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P Deficiency: A Major Limiting Factor for Rhizobial Symbiosis

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Legume Nitrogen Fixation in Soils with Low Phosphorus Availability

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Abstract

Together with nitrogen (N), phosphorus (P) has been described as the main plant macronutrient limiting growth. Although P is abundant in many soils, its availability for plants is low. For this reason, P is provided to plants largely through the application of P-enriched fertilizers. However, since rock phosphate reserves (the main source of P) are predicted to be depleted in the near future, it is crucial to understand the processes linked with a better P use efficiency. P is a target structural constituent of energetic compounds (ATP, ADP), nucleic acids, phosphate sugars, etc., that are essential for cell metabolism and plant development. Current knowledge highlights that low P availability negatively affects above- and below-ground organ growth, as a consequence, in part, of poor photosynthetic performance. While essential for all plants, the P requirement of N2-fixing plants has been described as larger than that of non N2-fixing plants, mainly as a consequence of the large P demand for biological N2 fixation (BNF) processes. Moreover, three main factors have been suggested to affect BNF under low P conditions: carbon supply, N-feedback and O2 diffusion have been identified as the main factors conditioning N2 fixation under low P availability conditions. In this chapter, we summarize current knowledge regarding P content in plant performance, with special emphasis on N2-fixing plants and the symbiotic relationship.

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References

  • Ae N, Arihara J, Okada K, Yoshihara T, Johansen C (1990) Phosphorus uptake by pigeon pea and its role in crop** systems of the Indian subcontinent. Science 248:477–480

    Article  CAS  PubMed  Google Scholar 

  • Agbariah K-T, Roth-Bejerano N (1990) The effect of blue light on energy levels in epidermal strips. Physiol Planta 78:100–104

    Article  CAS  Google Scholar 

  • Alexandratos N, Bruinsma J (2012) World agriculture towards 2030/2050: the 2012 revision. ESA Working paper No. 12–03. FAO, Rome

    Google Scholar 

  • Almeida JPF, Hartwig UA, Frehner M, Nosberger J, Luscher A (2000) Evidence that P deficiency induces N feedback regulation of symbiotic N2 fixation in white clover (Trifolium repens L.) J Exp Bot 51:1289–1297

    CAS  PubMed  Google Scholar 

  • Ankomah AB, Zapata F, Hardarson G, Danso SKA (1996) Yield, nodulation, and N2 fixation by cowpea cultivars at different phosphorus levels. Biol Fert Soils 22:10–15

    Article  Google Scholar 

  • Anuradha M, Narayanan A (1991) Promotion of root elongation by phosphorus deficiency. Plant Soil 136:273–275

    Article  CAS  Google Scholar 

  • Aranjuelo I, Arrese-Igor C, Molero G (2014) Nodule performance within a changing environmental context. J Plant Physiol 98:32–39

    Google Scholar 

  • Bieleski RL (1973) Phosphate pools, phosphate transport, and phosphate availability. Annu Rev Plant Physiol 24:225–252

    Article  CAS  Google Scholar 

  • Bottrill DE, Possingham JV, Kriedemann PE (1970) The effect of nutrient deficiencies on photosynthesis and respiration in spinach. Plant Soil 32:424–438

    Article  CAS  Google Scholar 

  • Brooks A (1986) Effects of phosphorus nutrition on ribulose-1,5-bisphosphate carboxylase activation, photosynthetic quantum yield and amounts of some Calvin cycle metabolites in spinach leaves. Aust J Plant Physiol 13:221–237

    Article  CAS  Google Scholar 

  • Bumb BL, Baanante CA (1996) The role of fertilizer in sustaining food security and protecting the environment. Food, Agriculture, and the Environment, Discussion Paper 17. International Food Policy Research Institute, Washington DC

    Google Scholar 

  • Busman L, Lamb J, Randall G, Rehm G, Schmitt M (2002) http://www.extension.umn.edu/agriculture/nutrient-management/phosphorus/the-nature-of-phosphorus/#quality

  • Cabeza RA et al (2014) RNA-seq transcriptome profiling reveals that Medicago truncatula nodules acclimate N2 fixation before emerging P deficiency reaches the nodules. J Exp Bot 65(20):6035–6048

