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Phosphorus homeostasis: acquisition, sensing, and long-distance signaling in plants

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Abstract

Phosphorus (P), an essential nutrient required by plants often becomes the limiting factor for plant growth and development. Plants employ various mechanisms to sense the continuously changing P content in the soil. Transcription factors, such as SHORT ROOT (SHR), AUXIN RESPONSE FACTOR19 (ARF19), and ETHYLENE-INSENSITIVE3 (EIN3) regulate the growth of primary roots, root hairs, and lateral roots under low P. Crop improvement strategies under low P depend either on improving P acquisition efficiency or increasing P utilization. The various phosphate transporters (PTs) are involved in the uptake and transport of P from the soil to various plant cellular organelles. A plethora of regulatory elements including transcription factors, microRNAs and several proteins play a critical role in the regulation of coordinated cellular P homeostasis. Among these, the well-established P starvation signaling pathway comprising of central transcriptional factor phosphate starvation response (PHR), microRNA399 (miR399) as a long-distance signal molecule, and PHOSPHATE 2 (PHO2), an E2 ubiquitin conjugase is crucial in the regulation of phosphorus starvation responsive genes. Under PHR control, several classes of PHTs, microRNAs, and proteins modulate root architecture, and metabolic processes to enable plants to adapt to low P. Even though sucrose and inositol phosphates are known to influence the phosphorus starvation response genes, the exact mechanism of regulation is still unclear. In this review, a basic understanding of P homeostasis under low P in plants and all the above aspects are discussed.

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Abbreviations

PTs:

Phosphate transporters

PHT1:

Phosphate transporter1

PHO2:

Phosphate2

IPS1:

Induced by phosphate starvation1

PHR/PSR:

Phosphate starvation response

HATs:

High-affinity transporters

LATs:

Low-affinity transporters

MFS:

Major facilitator superfamily

VPT1:

Vacuolar P transporter1

sRNAs:

Small RNAs

miRNA:

Micro RNAs

PAP1:

Production of anthocyanin pigment1

DFR:

Dihydroflavonol 4-reductase

TGS:

Transcriptional gene silencing

PTGS:

Post-transcriptional gene silencing

PHL1:

PHR1 Like

P1BS:

PHR1 binding site

PHF1:

Phosphate transporter traffic facilitator1

RAM:

Root apical meristem

LPR1:

Low phosphate root1

PDR2:

Phosphate deficiency response2

SHR:

Short root

EIN3:

Ethylene insensitive3

RSL4:

Root hair defective6 like4

TIR1:

Transport inhibitor response1

ARF19:

Auxin response factor19

References

  1. Ding N, Huertas R, Torres-Jerez I, Liu W, Watson B, Scheible WR, Udvardi M (2021) Transcriptional, metabolic, physiological and developmental responses of switchgrass to phosphorus limitation. Plant Cell Environ 44(1):186–202

    Article  CAS  PubMed  Google Scholar 

  2. Jiang M, Caldararu S, Zaehle S, Ellsworth DS, Medlyn BE (2019) Towards a more physiological representation of vegetation phosphorus processes in land surface models. New Phytol 222(3):1223–1229

    Article  PubMed  Google Scholar 

  3. Li Z, Hu J, Wu Y, Wang J, Song H, Chai M, Cong L, Miao F, Ma L, Tang W, Yang C (2022) Integrative analysis of the metabolome and transcriptome reveal the phosphate deficiency response pathways of alfalfa. Plant Physiol Biochem 170:49–63

    Article  CAS  PubMed  Google Scholar 

  4. Di Martino C, Crawford TW Jr (2021) 18 roles and implications of arbuscular. In: Mohammad P (ed) Handbook of plant and crop physiology, vol 12. CRC Press, Boca Raton, p 321

    Chapter  Google Scholar 

  5. Etesami H, Jeong BR (2021) Contribution of arbuscular mycorrhizal fungi, phosphate-solubilizing bacteria, and silicon to P uptake by plant: a review. Front Plant Sci 12:1355

    Article  Google Scholar 

  6. Lopez-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(4):450–453

    Article  CAS  PubMed  Google Scholar 

  7. Gautier AT, Cochetel N, Merlin I, Hevin C, Lauvergeat V, Vivin P, Mollier A, Ollat N, Cookson SJ (2020) Scion genotypes exert long distance control over rootstock transcriptome responses to low phosphate in grafted grapevine. BMC Plant Biol 20(1):1–5

