Abstract
Legumes are well recognized for their nutritional and health benefits as well as for their impact in the sustainability of agricultural systems. Phosphate (Pi) deficiency is a major nutritional factor limiting legume production, particularly in acidic and calcareous soils. Pi deficiency limits N2 fixation, since it has been described to have a strong impact on the growth and survival of both rhizobia and host plant. Legumes have evolved complex mechanisms to cope with Pi limitation. The maintenance of symbiotic N2 fixation seems to be a key aspect to assure legume productivity in low Pi environments. During the last decades, physiological components and molecular players underlying Pi-deficiency adaptation responses have been elucidated. Molecular, biochemical, physiological, and morphological responses are triggered to stimulate soil Pi uptake or to optimize its intracellular use efficiency and allocation over all plant organs. Research conducted on model species such as Medicago truncatula or important pulses such as common bean, soybean, and white lupin have provided valuable clues about the different mechanisms ensuring Pi homeostasis in nodules under Pi-limited conditions. In this chapter, we provide a general overview on the recent achievements on the impact of Pi deficiency on symbiotic N2 fixation in a broad range of legume species. A critical discussion of the main results and open questions is provided, highlighting the different approaches used to address the current needs of agriculture under the climate change context.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Abdel-Latief K, Bogusz D, Hocher V (2012) The role of flavonoids in the establishment of plant roots endosymbioses with arbuscular mycorrhiza fungi, rhizobia and Frankia bacteria. Plant Signal Behav 7:636–641. doi:10.4161/psb.20039
Abdolzadeh A, Wang X, Veneklaas EJ, Lambers H (2010) Effects of phosphorus supply on growth, phosphate concentration and cluster-root formation in three Lupinus species. Ann Bot 105:365–374. doi:10.1093/aob/mcp297
Almeida JPF, Hartwig UA, Frehner M, Josef N, Lüscher 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. doi:10.1093/jexbot/51.348.1289
Alunni B, Gourion B (2016) Terminal bacteroid differentiation in the legume-rhizobium symbiosis: nodule-specific cysteine-rich peptides and beyond. New Phytol 211:411–417. doi:10.1111/nph.14025
Amon J, Titgemeyer F, Burkovski A (2010) Common patterns – unique features: nitrogen metabolism and regulation in Gram-positive bacteria. FEMS Microbiol Rev 34:588–605. doi:10.1111/j.1574-6976.2010.00216.x
Aparicio-Fabre R, Guillén G, Loredo M, Arellano J, Valdés-López O, Ramírez M, Iñiguez LP, Panzeri B, Castiglioni P, Cremonesi P, Stronzzi F, Stella A, Girard L, Sparvoli F, Hernández G (2013) Common bean (Phaseolus vulgaris L.) PvTIFY orchestrates global changes in transcript profile response to jasmonate and phosphorus deficiency. BMC Plant Biol 13:26. doi:10.1186/1471-2229-13-26
Aranjuelo I, Arrese-Igor C, Molero G (2014) Nodule performance within a changing environmental context. J Plant Physiol 171:1076–1090. doi:10.1016/j.jplph.2014.04.002
Araújo AP, Plassard C, Drevon JJ (2008) Phosphatase and phytase activities in nodules of common bean genotypes at different levels of phosphorus supply. Plant Soil 312:129–138. doi:10.1007/s11104-008-9595-3
Araújo SS, Beebe S, Crespi M, Delbreil B, González EM, Gruber V, Lejeune-Henaut I, Link W, Monteros MJ, Prats E, Rao I, Vadez V, Vaz Patto MC (2015) Abiotic stress responses in legumes: strategies used to cope with environmental challenges. Crit Rev Plant Sci 34:237–280. doi:10.1080/07352689.2014.898450
Arthikala M-K, Sanchez-Lopez R, Nava N, Santana O, Cárdenas L, Quinto C (2014) RbohB, a Phaseolus vulgaris NADPH oxidase gene, enhances symbiosome number, bacteroid size, and nitrogen fixation in nodules and impairs mycorrhizal colonization. New Phytol 202:886–900. doi:10.1111/nph.12714
Balemi T, Negisho K (2012) Management of soil phosphorus and plant adaptation mechanisms to phosphorus stress for sustainable crop production: a review. J Soil Sci Plant Nutr 12:547–561
Barraclough D (1995) 15N isotope dilution techniques to study soil nitrogen transformations and plant uptake. Fertil Res 42:185–192. doi:10.1007/BF00750513
Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281–297. doi:10.1016/S0092-8674(04)00045-5
Batterman SA, Hedin LO, van Breugel M, Ransijn J, Craven DJ, Hall JS (2013) Key role of symbiotic dinitrogen fixation in tropical forest secondary succession. Nature 502:224–227. doi:10.1038/nature12525
Branscheid A, Sieh D, Pant BD, May P, Devers EA, Elkorg A, Schauser L, Scheible WR, Krajinski F (2010) Expression pattern suggests a role of MiR399 in the regulation of the cellular response to local Pi increase during arbuscular mycorrhizal symbiosis. Mol Plant-Microbe Interact 23:915–926. doi:10.1094/MPMI-23-7-0915
Breakspear A, Liu C, Roy S, Stacey N, Rogers C, Trick M, Morieri G, Mysore KS, Wen J, Oldroyd GE, Downie GA, Murray JD (2014) The root hair ‘infectome’ of Medicago truncatula uncovers changes in cell cycle genes and reveals a requirement for auxin signaling in rhizobial infection. Plant Cell 26:4680–4701. doi:10.1105/tpc.114.133496
Brockwell J, Bottomley PJ, Thies JE (1995) Manipulation of rhizobia microflora for improving legume productivity and soil fertility: a critical assessment. Plant Soil 174:143–180. doi:10.1007/BF00032245
