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Adaptation to Phosphate Stress by N2-Fixing Legumes: Lessons to Learn from the Model Medicago truncatula

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Abstract

The central importance of inorganic phosphate (Pi) in legume nutrition and agricultural sustainability has long been recognized. However, Pi concentration in soil solution is often low because it readily forms insoluble complexes with calcium in alkaline soils or with iron and aluminum oxides in acidic soils. Consequently, low Pi availability is frequently the most limiting nutrient for plant growth and development over the majority of the earth’s land surface. Among the legumes, the model plant Medicago truncatula has emerged as a well-established system for characterization of Pi deficiency on leguminous plants at the physiological and molecular levels. The recent published reports have contributed to major advances in understanding the physiological, biochemical, and molecular mechanisms/pathways in M. truncatula root nodules to ameliorate low Pi stress. Metabolic and gene expression profiles of M. truncatula nodules induced by Pi stress reveal interesting features, including rearrangement of Pi, carbon, and nitrogen homeostases, enabling plants to cope with Pi scarcity. In this context, the separate impacts of Pi deficiency on such candidate regulatory pathways should be considered, but moreover their interacting and entwined networks cannot be excluded. Therefore, understanding the responsive and adaptive mechanisms conferring Pi tolerance to the M. truncatula symbiotic system is very important for the development of selection and breeding strategies.

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References

  • Adolfsson L, Solymosi K, Andersson MX, Keresztes Á, Uddling J, Schoefs B, Spetea C (2015) Mycorrhiza symbiosis increases the surface for sunlight capture in Medicago truncatula for better photosynthetic production. PLoS One 10:e0115314

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Alkama N, Ounane G, Drevon JJ (2012) Is genotypic variation of H+ efflux under P deficiency linked with nodulated-root respiration of N2-fixing common-bean (Phaseolus vulgaris L.)? J Plant Physiol 169:1084–1089

    Article  CAS  PubMed  Google Scholar 

  • Almeida JP, 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 

  • Ané J-M, Kiss GB, Riely BK, Penmetsa RV, Oldroyd GED, Ayax C, Lévy J, Debellé F, Baek J-M, Kalo P, Rosenberg C, Roe BA, Long SR, Dénarié J, Cook DR (2004) Medicago truncatula DMI1 required for bacterial and fungal symbioses in legumes. Science 303:1364–1367

    Article  PubMed  CAS  Google Scholar 

  • Avenhaus U, Cabeza RA, Liese R, Lingner A, Dittert K, Salinas-Riester G, Pommerenke C, Schulze J (2016) Short-term molecular acclimation processes of legume nodules to increased external oxygen concentration. Front Plant Sci 6:1133

    Article  PubMed  PubMed Central  Google Scholar 

  • Bargaz A, Lazali M, Amenc L, Abadie J, Ghoulam C, Farissi M, Faghire M, Drevon JJ (2013) Differential expression of trehalose 6-P phosphatase and ascorbate peroxidase transcripts in nodule cortex of Phaseolus vulgaris and regulation of nodule O2 permeability. Planta 238:107–119

    Article  CAS  PubMed  Google Scholar 

  • Boldt K, Pörs Y, Haupt B, Bitterlich M, Kühn C, Grimm B, Franken P (2011) Photochemical processes, carbon assimilation and RNA accumulation of sucrose transporter genes in tomato arbuscular mycorrhiza. J Plant Physiol 168:1256–1263

    Article  CAS  PubMed  Google Scholar 

  • Bonneau L, Huguet S, Wipf D, Pauly N, Truong H-N (2013) Combined phosphate and nitrogen limitation generates a nutrient stress transcriptome favorable for arbuscular mycorrhizal symbiosis in Medicago truncatula. New Phytol 199:188–202

    Article  CAS  PubMed  Google Scholar 

  • Cabeza RA, Liese R, Lingner A, von Stieglitz I, Neumann J, Salinas-Riester G, Pommerenke C, Dittert K, Schulze J (2014a) RNA-seq transcriptome profiling reveals that Medicago truncatula nodules acclimate N2 fixation before emerging P deficiency reaches the nodules. J Exp Bot 65:6035–6048

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cabeza RA, Lingner A, Liese R, Sulieman S, Senbayram M, Tränkner M, Dittert K, Schulze J (2014b) The activity of nodules of the supernodulating mutant Mtsunn is not limited by photosynthesis under optimal growth conditions. Int J Mol Sci 15:6031–6045