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cooper J, Lombardi R, Boardman D, Carliell-Marquet C (2011) The future distribution and production of global phosphate rock reserves. Resour Conserv Recycl 57:78–86

    Article  Google Scholar 

  • Cordell D (2010) The story of phosphorus. Sustainability implications of global phosphorus scarcity for food security. Linkö** University, Linkö**

    Google Scholar 

  • De Haes HAU, Jansen J, Van Der Weijden LA, Smit WJAL (2009) Phosphate – from surplus to shortage. In: Policy memorandum of the Steering Committee for Technology Assessment. Ministry of Agriculture, Nature and Food Quality, Utrecht

    Google Scholar 

  • Divito GA, Sadras VO (2014) How do phosphorus, potassium and sulphur affect plant growth and biological nitrogen fixation in crop and pasture legumes? A meta-analysis. Field Crop Res 156:161–171

    Article  Google Scholar 

  • Dyson T (1999) World food trends and prospects to 2025. Proc Natl Acad Sci USA 96:5929–5936

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Edixhoven JD, Gupta J, Savenije HHG (2014) Recent revisions of phosphate rock reserves and resources: a critique. Earth Syst Dynam 5:491–507. doi:10.5194/esd-5-491-2014

    Article  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gálvez L, González EM, Arrese-Igor C (2005) Evidence for carbon flux shortage and strong carbon/nitrogen interactions in pea nodules at early stages of water stress. J Exp Bot 56: 2551–2561

    Google Scholar 

  • Gilroy S, Jones DL (2000) Through form to function Broot hair development and nutrient uptake. Trends Plant Sci 3:56–60

    Article  Google Scholar 

  • González EM, Gálvez L, Royuela M, Aparicio-Tejo PM, Arrese-Igor C (2001) Insights into the regulation of nitrogen fixation in pea nodules: lessons from drought, abscisic acid and increased photoassimilate availability. Agronomie 21:607–613

    Google Scholar 

  • Gordon AJ, Mitchell DF, Ryle GJA, Powell CE (1987) Diurnal production and utilization of photosynthates in nodulated white clover. J Exp Bot 38:84–98

    Google Scholar 

  • Gunawardena SFBN, Danso SKA, Zapata F (1992) Phosphorus requirements and nitrogen accumulation by 3 mungbean (Vigna radiata (L) Welzek) cultivars. Plant Soil 147:267–274

    Google Scholar 

  • Halsted M, Lynch J (1996) Phosphorus responses of C3 and C4 species. J Exp Bot 47:497–505

    Article  CAS  Google Scholar 

  • Harrison MJ (1997) The arbuscular mycorrhizal symbiosis: an underground association. Trends Plant Sci 2:54–60

    Article  Google Scholar 

  • Hernández G, Valdés-López O, Ramírez M, Goffard N, Weiller G, Aparicio-Fabre R, Fuentes SI, Erban A, Kopka J, Udvardi MK, Vance CP (2009) Global changes in the transcript and metabolic profiles during symbiotic nitrogen fixation in phosphorus-stressed common bean plants. Plant Physiol 151:1221–1238

    Article  PubMed  PubMed Central  Google Scholar 

  • Herold A (1980) Regulation of photosynthesis by sink activity—the missing link. New Phytol 86:131–144

    Article  CAS  Google Scholar 

  • Holford ICR (1997) Soil phosphorus: its measurement, and its uptake by plants. Aust J Soil Res 35:227–239

    Article  CAS  Google Scholar 

  • Horst WJ (1995) The role of the apoplast in aluminium toxicity and resistance of higher plants: a review. Z Pflanzenernähr Bodenkd 158:419–428

    Article  CAS  Google Scholar 

  • Horst WJ, Wang Y, Eticha D (2010) The role of the root apoplast in aluminium-induced inhibition of root elongation and in aluminium resistance of plants: a review. Ann Bot 106:185–197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hunt S, Layzell DB (1993) Gas exchange of legume nodules and the regulation of nitrogenase activity. Annu Rev Plant Physiol Plant Mol Biol 44:483–511