Browse J (2009) Jasmonate passes muster: a receptor and targets for the defense hormone. Annu Rev Plant Biol 60:183–205. doi:10.1146/annurev.arplant.043008.092007
Bullerjahn GS, Post AF (2014) Physiology and molecular biology of acquatic cyanobacteria. Front Microbiol 5:359. doi:10.3389/fmicb.2014.00359
Cabeza RA, Liese R, Lingner A, Stieglitz I, Neumann J, Salinas-Riester G, Pommerenke C, Dittert K, Schulze J (2014) 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. doi:10.1093/jxb/eru341
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. doi:10.1111/tpj.12751
Campbell BM, Thornton P, Zougmoré R, van Asten P, Lipper L (2014) Sustainable intensification: what is its role in climate smart agriculture? Curr Opin Environ Sustain 8:39–43. doi:10.1016/j.cosust.2014.07.002
Cardenas L, Martınez A, Sanchez F, Quinto C (2008) Fast, transient and specific intracellular ROS changes in living root hair cells responding to Nod factors (NFs). Plant J 56:802–813. doi:10.1111/j.1365-313X.2008.03644.x
Cardoso P, Freitas R, Figueira E (2015) Salt tolerance of rhizobial populations from contrasting environmental conditions: understanding the implications of climate change. Ecotoxicology 24:143–152. doi:10.1007/s10646-014-1366-8
Casteriano A, Wilkes MA, Deaker R (2013) Physiological changes in rhizobia after growth in peat extract may be related to improved desiccation tolerance. Appl Environ Microbiol 79:3998–4007. doi:10.1128/AEM.00082-13
Cernay C, Ben-Ari T, Pelzer E, Meynard J-M, Makowski D (2015) Estimating variability in grain legume yields across Europe and the Americas. Sci Rep 5:11171. doi:10.1038/srep11171
Chaia EE, Wall LG, Huss-Danell K (2010) Life in soil by the actinorhizal root nodule endophyte Frankia. A review. Symbiosis 5:201–226. doi:10.4161/psb.25453
Chandra A (2009) Diversity among Stylosanthes species: habitat, edaphic and agro-climatic affinities leading to cultivar development. J Environ Biol 30:471–478
Chaudhary MI, Adu-Gyamfi JJ, 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. doi:10.1007/s11738-008-0152-8
Chen C, Zhu H (2013) Are common symbiosis genes required for endophytic rice-rhizobial interactions? Plant Signal Behav 8:e25453. doi:10.4161/psb.25453
Chen YL, Dunbabin VM, Diggle AJ, Siddique KHM, Rengel Z (2013) Phosphorus starvation boosts carboxylate secretion in P-deficient genotypes of Lupinus angustifolius with contrasting root structure. Crop Pasture Sci 64:588–599. doi:10.1071/CP13012
Chiou T-J, Lin S-I (2011) Signaling network in sensing phosphate availability in plants. Annu Rev Plant Biol 62:185–206. doi:10.1146/annurev-arplant-042110-103849
Codex Alimentarius (2007) Cereals, pulses, legumes and vegetable proteins, 1st edn. WHO & FAO, Rome
COP21 (2015) http://www.cop21.gouv.fr/en/more-details-about-the-agreement/
Crews TE, Peoples MB (2004) Legume versus fertilizer sources of nitrogen. Agric Ecosyst Environ 102:279–297
Crook AD, Schnabel EL, Frugoli JA (2016) The systemic nodule number regulation kinase SUNN in Medicago truncatula interacts with MtCLV2 and MtCRN. Plant J. doi:10.1111/tpj.13234
Cytryn EJ, Sangurdekar DP, Streeter JG, Franck WL, Chang WS, Stacey G, Emerich DW, Joshi T, Xu D, Sadowsky MJ (2007) Transcriptional and physiological responses of Bradyrhizobium japonicum to desiccation induced stress. J Bacteriol 189:6751–6762. doi:10.1128/JB.01543-07
Czarnecki O, Yang J, Weston DJ, Tuskan GA, Chen J-G (2013) A dual role of strigolactones in phosphate acquisition and utilization in plants. Int J Mol Sci 14:7681–7701. doi:10.3390/ijms14047681
Danso SKA (1995) Assessment of biological nitrogen fixation. Fertil Res 42:33–41. doi:10.1007/BF00750498
de Lima M, Oresnik IJ, Fernando SM, Hunt S, Smith R, Turpin DH, Layzell DB (1994) The relationship between nodule adenylates and the regulation of nitrogenase activity by oxygen in soybean. Physiol Plant 91:687–695. doi:10.1111/j.1399-3054.1994.tb03006.x
Denison RF, Kiers ET (2004) Lifestyle alternatives for rhizobia: mutualism, parasitism, and forgoing symbiosis. FEMS Microbiol Lett 237:187–193. doi:10.1016/j.femsle.2004.07.013
Dilworth MJ (1966) Acetylene reduction by nitrogen-fixing preparations from Clostridium pasteurianum. Biochim Biophys Acta 127:285–294. doi:10.1016/0304-4165(66)90383-7
Djordjevic MA, Mohd-Radzman NA, Imin N (2015) Small peptide signals that control root nodule number, development, and symbiosis. J Exp Bot 66:5171–5181. doi:10.1093/jxb/erv357
Duff SMG, Sarath G, Plaxton WC (1994) The role of acid phosphatases in plant phosphorus metabolism. Physiol Plant 90:791–800. doi:10.1111/j.1399-3054.1994.tb02539.x
FAO (2013) Synthesis of guided principles on agriculture programming for nutrition. FAO, Rome
FAO (2015) Coping with climatic changes. The roles of genetic resources for food and agriculture. FAO, Rome
FAO (2016) http://www.fao.org/pulses-2016/en/
Fischinger SA, Schulze J (2010) The argon-induced decline in nitrogenase activity commences before the beginning of a decline in nodule oxygen uptake. J Plant Physiol 167:1112–1115. doi:10.1016/j.jplph.2010.03.014
Fournier J, Teillet A, Chabaud M, Ivanov S, Genre A, Limpens E, de Carvalho-Niebel F, Barker DG (2015) Remodeling of the infection chamber before infection thread formation reveals a two-step mechanism for rhizobial entry into the host legume root hair. Plant Physiol 167:1233–1242. doi:10.1104/pp.114.253302
