Nontachaiyapoom, S., Kinkema, M., & Gresshoff, P. M. J.

N. p. (2007). Agrobacterium rhizogenes-mediated transformation of soybean to study root biology. 2(4), 948-952.

. Kirkby, E. A., & Johnston, A. E. J. T. e. o. p.-p. i. (2008). Soil and fertilizer phosphorus in relation to crop nutrition.

-223.

. Klamer, F., Vogel, F., Li, X., Bremer, H., Neumann, G., Neuhäuser, B., . . . Ludewig, U. J. A. o. b. (2019).

Estimating the importance of maize root hairs in low phosphorus conditions and under drought. 124(6), 961-968.

. Kochian, L. V. J. N. (2012). Rooting for more phosphorus. 488(7412), 466-467.

. Kohli, P. S., Maurya, K., Thakur, J. K., Bhosale, R., Giri, J. J. P., Cell, & Environment. (2022). Significance of

root hairs in developing stress‐resilient plants for sustainable crop production. 45(3), 677-694.

. Kuo, H. F., Chang, T. Y., Chiang, S. F., Wang, W. D., Charng, Y. y., & Chiou, T. J. J. T. P. J. (2014). Arabidopsis

inositol pentakisphosphate 2‐kinase, A t IPK 1, is required for growth and modulates phosphate homeostasis at the

transcriptional level. 80(3), 503-515.

. Lambers, H., Albornoz, F., Kotula, L., Laliberté, E., Ranathunge, K., Teste, F. P., . . . Soil. (2018). How

belowground interactions contribute to the coexistence of mycorrhizal and non-mycorrhizal species in severely

phosphorus-impoverished hyperdiverse ecosystems. 424, 11-33.

. Li, M., Qin, C., Welti, R., & Wang, X. J. P. p. (2006). Double knockouts of phospholipases D ζ 1 and D ζ 2 in

Arabidopsis affect root elongation during phosphate-limited growth but do not affect root hair patterning. 140(2),

-770.

. Li, Z., Gao, Q., Liu, Y., He, C., Zhang, X., & Zhang, J. J. P. (2011). Overexpression of transcription factor ZmPTF1

improves low phosphate tolerance of maize by regulating carbon metabolism and root growth. 233, 1129-1143.31

. Liang, C. Y., Chen, Z. J., Yao, Z. F., Tian, J., & Liao, H. J. J. o. i. p. b. (2012). Characterization of two putative

protein phosphatase genes and their involvement in phosphorus efficiency in Phaseolus vulgaris F. 54(6), 400-411.

. Liu, R., & Lal, R. J. S. r. (2014). Synthetic apatite nanoparticles as a phosphorus fertilizer for soybean (Glycine

max). 4(1), 5686.

. Liu, T.-Y., Aung, K., Tseng, C.-Y., Chang, T.-Y., Chen, Y.-S., & Chiou, T.-J. J. P. P. (2011). Focus Issue on

Phosphorus Plant Physiology: Vacuolar Ca2+/H+ Transport Activity Is Required for Systemic Phosphate

Homeostasis Involving Shoot-to-Root Signaling in Arabidopsis. 156(3), 1176.

. Liu, X., Zhao, X., Zhang, L., Lu, W., Li, X., & Xiao, K. J. F. P. B. (2013). TaPht1; 4, a high-affinity phosphate

transporter gene in wheat (Triticum aestivum), plays an important role in plant phosphate acquisition under

phosphorus deprivation. 40(4), 329-341.

. López-Bucio, J., Hernández-Abreu, E., Sánchez-Calderón, L., Nieto-Jacobo, M. F., Simpson, J., & HerreraEstrella, L. J. P. p. (2002). Phosphate availability alters architecture and causes changes in hormone sensitivity in

the Arabidopsis root system. 129(1), 244-256.

. Lundmark, M., Nilsson, L., Kørner, C. J., & Nielsen, T. H. J. F. P. B. (2011). Overexpression of the MYB-related

transcription factor GCC7 in Arabidopsis thaliana leads to increased levels of Pi and changed P-dependent gene

regulation. 38(2), 151-162.