    Article  CAS  Google Scholar 

  • Irigoyen JJ, Goicoechea N, Antolín MC, Pascual I, Sánchez-Díaz M, Aguirreolea J, Morales F (2014) Growth, photosynthetic acclimation and yield quality in legumes grown under climate change simulations: an updated survey. Plant Sci 226:22–29

    Article  CAS  PubMed  Google Scholar 

  • Jakobsen I (1985) The role of phosphorus in nitrogen-fixation by young pea-plants (Pisum-Sativum). Physiol Plant 64:190–196

    Article  CAS  Google Scholar 

  • Jasinski SM (2011) Phosphate rock, mineral commodity summaries. U.S. Geological Survey, Reston

    Google Scholar 

  • Jebara M, Aouani ME, Payre H, Drevon JJ (2005) Nodule conductance varied among common bean (Phaseolus vulgaris) genotypes under phosphorus deficiency. J Plant Physiol 162:309–315

    Google Scholar 

  • Juszczuk IM, Rychter AM (2002) Pyruvate accumulation during phosphate deficiency stress of bean roots. Plant Physiol Biochem 40(9):783–788

    Article  CAS  Google Scholar 

  • Khamis S, Chaillou S, Lamaze T (1990) CO2 assimilation and partitioning of carbon in maize plants deprived of orthophosphate. J Exp Bot 41:1619–1625

    Article  CAS  Google Scholar 

  • Kleinert A, Venter M, Kossmann J, Valentine A (2014) The reallocation of carbon in P deficient lupins affects biological nitrogen fixation. J Plant Physiol 171:1619–1624

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Krapp A, Stitt M (1995) An evaluation of direct and indirect mechanisms for the sink regulation of photosynthesis in spinach—changes in gas exchange, carbohydrates, metabolites, enzyme activities and steady-state transcript levels after cold-girdling source leaves. Planta 195:313–323

    Article  CAS  Google Scholar 

  • Lauer MJ, Pallardy SG, Blevins DG, Randall DD (1989) Whole leaf carbon exchange characteristics of phosphate deficient soybeans (Glycine max L.) Plant Physiol 91:848–854

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Le Roux MR, Ward CL, Botha FC, Valentine AJ (2006) Routes of pyruvate synthesis in phosphorus-deficient lupin roots and nodules. New Phytol 169(2):399–408

    Article  PubMed  Google Scholar 

  • Le Roux MR, Khan S, Valentine AJ (2008) Organic acid accumulation may inhibit N2 fixation in phosphorus-stressed lupin nodules. New Phytol 177(4):956–964

    Article  PubMed  Google Scholar 

  • Lea PJ, Forde BG (1994) The use of mutants and transgenic plants to study amino acid metabolism plant. Cell Environ 17:541–556

    Google Scholar 

  • Liu Y, Villalba G, Ayres RU, Schroder H (2008) Global phosphorus flows and environmental impacts from a consumption perspective. J Ind Ecol 12:229–247

    Article  CAS  Google Scholar 

  • Lodwig E, Poole P (2003) Metabolism of rhizobium bacteroids. Crit Rev Plant Sci 22:37–78

    Article  CAS  Google Scholar 

  • Lynch J, Lauch HA, Epstein E (1991) Vegetative growth of the common bean in response to phosphorus nutrition. Crop Sci 31:380–387

    Article  CAS  Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants. Academic, London

    Google Scholar 

  • Marschner H, Dell B (1994) Nutrient uptake in mycorrhizal symbiosis. Plant Soil 159:89–102

    Article  CAS  Google Scholar 

  • Miao SJ, Qiao YF, Han XZ, An M (2007) Nodule formation and development in soybeans (Glycine max L.) in response to phosphorus supply in solution culture. Pedosphere 17:36–43

    Article  CAS  Google Scholar 

  • Mousavishalmani MA, Sagheb N, Hobbi MS, Rafh H, Khorasani A (2002) Fertilizer P distribution into different parts of plant and soil under trickle fertigation on tomato by 32P. In: 17th Word Congress Soil Science, Paper 2286, Thailand

    Google Scholar 

  • Nasr Esfahani MN, Kusanob M, Nguyend KH, Watanabee Y, Ha CV, Saitoc K, Sulieman S, Herrera-Estrella L, Tran LSP (2016) Adaptation of the symbiotic Mesorhizobium–chickpea relationship to phosphate deficiency relies on reprogramming of whole-plant metabolism. Proc Natl Acad Sci USA 113(32):E4610–E4619