    Article  CAS  Google Scholar 

  8. Rawat P, Das S, Shankhdhar D, Shankhdhar SC (2021) Phosphate-solubilizing microorganisms: mechanism and their role in phosphate solubilization and uptake. J Soil Sci Plant Nut 21(1):49–68

    Article  CAS  Google Scholar 

  9. López-Bucio J, Hernández-Abreu E, Sánchez-Calderón L, Nieto-Jacobo MF, Simpson J, Herrera-Estrella L (2002) Phosphate availability alters architecture and causes changes in hormone sensitivity in the Arabidopsis root system. Plant Physiol 129(1):244–256

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  10. Sánchez-Calderón L, López-Bucio J, Chacón-López A, Cruz-Ramírez A, Nieto-Jacobo F, Dubrovsky JG, Herrera-Estrella L (2005) Phosphate starvation induces a determinate developmental program in the roots of Arabidopsis thaliana. Plant Cell Physiol 46(1):174–184

    Article  PubMed  CAS  Google Scholar 

  11. Wu M, Wei Q, Xu L, Li H, Oelmüller R, Zhang W (2018) Piriformospora indica enhances phosphorus absorption by stimulating acid phosphatase activities and organic acid accumulation in Brassica napus. Plant Soil 432(1):333–344

    Article  CAS  Google Scholar 

  12. Brundrett MC, Tedersoo L (2018) Evolutionary history of mycorrhizal symbioses and global host plant diversity. New Phytol 220(4):1108–1115

    Article  PubMed  Google Scholar 

  13. Pang J, Yang J, Lambers H, Tibbett M, Siddique KH, Ryan MH (2015) Physiological and morphological adaptations of herbaceous perennial legumes allow differential access to sources of varyingly soluble phosphate. Physiol Plant 154(4):511–525

    Article  CAS  PubMed  Google Scholar 

  14. 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 Phytol 173(4):817–831

    Article  CAS  PubMed  Google Scholar 

  15. Liu F, Xu Y, Jiang H, Jiang C, Du Y, Gong C, Wang W, Zhu S, Han G, Cheng B (2016) Systematic identification, evolution and expression analysis of the Zea mays PHT1 gene family reveals several new members involved in root colonization by arbuscular mycorrhizal fungi. Int J Mol Sci 17(6):930

    Article  PubMed Central  CAS  Google Scholar 

  16. Liu F, Xu Y, Han G, Wang W, Li X, Cheng B (2018) Identification and functional characterization of a maize phosphate transporter induced by mycorrhiza formation. Plant Cell Physiol 59(8):1683–1694

    Article  CAS  PubMed  Google Scholar 

  17. Nagy R, Karandashov V, Chague V, Kalinkevich K, Tamasloukht MB, Xu G, 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. Plant J 42(2):236–250

    Article  CAS  PubMed  Google Scholar 

  18. Ezawa T, Saito K (2018) How do arbuscular mycorrhizal fungi handle phosphate? New insight into fine-tuning of phosphate metabolism. New Phytol 220(4):1116–1121

    Article  CAS  PubMed  Google Scholar 

  19. 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(6):792–796

    Article  CAS  PubMed  Google Scholar 

  20. López-Bucio JS, Salmerón-Barrera GJ, Ravelo-Ortega G, Raya-González J, León P, de la Cruz HR, Campos-García J, López-Bucio J, Guevara-García ÁA (2019) Mitogen-activated protein kinase 6 integrates phosphate and iron responses for indeterminate root growth in Arabidopsis thaliana. Planta 250(4):1177–1189

    Article  PubMed  CAS  Google Scholar 

  21. Raya-González J, Ojeda-Rivera JO, Mora-Macias J, Oropeza-Aburto A, Ruiz-Herrera LF, López-Bucio J, Herrera-Estrella L (2021) MEDIATOR16 orchestrates local and systemic responses to phosphate scarcity in Arabidopsis roots. New Phytol 229(3):1278–1288

    Article  PubMed  CAS  Google Scholar 

  22. Ravelo-Ortega G, Pelagio-Flores R, López-Bucio J, Campos-García J, Reyes de la Cruz H, López-Bucio JS (2021) Early sensing of phosphate deprivation triggers the formation of extra root cap cell layers via SOMBRERO through a process antagonized by auxin signaling. Plant Mol Biol 2:1–5