. Lv, X., Pu, X., Qin, G., Zhu, T., & Lin, H. J. A. (2014). The roles of autophagy in development and stress responses

in Arabidopsis thaliana. 19, 905-921.

. Lynch, J. P., Brown, K. M. J. P., & Soil. (2001). Topsoil foraging–an architectural adaptation of plants to low

phosphorus availability. 237, 225-237.

. Lynch, J. P., Ho, M. D., Phosphorus, L. J. P., & soil. (2005). Rhizoeconomics: carbon costs of phosphorus

acquisition. 269, 45-56.

. Lynch, J. P. J. A. J. o. B. (2007). Roots of the second green revolution. 55(5), 493-512.

. Ma, Z., Bielenberg, D., Brown, K., Lynch, J. J. P., cell, & environment. (2001). Regulation of root hair density by

phosphorus availability in Arabidopsis thaliana. 24(4), 459-467.

. Macrae, M., Ali, G., King, K., Plach, J., Pluer, W., Williams, M., . . . Tang, W. J. J. o. e. q. (2019). Evaluating

hydrologic response in tile‐drained landscapes: Implications for phosphorus transport. 48(5), 1347-1355.

. Maharajan, T., Ceasar, S. A., Ajeesh krishna, T. P., Ramakrishnan, M., Duraipandiyan, V., Naif Abdulla, A. D., &

Ignacimuthu, S. J. P. B. (2018). Utilization of molecular markers for improving the phosphorus efficiency in crop

plants. 137(1), 10-26.

. Marin, M., Feeney, D., Brown, L., Naveed, M., Ruiz, S., Koebernick, N., . . . Puértolas, J. J. A. o. B. (2021).

Significance of root hairs for plant performance under contrasting field conditions and water deficit. 128(1), 1-16.

. Misson, J., Thibaud, M.-C., Bechtold, N., Raghothama, K., & Nussaume, L. J. P. m. b. (2004). Transcriptional

regulation and functional properties of Arabidopsis Pht1; 4, a high affinity transporter contributing greatly to

phosphate uptake in phosphate deprived plants. 55, 727-741.

. Mudge, S. R., Rae, A. L., Diatloff, E., & Smith, F. W. J. T. P. J. (2002). Expression analysis suggests novel roles

for members of the Pht1 family of phosphate transporters in Arabidopsis. 31(3), 341-353.

. Nagarajan, V. K., Jain, A., Poling, M. D., Lewis, A. J., Raghothama, K. G., & Smith, A. P. J. P. P. (2011).

Arabidopsis Pht1; 5 mobilizes phosphate between source and sink organs and influences the interaction between

phosphate homeostasis and ethylene signaling. 156(3), 1149-1163.

. Niu, Y. F., Chai, R. S., Jin, G. L., Wang, H., Tang, C. X., & Zhang, Y. S. J. A. o. b. (2013). Responses of root

architecture development to low phosphorus availability: a review. 112(2), 391-408.

. Nussaume, L., Kanno, S., Javot, H., Marin, E., Pochon, N., Ayadi, A., . . . Thibaud, M.-C. J. F. i. p. s. (2011).

Phosphate import in plants: focus on the PHT1 transporters. 2, 83.

. Oberson, A., & Joner, E. J. J. O. p. i. t. e. (2005). Microbial turnover of phosphorus in soil. 133-164.

. Pang, J., Bansal, R., Zhao, H., Bohuon, E., Lambers, H., Ryan, M. H., . . . Siddique, K. H. J. N. P. (2018). The

carboxylate‐releasing phosphorus‐mobilizing strategy can be proxied by foliar manganese concentration in a large

set of chickpea germplasm under low phosphorus supply. 219(2), 518-529.

. Parker, J. S., Cavell, A. C., Dolan, L., Roberts, K., & Grierson, C. S. J. T. P. C. (2000). Genetic interactions during

root hair morphogenesis in Arabidopsis. 12(10), 1961-1974.

. Paszkowski, U., Kroken, S., Roux, C., & Briggs, S. P. J. P. o. t. N. A. o. S. (2002). Rice phosphate transporters

include an evolutionarily divergent gene specifically activated in arbuscular mycorrhizal symbiosis. 99(20), 13324-

. Pausch, J., Loeppmann, S., Kühnel, A., Forbush, K., Kuzyakov, Y., Cheng, W. J. S. B., & Biochemistry. (2016).