    Article  PubMed  PubMed Central  Google Scholar 

  • Peoples MB, Herridge DF, Ladha JK (1995) Biological nitrogen fixation: an efficient source of nitrogen for sustainable agricultural production. Plant Soil 174:3–28

    Article  CAS  Google Scholar 

  • Pieters AJ, Paul MJ, Lawlor DW (2001) Low sink demand limits photosynthesis under Pi deficiency. J Exp Bot 52:1083–1091

    Article  CAS  PubMed  Google Scholar 

  • Plaxton WC (2004) Plant response to stress: biochemical adaptations to phosphate deficiency. In: Goodman R (ed) Encyclopedia of plant and crop science. Marcel Dekker, New York, pp 976–980

    Chapter  Google Scholar 

  • Plesnicar M, Kastori R, Petrovic N, Pankovic D (1994) Photosynthesis and chlorophyll fluorescence in sunflower (Helianthus annuus L.) leaves as affected by phosphorus nutrition. J Exp Bot 45:919–924

    Article  CAS  Google Scholar 

  • Qiu J, Israel DW (1992) Diurnal starch accumulation and utilization in phosphorus-deficient soybean plants. Plant Physiol 98:316–323

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Radin JW (1990) Responses of transpiration and hydraulic conductance to root temperature in nitrogen- and phosphorus-deficient cotton seedlings. Plant Physiol 92:855–857

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  Google Scholar 

  • Rao IM, Terry N (1989a) Leaf phosphate status, photosynthesis and carbon partitioning in sugar beet. I. Changes in growth, gas exchange and Calvin cycle enzymes. Plant Physiol 90:814–819

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rao IM, Terry N (1989b) Leaf phosphate status, photosynthesis and carbon partitioning in sugar beet. II. Diurnal changes in sugar phosphates, adenylates and nicotinamide nucleotides. Plant Physiol 90:820–826

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rao IM, Terry N (1990) Leaf phosphate status, photosynthesis and carbon partitioning in sugar beet. III. Diurnal changes in carbon partitioning and carbon export. Plant Physiol 92:29–36

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rao IM, Terry N (1995) Leaf phosphate status, photosynthesis, and carbon partitioning in sugar beet. IV: changes with time following increased supply of phosphate to low phosphate plants. Plant Physiol 107:1313–1321

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ribet J, Drevon JJ (1995) Increase in conductance to oxygen and in oxygen uptake of soybean nodules under limiting phosphorus nutrition. Physiol Plant 94:298–304

    Article  CAS  Google Scholar 

  • Ribot C, Wang Y, Poirier Y (2008) Expression analysis of three members of the AtPHO1 family reveal differential interactions between signaling pathways involved in phosphate deficiency and the responses to auxin, cytokinin, and abscisic acid. Planta 227:1025–1036

    Article  CAS  PubMed  Google Scholar 

  • Rogers A, Gibon Y, Stitt M, Morgan PB, Bernacchi CJ, Ort DR, Long SP (2006) Increased C availability at elevated carbon dioxide concentration improves N assimilation in a legume. Plant Cell Environ 29:1651–1658

    Article  CAS  PubMed  Google Scholar 

  • Sawada S, Usuda H, Tsukui T (1992) Participation of inorganic orthophosphate in regulation of the ribulose-1,5-bisphosphate carboxylase activity in response to changes in the photosynthetic source-sink balance. Plant Cell Physiol 33:943–949

    CAS  Google Scholar 

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

    Google Scholar 

  • Scholz RW, Wellmer FW (2016) Comment on: “recent revisions of phosphate rock reserves and resources: a critique” by Edixhoven et al. (2014)—clarifying comments and thoughts on key conceptions, conclusions and interpretation to allow for sustainable action. Earth Syst Dynam 7:103–117

    Article  Google Scholar 

  • Schröder JJ, Cordell D, Smit AL, Rosemarin A (2010) Sustainable use of phosphorus, EU tender EN V. B.1/ETU/2009/0025. Plant Research International, Business Unit Agrosystems, Wageningen UR, Wageningen