    Google Scholar 

  23. Mora-Macías J, Ojeda-Rivera JO, 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(17):E3563–E3572

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  24. Balzergue C, Dartevelle T, Godon C, Laugier E, Meisrimler C, Teulon JM, Creff A, Bissler M, Brouchoud C, Hagège A, Müller J (2017) Low phosphate activates STOP1-ALMT1 to rapidly inhibit root cell elongation. Nat Commun 8(1):1–6

    Article  CAS  Google Scholar 

  25. Pérez-Torres CA, López-Bucio J, Cruz-Ramírez A, Ibarra-Laclette E, Dharmasiri S, Estelle M, Herrera-Estrella L (2008) Phosphate availability alters lateral root development in Arabidopsis by modulating auxin sensitivity via a mechanism involving the TIR1 auxin receptor. Plant Cell 20(12):3258–3272

    Article  PubMed  PubMed Central  Google Scholar 

  26. Jia H, Zhang S, Wang L, Yang Y, Zhang H, Cui H, Shao H, Xu G (2017) OsPht1; 8, a phosphate transporter, is involved in auxin and phosphate starvation response in rice. J Exp Bot 68(18):5057–5068

    Article  CAS  PubMed  Google Scholar 

  27. Hinsinger P (2001) Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review. Plant Soil 237(2):173–195

    Article  CAS  Google Scholar 

  28. Poli Y, Nallamothu V, Balakrishnan D, Ramesh P, Desiraju S, Mangrauthia SK, Voleti SR, Neelamraju S (2018) Increased catalase activity and maintenance of photosystem II distinguishes high-yield mutants from low-yield mutants of rice var. Nagina22 under low-phosphorus stress. Front Plant Sci 9:1543

    Article  PubMed  PubMed Central  Google Scholar 

  29. Młodzińska E, Zboińska M (2016) Phosphate uptake and allocation–a closer look at Arabidopsis thaliana L. and Oryza sativa L. Front Plant Sci 7:1198

    Article  PubMed  PubMed Central  Google Scholar 

  30. Srivastava S, Upadhyay MK, Srivastava AK, Abdelrahman M, Suprasanna P, Tran LS (2018) Cellular and subcellular phosphate transport machinery in plants. Int J Mol Sci 19(7):1914

    Article  PubMed Central  CAS  Google Scholar 

  31. Teng W, Zhao YY, Zhao XQ, He X, Ma WY, Deng Y, Chen XP, Tong YP (2017) Genome-wide identification, characterization, and expression analysis of PHT1 phosphate transporters in wheat. Front Plant Sci 8:543

    Article  PubMed  PubMed Central  Google Scholar 

  32. Wan Y, Wang Z, Xia J, Shen S, Guan M, Zhu M, Qiao C, Sun F, Liang Y, Li J, Lu K (2020) Genome-wide analysis of phosphorus transporter genes in brassica and their roles in heavy metal stress tolerance. Int J Mol Sci 21(6):2209

    Article  CAS  PubMed Central  Google Scholar 

  33. Gho YS, Jung KH (2019) Comparative expression analyses of rice and Arabidopsis phosphate transporter families revealed their conserved roles for the phosphate starvation response. Plant Breed Biotechnol 7(1):42–49

    Article  Google Scholar 

  34. Liu F, Chang XJ, Ye Y, Xie WB, Wu P, Lian XM (2011) Comprehensive sequence and whole-life-cycle expression profile analysis of the phosphate transporter gene family in rice. Mol plant 4(6):1105–1122

    Article  CAS  PubMed  Google Scholar 

  35. Wang D, Lv S, Jiang P, Li Y (2017) Roles, regulation, and agricultural application of plant phosphate transporters. Front Plant Sci 8:817

    Article  PubMed  PubMed Central  Google Scholar 

  36. Ai P, Sun S, Zhao J, Fan X, Xin W, Guo Q, Yu L, Shen Q, Wu P, Miller AJ, Xu G (2009) Two rice phosphate transporters, OsPht1; 2 and OsPht1; 6, have different functions and kinetic properties in uptake and translocation. Plant J 57(5):798–809

    Article  CAS  PubMed  Google Scholar 

  37. Shin H, Shin HS, Dewbre GR, Harrison MJ (2004) Phosphate transport in Arabidopsis: Pht1; 1 and Pht1; 4 play a major role in phosphate acquisition from both low-and high-phosphate environments. Plant J 39(4):629–642