Rhizosphere priming of barley with and without root hairs. 100, 74-82.

. Penn, C. J., & Camberato, J. J. J. A. (2019). A critical review on soil chemical processes that control how soil pH

affects phosphorus availability to plants. 9(6), 120.

. Péret, B., Clément, M., Nussaume, L., & Desnos, T. J. T. i. p. s. (2011). Root developmental adaptation to

phosphate starvation: better safe than sorry. 16(8), 442-450.

. Pérez-Torres, C.-A., Lopez-Bucio, J., Cruz-Ramírez, A., Ibarra-Laclette, E., Dharmasiri, S., Estelle, M., & HerreraEstrella, L. J. T. P. C. (2008). Phosphate availability alters lateral root development in Arabidopsis by modulating

auxin sensitivity via a mechanism involving the TIR1 auxin receptor. 20(12), 3258-3272.32

. Poirier, Y., & Bucher, M. J. T. A. b. A. S. o. P. B. (2002). Phosphate transport and homeostasis in Arabidopsis. 1.

. Poirier, Y., Thoma, S., Somerville, C., & Schiefelbein, J. J. P. p. (1991). Mutant of Arabidopsis deficient in xylem

loading of phosphate. 97(3), 1087-1093.

. Qin, L., Zhao, J., Tian, J., Chen, L., Sun, Z., Guo, Y., . . . Liao, H. J. P. p. (2012). The high-affinity phosphate

transporter GmPT5 regulates phosphate transport to nodules and nodulation in soybean. 159(4), 1634-1643.

. Quintero, C. E., Boschetti, N. G., Benavidez, R. A. J. C. i. s. s., & analysis, p. (2003). Effect of soil buffer capacity

on soil test phosphorus interpretation and fertilizer requirement. 34(9-10), 1435-1450.

. Raghothama, K., Karthikeyan, A. J. P., & Soil. (2005). Phosphate acquisition. 274, 37-49.

. Ramaekers, L., Remans, R., Rao, I. M., Blair, M. W., & Vanderleyden, J. J. F. C. R. (2010). Strategies for

improving phosphorus acquisition efficiency of crop plants. 117(2-3), 169-176.

. Rausch, C., & Bucher, M. J. P. (2002). Molecular mechanisms of phosphate transport in plants. 216, 23-37.

. Requejo, M. I., & Eichler-Löbermann, B. J. N. C. i. A. (2014). Organic and inorganic phosphorus forms in soil as

affected by long-term application of organic amendments. 100, 245-255.

. Richardson, A. E., & Simpson, R. J. J. P. p. (2011). Soil microorganisms mediating phosphorus availability update

on microbial phosphorus. 156(3), 989-996.

. Richardson, A. E. J. P., & soil. (2009). Regulating the phosphorus nutrition of plants: molecular biology meeting

agronomic needs. 322(1-2), 17-24.

. Roach, T., Beckett, R. P., Minibayeva, F. V., Colville, L., Whitaker, C., Chen, H., . . . Environment. (2010).

Extracellular superoxide production, viability and redox poise in response to desiccation in recalcitrant Castanea

sativa seeds. 33(1), 59-75.

. Roberts, T. L., Johnston, A. E. J. R., conservation, & recycling. (2015). Phosphorus use efficiency and management

in agriculture. 105, 275-281.

. Robertson-Albertyn, S., Alegria Terrazas, R., Balbirnie, K., Blank, M., Janiak, A., Szarejko, I., . . . Hedley, P. E.

J. F. i. p. s. (2017). Root hair mutations displace the barley rhizosphere microbiota. 8, 1094.

. Robles-Aguilar, A. A., Pang, J., Postma, J. A., Schrey, S. D., Lambers, H., Jablonowski, N. D. J. P., & soil. (2019).

The effect of pH on morphological and physiological root traits of Lupinus angustifolius treated with struvite as a

recycled phosphorus source. 434, 65-78.

. Ros, M. B., Koopmans, G. F., van Groenigen, K. J., Abalos, D., Oenema, O., Vos, H. M., & van Groenigen, J. W.

