Skip to main content

Advertisement

SpringerLink
Log in

An Overview of the Morphological, Genetic and Metabolic Mechanisms Regulating Phosphorus Efficiency Via Root Traits in Soybean

  • Review
  • Published:
Journal of Soil Science and Plant Nutrition Aims and scope Submit manuscript

Abstract

Phosphorus (P) is an essential macronutrient for optimum productivity of several crops including soybean, but it is largely limited in most arable lands. The persistent depletion of phosphate rocks is a major constraint for plant growth and development. Improved P efficiency (PE, uptake and use efficiency) drives an enhanced biological nitrogen fixation in soybean, which could consequently lead to an increased grain and biomass production. Thus, to mitigate P limitation in soybean production, a wide range of genetic approaches have been deployed. These approaches have unravelled the morphological, genetic, phytohormonal and metabolic mechanisms involved in soybean adaptations to P-deficient conditions. Most of the approaches are targeted at root modifications due to the importance of roots in the mediation of early responses to P-deficient conditions. PE among soybean genotypes in P-deficient conditions is mostly dependent on the root plasticity, development of shallow root architecture, symbiosis with arbuscular mycorrhizal fungi and exudation of phosphatases and organic acid anions. Genetic manipulation of soybean has revealed a number of important genes (GmPAPs, GmPTs, GmPLDZ2, GmIPS1 and GmExPB2), transcription factors (C2H2 zinc finger protein, WRKY and MYB) and quantitative trait loci (q14-2 and q19-2) modulating P mobilisation, uptake and utilization under P limiting conditions. Through the modification of root traits, the hormonal (biosynthesis, transport and secretion of ethylene, auxin and jasmonic acid) and metabolic (phenylpropanoid biosynthesis and phenylalanine metabolisms) pathways also modulate PE in soybean. Recent advances in genetic manipulations of root traits offer promising ways for enhancing soybean production, particularly in a P limiting environment.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Data Availability

Not applicable.

References

  • Alori ET, Glick BR, Babalola OO (2017) Microbial phosphorus solubilization and its potential for use in sustainable agriculture. Front Microbiol 8:971. https://doi.org/10.3389/fmicb.2017.00971

    Article  PubMed  PubMed Central  Google Scholar 

  • Anderson G (1980) Assessing organic phosphorus in soils. In: Khasawneh FE, Sample EC, Kamprath EJ (eds) The role of phosphorus in agriculture. American Society of Agronomy, Madison, Wisconsin, USA, pp 411–431

    Google Scholar 

  • Bao A, Chen H, Chen L, Chen S, Hao Q, Guo W, Qiu D, Shan Z, Yang Z, Yuan S, Zhang C, Zhang X, Liu B, Kong F, Li X, Zhou X, Tran LSP, Cao D (2019) CRISPR/Cas9-mediated targeted mutagenesis of GmSPL9 genes alters plant architecture in soybean. BMC Plant Biol 19:131. https://doi.org/10.1186/s12870-019-1746-6

    Article  PubMed  PubMed Central  Google Scholar 

  • Bari R, Pant BD, Stitt M, Scheible WR (2006) PHO2, MicroRNA399, and PHR1 Define a Phosphate-Signaling Pathway in Plants. Plant Physiology 141(3):988–999

  • Bates TR, Lynch JP (2000) The efficiency of Arabidopsis thaliana (Brassicaceae) root hairs in phosphorus acquisition. Am J Bot 87(7):964–970

    Article  CAS  PubMed  Google Scholar 

  • Behera B, Singdevsachan SK, Mishra R, Dutta S, Thatoi H (2014) Diversity, mechanism and biotechnology of phosphate solubilising microorganism in mangrove—a review. Biocatal Agric Biotechnol 3(2):97–110

    Article  Google Scholar 

  • Bengough AG, McKenzie B, Hallett P, Valentine T (2011) Root elongation, water stress, and mechanical impedance: a review of limiting stresses and beneficial root tip traits. J Exp Bot 62:59–68

    Article  CAS  PubMed  Google Scholar 

  • Bilyeu KD, Zeng P, Coello P, Zhang ZJ, Krishnan HB, Bailey A, Beuselinck PR, Polacco JC (2008) Quantitative conversion of phytate to inorganic phosphorus in soybean seeds expressing a bacterial phytase. Plant Physiol 146:468–477. https://doi.org/10.1104/pp.107.113480

  • Blair MW, Sandoval TA, Caldas GV, Beebe SE, Paez MI (2009) Quantitative trait locus analysis of seed phosphorus and seed phytate content in a recombinant inbred line population of common bean. Crop Sci 49:237–246

    Article  CAS  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(4):425–431

    Article  CAS  Google Scholar 

  • Cai XT, Xu P, Zhao PX, Liu R, Yu LH, Xiang CB (2014) Arabidopsis ERF109 mediates cross-talk between jasmonic acid and auxin biosynthesis during lateral root formation. Nat Commun 5:5833. https://doi.org/10.1038/ncomms6833

    Article  CAS  PubMed  Google Scholar 

  • Calderon-Vazquez C, Ibarra-Laclette E, Caballero-Perez J, Herrera-Estrella L (2008) Transcript profiling of Zea mays roots reveals gene responses to phosphate deficiency at the plant- and species-specific levels. J Exp Bot 59(9):2479–2497

    Article  CAS  PubMed  Google Scholar 

  • Ceasar SA (2018) Feeding world population amidst depleting phosphate reserves: the role of biotechnological interventions. Open Biotechnol J 12:51–55. https://doi.org/10.2174/1874070701812010051

  • Chapin LJ, Jones ML (2009) Ethylene regulates phosphorus remobilization and expression of a phosphate transporter (PhPT1) during petunia corolla senescence. J Exp Bot 60:2179–2190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen L, Liao H (2017) Engineering crop nutrient efficiency for sustainable agriculture. J Integr Plant Biol 10:4–29

    Google Scholar 

  • Chen J, Liu Y, Ni J, Wang Y, Bai Y, Shi J, Gan J, Wu Z, Wu P (2011a) OsPHF1 regulates the plasma membrane localization of low- and high-affinity inorganic phosphate transporters and determines inorganic phosphate uptake and translocation in rice. Plant Physiol 157(1):269–278