    Article  CAS  PubMed  Google Scholar 

  38. 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. Plant Cell 24(5):2168–2183

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. 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. Plant J 31(3):341–353

    Article  CAS  PubMed  Google Scholar 

  40. Wang Y, Secco D, Poirier Y (2008) Characterization of the PHO1 gene family and the responses to phosphate deficiency of Physcomitrella patens. Plant Physiol 146(2):646–656

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Bayle V, Arrighi JF, Creff A, Nespoulous C, Vialaret J, Rossignol M, Gonzalez E, Paz-Ares J, Nussaume L (2011) Arabidopsis thaliana high-affinity phosphate transporters exhibit multiple levels of post-translational regulation. Plant Cell 23(4):1523–1535

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Ceasar SA (2020) Regulation of low phosphate stress in plants. In: Tripathi DK, Singh VP, Chauhan DK, Sharma S, Prasad SM, Dubey NK, Ramawat N (eds) Plant life under changing environment: responses and management. Academic Press, Cambridge, pp 123–156

    Chapter  Google Scholar 

  43. 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(3):396–416

    Article  CAS  PubMed  Google Scholar 

  44. Rausch C, Bucher M (2002) Molecular mechanisms of phosphate transport in plants. Planta 216(1):23–37

    Article  CAS  PubMed  Google Scholar 

  45. Guo C, Zhao X, Liu X, Zhang L, Gu J, Li X, Lu W, Xiao K (2013) Function of wheat phosphate transporter gene TaPHT2; 1 in Pi translocation and plant growth regulation under replete and limited Pi supply conditions. Planta 237(4):1163–1178

    Article  CAS  PubMed  Google Scholar 

  46. Zhang C, Meng S, Li M, Zhao Z (2016) Genomic identification and expression analysis of the phosphate transporter gene family in poplar. Front Plant Sci 7:1398

    PubMed  PubMed Central  Google Scholar 

  47. Zhu W, Miao Q, Sun D, Yang G, Wu C, Huang J, Zheng C (2012) The mitochondrial phosphate transporters modulate plant responses to salt stress via affecting ATP and gibberellin metabolism in Arabidopsis thaliana. PLoS ONE 7:e43530

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Shukla V, Kaur M, Aggarwal S, Bhati KK, Kaur J, Mantri S, Pandey AK (2016) Tissue specific transcript profiling of wheat phosphate transporter genes and its association with phosphate allocation in grains. Sci Rep 6(1):1–2

    Article  CAS  Google Scholar 

  49. Hamburger D, Rezzonico E, Petétot JM, Somerville C, Poirier Y (2002) Identification and characterization of the Arabidopsis PHO1 gene involved in phosphate loading to the xylem. Plant Cell 14(4):889–902

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. 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 domain-containing proteins in phosphate homeostasis. New Phytol 193(4):842–851

    Article  CAS  PubMed  Google Scholar 

  51. Wege S, Khan GA, Jung JY, Vogiatzaki E, Pradervand S, Aller I, Meyer AJ, Poirier Y (2016) The EXS domain of PHO1 participates in the response of shoots to phosphate deficiency via a root-to-shoot signal. Plant Physiol 170(1):385–400

    Article  CAS  PubMed  Google Scholar 

  52. Austin S, Mayer A (2020) Phosphate homeostasis—a vital metabolic equilibrium maintained through the INPHORS signaling pathway. Front Microbiol 11:1367

    Article  PubMed  PubMed Central  Google Scholar 

  53. 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 Physiol 152(3):1693–1704

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Salazar-Vidal MN, Acosta-Segovia E, Sanchez-Leon N, Ahern KR, Brutnell TP, Sawers RJ (2016) Characterization and transposon mutagenesis of the maize (Zea mays) Pho1 gene family. PLoS ONE 11(9):e0161882

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  55. Yamaji N, Takemoto Y, Miyaji T, Mitani-Ueno N, Yoshida KT, Ma JF (2017) Reducing phosphorus accumulation in rice grains with an impaired transporter in the node. Nature 541(7635):92–95

    Article  CAS  PubMed  Google Scholar 

  56. Zhao H, Frank T, Tan Y, Zhou C, Jabnoune M, Arpat AB, Cui H, Huang J, He Z, Poirier Y, Engel KH (2016) Disruption of OsSULTR 3; 3 reduces phytate and phosphorus concentrations and alters the metabolite profile in rice grains. New Phytol 211(3):926–939