J. S. R. (2020). Towards optimal use of phosphorus fertiliser. 10(1), 17804.

. Rose, T. J., Rose, M. T., Pariasca-Tanaka, J., Heuer, S., & Wissuwa, M. J. F. i. P. S. (2011). The frustration with

utilization: why have improvements in internal phosphorus utilization efficiency in crops remained so elusive? , 2,

. Rouached, H., Stefanovic, A., Secco, D., Bulak Arpat, A., Gout, E., Bligny, R., & Poirier, Y. J. T. P. J. (2011).

Uncoupling phosphate deficiency from its major effects on growth and transcriptome via PHO1 expression in

Arabidopsis. 65(4), 557-570.

. Rubio, M. C., Becana, M., Kanematsu, S., Ushimaru, T., & James, E. K. J. N. P. (2009). Immunolocalization of

antioxidant enzymes in high‐pressure frozen root and stem nodules of Sesbania rostrata. 183(2), 395-407.

. Sánchez-Calderón, L., López-Bucio, J., Chacón-López, A., Gutiérrez-Ortega, A., Hernández-Abreu, E., & HerreraEstrella, L. J. P. p. (2006). Characterization of low phosphorus insensitive mutants reveals a crosstalk between low

phosphorus-induced determinate root development and the activation of genes involved in the adaptation of

Arabidopsis to phosphorus deficiency. 140(3), 879-889.

. Sanderson, K. R., & Sanderson, J. B. J. C. j. o. p. s. (2006). Prince Edward Island growers can reduce soil

phosphorus buildup while maintaining carrot crop yield. 86(Special Issue), 1401-1403.

. Schneider, K. D., Thiessen Martens, J. R., Zvomuya, F., Reid, D. K., Fraser, T. D., Lynch, D. H., . . . Wilson, H.

F. J. J. o. E. Q. (2019). Options for improved phosphorus cycling and use in agriculture at the field and regional

scales. 48(5), 1247-1264.

. Schunmann, P. H., Richardson, A. E., Vickers, C. E., & Delhaize, E. J. P. P. (2004). Promoter analysis of the barley

Pht1; 1 phosphate transporter gene identifies regions controlling root expression and responsiveness to phosphate

deprivation. 136(4), 4205-4214.

. Seeling, B., Zasoski, R. J. J. P., & Soil. (1993). Microbial effects in maintaining organic and inorganic solution

phosphorus concentrations in a grassland topsoil. 148, 277-284.

. Seo, H.-M., Jung, Y., Song, S., Kim, Y., Kwon, T., Kim, D.-H., . . . Nam, M.-H. J. B. L. (2008). Increased

expression of OsPT1, a high-affinity phosphate transporter, enhances phosphate acquisition in rice. 30, 1833-1838.

. Shen, J., Yuan, L., Zhang, J., Li, H., Bai, Z., Chen, X., . . . Zhang, F. J. P. p. (2011). Phosphorus dynamics: from

soil to plant. 156(3), 997-1005.

. Shi, J., Hu, H., Zhang, K., Zhang, W., Yu, Y., Wu, Z., & Wu, P. J. J. o. E. B. (2014). The paralogous SPX3 and

SPX5 genes redundantly modulate Pi homeostasis in rice. 65(3), 859-870.

. Shin, H., Shin, H. S., Dewbre, G. R., & Harrison, M. J. J. T. P. J. (2004). Phosphate transport in Arabidopsis: Pht1;

and Pht1; 4 play a major role in phosphate acquisition from both low‐and high‐phosphate environments. 39(4),

-642.

. Singh, R., & Yadav, M. J. J. o. F. L. (2008). Effect of phosphorus and biofertilizers on growth, yield and nutrient

uptake of long duration pigeonpea under rainfed condition. 21(1), 46-48.33

. Smith, S. E., Jakobsen, I., Grønlund, M., & Smith, F. A. J. P. p. (2011). Roles of arbuscular mycorrhizas in plant

phosphorus nutrition: interactions between pathways of phosphorus uptake in arbuscular mycorrhizal roots have

important implications for understanding and manipulating plant phosphorus acquisition. 156(3), 1050-1057.