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen Q, Sun J, Zhai Q, Zhou W, Qi L, Xu L, Wang B, Chen R, Jiang H, Qi J, Li X, Palme K, Li C (2011b) The basic helix-loop-helix transcription factor MYC2 directly represses PLETHORA expression during jasmonate-mediated modulation of the root stem cell niche in Arabidopsis. Plant Cell 23:3335–3352. https://doi.org/10.1105/tpc.111.089870

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen L, Qin L, Zhou L, Li X, Chen Z, Sun L, Wang W, Lin Z, Zhao J, Yamaji N, Ma JF, Gu M, Xu G, Liao HA (2019) Nodule-localized phosphate transporter GmPT7 plays an important role in enhancing symbiotic N2 fixation and yield in soybean. New Phytol 221(4):2013–2025. https://doi.org/10.1111/nph.15541

    Article  CAS  PubMed  Google Scholar 

  • Cheng Y, Dai X, Zhao Y (2006) Auxin biosynthesis by the YUCCA flavin monooxygenases controls the formation of floral organs and vascular tissues in Arabidopsis. Genes Dev 20:1790–1799. https://doi.org/10.1101/gad.1415106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng F, Tu P, Yan X, Wang X, Liao H (2010) Phosphorus nutrition characters for new soybean germplasms with high phosphorus efficiency in acid red soils. Plant Nutr Fertil Sci 16(1):71–81

    CAS  Google Scholar 

  • Chiera JM, Finer JJ, Grabau EA (2004) Ectopic expression of a soybean phytase in developing seeds of Glycine max to improve phosphorus availability. Plant Mol Biol 56:895–904. https://doi.org/10.1007/s11103-004-5293-6

    Article  CAS  PubMed  Google Scholar 

  • Clemens C, van de Wiel M, van der Linden CG, Scholten OE (2016) Improving phosphorus use efficiency in agriculture: opportunities for breeding. Euphytica 207:1–22. https://doi.org/10.1007/s10681-015-1572-3

    Article  Google Scholar 

  • Curtin SJ, Zhang F, Sander JD, Haun WJ, Starker C, Baltes NJ, Reyon D, Dahlborg EJ, Goodwin MJ, Coffman AP, Dobbs D, Joung JK, Voytas DF, Stupar RM (2011) Targeted mutagenesis of duplicated genes in soybean with zinc-finger nucleases. Plant Physiol 156(2):466–473. https://doi.org/10.1104/pp.111.172981

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dash S, Campbell JD, Cannon EK et al (2015) Legume information system (LegumeInfo.org): a key component of a set of federated data resources for the legume family. Nucleic Acids Res 44:D1181–D1188

    Article  PubMed  PubMed Central  Google Scholar 

  • Deng Y, Teng W, Tong Y-P, Chen X-P, Zou C-Q (2018) Phosphorus efficiency mechanisms of two wheat cultivars as affected by a range of phosphorus levels in the field. Front Plant Sci 9:1614. https://doi.org/10.3389/fpls.2018.01614

    Article  PubMed  PubMed Central  Google Scholar 

  • Duan K, Yi K, Dang L, Huang H, Wu W, Wu P (2008) Characterization of a sub-family of Arabidopsis genes with the SPX domain reveals their diverse functions in plant tolerance to phosphorus starvation. Plant J 54(6):965–975

    Article  CAS  PubMed  Google Scholar 

  • Ezawa T, Hayatsu M, Saito M (2005) A new hypothesis on the strategy for acquisition of phosphorus in arbuscular mycorrhiza: up-regulation of secreted acid phosphatase gene in the host plant. Mol Plant-Microbe Interact 18:1046–1053

    Article  CAS  PubMed  Google Scholar 

  • Falk KG, Jubery TZ, O’Rourke JA, Singh A, Sarkar S, Ganapathysubramanian B, Singh AK (2020, 2020) Soybean root system architecture trait study through genotypic, phenotypic, and shape-based clusters. Plant Phenomics:1925495. https://doi.org/10.34133/2020/1925495

  • Fan C, Wang X, Hu R, Wang Y, Xiao C, Jiang Y, Zhang X, Zheng C, Fu YF (2013) The pattern of phosphate transporter 1 genes evolutionary divergence in Glycine max L. BMC Plant Biol 13:48

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Föhse D, Claassen N, Jungk A (1988) Phosphorus efficiency of plants. Plant Soil 110:101–109. https://doi.org/10.1007/BF02143545

    Article  Google Scholar 

  • Fredeen AL, Rao IM, Terry N (1989) Influence of phosphorus nutrition on growth and carbon partitioning in Glycine max. Plant Physiol 89(1):225–230

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fu X, Harberd NP (2003) Auxin promotes Arabidopsis root growth by modulating gibberellin response. Nature 421:740–743. https://doi.org/10.1038/nature01387

    Article  CAS  PubMed  Google Scholar 

  • Fu S, Sun J, Qian L, Li Z (2008) Bacillus phytases: present scenario and future perspectives. Appl Biochem Biotechnol 151:1–8. https://doi.org/10.1007/s12010008-8158-7

    Article  CAS  PubMed  Google Scholar 

  • Gahoonia TS, Nielsen NE (1997) Variation in root hairs of barley cultivars doubled soil phosphorus uptake. Euphytica 98(3):177–182

    Article  Google Scholar 

  • Gahoonia TS, Nielsen NE (2004) Root traits as tools for creating phosphorus efficient crop varieties. Plant Soil 260(1–2):47–57

    Article  Google Scholar 

  • Gao B, Cao C, Li T (2012) Effect of ethylene on the morphology and physiological characteristic of soybean seedlings under phosphate deficiency. Soybean Sci 31(1):58–63

    CAS  Google Scholar 

  • George TS, Richardson AE, Hadobas PA, Simpson RJ (2004) Characterization of transgenic Trifolium subterraneum L. which expresses phyA and releases extracellular phytase: growth and P nutrition in laboratory media and soil. Plant Cell Environ 27:1351–1361

    Article  CAS  Google Scholar 

  • George TS, Gregory PJ, Hocking P, Richardson AE (2008) Variation in root-associated phosphatase activities in wheat contributes to the utilization of organic P substrates in vitro, but does not explain differences in the P-nutrition of plants when grown in soils. Environ Exp Bot 64:239–249. https://doi.org/10.1016/j.envexpbot.2008.05.002

    Article  CAS  Google Scholar 

  • Gontia I, Tantwai K, Rajput LPS, Tiwari S (2012) Transgenic plants expressing phytase gene of microbial origin and their prospective application as feed. Food Technol Biotechnol 50:3–10