    Article  CAS  PubMed  Google Scholar 

  57. Tiwari M, Sharma D, Trivedi PK (2014) Artificial microRNA mediated gene silencing in plants: progress and perspectives. Plant Mol Biol 86(1–2):1–8

    Article  CAS  PubMed  Google Scholar 

  58. 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 Physiol 151(4):2120–2132

    Article  PubMed  PubMed Central  Google Scholar 

  59. Pant BD, Buhtz A, Kehr J, Scheible WR (2008) MicroRNA399 is a long-distance signal for the regulation of plant phosphate homeostasis. Plant J 53(5):731–738

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Kant S, Peng M, Rothstein SJ (2011) Genetic regulation by NLA and microRNA827 for maintaining nitrate-dependent phosphate homeostasis in Arabidopsis. PLoS Genet 7(3):e1002021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Huen A, Bally J, Smith P (2018) Identification and characterisation of microRNAs and their target genes in phosphate-starved Nicotiana benthamiana by small RNA deep sequencing and 5’RACE analysis. BMC Genom 19(1):1–8

    Article  CAS  Google Scholar 

  62. Lin SI, Santi C, Jobet E, Lacut E, El Kholti N, Karlowski WM, Verdeil JL, Breitler JC, Périn C, Ko SS, Guiderdoni E (2010) Complex regulation of two target genes encoding SPX-MFS proteins by rice miR827 in response to phosphate starvation. Plant Cell Physiol 51(12):2119–2131

    Article  CAS  PubMed  Google Scholar 

  63. Yan W, Chen GH, Yang LF, Gai JY, Zhu YL (2014) Overexpression of the rice phosphate transporter gene OsPT6 enhances tolerance to low phosphorus stress in vegetable soybean. Sci Hortic 177:71–76

    Article  CAS  Google Scholar 

  64. Zhao X, Liu X, Guo C, Gu J, Xiao K (2013) Identification and characterization of microRNAs from wheat (Triticum aestivum L.) under phosphorus deprivation. J Plant Biochem Biotechnol 22(1):113–123

    Article  CAS  Google Scholar 

  65. Valdés-López O, Yang SS, Aparicio-Fabre R, Graham PH, Reyes JL, Vance CP, Hernández G (2010) MicroRNA expression profile in common bean (Phaseolus vulgaris) under nutrient deficiency stresses and manganese toxicity. New Phytol 187(3):805–818

    Article  PubMed  CAS  Google Scholar 

  66. Liu X, Chu S, Sun C, Xu H, Zhang J, Jiao Y, Zhang D (2020) Genome-wide identification of low phosphorus responsive microRNAs in two soybean genotypes by high-throughput sequencing. Funct Integr Genom 20(6):825–838

    Article  CAS  Google Scholar 

  67. Gu M, Xu K, Chen A, Zhu Y, Tang G, Xu G (2010) Expression analysis suggests potential roles of microRNAs for phosphate and arbuscular mycorrhizal signaling in Solanum lycopersicum. Physiol Plantarum 138(2):226–237

    Article  CAS  Google Scholar 

  68. Jaeger KE, Wigge PA (2007) FT protein acts as a long-range signal in Arabidopsis. Curr Biol 17(12):1050–1054

    Article  CAS  PubMed  Google Scholar 

  69. Buhtz A, Springer F, Chappell L, Baulcombe DC, Kehr J (2008) Identification and characterization of small RNAs from the phloem of Brassica napus. Plant J 53(5):739–749

    Article  CAS  PubMed  Google Scholar 

  70. Wang F, Ding D, Li J, He L, Xu X, Zhao Y, Yan B, Li Z, Xu J (2020) Characterisation of genes involved in galactolipids and sulfolipids metabolism in maize and Arabidopsis and their differential responses to phosphate deficiency. Funct Plant Biol 47(4):279–292

    Article  CAS  PubMed  Google Scholar 

  71. Bari R, Pant BD, Stitt M, Scheible WR (2006) PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol 141(3):988–999

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Allen E, Xie Z, Gustafson AM, Carrington JC (2005) microRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121(2):207–221

    Article  CAS  PubMed  Google Scholar 

  73. Fujii H, Chiou TJ, Lin SI, Aung K, Zhu JK (2005) A miRNA involved in phosphate-starvation response in Arabidopsis. Curr Biol 15(22):2038–2043