. Song, G., & Liu, S. J. A. O. S. (2015). Phosphorus speciation and distribution in surface sediments of the Yellow

Sea and East China Sea and potential impacts on ecosystem. 34, 84-91.

. Stefanovic, A., Arpat, A. B., Bligny, R., Gout, E., Vidoudez, C., Bensimon, M., & Poirier, Y. J. T. P. J. (2011).

Over‐expression of PHO1 in Arabidopsis leaves reveals its role in mediating phosphate efflux. 66(4), 689-699.

. Stefanovic, A., Ribot, C., Rouached, H., Wang, Y., Chong, J., Belbahri, L., . . . Poirier, Y. J. T. P. J. (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. 50(6), 982-994.

. Sun, D., Hale, L., Kar, G., Soolanayakanahally, R., & Adl, S. J. C. (2018). Phosphorus recovery and reuse by

pyrolysis: Applications for agriculture and environment. 194, 682-691.

. Svistoonoff, S., Creff, A., Reymond, M., Sigoillot-Claude, C., Ricaud, L., Blanchet, A., . . . Desnos, T. J. N. g.

(2007). Root tip contact with low-phosphate media reprograms plant root architecture. 39(6), 792-796.

. Szarejko, I., Janiak, A., Chmielewska, B., & Nawrot, M. J. B. G. N. (2005). Genetic analysis of several root hair

mutants of barley. 35, 36-38.

. Ticconi, C. A., Delatorre, C. A., Lahner, B., Salt, D. E., & Abel, S. J. T. P. J. (2004). Arabidopsis pdr2 reveals a

phosphate‐sensitive checkpoint in root development. 37(6), 801-814.

. Tran, H. T., Qian, W., Hurley, B. A., SHE, Y. M., Wang, D., Plaxton, W. C. J. P., cell, & environment. (2010).

Biochemical and molecular characterization of AtPAP12 and AtPAP26: the predominant purple acid phosphatase

isozymes secreted by phosphate‐starved Arabidopsis thaliana. 33(11), 1789-1803.

. Tyburski, J., Dunajska-Ordak, K., Skorupa, M., & Tretyn, A. J. J. o. B. (2012). Role of ascorbate in the regulation

of the Arabidopsis thaliana root growth by phosphate availability. 2012.

. Tyburski, J., Dunajska, K., Tretyn, A. J. P. s., & behavior. (2010). A role for redox factors in shaping root

architecture under phosphorus deficiency. 5(1), 64-66.

. Uddin, M. J., Ahmed, S., Rashid, M., Hasan, M. M., & Asaduzzaman, M. J. J. o. A. R. (2011). Effect of spacing

on the yield and yield attributes of transplanted aman rice cultivars in medium lowland ecosystem of Bangladesh.

(4), 465-476.

. van de Wiel, C. C., van der Linden, C. G., & Scholten, O. E. J. E. (2016). Improving phosphorus use efficiency in

agriculture: opportunities for breeding. 207, 1-22.

. Vance, C. P., Uhde‐Stone, C., & Allan, D. L. J. N. p. (2003). Phosphorus acquisition and use: critical adaptations

by plants for securing a nonrenewable resource. 157(3), 423-447.

. Wang, Q., Wang, J., Yang, Y., Du, W., Zhang, D., Yu, D., & Cheng, H. J. B. g. (2016). A genome-wide expression

profile analysis reveals active genes and pathways coping with phosphate starvation in soybean. 17, 1-11.

. Wang, X., Wang, Y., Tian, J., Lim, B. L., Yan, X., & Liao, H. J. P. P. (2009). Overexpressing AtPAP15 enhances

phosphorus efficiency in soybean. 151(1), 233-240.

. Wang, Y., Lambers, H. J. P., & Soil. (2020). Root-released organic anions in response to low phosphorus

availability: recent progress, challenges and future perspectives. 447, 135-156.

. Wang, Y., Thorup-Kristensen, K., Jensen, L. S., & Magid, J. J. F. i. p. s. (2016). Vigorous root growth is a better

indicator of early nutrient uptake than root hair traits in spring wheat grown under low fertility. 7, 865.