    CAS  Google Scholar 

  • Graham PH, Vance CP (2003) Legumes: importance and constraints to greater use. Plant Physiol 131(3):872–877. https://doi.org/10.1104/pp.017004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grant D, Nelson RT, Cannon SB, Shoemaker RC (2010) SoyBase, the USDA-ARS soybean genetics and genomics database. Nucleic Acids Res 38:D843–D846

    Article  CAS  PubMed  Google Scholar 

  • Guo W (2008) Cloning and functional analysis of expansin gene GmEXPB2 in soybean. PhD thesis, South China Agricultural University, Guangzhou

  • Guo W, Zhao J, Li X, Qin L, Yan X, Liao H (2011) A soybean β-expansin gene GmEXPB2 intrinsically involved in root system architecture responses to abiotic stresses. Plant J 66(3):541–552. https://doi.org/10.1111/j.1365-313X.2011.04511.x

    Article  CAS  PubMed  Google Scholar 

  • Hacisalihoglu G, Burton AL, Gustin JL, Eker S, Asikli S, Heybet EH, Ozturk L, Cakmak I, Yazici A, Burkey KO, Orf J, Settles AM (2018) Quantitative trait loci associated with soybean seed weight and composition under different phosphorus levels. J Integr Plant Biol 60:232–241. https://doi.org/10.1111/jipb.12612

    Article  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(4):889–902

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Han F, Zhu B (2011) Evolutionary analysis of three gibberellin oxidase genes in rice, Arabidopsis, and soybean. Gene 473(1):23–35

    Article  CAS  PubMed  Google Scholar 

  • Hanlon MT, Ray S, Saengwilai P, Luthe D, Lynch JP, Brown KM (2018) Buffered delivery of phosphate to Arabidopsis alters responses to low phosphate. J Exp Bot 69(5):1207–1219. https://doi.org/10.1093/jxb/erx454

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hartman GL, West ED, Herman TK (2011) Crops that feed the world 2. Soybean—worldwide production, use, and constraints caused by pathogens and pests. Food Sec 3:5–17

    Article  Google Scholar 

  • Havlin J (1999) Soil fertility and fertilizers: an introduction to nutrient management, 6th edn. Prentice Hall, Upper Saddle River, N.J

    Google Scholar 

  • Hellal FA, Abdelhamid MT (2013) Nutrient management practices for enhancing soybean (Glycine max L.) production. Acta Biol Colomb 18(2):239–250

    Google Scholar 

  • Hernandez G, Ramirez M, Valdes-López O, Tesfaye M, Graham MA, Czechowski T, Schlereth A, Wandrey M, Erban A, Cheung F et al (2007) Phosphorus stress in common bean: root transcript and metabolic responses. Plant Physiol 144:752–767

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hocking PJ (2001) Organic acid exuded from roots in phosphorus uptake and aluminium tolerance of plants in acid soils. Adv Agron 74:63–97

    Article  CAS  Google Scholar 

  • Huang TK, Han CL, Lin SI, Chen YJ, Tsai YC, Chen YR, Chen JW, Lin WY, Chen PM, Liu TY, Chen YS, Sun CM, Chiou TJ (2013) Identification of downstream components of ubiquitin-conjugating enzyme PHOSPHATE2 by quantitative membrane proteomics in Arabidopsis roots. Plant Cell 25(10):4044–4060

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Inoue Y, Kobae Y, Omoto E, Tanaka A, Banba M, Takai S, Tamura Y, Hirose A, Komatsu K, Otagaki S, Matsumoto S, Taniguchi M, Masuta C, Ishimoto M, Hata S (2014) The soybean mycorrhiza-inducible phosphate transporter gene, GmPT7, also shows localized expression at the tips of vein endings of senescent leaves. Plant Cell Physiol 55(12):2102–2111. https://doi.org/10.1093/pcp/pcu138

    Article  CAS  PubMed  Google Scholar 

  • Jain A, Vasconcelos MJ, Raghothama K, Sahi SV (2007) Molecular mechanisms of plant adaptation to phosphate deficiency. Plant Breed Rev 29:359–419. https://doi.org/10.1002/9780470168035.ch7

  • Joshi T, Patil K, Fitzpatrick MR, Franklin LD, Yao Q, Cook JR, Wang Z, Libault M, Brechenmacher L, Valliyodan B, Wu X, Cheng J, Stacey G, Nguyen HT, Xu D (2012) Soybean Knowledge Base (SoyKB): a web resource for soybean translational genomics. BMC Genomics 13:S15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jung JKH, McCouch S (2013) Getting to the roots of it: genetic and hormonal control of root architecture. Front Plant Sci 4:186. https://doi.org/10.3389/fpls.2013.00186

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kartal G, Temel A, Arican E, Gozukirmizi N (2009) Effects of brassinosteroids on barley root growth, antioxidant system and cell division. Plant Growth Regul 58:261–267. https://doi.org/10.1007/s10725-009-9374-z

    Article  CAS  Google Scholar 

  • Kereszt A, Li D, Indrasumunar A, Nguyen CDT, Nontachaiyapoom S, Kinkema M, Gresshoff PM (2007) Agrobacterium rhizogenes-mediated transformation of soybean to study root biology. Nat Protoc 2:948–952

    Article  CAS  PubMed  Google Scholar 

  • Keyes SD, Daly KR, Gostling NJ, Jones DL, Talboys P, Pinzer BR, Boardman R, Sinclair I, Marchant A, Roose T (2013) High resolution synchrotron imaging of wheat root hairs growing in soil and image based modelling of phosphate uptake. New Phytol 198:1023–1029

    Article  CAS  PubMed  Google Scholar 

  • Khademi Z, Jones DL, Malakouti MJ, Asadi F (2010) Organic acids differ in enhancing phosphorus uptake by Triticum aestivum L.- effects of rhizosphere concentration and counterion. Plant Soil 334:151–159

    Article  CAS  Google Scholar 

  • Kumawat G, Gupta S, Ratnaparkhe MB, Maranna S, Satpute GK (2016) QTLomics in soybean: a way forward for translational genomics and breeding. Front Plant Sci 7:1852. https://doi.org/10.3389/fpls.2016.01852

    Article  PubMed  PubMed Central  Google Scholar 

  • Lapis-Gaza HR, Jost R, Finnegan PM (2014) Arabidopsis PHOSPHATE TRANSPORTER1 genes PHT1;8 and PHT1;9 are involved in root-to-shoot translocation of orthophosphate. BMC Plant Biol 14:334