Freund DM, Hegeman AD (2016) Recent advances in stable isotope-enabled mass spectrometry-based plant metabolites. Curr Opin Biotechnol 43:41–48. http://dx.doi.org/10.1016/j.copbio.2016.08.002
Goh C-H, Veliz Vallejos DF, Nicotra AB, Mathesius U (2013) The impact of beneficial plant-associated microbes on plant phenotypic plasticity. J Chem Ecol 39:826–839. doi:10.1007/s10886-013-0326-8
Gonzalez EM, Aparicio-Tejo PM, Gordon AJ, Minchin JR, Royuela M, Arrese-Igor C (1998) Water-deficit effects on carbon and nitrogen metabolism of pea nodules. J Exp Bot 49:1705–1714. doi:10.1093/jxb/49.327.1705
Gordon AJ, Skot L, James CL, Minchin FR (2002) Short-term metabolic responses of soybean root nodules to nitrate. J Exp Bot 53:423–428. doi:10.1093/jexbot/53.368.423
Guinel FC (2015) Ethylene a hormone at the center-stage of nodulation. Front Plant Sci 6:1121. doi:10.3389/fpls.2015.01121
Guo WB, Zhao J, Li XX, Qin L, Yan XL, Liao H (2011) A soybean β-expansin gene GmEXPB2 intrinsically involved in root system architecture responses to abiotic stresses. Plant J 66:541–552. doi:10.1111/j.1365-313X.2011.04511.x
Gupta R, Bisaria VS, Sharma S (2015) Effect of agricultural amendments on Cajanus cajan (pigeon pea) and its rhizospheric microbial communities – a comparison between chemical fertilizers and bioinoculants. PLoS One 10:e0132770. doi:10.1371/journal.pone.0132770
Gutiérrez-Boem FH, Thomas GW (1999) Phosphorus nutrition and water deficit in field-grown soybeans. Plant Soil 207:87–96. doi:10.1023/A:1004469403667
Gyaneshwar P, Hirsch AM, Moulin L, Chen WM, Elliott GN, Bontemps C, Estrada-de Los Santos P, Gross E, Dos Reis FB, Sprent JI, Young JP, James EK (2011) Legume-nodulating betaproteobacteria: diversity, host range, and future prospects. Mol Plant Microbe Interact 24:1276–1288. doi:10.1094/MPMI-06-11-0172
Haag AF, Arnold MF, Myka KK, Kerscher B, Dall’Angelo S, Zanda M, Mergaert P, Ferguson GP (2013) Molecular insights into bacteroid development during Rhizobium-legume symbiosis. FEMS Microbiol Rev 37:364–383. doi:10.1111/1574-6976.12003
Hammond JP, White PJ (2011) Sugar signaling in root responses to low phosphorus availability. Plant Physiol 156:1033–1040. doi:10.1104/pp.111.175380
Hardy RWF, Holsten RD, Jackson EK, Burns RC (1968) The acetylene-ethylene assay for N2-fixation: laboratory and field evaluation. Plant Physiol 43:1185–1207. doi:10.1104/pp.43.8.1185
Hernández G, Ramírez M, Valdés-López O, Tesfaye M, Graham MA, Czechowski T, Schlereth A, Wandrey M, Erban A, Cheung F, Wu HC, Lara M, Town CD, Kopka J, Udvardi MK, Vance CP (2007) Phosphorus stress in common bean: root transcript and metabolic responses. Plant Physiol 144:752–767. doi:10.1104/pp.107.096958
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. doi:10.1104/pp.109.143842
Høgh-Jensen H, Schjoerring JK, Soussana J-F (2002) The influence of phosphorus deficiency on growth and nitrogen fixation of white clover plants. Ann Bot 90:745–753. doi:10.1093/aob/mcf260
Hu Y, Ribbe MW (2015) Nitrogenase and homologs. J Biol Inorg Chem 20:435–445. doi:10.1007/s00775-014-1225-3
Hunt S, King BJ, Canvin DT, Layzell DB (1987) Steady and non steady state gas exchange characteristics of soybean nodules in relation to the oxygen diffusion barrier. Plant Physiol 84:164–172
IPCC (2007) Climate change impacts, adaptation and vulnerability working group II. Contribution to the intergovernmental panel on climate change. In Fourth Assessment Report. Summary for policymakers
James EK, Olivares FL, Baldani JI, Döbereiner J (1997) Herbaspirillum, an endophytic diazotroph colonizing vascular tissue in the leaves of Sorghum bicolor. J Exp Bot 48:785–798. doi:10.1093/jxb/48.3.785
Ji KX, Chi F, Yang MF, Shen SH, Jing YX, Dazzo FB, Cheng HP (2010) Movement of rhizobia inside tobacco and lifestyle alternation from endophytes to free-living rhizobia on leaves. J Microbiol Biotechnol 20:238–244. doi:10.4014/jmb.0906.06042
Jia H, Ren H, Gu M, Zhao J, Sun S, Zhang X, Chen J, Wu P, Xu G (2011) The phosphate transporter gene OsPht1;8 is involved in phosphate homeostasis in rice. Plant Physiol 156:1164–1175. doi:10.1104/pp.111.175240
Jones-Rhoades MW, Bartel DP, Bartel B (2006) MicroRNAS and their regulatory roles in plants. Annu Rev Plant Biol 57:19–53. doi:10.1146/annurev.arplant.57.032905.105218
Kerr RB, Shumba L, Dakishoni L, Lupafya E, Berti PR, Classen L, Snapp SS, Katundu M (2013) Participatory, agroecological and gender-sensitive approaches to improved nutrition: a case study in Malawi. FAO Expert Meeting ‘Nutrition-Sensitive Food and Agriculture Systems’
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. doi:10.1016/j.jplph.2014.07.017
Knowles R (1980) Nitrogen fixation in natural plant communities and soils. In: Bergersen FJ (ed) Methods for evaluating biological nitrogen fixation. Wiley, New York, pp 557–582
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. doi:10.1051/agro:2005034
Lambers H, Raven JA, Shaver GR, Smith SE (2008) Plant nutrient-acquisition strategies change with soil age. Trends Ecol Evol 23:95–103. doi:10.1016/j.tree.2007.10.008
Larrainzar E, Riely BK, Kim SC, Carrasquilla-Garcia N, Yu HJ, Hwang HJ, Oh M, Kim GB, Surendrarao AK, Chasman D, Siahpirani AF, Penmetsa RV, Lee GS, Kim N, Roy S, Mun JH, Cook DR (2015) Deep sequencing of the Medicago truncatula root transcriptome reveals a massive and early interaction between nodulation factor and ethylene signals. Plant Physiol 169:233–265. doi:10.1104/pp.15.00350