. Wang, Z., Ruan, W., Shi, J., Zhang, L., Xiang, D., Yang, C., . . . Yu, Y. J. P. o. t. N. A. o. S. (2014). Rice SPX1

and SPX2 inhibit phosphate starvation responses through interacting with PHR2 in a phosphate-dependent manner.

(41), 14953-14958.

. Wasaki, J., Maruyama, H., Tanaka, M., Yamamura, T., Dateki, H., Shinano, T., . . . nutrition, p. (2009).

Overexpression of the LASAP2 gene for secretory acid phosphatase in white lupin improves the phosphorus uptake

and growth of tobacco plants. 55(1), 107-113.

. Wen, T. J., & Schnable, P. S. J. A. j. o. b. (1994). Analyses of mutants of three genes that influence root hair

development in Zea mays (Gramineae) suggest that root hairs are dispensable. 81(7), 833-842.

. Wen, Z., Li, H., Shen, Q., Tang, X., Xiong, C., Li, H., . . . Shen, J. J. N. P. (2019). Tradeoffs among root

morphology, exudation and mycorrhizal symbioses for phosphorus‐acquisition strategies of 16 crop species.

(2), 882-895.

. Wendrich, J. R., Yang, B., Vandamme, N., Verstaen, K., Smet, W., Van de Velde, C., . . . Arents, H. E. J. S. (2020).

Vascular transcription factors guide plant epidermal responses to limiting phosphate conditions. 370(6518),

eaay4970.

. White, P. J., George, T. S., Dupuy, L. X., Karley, A. J., Valentine, T. A., Wiesel, L., & Wishart, J. J. F. i. p. s.

(2013). Root traits for infertile soils. 4, 193.

. White, P. J., Veneklaas, E. J. J. P., & soil. (2012). Nature and nurture: the importance of seed phosphorus content.

, 1-8.

. Wild, M., Davière, J.-M., Regnault, T., Sakvarelidze-Achard, L., Carrera, E., Diaz, I. L., . . . Achard, P. J. D. C.

(2016). Tissue-specific regulation of gibberellin signaling fine-tunes Arabidopsis iron-deficiency responses. 37(2),

-200.34

. Williamson, L. C., Ribrioux, S. P., Fitter, A. H., & Leyser, H. O. J. P. p. (2001). Phosphate availability regulates

root system architecture in Arabidopsis. 126(2), 875-882.

. Wu, P., Shou, H., Xu, G., & Lian, X. J. C. o. i. p. b. (2013). Improvement of phosphorus efficiency in rice on the

basis of understanding phosphate signaling and homeostasis. 16(2), 205-212.

. Wu, P., & Wang, Z. J. F. i. B. (2011). Molecular mechanisms regulating Pi-signaling and Pi homeostasis under

OsPHR2, a central Pi-signaling regulator, in rice. 6, 242-245.

. Yamada, T. M., Sueitt, A., Beraldo, D., Botta, C., Fadini, P., Nascimento, M., . . . Mozeto, A. J. W. R. (2012).

Calcium nitrate addition to control the internal load of phosphorus from sediments of a tropical eutrophic reservoir:

microcosm experiments. 46(19), 6463-6475.

. Yang, H., Knapp, J., Koirala, P., Rajagopal, D., Peer, W. A., Silbart, L. K., . . . Gaxiola, R. A. J. P. b. j. (2007).

Enhanced phosphorus nutrition in monocots and dicots over‐expressing a phosphorus‐responsive type I H+‐

pyrophosphatase. 5(6), 735-745.

. Yang, K., Jeong, N., Moon, J.-K., Lee, Y.-H., Lee, S.-H., Kim, H. M., . . . Jeong, S.-C. J. J. o. H. (2010). Genetic

analysis of genes controlling natural variation of seed coat and flower colors in soybean. 101(6), 757-768.

. Yang, S.-Y., Grønlund, M., Jakobsen, I., Grotemeyer, M. S., Rentsch, D., Miyao, A., . . . Salamin, N. J. T. P. C.

(2012). Nonredundant regulation of rice arbuscular mycorrhizal symbiosis by two members of the PHOSPHATE

TRANSPORTER1 gene family. 24(10), 4236-4251.