    Article  PubMed  PubMed Central  Google Scholar 

  • Laplaze L, Benkova E, Casimiro I, Maes L, Vanneste S, Swarup R, Weijers D, Calvo V, Parizot B, Herrera-Rodriguez MB, Offringa R, Graham N, Doumas P, Friml J, Bogusz D, Beeckman T, Bennett M (2007) Cytokinins act directly on lateral root founder cells to inhibit root initiation. Plant Cell 19:3889–3900. https://doi.org/10.1105/tpc.107.055863

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lavenus J, Goh T, Roberts I, Guyomarc’h S, Lucas M, de Smet I, Fukaki H, Beeckman T, Bennett M, Laplaze L (2013) Lateral root development in Arabidopsis: fifty shades of auxin. Trends Plant Sci 18(8):450–458. https://doi.org/10.1016/j.tplants.2013.04.006

    Article  CAS  PubMed  Google Scholar 

  • Li G, Yang S, Li M, Qiao Y, Wang J (2009) Functional analysis of an Aspergillus ficuum phytase gene in Saccharomyces cerevisiae and its root specific, secretory expression in transgenic soybean plants. Biotechnol Lett 31:1297–1303. https://doi.org/10.1007/s10529-009-9992-6

    Article  CAS  PubMed  Google Scholar 

  • Li C, Gui S, Yang T, Walk T, Wang X, Liao H (2012) Identification of soybean purple acid phosphatase genes and their expression responses to phosphorus availability and symbiosis. Ann Bot 109:275–285. https://doi.org/10.1093/aob/mcr246

    Article  CAS  PubMed  Google Scholar 

  • Li H, Yang Y, Zhang H et al (2016) A genetic relationship between phosphorus efficiency and photosynthetic traits in soybean as revealed by QTL analysis using a high-density genetic map. Front Plant Sci 7:924. https://doi.org/10.3389/fpls.2016.00924

    Article  PubMed  PubMed Central  Google Scholar 

  • Li L, Wei S, Shen W (2020) The role of methane in plant physiology: a review. Plant Cell Rep 39:171–179. https://doi.org/10.1007/s00299-019-02478-y

    Article  CAS  PubMed  Google Scholar 

  • Liang QA, Cheng XH, Mei MT, Yan XL, Liao H (2010) QTL analysis of root traits as related to phosphorus efficiency in soybean. Ann Bot 106(1):223–234

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liao H, Wan H, Shaff J, Wang X, Yan X, Kochian LV (2006) Phosphorus and aluminum interactions in soybean in relation to aluminum tolerance. Exudation of specific organic acids from different regions of the intact root system. Plant Physiol 141(2):674–684. https://doi.org/10.1104/pp.105.076497

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu J, Zhou M (2018) The ALMT gene family performs multiple functions in plants. Agronomy 8:20. https://doi.org/10.3390/agronomy8020020

    Article  CAS  Google Scholar 

  • Liu L, Liao H, Wang XR, Yan XL (2008) Regulation effect of soil P availability on mycorrhizal infection in relation to root architecture and P efficiency of Glycine max. Chin J Appl Ecol 19(3):564–568

    CAS  Google Scholar 

  • Liu JF, Zhao CY, Ma J, Zhang GY, Li MG, Yan GJ, Wang XF, Ma ZY (2011) Agrobacterium-mediated transformation of cotton (Gossypium hirsutum L.) with a fungal phytase gene improves phosphorus acquisition. Euphytica 181:31–40

    Article  CAS  Google Scholar 

  • Liu N, Li M, Hu X, Ma Q, Mu Y, Tan Z, Xia Q, Zhang G, Nian H (2017) Construction of high-density genetic map and QTL mapping of yield-related and two quality traits in soybean RILs population by RAD-sequencing. BMC Genomics 18(466):1–13. https://doi.org/10.1186/s12864-017-3854-8

    Article  CAS  Google Scholar 

  • López-Arredondo DL, Leyva-Gonzalez MA, Gonzalez-Morales SI, López-Bucio J, Herrera-Estrella L (2014) Phosphate nutrition: improving low-phosphate tolerance in crops. Annu Rev Plant Biol 65:95–123. https://doi.org/10.1146/annurev-arplant-050213-035949

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Lynch JP (2019) Root phenotypes for improved nutrient capture: an underexploited opportunity for global agriculture. New Phytol 223:548–564. https://doi.org/10.1111/nph.15738

    Article  PubMed  Google Scholar 

  • Lynch JP, Ho MD (2005) Rhizoeconomics: carbon costs of phosphorus acquisition. Plant Soil 269(1–2):45–56

    Article  CAS  Google Scholar 

  • Ma Z, Baskin TI, Brown KM, Lynch JP (2003) Regulation of root elongation under phosphorus stress involves changes in ethylene responsiveness. Plant Physiol 131(3):1381–1390

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marschner H, Romheld V, Horst WJ, Martin P (1986) Root induced changes in the rhizosphere: importance for mineral nutrition of plants. Z Pflanzenernachr Bodenkd 149:441–456

    Article  CAS  Google Scholar 

  • Maruyama H, Yamamura T, Kaneko Y, Matsui H, Watanabe T, Shinano T, Osaki M, Wasaki J (2012) Effect of exogenous phosphatase and phytase activities on organic phosphate mobilization in soils with different phosphate adsorption capacities. Soil Sci Plant Nutr 58(1):41–51. https://doi.org/10.1080/00380768.2012.656298

    Article  CAS  Google Scholar 

  • Mederski HJ (1953) Relation of varying phosphorus supply to dry matter production, and to N and P partition during the development of the soybean plant. Ohio State University, Abstracts of Doctoral Dissertations. Vol. 64

  • Messiga AJ, Ziadi N, Morel C, Grant C, Tremblay G, Lamarre G, Parent LE (2012) Long term impact of tillage practices and biennial P and N fertilization on maize and soybean yields and soil P status. Field Crop Res 133:10–22. https://doi.org/10.1016/j.fcr.2012.03.009

    Article  Google Scholar 

  • Misson J, Raghothama KG, Jain A, Jouhet J, Block MA, Bligny R, Ortet P, Creff A, Somerville S, Rolland N, Doumas P, Nacry P, Herrerra-Estrella L, Nussaume L, Thibaud MC (2005) A genome-wide transcriptional analysis using Arabidopsis thaliana Affymetrix gene chips determined plant responses to phosphate deprivation. Proc Natl Acad Sci U S A 102(33):11934–11939