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cabeza RA, Liese R, Fischinger SA, Sulieman S, Avenhaus U, Lingner A, Hein H, Koester B, Baumgarten V, Dittert K, Schulze J (2015) Long-term non-invasive and continuous measurements of legume nodule activity. Plant J 81:637–648

    Article  CAS  PubMed  Google Scholar 

  • Caravaca F, Díaz E, Barea JM, Azcón-Aguilar C, Roldán A (2003) Photosynthetic and transpiration rates of Olea europaea subsp. sylvestris and Rhamnus lycioides as affected by water deficit and mycorrhiza. Biol Plant 46:637–639

    Article  Google Scholar 

  • Chaudhary MI, Adu-Gyamfi JJ, Hirofumi Saneoka H, Nguyen NT, Suwa R, Kanai S, El-Shemy HA, Lightfoot DA, Fujita K (2008) The effect of phosphorus deficiency on nutrient uptake, nitrogen fixation and photosynthetic rate in mashbean, mungbean and soybean. Acta Physiol Plant 30:537–544

    Article  CAS  Google Scholar 

  • Cheng X, Wang M, Lee H-K, Tadege M, Ratet P, Udvardi M, Mysore KS, Wen J (2014) An efficient reverse genetics platform in the model legume Medicago truncatula. New Phytol 201:1065–1076

    Article  CAS  PubMed  Google Scholar 

  • Drevon J-J, Alkama N, Bargaz A, Rodiño AP, Sungthongwises K, Zaman-Allah M (2015) The legume–rhizobia symbiosis. In: De Ron AM (ed) Grain legumes, Handbook of plant breeding 10. Springer Science+Business Media, New York, pp 267–290

    Chapter  Google Scholar 

  • Fischinger SA, Schulze J (2010) The importance of nodule CO2 fixation for the efficiency of symbiotic nitrogen fixation in pea at vegetative growth and during pod formation. J Exp Bot 61:2281–2291

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fischinger SA, Drevon JJ, Claassen N, Schulze J (2006) Nitrogen from senescing lower leaves of common bean is re-translocated to nodules and might be involved in a N-feedback regulation of nitrogen fixation. J Plant Physiol 163:987–995

    Article  CAS  PubMed  Google Scholar 

  • Fischinger SA, Hristozkova M, Mainassara Z, Schulze J (2010) Elevated CO2 concentration around alfalfa nodules increases N2 fixation. J Exp Bot 61:121–130

    Article  CAS  PubMed  Google Scholar 

  • Foo E, Yoneyama K, Hugill CJ, Quittenden LJ, Reid JB (2013) Strigolactones and the regulation of pea symbioses in response to nitrate and phosphate deficiency. Mol Plant 6:76–87

    Article  CAS  PubMed  Google Scholar 

  • Goicoechea N, Baslam M, Erice G, Irigoyen JJ (2014) Increased photosynthetic acclimation in alfalfa associated with arbuscular mycorrhizal fungi (AMF) and cultivated in greenhouse under elevated CO2. J Plant Physiol 171:1774–1781

    Article  CAS  PubMed  Google Scholar 

  • Gordon AJ, Skøt L, James CL, Minchin FR (2002) Short-term metabolic responses of soybean root nodules to nitrate. J Exp Bot 53:423–428

    Article  CAS  PubMed  Google Scholar 

  • Ha S, Tran LS (2014) Understanding plant responses to phosphorus starvation for improvement of plant tolerance to phosphorus deficiency by biotechnological approaches. Crit Rev Biotechnol 34:16–30

    Article  CAS  PubMed  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  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Hinsinger P, Plassard C, Tang C, Jaillard B (2003) Origins of root-mediated pH changes in the rhizosphere and their responses to environmental constraints: a review. Plant Soil 248:43–59

    Article  CAS  Google Scholar 

  • Høgh-Jensen H, Schjoerring J, Soussana JF (2002) The influence of phosphorus deficiency on growth and nitrogen fixation of white clover plants. Ann Bot 90:745–753

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hohnjec N, Henckel K, Bekel T, Gouzy J, Dondrup M, Goesmann A, Küster H (2006) Transcriptional snapshots provide insights into the molecular basis of arbuscular mycorrhiza in the model legume Medicago truncatula. Funct Plant Biol 33:737–748