. Yang, Y., Shi, X., Ballent, W., & Mayer, B. K. J. W. E. R. (2017). Biological phosphorus recovery: Review of

current progress and future needs: Yang et al. 89(12), 2122-2135.

. Yi, K., Wu, Z., Zhou, J., Du, L., Guo, L., Wu, Y., & Wu, P. J. P. p. (2005). OsPTF1, a novel transcription factor

involved in tolerance to phosphate starvation in rice. 138(4), 2087-2096.

. Yu, H., Xie, W., Wang, J., Xing, Y., Xu, C., Li, X., . . . Zhang, Q. J. P. o. (2011). Gains in QTL detection using an

ultra-high density SNP map based on population sequencing relative to traditional RFLP/SSR markers. 6(3),

e17595.

. Zak, D., Goldhammer, T., Cabezas, A., Gelbrecht, J., Gurke, R., Wagner, C., . . . McInnes, R. J. J. o. A. E. (2018).

Top soil removal reduces water pollution from phosphorus and dissolved organic matter and lowers methane

emissions from rewetted peatlands. 55(1), 311-320.

. Zhang, C., Ding, S., Xu, D., Tang, Y., Wong, M. H. J. E. M., & Assessment. (2014). Bioavailability assessment of

phosphorus and metals in soils and sediments: a review of diffusive gradients in thin films (DGT). 186, 7367-7378.

. Zhang, D., Song, H., Cheng, H., Hao, D., Wang, H., Kan, G., . . . Yu, D. J. P. g. (2014). The acid phosphataseencoding gene GmACP1 contributes to soybean tolerance to low-phosphorus stress. 10(1), e1004061.

. Zhang, H., Kovar, J. J. M. o. p. a. f. s., sediments, residuals,, & waters. (2009). Fractionation of soil phosphorus.

, 50-60.

. Zhang, J. L., Zhao, S., Han, C., Wang, Z., Zhong, S., Sun, S., . . . Yuan, K. D. J. N. l. (2016). Epitaxial growth of

single layer blue phosphorus: a new phase of two-dimensional phosphorus. 16(8), 4903-4908.

. Zhang, L., Hu, B., Li, W., Che, R., Deng, K., Li, H., . . . Chu, C. J. N. P. (2014). Os PT 2, a phosphate transporter,

is involved in the active uptake of selenite in rice. 201(4), 1183-1191.

. Zhang, T., Hu, Y., Zhang, K., Tian, C., Guo, J. J. I. C., & Products. (2018). Arbuscular mycorrhizal fungi improve

plant growth of Ricinus communis by altering photosynthetic properties and increasing pigments under drought

and salt stress. 117, 13-19.

. Zhang, Y.-Q., Deng, Y., Chen, R.-Y., Cui, Z.-L., Chen, X.-P., Yost, R., . . . Soil. (2012). The reduction in zinc

concentration of wheat grain upon increased phosphorus-fertilization and its mitigation by foliar zinc application.

, 143-152.

. Zhang, Y., Xu, F., Ding, Y., Du, H., Zhang, Q., Dang, X., . . . Environment. (2021). Abscisic acid mediates barley

rhizosheath formation under mild soil drying by promoting root hair growth and auxin response. 44(6), 1935-1945.

. Zhong, Y., Wang, Y., Guo, J., Zhu, X., Shi, J., He, Q., . . . Lv, Q. J. N. P. (2018). Rice SPX6 negatively regulates

the phosphate starvation response through suppression of the transcription factor PHR2. 219(1), 135-148.

. Zhou, Q. Y., Tian, A. G., Zou, H. F., Xie, Z. M., Lei, G., Huang, J., . . . Chen, S. Y. J. P. b. j. (2008). Soybean

WRKY‐type transcription factor genes, GmWRKY13, GmWRKY21, and GmWRKY54, confer differential

tolerance to abiotic stresses in transgenic Arabidopsis plants. 6(5), 486-503.

. Zhu, J., Kaeppler, S. M., Lynch, J. P. J. P., & Soil. (2005). Mapping of QTL controlling root hair length in maize

(Zea mays L.) under phosphorus deficiency. 270, 299-310.

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2024-01-31