Layzell DB, Gaito ST, Hunt S (1988) Model of gas exchange and diffusion in legume nodules (I. Calculation of gas exchange rates and the energy cost of N2 fixation). Planta 173:117–127. doi:10.1007/BF00394496
Lazali M, Zaman-Allah M, Amenc L, Ounane G, Abadie J, Drevon JJ (2013) A phytase gene is overexpressed in root nodules cortex of Phaseolus vulgaris–rhizobia symbiosis under phosphorus deficiency. Planta 238:317–324. doi:10.1007/s00425-013-1893-1
Lelandais-Briere C, Naya L, Sallet E, Calenge F, Frugier F, Hartmann C, Gouzy J, Crespi M (2009) Genome-wide Medicago truncatula small RNA analysis revealed novel microRNAs and isoforms differentially regulated in roots and nodules. Plant Cell 21:2780–2796. doi:10.1105/tpc.109.068130
Li L, Zhang F, Li X, Christie P, Sun J, Yang S, Tang C (2003) Interspecific facilitation of nutrient uptake by intercropped maize and faba bean. Nutr Cycl Agroecosyst 65:61–71. doi:10.1023/A:1021885032241
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. doi:10.1093/aob/mcr246
Li C, Dong Y, Li H, Shen J, Zhang F (2015a) Shift from complementarily to facilitate on P uptake by intercropped wheat neighboring with faba bean when available soil P is depleted. Sci Rep 6:18663. doi:10.1038/srep18663
Li Y, Xu M, Wang N, Li Y (2015b) A JAZ protein in Astragalus sinicus interacts with a leghemoglobin through the TIFY domain and is involved in nodule development and nitrogen fixation. PLoS One 10:1–18. doi:10.1371/journal.pone.0139964
Lin W-Y, Lin S-I, Chiou T-J (2009) Molecular regulators of phosphate homeostasis in plants. J Exp Bot 60:1427–1438. doi:10.1093/jxb/ern303
Lin W-Y, Huang T-K, Leong SJ, Chiou T-J (2014) Long-distance call from phosphate: systemic regulation of phosphate starvation responses. J Exp Bot 65:1817–1827. doi:10.1093/jxb/ert431
Liu J, Samac DA, Bucciarelli B, Allan DL, Vance CP (2005) Signaling of phosphorus deficiency-induced gene expression in white lupin requires sugar and phloem transport. Plant J 41:257–268. doi:10.1111/j.1365-313X.2004.02289.x
Liu P, Chen S, Song A, Zhao S, Fang W, Guan Z, Liao Y, Jiang J, Chen F (2014a) A putative high affinity phosphate transporter, CmPT1, enhances tolerance to Pi deficiency of chrysanthemum. BMC Plant Biol 14:18. doi:10.1186/1471-2229-14-18
Liu C-W, Sung Y, Chen B-C, Lai H-Y (2014b) Effects of nitrogen fertilizers on the growth and nitrate content of lettuce (Lactuca sativa L.) Int J Environ Res Public Health 11:4427–4440. doi:10.3390/ijerph110404427
Liu P, Xue Y-B, Chen Z-J, Liu G-D, Tian J (2016) Characterization of purple acid phosphatases involved in extracellular dNTP utilization in Stylosanthes. J Exp Bot 67:4141–4154. doi:10.1093/jxb/erw190
Lohar DP, Haridas S, Gantt JS, VandenBosch KA (2007) A transient decrease in reactive oxygen species in roots leads to root hair deformation in the legume-rhizobia symbiosis. New Phytol 173:39–49. doi:10.1111/j.1469-8137.2006.01901.x
Magadlela A, Kleinert A, Dreyer L, Valentine AJ (2014) Low-phosphorus conditions affect the nitrogen nutrition and associated carbon costs of two legume tree species from a Mediterranean-type ecosystem. Aust J Bot 62:1–9. doi:10.1071/BT13264
Marlow VL, Haah AF, Kobayashi H, Fletcher V, Scocchi M, Walker GC, Ferguson GP (2009) Essential role for the BacA protein in the uptake of a truncated eukaryotic peptide in Sinorhizobium meliloti. J Bacteriol 191:1519–1527. doi:10.1128/JB.01661-08
Marschner H, Marschner P (2012) Marschner’s mineral nutrition of higher plants. Academic Press, Amsterdam
Matar A, Torrent J, Ryan J (1992) Soil and fertilizer phosphorus and crop responses in the dryland mediterranean zone. Adv Soil Sci 18:81–146. doi:10.1007/978-1-4612-2844-8_3
McAuliffe CC, Chamblee DS, Uribe-Arango H, Woodhouse WW Jr (1958) Influence of inorganic nitrogen on nitrogen fixation by legumes as revealed by 15N dilution method. Agron J 50:334–337. doi:10.2134/agronj1958.00021962005000060014x
McIntyre HJ, Davies H, Hore TA, Miller SH, Dufour JP, Ronson CW (2007) Trehalose biosynthesis in Rhizobium leguminosarum bv. trifolii and its role in desiccation tolerance. Appl Environ Microbiol 73:3984–3992. doi:10.1128/AEM.00412-07
Mergaert P, Uchiumi T, Alunni B, Evanno G, Cheron A, Catrice O, Mausset AE, Barloy-Hubler F, Galibert F, Kondorosi A, Kondorosi E (2006) Eukaryotic control on bacterial cell cycle and differentiation in the Rhizobium-legume symbiosis. Proc Natl Acad Sci U S A 103:5230–5235. doi:10.1073/pnas.0600912103
Messina MJ (1999) Legumes and soybeans: overview of their nutritional profiles and health effects. Am J Clin Nutr 70:439–450
Mhamdi R, Nouairi I, ben Hammouda T, Mhamdi R, Mhadhbi H (2015) Growth capacity and biochemical mechanisms involved in rhizobia tolerance to salinity and water deficit. J Basic Microbiol 55:451–461. doi:10.1002/jobm.201400451
Miguel MA, Widrig A, Vieira RF, Brown KM, Lynch JP (2013) Basal root whorl number: a modulator of phosphorus acquisition in common bean (Phaseolus vulgaris). Ann Bot 112:973–982. doi:10.1093/aob/mct164
Minami T, Anda M, Mitsui H, Sugawara M, Kaneko T, Sato S, Ikeda S, Okubo T, Tsurumaro H, Minamisawa K (2016) Metagenomic analysis revealed methylamine and ureide utilization of soybean-associated Methylbacterium. Microbes Environ. doi:10.1264/jsme2.ME16035
Minchin FR, Sheehy JE, Witty JF (1986) Further errors in the acetylene reduction assay: effect of plant disturbance. J Exp Bot 37:1581–1591