    Article  CAS  Google Scholar 

  • Horváth B, Yeun LH, Domonkos Á, Halász G, Gobbato E, Ayaydin F, Miró K, Hirsch S, Sun J, Tadege M, Ratet P, Mysore KS, Ané J-M, Oldroyd GED, Kaló P (2011) Medicago truncatula IPD3 is a member of the common symbiotic signaling pathway required for rhizobial and mycorrhizal symbioses. Mol Plant-Microbe Interact 24:1345–1358

    Article  PubMed  Google Scholar 

  • Horváth B, Domonkos Á, Kereszt A, Szȕcs A, Ábrahám E, Ayaydin F, Bóka K, Chen Y, Chen R, Murray JD, Udvardi MK, Kondorosi É, Kaló P (2015) Loss of the nodule-specific cysteine rich peptide, NCR169, abolishes symbiotic nitrogen fixation in the Medicago truncatula dnf7 mutant. Proc Natl Acad Sci USA 112:15232–15237

    Article  PubMed  PubMed Central  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 under climate change simulations: an updated survey. Plant Sci 226:22–29

    Article  CAS  PubMed  Google Scholar 

  • Jain A, Vasconcelos MJ, Roghothama KG, Sahi SV (2007) Molecular mechanisms of plant adaptation to phosphate deficiency. In: Janick J (ed) Plant breeding reviews, vol 29. Wiley, Hoboken, pp 359–419

    Chapter  Google Scholar 

  • Javot H, Penmetsa RV, Terzaghi N, Cook DR, Harrison MJ (2007) A Medicago truncatula phosphate transporter indispensable for the arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci USA 104:1720–1725

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Keller SY (2003) The influence of P nutrition on the root metabolism in Lotus japonicus (Regel) K. Larsen: an approach at transcriptional level. PhD thesis, Swiss Federal Institute of Technology, Zurich

    Google Scholar 

  • Kleinert A, Thuynsma R, Magadlela A, Benedito VA, Valentine AJ (2017a) Metabolism and transport of carbon in legume nodules under P deficiency. In: Sulieman S, Tran LS (eds) Legume N2 fixation in soils with low phosphorus availability – adaptation and regulatory implication. Springer, New York. In press

    Google Scholar 

  • Kleinert A, Le Roux M, Kang Y, Valentine AJ (2017b) Oxygen and the regulation of N2 fixation in legume nodules under P scarcity. In: Sulieman S, Tran LS (eds) Legume N2 fixation in soils with low phosphorus availability – adaptation and regulatory implication. Springer, New York. In press

    Google Scholar 

  • Kouas S, Debez A, Plassard C, Drevon JJ, Abdelly C (2009) Effect of phosphorus limiting on phytase activity, proton efflux and oxygen consumption by nodulated-roots of common bean (Phaseolus vulgaris). Afr J Biotechnol 8:5301–5309

    CAS  Google Scholar 

  • Larrainzar E, Gil-Quintana E, Seminario A, Arrese-Igor C, González EM (2014) Nodule carbohydrate catabolism is enhanced in the Medicago truncatula A17-Sinorhizobium medicae WSM419 symbiosis. Front Microbiol 5: Article 447, 4 pages

    Google Scholar 

  • Lazali M, Bargaz A, Carlsson G, Ounane SM, Drevon JJ (2014) Discrimination against 15N among recombinant inbred lines of Phaseolus vulgaris L. contrasting in phosphorus use efficiency for nitrogen fixation. J Plant Physiol 171:199–204

    Article  CAS  PubMed  Google Scholar 

  • Li Y-S, Gao Y, Tian Q-Y, Shi F-L, Li L-H, Zhang W-H (2011) Stimulation of root acid phosphatase by phosphorus deficiency is regulated by ethylene in Medicago falcate. Environ Exp Bot 71:114–120

    Article  CAS  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

    Article  CAS  PubMed  Google Scholar 

  • Liu PP, Montgomery TA, Fahlgren N, Kasschau KD, Nonogaki H, Carrington JC (2007) Repression of AUXIN RESPONSE FACTOR10 by microRNA160 is critical for seed germination and post-germination stages. Plant J 52:133–146

    Article  CAS  PubMed  Google Scholar 

  • Liu J, Novero M, Charnikhova T, Ferrandino A, Schubert A, Ruyter-Spira C, Bonfante P, Lovisolo C, Bouwmeester HJ, Cardinale F (2013) Carotenoid Cleavage Dioxygenase 7 modulates plant growth, reproduction, senescence, and determinate nodulation in the model legume Lotus japonicus. J Exp Bot 64:1967–1981