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morcuende R, Bari R, Gibon Y, Zheng W, Pant BD, Blasing O, Usadel B, Czechowski T, Udvardi MK, Stitt M et al (2007) Genome-wide reprogramming of metabolism and regulatory networks of Arabidopsis in response to phosphorus. Plant Cell Environ 30(1):85–112

    Article  CAS  PubMed  Google Scholar 

  • Motte H, Vanneste S, Beeckman T (2019) Molecular and environmental regulation of root development. Annu Rev Plant Biol 70:465–488. https://doi.org/10.1146/annurev-arplant-050718-100423

    Article  CAS  PubMed  Google Scholar 

  • Nagatoshi Y, Fujita Y (2019) Accelerating soybean breeding in a CO2-supplemented growth chamber. Plant Cell Physiol 60(1):77–84. https://doi.org/10.1093/pcp/pcy189

    Article  CAS  PubMed  Google Scholar 

  • Narayanan A, Reddy BK (1982) Effect of phosphorus deficiency on the form of plant root system. In: Scaife A (ed) Plant nutrition, vol 2. Slough, UK, Commonwealth Agricultural Bureau, pp 412–417

    Google Scholar 

  • Navea IP, Dwiyanti MS, Park J, Kim B, Lee S, Huang X, Koh HJ, Chin JH (2017) Identification of quantitative trait loci for panicle length and yield related traits under different water and P application conditions in tropical region in rice (Oryza sativa, L.). Euphytica 213:37. https://doi.org/10.1007/s10681-016-1822-z

    Article  Google Scholar 

  • Neumann G, Massonneau A, Martinola E, Römheld V (1999) Physiological adaptation to phosphorus deficiency during proteoid root development in white lupin. Planta 208:373–382

    Article  CAS  Google Scholar 

  • Ning L, Kan G, Du W, Guo S, Wang Q, Zhang G, Cheng H, Yu D (2016) Association analysis for detecting significant single nucleotide polymorphisms for phosphorus-deficiency tolerance at the seedling stage in soybean (Glycine max (L.) Merr.). Breed Sci 66(2):191–203. https://doi.org/10.1270/jsbbs.66.191

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nishant BA, Singh MN, Srivastava K et al (2016) Molecular mapping and breeding of physiological traits. Adv Plants Agric Res 3(6):193–206. https://doi.org/10.15406/apar.2016.03.00120

    Article  Google Scholar 

  • Niu YF, Chai RS, Jin GL, Wang H, Tang CX, Zhang YS (2013) Responses of root architecture development to low phosphorus availability: a review. Ann Bot 112(2):391–408. https://doi.org/10.1093/aob/mcs285

    Article  CAS  PubMed  Google Scholar 

  • O’Rourke JA, McCabe CE, Graham MA (2019) Dynamic gene expression changes in response to micronutrient, macronutrient, and multiple stress exposures in soybean. Funct Integr Genomics 20:321–341. https://doi.org/10.1007/s10142-019-00709-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Penn CJ, Camberato JJ (2019) A critical review on soil chemical processes that control how soil pH affects phosphorus availability to plants. Agriculture 9(6):120. https://doi.org/10.3390/agriculture9060120

    Article  Google Scholar 

  • Pérez-Torres C-A, 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 20:3258–3272

    Article  PubMed  PubMed Central  Google Scholar 

  • Petricka JJ, Winter CM, Benfey PN (2012) Control of Arabidopsis root development. Annu Rev Plant Biol 63:563–590. https://doi.org/10.1146/annurev-arplant-042811-105501

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Plaxton WC, Tran HT (2011) Metabolic adaptations of phosphate-starved plants. Plant Physiol 156(3):1006–1015. https://doi.org/10.1104/pp.111.175281

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Poirier Y, Jung JY (2015) “Phosphate transporters,” In: Plaxton WC, Lambers H (eds) Annual plant reviews: phosphorus metabolism in plants, Vol 48 (Hoboken, NJ: John Wiley & Sons, Ltd.), 125–158. https://doi.org/10.1002/9781118958841.ch5

  • Postma JA, Lynch JP (2011) Root cortical aerenchyma enhances the growth of maize on soils with suboptimal availability of nitrogen, phosphorus, and potassium. Plant Physiol 156:1190–1201

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Prince SJ, Murphy M, Mutava RN et al (2015) Evaluation of high yielding soybean germplasm under water limitation. J Integr Plant Biol 58:475–491

    Article  PubMed  Google Scholar 

  • Prince SJ, Murphy M, Mutava RN, Durnell LA, Valliyodan B, Shannon JG, Nguyen HT (2017) Root xylem plasticity to improve water use and yield in water-stressed soybean. J Exp Bot 68(8): 2027–2036. https://doi.org/10.1093/jxb/erw472

  • Prince SJ, Valliyodan B, Ye H, Yang M, Tai S, Hu W, Murphy M, Durnell LA, Song L, Joshi T, Liu Y, van de Velde J, Vandepoele K, Grover Shannon J, Nguyen HT (2018) Understanding genetic control of root system architecture in soybean: insights into the genetic basis of lateral root number. Plant Cell Environ 42:212–229. https://doi.org/10.1111/pce.13333

    Article  CAS  PubMed  Google Scholar 

  • Qin L, Zhao J, Tian J, Chen L, Sun Z, Guo Y, Lu X, Gu M, Xu G, Liao H (2012) The high-affinity phosphate transporter GmPT5 regulates phosphate transport to nodules and nodulation in soybean. Plant Physiol 159(4):1634–1643. https://doi.org/10.1104/pp.112.199786

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raghothama KG, Karthikeyan AS (2005) Phosphate acquisition. Plant Soil 274(1–2):37–49

    Article  CAS  Google Scholar 

  • Ramaekers L, Remans R, Rao IM, Blair MW, Vanderleyden J (2010) Strategies for improving phosphorus acquisition efficiency of crop plants. Field Crop Res 117:169–176

    Article  Google Scholar 

  • Ramesh A, Sharma SK, Joshi OP, Khan IR (2011) Phytase, phosphatase activity and p-nutrition of soybean as influenced by inoculation of Bacillus. Indian J Microbiol 51(1):94–99. https://doi.org/10.1007/s12088-011-0104-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reddy CS, Kim S-C, Kaul T (2017) Genetically modified phytase crops role in sustainable plant and animal nutrition and ecological development: a review. 3 Biotech 7(3):195