Mochida K, Shinozaki K (2011) Advances in omics and bioinformatics tools for systems analyses of plant functions. Plant Cell Physiol 52:2017–2038. doi:10.1093/pcp/pcr153
Molero G, Aranjuelo I, Teixidor P, Araus JL, Nogue S (2011) Measurement of 13C and 15N isotope labeling by gas chromatography/combustion/isotope ratio mass spectrometry to study amino acid fluxes in a plant–microbe symbiotic association. Rapid Commun Mass Spectrom 25:599–607. doi:10.1002/rcm.4895
Moloney AHM, Layzell DB (1993) A model of the regulation of nitrogenase electron allocation in legume nodules (I. The diffusion barrier and H2 inhibition of N2 fixation). Plant Physiol 103:421–428
Moloney AHM, Guy RD, Layzell DB (1994) A model of the regulation of nitrogenase electron allocation in legume nodules (II. Comparison of empirical and theoretical studies in soybean). Plant Physiol 104:541–550
Mori A, Fukuda T, Vejchasarn P, Nestler J, Pariasca-Tanaka J, Wissuwa M (2016) The role of root size versus root efficiency in phosphorus acquisition in rice. J Exp Bot 67:1179–1189. doi:10.1093/jxb/erv557
Mortier V, Holsters M, Goormachtig S (2012) Never too many? How legumes control nodule numbers. Plant Cell Environ 35:245–258. doi:10.1111/j.1365-3040.2011.02406.x
Mus F, Crook MB, Garcia K, Costas AG, Geddes BA, Kouri ED, Paramasivan P, Ryu M-H, Oldroyd GED, Poole PS, Udvardi MK, Voigt CA, Ané J-M, Peters JW (2016) Symbiotic nitrogen fixation and the challenges to its extension to nonlegumes. Appl Environ Microbiol 82:3698–3710. doi:10.1128/AEM.01055-16
Nasr Esfahani MN, Kusano M, Nguyen KH, Watanabe Y, Van Ha C, Saito K, Sulieman S, Herrera-Estrella L, Tran L-SP (2016) Adaption of the symbiotic Mesorhizobium –chickpea relationship to phosphate deficiency relies on reprogramming of whole-plant metabolism. Proc Natl Acad Sci 113:4610–4619. doi:10.1073/pnas.1609440113
Negi M, Sanagala R, Rai V, Jain A (2016) Deciphering phosphate deficiency-mediated temporal effects on different root traits in rice grown in a modified hydroponic system. Front Plant Sci 7:550. doi:10.3389/fpls.2016.00550
Nova-Franco B, Íñiguez LP, Valdés-López O, ALvarado-Affantranger X, Leija A, Fuentes SI, Ramírez M, Paul S, Reyes JL, Girard L, Hernández G (2015) The micro-RNA172c-APETALA2-1 node as a key regulator of the common bean- Rhizobium etli nitrogen fixation symbiosis. Plant Physiol 168:273–291. doi:10.1104/pp.114.255547
Ohkama-Ohtsu N, Ichida S, Yamaya H, Ohwada T, Itakura M, Hara Y, Mitsui H, Kaneko T, Tabata S, Tejima K, Saeki K, Omori H, Hayashi M, Maekawa T, Murooka Y, Tajima S, Simomura K, Nomura M, Uchiumi T, Suzuki A, Shimoda Y, Abe M, Minamisawa K, Arima Y, Yokoyama T (2015) Peribacteroid solution of soybean root nodules partly induces genomic loci for differentiation into bacteroids of free-living Bradyrhizobium diazoefficiens cells. Soil Sci Plant Nutr 61:461–470. doi:10.1080/00380768.2014.994470
Oldroyd GE, Murray JD, Poole PS, Downie JA (2011) The rules of engagement in the legume-rhizobial symbiosis. Annu Rev Genet 45:119–144. doi:10.1146/annurev-genet-110410-132549
Olivera M, Tejera N, Iribarne C, Ocaña A, Lluch C (2004) Growth, nitrogen fixation and ammonium assimilation in common bean (Phaseolus vulgaris): effect of phosphorus. Physiol Plant 121:498–505. doi:10.1111/j.0031-9317.2004.00355.x
Peláez P, Trejo MS, Iñiguez LP, Estrada-Navarrete G, Covarrubias AA, Reyes JL, Sanchez F (2012) Identification and characterization of microRNAs in Phaseolus vulgaris by high-throughput sequencing. BMC Genomics 13:83. doi:10.1186/1471-2164-13-83
Peleg-Grossman S, Volpin H, Levine A (2007) Root hair curling and Rhizobium infection in Medicago truncatula are mediated by phosphatidylinositide regulated endocytosis and reactive oxygen species. J Exp Bot 58:1637–1649. doi:10.1093/jxb/erm013
Plaxton WC, Tran HT (2011) Metabolic adaptations of phosphate-starved plants. Plant Physiol 156:1006–1015. doi:10.1104/pp.111.175281
Priefer UB, Aurag J, Boesten B, Bouhmouch I, Defez R, Filali-Maltouf A, Miklis M, Moawad H, Mouhsine B, Prell J, Schluter A, Senatore B (2001) Characterisation of Phaseolus symbionts isolated from Mediterranean soils and analysis of genetic factors related to pH tolerance. J Biotechnol 91:223–236. doi:10.1016/S0168-1656(01)00329-7
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 tonodules and nodulation in soybean. Plant Physiol 159:1634–1643. doi:10.1104/pp.112.199786
Qin S, Tang Y, Chen Y, Wu P, Li M, Wu G, Jiang H (2016) Overexpression of the starch phosphatase-like gene (PHO3) in Lotus japonicus has a profound effect on the growth of plants and reduction of transitory starch accumulation. Front Plant Sci 7:1315. doi:10.3389/fpls.2016.01315
Ramírez M, Flores-Pacheco G, Reyes JL, Luzlvarez A, Drevon JJ, Girard L, Hernández G (2013) Two common bean genotypes with contrasting response to phosphorus deficiency show variations in the microRNA 399-mediated PvPHO2 regulation within the PvPHR1 signaling pathway. Int J Mol Sci 14:8328–8344. doi:10.3390/ijms14048328
Ramos MLG, Gordon AJ, Minchin FR, Sprent JI, Parsons R (1999) Effect of water stress on nodule physiology and biochemistry of a drought tolerant cultivar of common bean (Phaseolus vulgaris L.) Ann Bot 83:57–63
Reed SC, Cleveland CC, Townsend AR (2011) Functional ecology of free-living nitrogen fixation: a contemporary perspective. Annu Rev Ecol Evol Syst 42:489–512. doi:10.1146/annurev-ecolsys-102710-145034