    Article  CAS  PubMed  Google Scholar 

  74. Rubio V, Linhares F, Solano R, Martín 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 Dev 15(16):2122–2133

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Sun L, Song L, Zhang Y, Zheng Z, Liu D (2016) Arabidopsis PHL2 and PHR1 act redundantly as the key components of the central regulatory system controlling transcriptional responses to phosphate starvation. Plant Physiol 170(1):499–514

    Article  CAS  PubMed  Google Scholar 

  76. Xue YB, Xiao BX, Zhu SN, Mo XH, Liang CY, Tian J, Liao H, Miriam G (2017) GmPHR25, a GmPHR member up-regulated by phosphate starvation, controls phosphate homeostasis in soybean. J Exp Bot 68(17):4951–4967

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Guo M, Ruan W, Li C, Huang F, Zeng M, Liu Y, Yu Y, Ding X, Wu Y, Wu Z, Mao C (2015) Integrative comparison of the role of the PHOSPHATE RESPONSE1 subfamily in phosphate signaling and homeostasis in rice. Plant Physiol 168(4):1762–1776

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Sega P, Pacak A (2019) Plant PHR transcription factors: put on a map. Genes 10(12):1018

    Article  CAS  PubMed Central  Google Scholar 

  79. Ruan W, Guo M, Wu P, Yi K (2017) Phosphate starvation induced OsPHR4 mediates Pi-signaling and homeostasis in rice. Plant Mol Biol 93(3):327–340

    Article  CAS  PubMed  Google Scholar 

  80. He Y, Zhang X, Li L, Sun Z, Li J, Chen X, Hong G (2021) SPX4 interacts with both PHR1 and PAP1 to regulate critical steps in phosphorus-status-dependent anthocyanin biosynthesis. New Phytol 230(1):205–217

    Article  CAS  PubMed  Google Scholar 

  81. Wang Z, Ruan W, Shi J, Zhang L, Xiang D, Yang C, Li C, Wu Z, Liu Y, Yu Y, Shou H (2014) Rice SPX1, and SPX2 inhibit phosphate starvation responses through interacting with PHR2 in a phosphate-dependent manner. Proc Natl Acad Sci 111(41):14953–14958

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Zhang J, Jiang F, Shen Y, Zhan Q, Bai B, Chen W, Chi Y (2019) Transcriptome analysis reveals candidate genes related to phosphorus starvation tolerance in sorghum. BMC Plant Biol 19(1):1–8

    Article  Google Scholar 

  83. Miura K, Rus A, Sharkhuu A, Yokoi S, Karthikeyan AS, Raghothama KG, Baek D, Koo YD, Jin JB, Bressan RA, Yun DJ (2005) The Arabidopsis SUMO E3 ligase SIZ1 controls phosphate deficiency responses. Proc Natl Acad Sci 102(21):7760–7765

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Wang H, Sun R, Cao Y, Pei W, Sun Y, Zhou H, Wu X, Zhang F, Luo L, Shen Q, Xu G (2015) OsSIZ1, a SUMO E3 ligase gene, is involved in the regulation of the responses to phosphate and nitrogen in rice. Plant Cell Physiol 56(12):2381–2395

    Article  CAS  PubMed  Google Scholar 

  85. Puga MI, Mateos I, Charukesi R, Wang Z, Franco-Zorrilla JM, de Lorenzo L, Irigoyen ML, Masiero S, Bustos R, Rodríguez J, Leyva A (2014) SPX1 is a phosphate-dependent inhibitor of Phosphate Starvation Response 1 in Arabidopsis. Proc Natl Acad Sci 111(41):14947–14952

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Osorio MB, Ng S, Berkowitz O, De Clercq I, Mao C, Shou H, Whelan J, Jost R (2019) SPX4 acts on PHR1-dependent and-independent regulation of shoot phosphorus status in Arabidopsis. Plant Physiol 181(1):332–352

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Liu N, Shang W, Li C, Jia L, Wang X, Xing G, Zheng W (2018) Evolution of the SPX gene family in plants and its role in the response mechanism to phosphorus stress. Open Biol 8(1):170231