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu H, Tang C, Li C (2016) The effects of nitrogen form on root morphological and physiological adaptations of maize, white lupin and faba bean under phosphorus deficiency. AoB Plants 8: plw058. doi:10.1093/aobpla/plw058

  • López-Arredondo DL, Leyva-González MA, González-Morales SI, López-Bucio JL, Herrera-Estrella L (2014) Phosphate nutrition: improving low-phosphate tolerance in crops. Annu Rev Plant Biol 65:95–123

    Article  PubMed  CAS  Google Scholar 

  • Mathesius U, Mulders S, Gao M, Teplitski M, Caetano-Anollés G, Rolfe BG, Bauer WD (2003) Extensive and specific responses of a eukaryote to bacterial quorum-sensing signals. Proc Natl Acad Sci USA 100:1444–1449

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McIntosh M, Meyer S, Becker A (2009) Novel Sinorhizobium meliloti quorum sensing positive and negative regulatory feedback mechanisms respond to phosphate availability. Mol Microbiol 74:1238–1256

    Article  CAS  PubMed  Google Scholar 

  • Mortimer PE, Pérez-Fernández MA, Valentine AJ (2012) Arbuscular mycorrhiza maintains nodule function during external NH4 + supply in Phaseolus vulgaris (L.) Mycorrhiza 22:237–245

    Article  CAS  PubMed  Google Scholar 

  • Nasr Esfahani M, Sulieman S, Schulze J, Yamaguchi-Shinozaki K, Shinozaki K, Tran LS (2014a) Approaches for enhancement of N2 fixation efficiency of chickpea (Cicer arietinum L.) under limiting nitrogen conditions. Plant Biotechnol J 12:387–397

    Article  CAS  Google Scholar 

  • Nasr Esfahani M, Sulieman S, Schulze J, Yamaguchi-Shinozaki K, Shinozaki K, Tran LS (2014b) Mechanisms of physiological adjustment of N2 fixation in Cicer arietinum L. (chickpea) during early stages of water deficit: single or multi-factor controls. Plant J 79:964–980

    Article  CAS  PubMed  Google Scholar 

  • Nasr Esfahani M, Kusano M, Nguyen KH, Watanabe Y, Ha CV, Saito K, Sulieman S, Herrera-Estrella L, Tran LS (2016) Adaptation of the symbiotic Mesorhizobium-chickpea relationship to phosphate deficiency relies on reprogramming of whole-plant metabolism. Proc Natl Acad Sci USA 113:E4610–E4619

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nouri E, Breuillin-Sessoms F, Feller U, Reinhardt D (2014) Phosphorus and nitrogen regulate arbuscular mycorrhizal symbiosis in Petunia hybrid. PLoS One 9:e90841

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pakdaman N, Mostajeran A, Hojati Z (2014) Phosphate concentration alters the effective bacterial quorum in the symbiosis of Medicago truncatula-Sinorhizobium meliloti. Symbiosis 62:151–155

    Article  CAS  Google Scholar 

  • Panara F, Calderini O, Porceddu A (2012) Medicago truncatula Functional genomics – an invaluable resource for studies on agriculture sustainability. In: Meroni G, Petrera F (eds) Functional genomics. InTech Publisher, Rijeka, pp 131–154

    Google Scholar 

  • Parniske M (2004) Molecular genetics of the arbuscular mycorrhizal symbiosis. Curr Opin Plant Biol 7:414–421

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  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 159:1634–1643

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Richardson AE, Lynch JP, Ryan PR, Delhaize E, Smith A, 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

    Article  CAS  Google Scholar 

  • Rodiño AP, Metral R, Guglielmi S, Drevon JJ (2009) Variation among common-bean accessions (Phaseolus vulgaris L.) from the Iberian peninsula for N2-dependent growth and phosphorus requirement. Symbiosis 47:161–174

    Article  Google Scholar 

  • Rose RJ (2008) Medicago truncatula As a model for understanding plant interactions with other organisms, plant development and stress biology: past, present and future. Funct Plant Biol 35:253–264

    Article  Google Scholar 

  • Rotaru V, Sinclair TR (2009) Interactive influence of phosphorus and iron on nitrogen fixation by soybean. Environ Exp Bot 66:94–99

    Article  CAS  Google Scholar 

  • Ruffel S, Freixes S, Balzergue S, Tillard P, Jeudy C, Martin-Magniette ML, van der Merwe MJ, Kakar K, Gouzy J, Fernie AR, Udvardi M, Salon C, Gojon A, Lepetit M (2008) Systemic signaling of the plant nitrogen status triggers specific transcriptome responses depending on the nitrogen source in Medicago truncatula. Plant Physiol 146:2020–2035