    Article  PubMed  PubMed Central  Google Scholar 

  • Richardson AE, Simpson RJ (2011) Soil microorganisms mediating phosphorus availability update on microbial phosphorus. Plant Physiol 156:989–996. https://doi.org/10.1104/pp.111.175448

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Richardson AE, Hadobas PA, Hayes JE (2001) Extracellular secretion of Aspergillus phytase from Arabidopsis roots enables plants to obtain phosphorus from phytate. Plant J 25:641–649. https://doi.org/10.1046/j.1365-313x.2001.00998.x

    Article  CAS  PubMed  Google Scholar 

  • Richardson AE, George TS, Hens M, Simpson RJ (2005) Utilization of soil organic phosphorus by higher plants. In: Turner BL, Frossard E, Baldwin DS (eds) Organic phosphorus in the environment. CAB International, Wallingford, pp 165–184

    Chapter  Google Scholar 

  • Richardson AE, Lynch JP, Ryan PR, Delhaize E, Smith FA, Smith SE, Harvey PR, Ryan MH, Veneklaas EJ, Lambers H, Oberson A, Culvenor RA, Simpson RJ (2011) Plant and microbial strategies to improve the phosphorus efficiency of agriculture. Plant Soil 349:121–156. https://doi.org/10.1007/s11104-011-0950-4

    Article  CAS  Google Scholar 

  • Rose TJ, Rengel Z, Ma Q, Bowden JW (2008) Post-flowering supply of P, but not K, is required for maximum canola seed yields. Eur J Agron 28:371–379. https://doi.org/10.1016/j.eja.2007.11.003

    Article  CAS  Google Scholar 

  • Rubio V, Linhares F, Solano R, Martin AC, Iglesias J, Leyva A, Paz-Ares J (2001) A conserved MYB transcription factor involved in phosphate starvation signalling both in vascular plants and in unicellular algae. Genes Dev 15(16):2122–2133

  • Rugova A, Puschenreiter M, Santner J, Fischer L, Neubauer S, Koellensperger G, Hann S (2014) Speciation analysis of orthophosphate and myo-inositolhexakisphosphate in soil and plant-related samples by high performance ion chromatography combined with inductively coupled plasma mass spectrometry. J Sep Sci 37:1711–1719. https://doi.org/10.1002/jssc.201400026

  • Ruiz S, Koebernick N, Duncan S, Fletcher DMK, Scotson C, Boghi A, Marin M, Bengough AG, George TS, Brown LK, Hallett PD, Roose T (2020) Significance of root hairs at the field scale – modelling root water and phosphorus uptake under different field conditions. Plant Soil 447:281–304. https://doi.org/10.1007/s11104-019-04308-2

    Article  CAS  PubMed  Google Scholar 

  • Růžička K, Ljung K, Vanneste S, Podhorská R, Beeckman T, Frim J, Benková E (2007) Ethylene regulates root growth through effects on auxin biosynthesis and transport-dependent auxin distribution. Plant Cell 19:2197–2212. https://doi.org/10.1105/tpc.107.052126

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sánchez-Calderón L, López-Bucio J, Chacón-López A, Gutiérrez-Ortega A, Hernández-Abreu E, Herrera-Estrella L (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. Plant Physiol 140(3):879–889. https://doi.org/10.1104/pp.105.073825

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schachtman DP, Reid RJ, Ayling SM (1998) Phosphorus uptake by plants: from soil to cell. Plant Physiol 116(2):447–453

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schmutz J, Cannon SB, Schlueter J et al (2010) Genome sequence of the palaeopolyploid soybean. Nature 14 463(7278):178–183. https://doi.org/10.1038/nature08670

    Article  CAS  PubMed  Google Scholar 

  • Secco D, Bouain N, Rouached A, Prom-u-thai C, Hanin M, Pandey AK, Rouached H (2017) Phosphate, phytate and phytases in plants: from fundamental knowledge gained in Arabidopsis to potential biotechnological applications in wheat. Crit Rev Biotechnol 37:898–910. https://doi.org/10.1080/07388551.2016.1268089

    Article  CAS  PubMed  Google Scholar 

  • Severin AJ, Woody JL, Bolon YT, Joseph B, Diers BW, Farmer AD, Muehlbauer GJ, Nelson RT, Grant D, Specht JE, Graham MA, Cannon SB, May GD, Vance CP, Shoemaker RC (2010) RNA-Seq Atlas of Glycine max: a guide to the soybean transcriptome. BMC Plant Biol 10:160

    Article  PubMed  PubMed Central  Google Scholar 

  • Smith SE (2002) Soil microbes and plants – raising interest, mutual gains. New Phytol 156:142–144

    Article  PubMed  Google Scholar 

  • Smith SE, Read DJ (2010) Mycorrhizal symbiosis. Academic Press, Cambridge, MA

    Google Scholar 

  • Smith SE, Smith FA (2011) Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annu Rev Plant Biol 62:227–250. https://doi.org/10.1146/annurev-arplant-042110-103846

    Article  CAS  PubMed  Google Scholar 

  • Song H, Yin Z, Chao M, Ning L, Zhang D, Yu D (2014) Functional properties and expression quantitative trait loci for phosphate transporter GmPT1 in soybean. Plant Cell Environ 37(2):462–472

    Article  CAS  PubMed  Google Scholar 

  • Stefanovic A, Arpat AB, Bligny R, Gout E, Vidoudez C, Bensimon M, Poirier Y (2011) Over-expression of PHO1 in Arabidopsis leaves reveals its role in mediating phosphate efflux. Plant J 66(4):689–699

    Article  CAS  PubMed  Google Scholar 

  • Stein LD, Mungall C, Shu S, Caudy M, Mangone M, Day A, Nickerson E, Stajich JE, Harris TW, Arva A, Lewis S (2002) The generic genome browser: a building block for a model organism system database. Genome Res 12:1599–1610

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Strock CF, Morrow de la Riva L, Lynch J (2018) Reduction in root secondary growth as a strategy for phosphorus acquisition. Plant Physiol 176:691–703

    Article  CAS  PubMed  Google Scholar 

  • Subramanian S, Graham MY, Yu O, Graham TL (2005) RNA interference of soybean isoflavone synthase genes leads to silencing in tissues distal to the transformation site and to enhanced susceptibility to Phytophthora sojae. Plant Physiol 137:1345–1353