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  88. Ruan W, Guo M, Wang X, Guo Z, Xu Z, Xu L, Zhao H, Sun H, Yan C, Yi K (2019) Two RING-finger ubiquitin E3 ligases regulate the degradation of SPX4, an internal phosphate sensor, for phosphate homeostasis and signaling in rice. Mol Plant 12(8):1060–1074

    Article  CAS  PubMed  Google Scholar 

  89. Gu M, Zhang J, Li H, Meng D, Li R, Dai X, Wang S, Liu W, Qu H, Xu G (2017) Maintenance of phosphate homeostasis and root development are coordinately regulated by MYB1, an R2R3-type MYB transcription factor in rice. J Exp Bot 68(13):3603–3615

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Peng Z, Tian J, Luo R, Kang Y, Lu Y, Hu Y, Liu N, Zhang J, Cheng H, Niu S, Zhang J (2020) MiR399d and epigenetic modification comodulate anthocyanin accumulation in Malus leaves suffering from phosphorus deficiency. Plant Cell Environ 43(5):1148–1159

    Article  CAS  PubMed  Google Scholar 

  91. Chen CY, Schmidt W (2015) The paralogous R3 MYB proteins CAPRICE, TRIPTYCHON and ENHANCER OF TRY AND CPC1 play pleiotropic and partly non-redundant roles in the phosphate starvation response of Arabidopsis roots. J Exp Bot 66(15):4821–4834

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Chen F, Hu Y, Vannozzi A, Wu K, Cai H, Qin Y, Mullis A, Lin Z, Zhang L (2017) The WRKY transcription factor family in model plants and crops. CRC Crit Rev Plant Sci 36(5–6):311–335

    Article  Google Scholar 

  93. Briat JF, Rouached H, Tissot N, Gaymard F, Dubos C (2015) Integration of P, S, Fe, and Zn nutrition signals in Arabidopsis thaliana: potential involvement of PHOSPHATE STARVATION RESPONSE 1 (PHR1). Front Plant Sci 6:290

    Article  PubMed  PubMed Central  Google Scholar 

  94. Bhalla K, Qu X, Kretschmer M, Kronstad JW (2021) The phosphate language of fungi. Trends Microbiol. https://doi.org/10.1016/j.tim.2021.08.002

    Article  PubMed  Google Scholar 

  95. Prathap V, Ali K, Singh A, Vishwakarma C, Krishnan V, Chinnusamy V, Tyagi A (2019) Starch accumulation in rice grains subjected to drought during grain filling stage. Plant Physiol Biochem 142:440–451

    Article  CAS  Google Scholar 

  96. 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. Plant J 41(2):257–268

    Article  CAS  PubMed  Google Scholar 

  97. 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(4):907–918

    Article  CAS  PubMed  Google Scholar 

  98. Ried MK, Wild R, Zhu J, Pipercevic J, Sturm K, Broger L, Harmel RK, Abriata LA, Hothorn LA, Fiedler D, Hiller S (2021) Inositol pyrophosphates promote the interaction of SPX domains with the coiled-coil motif of PHR transcription factors to regulate plant phosphate homeostasis. Nat Commun 12(1):1–3

    Article  CAS  Google Scholar 

  99. Azevedo C, Saiardi A (2017) Eukaryotic phosphate homeostasis: the inositol pyrophosphate perspective. Trends Biochem Sci 42(3):219–231

    Article  CAS  PubMed  Google Scholar 

  100. Chien PS, Chiang CP, Leong SJ, Chiou TJ (2018) Sensing and signaling of phosphate starvation: from local to long distance. Plant Cell Physiol 59(9):1714–1722

    Article  CAS  PubMed  Google Scholar 

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  1. Division of Biochemistry, ICAR-Indian Agricultural Research Institute, New Delhi, India

    V. Prathap, Chirag Maheshwari & Aruna Tyagi

  2. ICAR- Indian Agricultural Statistical Research Institute, New Delhi, India

    Anuj Kumar

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  1. V. Prathap
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  2. Anuj Kumar
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  3. Chirag Maheshwari
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PV wrote the first draft of the review article. Whereas AT and AK have contributed equally to the literature collection, and manuscript documentation. CM and all authors contributed to the revision of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Aruna Tyagi.

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Prathap, V., Kumar, A., Maheshwari, C. et al. Phosphorus homeostasis: acquisition, sensing, and long-distance signaling in plants. Mol Biol Rep 49, 8071–8086 (2022). https://doi.org/10.1007/s11033-022-07354-9

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