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sánchez-Correa MS, Valdés-López O (2017) Physiological mechanisms and adaptation strategies in common bean (Phaseolus vulgaris L.) under P deficiency. In: Sulieman S, Tran LS (eds) Legume N2 fixation in soils with low phosphorus availability – adaptation and regulatory implication. Springer, New York. In press

    Google Scholar 

  • Schubert S (2007) The apoplast of indeterminate legume nodules: compartment for transport of amino acids, amides and sugars? In: Sattelmacher B, Horst WJ (eds) The apoplast of higher plants: compartment of storage, transport and reactions. Springer, Dordrecht, pp 445–454

    Chapter  Google Scholar 

  • Schulze J (2004) How are nitrogen fixation rates regulated in legumes? J Plant Nutr Soil Sci 167:125–137

    Article  CAS  Google Scholar 

  • Schulze J, Drevon J-J (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, Temple G, Temple SJ, Beschow H, Vance CP (2006) Nitrogen fixation by white lupin under phosphorus deficiency. Ann Bot 98:731–740

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Smith SE, Jakobsen I, Grønlund M, Smith FA (2011) Roles of arbuscular mycorrhizas in plant phosphorus nutrition: interactions between pathways of phosphorus uptake in arbuscular mycorrhizal roots have important implications for understanding and manipulating plant phosphorus acquisition. Plant Physiol 156:1050–1057

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Soto MJ, Fernández-Aparicio M, Castellanos-Morales V, García-Garrido JM, Ocampo JA, Delgado MJ, Vierheilig H (2010) First indications for the involvement of strigolactones on nodule formation in alfalfa (Medicago sativa). Soil Biol Biochem 42:383–385

    Article  CAS  Google Scholar 

  • Soussana J-F, Tallec T (2010) Can we understand and predict the regulation of biological N2 fixation in grassland ecosystems? Nutr Cycl Agroecosyst 88:197–213

    Article  CAS  Google Scholar 

  • Stacey G, Libault M, Brechenmacher L, Wan J, May D (2006) Genetics and functional genomics of legume nodulation. Curr Opin Plant Biol 9:110–121

    Article  CAS  PubMed  Google Scholar 

  • Staudinger C, Mehmeti-Tershani V, Gil-Quintana E, Gonzalez EM, Hofhansl F, Bachmann G, Wienkoop S (2016) Evidence for a rhizobia-induced drought stress response strategy in Medicago truncatula. J Proteome 136:202–213

    Article  CAS  Google Scholar 

  • Sujkowska M, Górska-Czekaj M, Bederska M, Borucki W (2011) Vacuolar organization in the nodule parenchyma is important for the functioning of pea root nodules. Symbiosis 54:1–16

    Article  PubMed  PubMed Central  Google Scholar 

  • Sulieman S (2011) Does GABA increase the efficiency of symbiotic N2 fixation in legumes? Plant Signal Behav 6:32–36

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sulieman S (2015) Metabolic and regulatory networks related to nodule symbiosis. Lap Lambert Academic Publishing, Saarbrücken

    Google Scholar 

  • Sulieman S, Schulze J (2010a) The efficiency of nitrogen fixation of the model legume Medicago truncatula (Jemalong A17) is low compared to Medicago sativa. J Plant Physiol 167:683–692

    Article  CAS  PubMed  Google Scholar 

  • Sulieman S, Schulze J (2010b) Phloem-derived γ-aminobutyric acid (GABA) is involved in upregulating nodule N2 fixation efficiency in the model legume Medicago truncatula. Plant Cell Environ 33:2162–2172

    Article  CAS  PubMed  Google Scholar 

  • Sulieman S, Tran LS (2013) Asparagine: an amide of particular distinction in the regulation of symbiotic nitrogen fixation of legumes. Crit Rev Biotechnol 33:309–327

    Article  CAS  PubMed  Google Scholar 

  • Sulieman S, Tran LS (2015) Phosphorus homeostasis in legume nodules as an adaptive strategy to phosphorus deficiency. Plant Sci 239:36–43

    Article  CAS  PubMed  Google Scholar 

  • Sulieman S, Fischinger S, Schulze J (2008) N-feedback regulation of N2 fixation in Medicago truncatula under P-deficiency. Gen Appl Plant Physiol 34:33–54