    Google Scholar 

  • Schulze J, Drevon JJ (2005) P-deficiency increases the O2 uptake per N2 reduced in alfalfa. J Exp Bot 56:1779–1784

    Article  CAS  PubMed  Google Scholar 

  • Schulze J, Adgo E, Merbach W (1999) Carbon costs associated with N2 fixation in Vicia faba L. and Pisum sativum L. over a 14-day period. Plant Biol 1:625–631

    Article  Google Scholar 

  • Schulze J, Tesfaye M, Litjens R, Bucciarelli B, Trepp G, Miller S et al (2002) Malate plays a central role in plant nutrition. Plant Soil 247:133–139

    Article  CAS  Google Scholar 

  • Schulze J, Mohamed MAN, Carlsson G, Drevon JJ (2011) Phosphorus deficiency decreases nitrogenase activity but increases proton efflux in N2-fixing Medicago truncatula. Plant Physiol Biochem 49:458–460

    Article  CAS  PubMed  Google Scholar 

  • Serraj R, Sinclair TR (1996) Inhibition of nitrogenase activity and nodule oxygen permeability by water deficit. J Exp Bot 47:1067–1073

    Article  CAS  Google Scholar 

  • Smit AL, Bindraban PS, Schröder JJ, Conijn JG, Van Der Meer HG (2009) Phosphorus in agriculture: global resources trends and developments. Plant Research International B.V, Wageningen

    Google Scholar 

  • Smith FW, Jackson WA, van den Berg PJ (1990) Internal phosphorus flows during development of phosphorus stress in Stylosanthes hamata. Aust J Plant Physiol 17:451–464

    Article  CAS  Google Scholar 

  • Sulieman S, Ha CV, Schulze J, Tran L-SP (2013) Growth and nodulation of symbiotic Medicago truncatula at different levels of phosphorus availability. J Exp Bot 64(10):2701–2712

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sulieman S, Schulze J, Tran LSP (2014) N-feedback regulation is synchronized with nodule carbon alteration in Medicago truncatula under excessive nitrate or low phosphorus conditions. J Plant Physiol 171:407–410

    Article  CAS  PubMed  Google Scholar 

  • Terry N, Ulrich A (1973) Effects of phosphorus deficiency on the photosynthesis and respiration of leaves of sugar beet. Plant Physiol 51:43–47

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Treeby MT, Van Steveninck RFM, de Vries HM (1987) Quantitative estimates of phosphorus concentrations within Lupinus luteus leaflets by means of electron probe X-ray microanalysis. Plant Physiol 85:331–334

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Turnbull TL, Warren CR, Adams MA (2007) Novel mannose-sequestration technique reveals variation in subcellular orthophosphate pools do not explain the effects of phosphorus nutrition on photosynthesis in Eucalyptus globulus seedlings. New Phytol 176:849–861

    Article  CAS  PubMed  Google Scholar 

  • United Nations, Department of Economic and Social Affairs, Population Division (2015). World population prospects: The 2015 revision, key findings and advance tables, Working paper No. ESA/P/WP.241

    Google Scholar 

  • USGS (2011) Mineral commodity summaries, Phosphate Rock. US Geological Survey, Washington, DC

    Google Scholar 

  • USGS (2014) Mineral commodity survey: mineral commodity summaries. US Geological Survey, Washington, DC

    Google Scholar 

  • Vaccari DA (2009) Phosphorus, a looming crisis. Sci Am 300:42–47

    Article  Google Scholar 

  • Vadez V, Rodier F, Payre H, Drevon JJ (1996) Nodule permeability to O2 and nitrogenase-linked respiration in bean genotypes varying in the tolerance of N2 fixation to P deficiency. Plant Physiol Biochem 34(6):871–878

    Google Scholar 

  • Vance CP (2001) Symbiotic nitrogen fixation and phosphorus acquisition. Plant nutrition in a world of declining renewable resources. Plant Physiol 127:390–397

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vance CP, Graham PH, Allan DL (2000) Biological nitrogen fixation: phosphorus Ba critical future need? In: Pederosa FO, Hungria M, Yates MG, Newton WE (eds) Nitrogen fixation: from molecules to crop productivity. Kluwer, Dordrecht, pp 506–514