Reid DE, Heckmann AB, Novák O, Kelly S, Stougaard J (2016) CYTOKININ OXIDASE/DEHYDROGENASE3 maintains cytokinin homeostasis during root and nodule development in Lotus japonicus. Plant Physiol 170:1060–1074. doi:10.1104/pp.15.00650
Rejili M, Mahdhi M, Fterich A, Dhaoui S, Guefrachi I, Andeddayem R, Mars M (2012) Symbiotic nitrogen fixation of wild legumes in Tunisia: soil fertility dynamics, field nodulation and nodules effectiveness. Agric Ecosyst Environ 157:60–69. doi:10.1016/j.agee.2012.01.015
Ribaudo M, Delgado J, Hansen L, Livingston M, Mosheim R, Williamson J (2011) Nitrogen in agricultural systems: implications for conservation policy, USDA Economic Research report, vol 127. BiblioGov, Charleston. ERR-127. U.S. Dept. of Agriculture, Econ. Res. Serv. September 2011
Richardson AE, Simpson RJ (2011) Soil microorganisms mediating phosphorus availability update on microbial phosphorus. Plant Physiol 56:989–996. doi:10.1104/pp.111.175448
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. doi:10.1007/s11104-011-0950-4
Rivas R, Willems A, Subba-Rao NS, Mateos PF, Dazzo FB, Kroppenstedt RM, Martínez-Molina E, Gillis M, Velázquez E (2003) Description of Devosia neptuniae sp. nov. that nodulates and fixes nitrogen in symbiosis with Neptunia natans, an aquatic legume from India. Syst Appl Microbiol 26:47–53. doi:10.1078/072320203322337308
Rodrı́guez H, Fraga R (1999) Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol Adv 17:319–339. doi:10.1016/S0734-9750(99)00014-2
Rozrokh M, Sabaghpour SH, Armin M, Asgharipour M (2012) The effects of drought stress on some biochemical traits in twenty genotypes of chickpea. Eur J Exp Biol 2:1980–1987
Ruiz-Lozano JM (2003) Arbuscular mycorrhizal symbiosis and alleviation of osmotic stress. New perspectives for molecular studies. Mycorrhiza 13:309–317. doi:10.1007/s00572-003-0237-6
Rychter AM, Randall DD (1994) The effect of phosphate deficiency on carbohydrate metabolism in bean roots. Physiol Plant 91:383–388. doi:10.1111/j.1399-3054.1994.tb02964.x
Sa T-M, Israel DW (1991) Energy status and functioning of phosphorus-deficient soybean nodules. Plant Physiol 97:928–935
Sahoo RK, Ansari MW, Dangar TK, Mohanty S, Tuteja N (2014) Phenotypic and molecular characterisation of efficient nitrogen-fixing Azotobacter strains from rice fields for crop improvement. Protoplasma 251:511–523. doi:10.1007/s00709-013-0547-2
Saia S, Amato G, Frenda AS, Giambalvo D, Ruisi P (2014) Influence of arbuscular mycorrhizae on biomass production and nitrogen fixation of berseem clover plants subjected to water stress. PLoS One 9:e90738. doi:10.1371/journal.pone.0090738
Salazar-Henao JE, Vélez-Bermúdez IC, Schmidt W (2016) The regulation and plasticity of root hair patterning and morphogenesis. Development 143:1848–1858. doi:10.1242/dev.132845
Sarker BC, Karmoker JL (2011) Effects of phosphorus deficiency on accumulation of biochemical compounds in lentil (Lens culinaris Medik.) Bangladesh J Bot 40:23–27. doi:10.3329/bjb.v40i1.7992
Schaller GE, Bishopp A, Kieber JJ (2015) The yin-yang of hormones: cytokinin and auxin interactions in plant development. Plant Cell 27:44–63. doi:10.1105/tpc.114.133595
Schulze J (2004) How are nitrogen fixation rates regulated in legumes? J Plant Nutr Soil Sci 167:125–137. doi:10.1002/jpln.200320358
Schulze J, Drevon J-J (2005) P-deficiency increases the O2 uptake per N2 reduced in alfalfa. J Exp Bot 56:1779–1784. doi:10.1093/jxb/eri166
Schulze J, Temple G, Temple SJ, Beschow H, Vance CP (2006) Nitrogen fixation by white lupin under phosphorus deficiency. Ann Bot 98:731–740. doi:10.1093/aob/mcl154
Seefeldt LC, Hoffman BH, Dean DR (2009) Mechanism of Mo-dependent nitrogenase. Annu Rev Biochem 78:701–722. doi:10.1146/annurev.biochem.78.070907.103812
Serraj R, Vadez V, Sinclair TR (2001) Feedback regulation of symbiotic N2 fixation under drought stress. Agronomie 21:621–626. doi:10.1051/agro:2001153
Sha A, Li M, Yang P (2016) Identification of phosphorus deficiency responsive proteins in a high phosphorus acquisition soybean (Glycine max) cultivar through proteomic analysis. Biochim Biophys Acta 1864:427–434. doi:10.1016/j.bbapap.2016.02.001
Shane MW, Lambers H (2005) Cluster roots: a curiosity in context. Plant Soil 274:101–125. doi:10.1007/s11104-004-2725-7
Shearer G, Kohl DH (1986) N2 fixation in field settings: estimations based on natural 15N abundance. Aust J Plant Physiol 13:699–756. doi:10.1071/PP9860699
Singh DK, Sale PWG, McKenzie BM (1997) Water relations of white clover (Trifolium repens L.) in a drying soil, as a function of phosphorus supply and defoliation frequency. Aust J Agric Res 48:675–681. doi:10.1071/A96156
Singh JS, Kumar A, Rai AN, Singh DP (2016) Cyanobacteria: a precious bio-resource in agriculture, ecosystem, and environmental sustainability. Front Microbiol 7:529. doi:10.3389/fmicb.2016.00529
Smith FW, Jackson WA (1987) Nitrogen enhancement of phosphate transport in roots of Zea mays L. (I. Effects of ammonium and nitrate pretreatment). Plant Physiol 84:1314–1318
Smith FA, Jakobsen I, Smith SE (2000) Spatial differences in acquisition of soil phosphate between two arbuscular mycorrhizal fungi in symbiosis with Medicago truncatula. New Phytol 147:357–366. doi:10.1046/j.1469-8137.2000.00695.x
Sprent JI, James EK (2007) Legume evolution: where do nodules and mycorrhizas fit in? Plant Physiol 144:575–581. doi:10.1104/pp.107.096156