    CAS  Google Scholar 

  • Sulieman S, Fischinger SA, Gresshoff PM, Schulze J (2010) Asparagine as a major factor in the N-feedback regulation of N2 fixation in Medicago truncatula. Physiol Plant 140:21–31

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sulieman S, Schulze J, Tran LS (2013b) Comparative analysis of the symbiotic efficiency of Medicago truncatula and Medicago sativa under phosphorus deficiency. Int J Mol Sci 14:5198–5213

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sulieman S, Schulze J, Tran LS (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 

  • Sulieman S, Thao NP, Tran LS (2015) Does elevated CO2 provide real benefits for N2-fixing leguminous symbioses? In: Sulieman S, Tran LS (eds) Legume nitrogen fixation in a changing environment. Springer International Publishing, Cham, pp 89–112

    Google Scholar 

  • Tang C, Hinsinger P, Drevon JJ, Jaillard B (2001) Phosphorus deficiency impairs early nodule functioning and enhances proton release in roots of Medicago truncatula L. Ann Bot 88:131–138

    Article  CAS  Google Scholar 

  • Tang C, Han XZ, Qiao YF, Zheng SJ (2009) Phosphorus deficiency does not enhance proton release by roots of soybean [Glycine max (L.) Murr.] Environ Exp Bot 67:228–234

    Article  CAS  Google Scholar 

  • Tesfaye M, Liu J, Allan DL, Vance CP (2007) Genomic and genetic control of phosphate stress in legumes. Plant Physiol 144:594–603

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thuynsma R, Valentine A, Kleinert A (2014) Phosphorus deficiency affects the allocation of below-ground resources to combined cluster roots and nodules in Lupinus albus. J Plant Physiol 171:285–291

    Article  CAS  PubMed  Google Scholar 

  • Udvardi M, Poole PS (2013) Transport and metabolism in legume-rhizobia symbioses. Annu Rev Plant Biol 64:781–805

    Article  CAS  PubMed  Google Scholar 

  • Uhde-Stone C (2017) White lupin: a model system for understanding plant adaptation to low phosphorus availability. In: Sulieman S, Tran LS (eds) Legume N2 fixation in soils with low phosphorus availability – adaptation and regulatory implication. Springer, New York. In press

    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 34:871–878

    CAS  Google Scholar 

  • Valdés-López O, Hernández G (2008) Transcriptional regulation and signaling in phosphorus starvation: what about legumes? J Integr Plant Biol 50:1213–1222

    Article  PubMed  CAS  Google Scholar 

  • Valentine AJ, Benedito VA, Kang Y (2011) Legume nitrogen fixation and soil abiotic stress: from physiology to genome and beyond. In: Foyer CH, Zhang H (eds) Annual plant reviews. Wiley-Blackwell, Oxford, pp 207–248

    Google Scholar 

  • van Zeijl A, Liu W, Xiao TT, Kohlen W, Yang W-C, Bisseling T, Geurts R (2015) The strigolactone biosynthesis gene DWARF27 is co-opted in rhizobium symbiosis. BMC Plant Biol 15:260

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Vance CP (2010) Quantitative trait loci, epigenetics, sugars, and microRNAs: quaternaries in phosphate acquisition and use. Plant Physiol 154:582–588

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vance CP, Chiou T-J (2011) Phosphorus focus editorial. Plant Physiol 156:987–988

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vardien W, Steenkamp 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

    Article  CAS  PubMed  Google Scholar 

  • Wang E, Yu N, Bano SA, Liu C, Miller AJ, Cousins D, Zhang X, Ratet P, Tadege M, Mysore KS, Downie JA, Murray JD, Oldroyd GED, Schultze M (2014) A H+-ATPase that energizes nutrient uptake during mycorrhizal symbioses in rice and Medicago truncatula. Plant Cell 26:1818–1830

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Zogli P, Pingault L, Libault M (2017) Physiological and molecular mechanisms and adaptation strategies in soybean (Glycine max) under phosphate deficiency. In: Sulieman S, Tran LS (eds) Legume N2 fixation in soils with low phosphorus availability – adaptation and regulatory implication. Springer, New York. In press

    Google Scholar 

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Acknowledgments

Preparation of this contribution was supported in part by the Japan Society of the Promotion of Science (JSPS) to Saad Sulieman.

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Correspondence to Saad Sulieman or Lam-Son Phan Tran .

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Sulieman, S., Tran, LS.P. (2017). Adaptation to Phosphate Stress by N2-Fixing Legumes: Lessons to Learn from the Model Medicago truncatula . 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_10

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