    Google Scholar 

  • Vardien W, Mesjasz-Przybylowicz J, Przybylowicz WJ, Wang YD, Steenkamp ET, Valentine AJ (2014) Nodules from Fynbos legume Virgilia divaricata have high functional plasticity under variable P supply levels. J Plant Physiol 171:1732–1739

    Article  CAS  PubMed  Google Scholar 

  • Vardien W, Steenkampb ET, Valentine AJ (2016) Legume nodules from nutrient-poor soils exhibit high plasticity of cellular phosphorus recycling and conservation during variable phosphorus supply. J Plant Physiol 191:73–81

    Google Scholar 

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

    Article  Google Scholar 

  • Vysotskaya LB, Trekozova AW, Kudoyarova GR (2016) Effect of phosphorus starvation on hormone content and growth of barley plants. Acta Physiol Plant 38:108

    Article  Google Scholar 

  • Walker DA, Sivak MN (1985) Can phosphate limit photosynthetic carbon assimilation in vivo? Physiol Veg 23:829–841

    CAS  Google Scholar 

  • Walker DA, Sivak MN (1986) Photosynthesis and phosphate: a cellular affair? Trends Biochem Sci 11:176–179

    Article  CAS  Google Scholar 

  • Warren CR (2011) How does P affect photosynthesis and metabolite profiles of Eucalyptus globulus? Tree Physiol 31:727–739

    Article  CAS  PubMed  Google Scholar 

  • Warren CR, Adams MA (2002) Phosphorus affects growth and partitioning of nitrogen to Rubisco in Pinus pinaster. Tree Physiol 22:11–19

    Article  CAS  PubMed  Google Scholar 

  • Xu HX, Weng XY, Yang Y (2007) Effect of phosphorus deficiency on the photosynthetic characteristics of rice plants. Russ J Plant Physiol 54:741–748

    Article  CAS  Google Scholar 

  • Yang N, Zavisic A, Pena R, Polle A (2016) Phenology, photosynthesis, and phosphorus in European beech (Fagus sylvatica L.) in two forest soils with contrasting P contents. J Plant Nutr Soil Sci 179:151–158

    Article  CAS  Google Scholar 

  • Zheng SJ (2010) Crop production on acidic soils: overcoming aluminium toxicity and phosphorus deficiency. Ann Bot 106:183–184

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

This work was funded by the Spanish National Research and Development Programme (AGL2014-56561-P), the “I-COOP Suelos y Legumbres” Programme (2016SU0016) and their corresponding FEDER funding, and Aragón Government (A03 research group).

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Authors and Affiliations

  1. Division of Plant Sciences, University of Missouri, Columbia, MO, 65211, USA

    Alvaro Sanz-Saez

  2. Estación Experimental de Aula Dei (EEAD), CSIC, Dpto. Nutrición Vegetal, Apdo 13034, E-50080, Zaragoza, Spain

    Fermín Morales

  3. Dpto. Ciencias del Medio Natural, Universidad Pública de Navarra, Campus de Arrosadía, E-31006, Pamplona, Spain

    Cesar Arrese-Igor

  4. Instituto de Agrobiotecnología (IdAB), Universidad Pública de Navarra-CSIC-Gobierno de Navarra, Campus de Arrosadía, E-31192, Pamplona, Spain

    Iker Aranjuelo

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  3. Cesar Arrese-Igor
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  1. Department of Agronomy, Faculty of Agriculture, University of Khartoum, Shambat, Khartoum North, Sudan

    Saad Sulieman

  2. Signaling Pathway Research Unit, RIKEN Center for Sustainable Resource Science (CSRS), Tsurumi, Yokohama, Japan

    Lam-Son Phan Tran

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Sanz-Saez, A., Morales, F., Arrese-Igor, C., Aranjuelo, I. (2017). P Deficiency: A Major Limiting Factor for Rhizobial Symbiosis. In: Sulieman, S., Tran, LS. (eds) Legume Nitrogen Fixation in Soils with Low Phosphorus Availability. Springer, Cham. https://doi.org/10.1007/978-3-319-55729-8_2

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