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. doi:10.1016/j.jprot.2016.01.006
Streeter JG (2003) Effect of trehalose on survival of Bradyrhizobium japonicum during desiccation. J Appl Microbiol 95:484–491. doi:10.1046/j.1365-2672.2003.02017.x
Sulieman S, Tran L-SP (2015) Phosphorus homeostasis in legume nodules as an adaptive strategy to phosphorus deficiency. Plant Sci 239:36–43. doi:10.1016/j.plantsci.2015.06.018
Sulieman S, Schulze J, Tran LS (2013a) Comparative analysis of the symbiotic efficiency of Medicago truncatula and Medicago sativa under phosphorus deficiency. Int J Mol Sci 14:5198–5213. doi:10.3390/ijms14035198
Sulieman S, Van Ha C, Schulze J, Tran LSP (2013b) Growth and nodulation of symbiotic Medicago truncatula at different levels of phosphorus availability. J Exp Bot 64:2701–2712. doi:10.1093/jxb/ert122
Sullivan BW, Smith WK, Townsend AR, Nasto MK, Reed SC, Chazdon RL, Cleveland CC (2014) Spatially robust estimates of biological nitrogen (N) fixation imply substantial human alteration of the tropical N cycle. Proc Natl Acad Sci U S A 111:8101–8106. doi:10.1073/pnas.1320646111
Suter M, Connolly J, Finn JA, Loges R, Kirwan L, Sebastia M-T, Lüscher A (2015) Nitrogen yield advantage from grass-legume mixtures is robust over a wide range of legume proportions and environmental conditions. Glob Chang Biol 21:2424–2438. doi:10.1111/gcb.12880
Svistoonoff S, Creff A, Reymond M, Sigoillot-Claude C, Ricaud L, Blanchet A, Nussaume L, Desnos T (2007) Root tip contact with low-phosphate media reprograms plant root architecture. Nat Genet 39:792–796. doi:10.1038/ng2041
Tatsukami Y, Nambu M, Morisaka H, Kuroda K, Ueda M (2013) Disclosure of the differences of Mesorhizobium loti under the free-living and symbiotic conditions by comparative proteome analysis without bacteroid isolation. BMC Microbiol 13:180. doi:10.1186/1471-2180-13-180
Teijma K, Arima Y, Yokoama T, Sekimoto H (2003) Composition of amino acids, organic acids, and sugars in the peribacteroid space of soybean root nodules. Soil Sci Plant Nutr 49:239–247. doi:10.1080/00380768.2003.10410003
Tesfaye M, Liu J, Allan DL, Vance CP (2007) Genomic and genetic control of phosphate stress in legumes. Plant Physiol 144:594–603. doi:10.1104/pp.107.097386
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. doi:10.1016/j.jplph.2013.09.001
Ticconi CA, Delatorre CA, Lahner B, Salt DE, Abel S (2004) Arabidopsis pdr2 reveals a phosphate-sensitive checkpoint in root development. Plant J 37:801–814. doi:10.1111/j.1365-313X.2004.02005.x
Tilman D, Cassman KG, Matson PA, Naylor R, Polasky S (2002) Agricultural sustainability and intensive production practices. Nature 418:671–677. doi:10.1038/nature01014
Toth K, Stacey G (2015) Does plant immunity play a critical role during initiation of the legume-rhizobium symbiosis? Front Plant Sci 6:401. doi:10.3389/fpls.2015.00401
Tredeser KK, Vitousek PM (2001) Effects of soil nutrient availability on investment in acquisition of N and P in Hawaiian rain forests. Ecology 82:946–954. doi:10.1890/0012-9658(2001)082[0946:EOSNAO]2.0.CO;2
Uhde-Stone C, Zinn KE, Ramírez-Yañez M, Li A, Vance CP, Allan DL (2003) Nylon filter arrays reveal differential gene expression in proteoid roots of white lupin in response to phosphorus deficiency. Plant Physiol 131:1064–1079. doi:10.1104/pp.102.016881
Valdés-López O, Hernández G (2008) Transcriptional regulation and signaling in phosphorus starvation: what about legumes? J Integr Plant Biol 5:1213–1222. doi:10.1111/j.1744-7909.2008.00758.x
Valdés-López O, Yang SS, Aparicio-Fabre R, Graham PH, Reyes JL, Vance CP, Hernández G (2010) MicroRNA expression profile in common bean (Phaseolus vulgaris) under nutrient deficiency stresses and manganese toxicity. New Phytol 187:805–818. doi:10.1111/j.1469-8137.2010.03320.x
van Berkum PR, Tully E, Keister DL (1995) Nonpigmented and bacteriochlorophyll-containing bradyrhizobia isolated from Aeschynomene indica. Appl Environ Microbiol 61:623–629
van Noorden EE, Verbeek R, Dinh QD, Jin J, Green A, Ng JLP, Mathesius U (2016) Molecular signals controlling the inhibition of nodulation by nitrate in Medicago truncatula. Int J Mol Sci 17:1060. doi:10.3390/jims17071060
Vance CP, Uhde-Stone C, Allan D (2003) Phosphorus acquisition and use: critical adaptation by plants for securing non-renewable resources. New Phytol 157:423–447. doi:10.1046/j.1469-8137.2003.00695.x
Vanderlinde EM, Harrison JJ, Muszyński A, Carlson RW, Turner RJ, Yost CK (2010) Identification of a novel ABC transporter required for desiccation tolerance, and biofilm formation in Rhizobium leguminosarum bv. viciae 3841. FEMS Microbiol Ecol 71:327–340. doi:10.1111/j.1574-6941.2009.00824.x
Vessey JK (1994) Measurement of nitrogenase activity in legume root nodules: in defense of the acetylene reduction assay. Plant Soil 158:151–162. doi:10.1007/BF00009490
Vitousek PM, Menge DNL, Reed SC, Cleveland CC (2013) Biological nitrogen fixation: rates, patterns and ecological controls in terrestrial ecosystems. Philos Trans R Soc Lond B Biol Sci 368:20130119. doi:10.1098/rstb.2013.0119
Volpe V, Giovannetti M, Sun X-G, Fiorilli V, Bonfante P (2016) The phosphate transporters LjPT4 and MtPT4 mediate early root responses to phosphate status in non mycorrhizal roots. Plant Cell Environ 39:660–671. doi:10.1111/pce.12659