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Syers J, Johnston A, Curtin D (2008) Efficiency of soil and fertilizer phosphorus use. FAO fertilizer and plant nutrition bulletin, Rome

    Google Scholar 

  • Taliman NA, Dong Q, Echigo K, Raboy V, Saneoka H (2019) Effect of phosphorus fertilization on the growth, photosynthesis, nitrogen fixation, mineral accumulation, seed yield, and seed quality of a soybean low-phytate line. Plants 8(5):119. https://doi.org/10.3390/plants8050119

    Article  CAS  PubMed Central  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 Physiol 170:1243–1250. https://doi.org/10.1016/j.jplph.2013.04.015

    Article  CAS  PubMed  Google Scholar 

  • Tarafdar JC (1989) Use of electrofocussing technique for characterizing the phosphatases in the soil and root exudates. J Indian Soc Soil Sci 37:393–395

    CAS  Google Scholar 

  • Tawaraya K, Horie R, Saito S, Wagatsuma T, Saito K, Oikawa A (2014) Metabolite profiling of root exudates of common bean under phosphorus deficiency. Metabolites 4:599–611. https://doi.org/10.3390/metabo4030599

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tian J, Wang X, Tong Y, Chen X, Liao H (2012) Bioengineering and management for efficient phosphorus utilization in crops and pastures. Curr Opin Biotechnol 23(6):866–871. https://doi.org/10.1016/j.copbio.2012.03.002

    Article  CAS  PubMed  Google Scholar 

  • Ticconi CA, Lucero RD, Sakhonwasee S, Adamson AW, Creff A, Nussaume L, Desnos T, Abel S (2009) ER-resident proteins PDR2 and LPR1 mediate the developmental response of root meristems to phosphate availability. Proc Natl Acad Sci U S A 106(33):14174–14179

    Article  CAS  PubMed  PubMed Central  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

    Article  CAS  Google Scholar 

  • Umezawa T, Sakurai T, Totoki Y, Toyoda A, Seki M, Ishiwata A, Akiyama K, Kurotani A, Yoshida T, Mochida K, Kasuga M, Todaka D, Maruyama K, Nakashima K, Enju A, Mizukado S, Ahmed S, Yoshiwara K, Harada K, Tsubokura Y, Hayashi M, Sato S, Anai T, Ishimoto M, Funatsuki H, Teraishi M, Osaki M, Shinano T, Akashi R, Sakaki Y, Yamaguchi-Shinozaki K, Shinozaki K (2008) Sequencing and analysis of approximately 40000 soybean cDNA clones from a full-length-enriched cDNA library. DNA Res 15:333–346

  • USDA, United States Department of Agriculture (2021) World agricultural production. USDA Foreign Agricultural Service, Circular Series WAP 1-21, p. 31.https://apps.fas.usda.gov/psdonline/circulars/production.pdf

  • Valeeva LR, Nyamsuren C, Sharipova MR, Shakirov EV (2018) Heterologous expression of secreted bacterial BPP and HAP phytases in plants stimulates Arabidopsis thaliana growth on phytate. Front Plant Sci 9:186. https://doi.org/10.3389/fpls.2018.00186

  • Vance CP (2001) Symbiotic nitrogen fixation and phosphorus acquisition. Plant nutrition in a world of declining renewable resources. Plant Physiol 127(2):390–397. https://doi.org/10.1104/pp.010331

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vance CP, Uhde-Stone C, Allan DL (2003) Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. New Phytol 157(3):423–447

    Article  CAS  PubMed  Google Scholar 

  • Veneklaas EJ, Lambers H, Bragg J, Finnegan PM, Lovelock CE, Plaxton WC, Price CA, Scheible WR, Shane MW, White PJ, Raven JA (2012) Opportunities for improving phosphorus-use efficiency in crop plants. New Phytol 195:306–320. https://doi.org/10.1111/j.1469-8137.2012.04190.x

    Article  CAS  PubMed  Google Scholar 

  • Wacker-Fester K, Uptmoor R, Pfahler V, Dehmer KJ, Bachmann-Pfabe S, Kavka M (2019) Genotype-specific differences in phosphorus efficiency of potato (Solanum tuberosum L.). Front Plant Sci 10:1029. https://doi.org/10.3389/fpls.2019.01029

  • Wang L, Liao H, Yan X, Zhuang B, Dong Y (2004) Genetic variability for root hair traits as related to phosphorus status in soybean. Plant Soil 261(2004):77–84. https://doi.org/10.1023/B:PLSO.10000035552.94249.6a

  • Wang X, Wang Y, Tian J, Lim BL, Yan X, Liao H (2009) Overexpressing AtPAP15 enhances phosphorus efficiency in soybean. Plant Physiol 151(1):233–240. https://doi.org/10.1104/pp.109.138891

    Article  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(1):215–222

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang X, Pan Q, Chen F, Yan X, Liao H (2011) Effects of co-inoculation with arbuscular mycorrhizal fungi and rhizobia on soybean growth as related to root architecture and availability of N and P. Mycorrhiza 21:173–181. https://doi.org/10.1007/s00572-010-0319-1

  • Wang W, Ding G, White PJ, Wang X, Jin K, Xu F, Shi L (2019) Mapping and cloning of quantitative trait loci for phosphorus efficiency in crops: opportunities and challenges. Plant Soil 439:91–112. https://doi.org/10.1007/s11104-018-3706-6

  • Wang Q, Wang J, Yang Y, Du W, Zhang D, Yu D, Cheng H (2016a) A genome-wide expression profile analysis reveals active genes and pathways coping with phosphate starvation in soybean. BMC Genomics 17:192. https://doi.org/10.1186/s12864-016-2558-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang X, Zhao S, Bücking H (2016b) Arbuscular mycorrhizal growth responses are fungal specific but do not differ between soybean genotypes with different phosphate efficiency. Ann Bot 118(1):11–21. https://doi.org/10.1093/aob/mcw074

  • Wasaki J, Yonetani R, Kuroda S et al (2003) Transcriptomic analysis of metabolic changes by phosphorus stress in rice plant roots. Plant Cell Environ 26(9):1515–1523

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu J, Ma F, Lin H, Liu L, Zhong P, Lin W, Dong D, Wang J, Liu D (2010) Assimilate accumulation, photosynthetic characteristics and yield of soybean genotypes with different phosphorus efficiency. Soybean Sci 29(2):247–250