Vriezen JA, de Bruijn FJ, Nüsslein K (2007) Responses of rhizobia to desiccation in relation to osmotic stress, oxygen, and temperature. Appl Environ Microbiol 73:3451–3459. doi:10.1128/AEM.02991-06
Wang X, Pan QA, Chen FX, Yan XL, Liao H (2011) Effects of co-inoculation with arbuscolar mychorrizal fungi and rhizobia on soybean growth as related to root architecture and availability of N and P. Mycorrhiza 21:173–181. doi:10.1007/s00572-010-0319-1
Wang X, Veneklaas EJ, Pearse SJ, Lambers H (2015) Interactions among cluster-root investment, leaf phosphorus concentration, and relative growth rate in two Lupinus species. Am J Bot 102:1529–1537. doi:10.3732/ajb.1500268
Watanabe T, Osaki M, Tadano T (1998) Effects of nitrogen source and aluminum on growth of tropical tree seedlings adapted to low pH soils. Soil Sci Plant Nutr 44:655–656. doi:10.1080/00380768.1998.10414489
Weaver RW, Danso SKA (1994) Dinitrogen fixation. In: Weaver RW, Angle S, Bottomley P, Bezdicek D, Tabatabai A, Wollum A (eds) Methods of soil analysis. Part 2, Microbiological and biochemical properties. Soil Sci Soc Am, Madison, pp 1019–1045. doi:10.2136/sssabookser5.2
Weese DJ, Heath KD, Dentinger BT, Lau JA (2015) Long-term nitrogen addition causes the evolution of less-cooperative mutualists. Evolution 69:631–642. doi:10.1111/evo.12594
Wei H, Atkins CA, Layzell DB (2004) Adenylate gradients and Ar:O2 effects on legume nodules (II. Changes in the subcellular adenylate pools). Plant Physiol 134:1775–1783. doi:10.1104/pp.103.038547
Xu J, Xiao-Lin L, Luo L (2012) Effects of engineered Sinorhizobium meliloti on cytokinin synthesis and tolerance of alfalfa to extreme drought stress. Appl Environ Microbiol 78:8056–8061. doi:10.1128/AEM.01276-12
Xue Y, Xia H, Christie P, Zhang Z, Li L, Tang C (2016) Crop acquisition of phosphorus, iron and zinc from soil in cereal/legume intercropping systems: a critical review. Ann Bot 117:363–377. doi:10.1093/aob/mcv182
Yanni YG, Rizk RY, Corich V, Squartini A, Ninke K, Philip-Hollingsworth S, Orgambide G, de Bruijn F, Stoltzfus J, Buckley D, Schmidt TM, Mateos PF, Ladha JK, Dazzo FB (1997) Natural endophytic association between Rhizobium leguminosarum bv. trifolii and rice roots and assessment of its potential to promote rice growth. Plant Soil 194:99–114. doi:10.1023/A:1004269902246
Yao Z-F, Liang C-Y, Zhang Q, Chen Z-Y, Xiao B-I, Tian J, Liao H (2014) SPX1 is an important component in the phosphorus signalling network of common bean regulating root growth and phosphorus homeostasis. J Exp Bot 12:3299–3310. doi:10.1093/jxb/eru183
Yuan P, Ding G-D, Cai H-M, Jin K-M, Broadley MR, Xu F-S, Shi L (2016) A novel Brassica-rhizotron system to unravel the dynamic changes in root system architecture of oilseed rape under phosphorus deficiency. Ann Bot 118:173–184. doi:10.1093/aob/mcw083
Zehr JP, Ward BB (2002) Nitrogen cycling in the ocean: new perspectives on processes and paradigms. Appl Environ Microbiol 68:1015–1024. doi:10.1128/AEM.68.3.1015-1024.2002
Zeng HQ, Zhu YY, Huang SQ, Yang ZM (2010) Analysis of phosphorus-deficient responsive miRNAs and cis-elements from soybean (Glycine max L.) J Plant Physiol 167:1289–1297. doi:10.1016/j.jplph.2010.04.017
Zeng HQ, Liu G, Kinoshita T, Zhang R, Zhu Y, Shen Q, Xu G (2012) Stimulation of phosphorus uptake by ammonium nutrition involves plasma membrane H+ ATPase in rice roots. Plant Soil 357:205–214. doi:10.1007/s11104-012-1136-4
Zhang J, Yin B, Xie Y, Li J, Yang Z, Zhang G (2015) Legume-cereal intercropping improves forage yield, quality and degradability. PLoS One 10:e0144813. doi:10.1371/journal.pone.0144813
Zhao XQ, Shen RF, Sun QB (2009) Ammonium under solution culture alleviates aluminum toxicity in rice and reduces aluminum accumulation in roots compared with nitrate. Plant Soil 315:107–121. doi:10.1007/s11104-008-9736-8
Zhu CQ, Zhu XF, Hu AY, Wang C, Wang B, Dong XY, Shen RF (2016) Differential effects of nitrogen forms on cell wall phosphorus remobilization in rice (Oryza sativa) are mediated by nitric oxide, pectin content, and phosphate transporter expression. Plant Physiol 171:1407–1417. doi:10.1104/pp.16.00176
Acknowledgments
The financial support from the University of Pavia (Italy) and Fundação para a Ciência e a Tecnologia (Lisbon, Portugal) is acknowledged through the research unit “GREEN-it: Bioresources for Sustainability” (UID/Multi/04551/2013), GREEN-IT fellowship of D.M (036/BTI/2016), PhD grant (PD/BD/128498/2017) of D.M. within the scope of the PhD program Plants for Life (PD/00035/2013) and S.S.A. postdoctoral grant (SFRH/BPD/108032/2015). This work has been partially supported by Reg.CE n. 1698/2005 Programma di Sviluppo rurale per la Puglia 2007/2013 (Misura 214 – Azione 4 Sub azione a) “SaVeGraINPuglia – Progetti integrati per la Biodiversità- Recupero, caratterizzazione, salvaguardia e valorizzazione di leguminose, cereali da granella e foraggio in Puglia.”
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2017 Springer International Publishing AG
About this chapter
Cite this chapter
Martins, D., Macovei, A., Leonetti, P., Balestrazzi, A., Araújo, S. (2017). The Influence of Phosphate Deficiency on Legume Symbiotic N2 Fixation. 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_3
Download citation
DOI: https://doi.org/10.1007/978-3-319-55729-8_3
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-55728-1
Online ISBN: 978-3-319-55729-8
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)