    Google Scholar 

  • Xu W, Zhang Q, Yuan W, Xu F, Muhammad Aslam M, Miao R, Li Y, Wang Q, Li X, Zhang X, Zhang K, Xia T, Cheng F (2020a) The genome evolution and low-phosphorus adaptation in white lupin. Nat Commun 11:1069. https://doi.org/10.1038/s41467-020-14891-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu P, Zhao P-X, Cai X-T, Mao J-L, Miao Z-Q, Xiang C-B (2020b) Integration of Jasmonic acid and ethylene into auxin signalling in root development. Front Plant Sci 11:271. https://doi.org/10.3389/fpls.2020.00271

    Article  PubMed  PubMed Central  Google Scholar 

  • Yamada T, Takagi K, Ishimoto M (2012) Recent advances in soybean transformation and their application to molecular breeding and genomic analysis. Breed Sci 61(5):480–494. 10.1270 /jsbbs.61.480

  • Yang SM, Tang F, Gao MQ, Krishnan HB, Zhu HY (2010) R gene-controlled host specificity in the legume-rhizobia symbiosis. Proc Natl Acad Sci U S A 107:18735–18740

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang Y, Zhao Q, Li X, Liu D, Qi W, Zhang M, Yang C, Liao H (2017) Characterization of genetic basis on synergistic interactions between root architecture and biological nitrogen fixation in soybean. Front Plant Sci 8:1466

    Article  PubMed  PubMed Central  Google Scholar 

  • Yang Y, Tong Y, Li X, He Y, Xu R, Liu D, Yang D, Lv H, Liao H (2019) Genetic analysis and fine mapping of phosphorus efficiency locus 1 (PE1) in soybean. Theor Appl Genet 132:2847–2858. https://doi.org/10.1007/s00122-019-03392-3

    Article  CAS  PubMed  Google Scholar 

  • Yang A, Kong L, Wang H, Yao X, Xie F, Wang H, Ao X (2020) Response of soybean root to phosphorus deficiency under sucrose feeding: insight from morphological and metabolome characterizations. Biomed Res Int 2148032:11–11. https://doi.org/10.1155/2020/2148032

    Article  CAS  Google Scholar 

  • Yu O, Shi J, Hession AO, Maxwell CA, McGonigle B, Odell JT (2003) Metabolic engineering to increase isoflavone biosynthesis in soybean seed. Phytochemistry 63(7):753–763

    Article  CAS  PubMed  Google Scholar 

  • Yuan H, Liu D (2008) Signalling components involved in plant responses to phosphate starvation. J Integr Plant Biol 50(7):849–859

    Article  CAS  PubMed  Google Scholar 

  • Zeng H, Wang G, Zhang Y, Hu X, Pi E, Zhu Y, Wang H, Du L (2016) Genome-wide identification of phosphate-deficiency-responsive genes in soybean roots by high-throughput sequencing. Plant Soil 398:207–227. https://doi.org/10.1007/s11104-015-2657-4

    Article  CAS  Google Scholar 

  • Zhang D, Liu C, Cheng H et al (2010) Quantitative trait loci associated with soybean tolerance to low phosphorus stress based on flower and pod abscission. Plant Breed 129(3):243–249

    Article  CAS  Google Scholar 

  • Zhang D, Song H, Cheng H, Hao D, Wang H, Kan G, Jin H, Yu D (2014) The acid phosphatase-encoding gene GmACP1 contributes to soybean tolerance to low-phosphorus stress. PLoS Genet 10(1):–e1004061. https://doi.org/10.1371/journal.pgen.1004061

  • Zhang D, Li H, Wang J, Zhang H, Hu Z, Chu S, Lv H, Yu D (2016) High-density genetic mapping identifies new major loci for tolerance to low-phosphorus stress in soybean. Front Plant Sci 7:372. https://doi.org/10.3389/fpls.2016.00372

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang D, Zhang H, Chu S, Li H, Chi Y, Triebwasser-Freese D, Lv H, Yu D (2017) Integrating QTL mapping and transcriptomics identifies candidate genes underlying QTLs associated with soybean tolerance to low-phosphorus stress. Plant Mol Biol 93:137–150. https://doi.org/10.1007/s11103-016-0552-x

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Li W, Lin Y, Zhang L, Wang C, Xu R (2018) Construction of a high-density genetic map and mapping of QTLs for soybean (Glycine max) agronomic and seed quality traits by specific length amplified fragment sequencing. BMC Genomics 19(641):1–14. https://doi.org/10.1186/s12864-018-5035-9

    Article  CAS  Google Scholar 

  • Zhao J, Fu J, Liao H, He Y, Nian H, Hu Y, Qiu L, Dong Y, Yan X (2004) Characterization of root architecture in an applied core collection for phosphorus efficiency of soybean germplasm. Chin Sci Bull 49:1611–1620. https://doi.org/10.1007/BF03184131

    Article  CAS  Google Scholar 

  • Zhou R, Chen HF, Wang XZ et al (2011) Analysis of QTLs for root traits at seedling stage in soybean. Acta Agron Sin 37(7):1151–1158. https://doi.org/10.1016/s1875-2780(11)60032-1

    Article  Google Scholar 

  • Zhou W, Lozano-Torres JL, Blilou I et al (2019) A jasmonate signalling network activates root stem cells and promotes regeneration. Cell 177:942.e14–956e.14. https://doi.org/10.1016/j.cell.2019.03.006

Download references

Acknowledgements

The author is grateful to the editor and reviewers for their constructive comments.

Author information

Authors and Affiliations

  1. Department of Arid Land Agriculture, Faculty of Meteorology, Environment and Arid Land Agriculture, King Abdulaziz University, Jeddah, 80200, Kingdom of Saudi Arabia

    Suleiman K. Bello

  2. Department of Soil Science, Faculty of Agriculture/Institute for Agricultural Research, Ahmadu Bello University, Zaria, Kaduna State, 1044, Nigeria

    Suleiman K. Bello

Authors
  1. Suleiman K. Bello
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Suleiman K. Bello.

Ethics declarations

Conflicts of Interest

The authors declare that they have no conflict of interest.

Code Availability

Not applicable.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bello, S.K. An Overview of the Morphological, Genetic and Metabolic Mechanisms Regulating Phosphorus Efficiency Via Root Traits in Soybean. J Soil Sci Plant Nutr 21, 1013–1029 (2021). https://doi.org/10.1007/s42729-021-00418-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s42729-021-00418-y

Keywords

Search

Navigation