Abstract
The effect of phosphorus deficiency on growth, nodulation and phytase activity was studied in glasshouse for four symbioses involving two faba bean cultivars, namely Aguadulce (AG) and Alfia (AL), and two local rhizobial isolates, namely RhF1 and RhF2. The P deficiency was applied by adding 25 µmol of Pi plant−1 week−1 to nutrient solution, whereas the sufficient control received 125 µmol plant−1 week−1. At flowering stage, the plants were harvested for assessment of growth and nodulation, P and N contents in organs as well as activities of phytase and phosphatases in nodules. The latter were highly stimulated by P deficiency, particularly for AL–RhF1 symbiosis for which shoot growth and P content were not affected by P deficiency. Using in situ RT-PCR, the expression of a plant histidine acid phytase HAP gene was detected in the nodule cortex under P deficiency. It is concluded that high nodule phytase activity constitutes a mechanism for faba bean plants to adapt their nitrogen fixation to P deficiency.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Abbreviations
- AG:
-
Aguadulce
- AL:
-
Alfia
- APase:
-
Acid phosphatase
- DEPC:
-
Diethyl pyrocarbonate
- EURS:
-
Efficiency in use of rhizobial symbiosis
- NDW:
-
Nodule dry weight
- PBS:
-
Phosphate-buffering saline
- pNPP:
-
para-Nitrophenyl phosphate
- PUE:
-
Phosphorus use efficiency
- SDW:
-
Shoot dry weight
- SNF:
-
Symbiotic nitrogen fixation
References
Achat DL, Pousse N, Nicolas M et al (2016) Soil properties controlling inorganic phosphorus availability: general results from a national forest network and a global compilation of the literature. Biogeochemistry 127:255–272. https://doi.org/10.1007/s10533-015-0178-0
Afolayan AJ, Bvenura C (2016) Proximate and phytate accumulation in Solanum nigrum L. cultivated on fertilizer-amended soils. Commun Soil Sci Plant Anal. https://doi.org/10.1080/00103624.2016.1178763
Araújo AP, Plassard C, Drevon J-J (2008) Phosphatase and phytase activities in nodules of common bean genotypes at different levels of phosphorus supply. Plant Soil 312(1–2):129–138
Bargaz A, Drevon J-J, Oufdou K et al (2011) Nodule phosphorus requirement and O2 uptake in common bean genotypes under phosphorus deficiency. Acta Agric Scand Sect B Soil Plant Sci 61:602–611. https://doi.org/10.1080/09064710.2010.533188
Bargaz A, Faghire M, Abdi N et al (2012) Low soil phosphorus availability increases acid phosphatases activities and affects P partitioning in nodules, seeds and rhizosphere of Phaseolus vulgaris. Agriculture 2:139–153. https://doi.org/10.3390/agriculture2020139
Bargaz A, Lazali M, Amenc L et al (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. https://doi.org/10.1007/s00425-013-1877-1
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Chapagain T, Riseman A (2015) Nitrogen and carbon transformations, water use efficiency and ecosystem productivity in monocultures and wheat-bean intercropping systems. Nutr Cycl Agroecosyst 101:107–121. https://doi.org/10.1007/s10705-014-9647-4
Chen ZC, Liao H (2016) Organic acid anions: an effective defensive weapon for plants against aluminum toxicity and phosphorus deficiency in acidic soils. J Genet Genom. https://doi.org/10.1016/j.jgg.2016.11.003
Daly K, Styles D, Lalor S, Wall DP (2015) Phosphorus sorption, supply potential and availability in soils with contrasting parent material and soil chemical properties. Eur J Soil Sci 66:792–801. https://doi.org/10.1111/ejss.12260
Doolette AL, Smernik RJ (2016) Phosphorus speciation of dormant grapevine (Vitis vinifera L.) canes in the Barossa Valley, South Australia. Aust J Grape Wine Res 22:462–468. https://doi.org/10.1111/ajgw.12234
Drevon JJ, Hartwig UA (1997) Phosphorus deficiency increases the argon-induced decline of nodule nitrogenase activity in soybean and alfalfa. Planta 201:463–469. https://doi.org/10.1007/s004250050090
Drevon JJ, Alkama N, Araujo A et al (2011) Nodular diagnosis for ecological engineering of the symbiotic nitrogen fixation with legumes. Proc Environ Sci 9:40–46. https://doi.org/10.1016/j.proenv.2011.11.008
Estève-Saillard M (2016) Tendance de marché en France sur la présence des protéines végétales dans les produits alimentaires. OCL-Ol Corps Gras Lipides 23:1–3. https://doi.org/10.1051/ocl/2016015
FAOSTAT (2014) Broad bean production. http://www.fao.org/faostat/en/#data/QC
Foucher F, Kondorosi E (2000) Cell cycle regulation in the course of nodule organogenesis in Medicago. Plant Mol Biol 43:773–786. https://doi.org/10.1023/a:1006405029600
Funayama-Noguchi S, Noguchi K, Terashima I (2014) Comparison of the response to phosphorus deficiency in two lupin species, Lupinus albus and L. angustifolius, with contrasting root morphology. Plant Cell Environ. https://doi.org/10.1111/pce.12390
Gemenet DC, Leiser WL, Beggi F et al (2016) Overcoming phosphorus deficiency in West African pearl millet and sorghum production systems: promising options for crop improvement. Front Plant Sci 7:1–10. https://doi.org/10.3389/fpls.2016.01389
Ha S, Tran L-S (2014) Understanding plant responses to phosphorus starvation for improvement of plant tolerance to phosphorus deficiency by biotechnological approaches. Crit Rev Biotechnol 34:16–30. https://doi.org/10.3109/07388551.2013.783549
Haling RE, Yang Z, Shadwell N et al (2016) Growth and root dry matter allocation by pasture legumes and a grass with contrasting external critical phosphorus requirements. Plant Soil 407:67–79. https://doi.org/10.1007/s11104-016-2808-2
Kaur G, Prabhavathi V, Bamel K, Sarwat M (2017) Phosphate signaling in plants: biochemical and molecular approach. In: Sarwat M, Ahmad A, Abdin MZ, Ibrahim MM (eds) Stress signaling in plants: genomics and proteomics perspective, vol 2. Springer, Cham, Switzerland, pp 83–110
Kudlinskiene I, Gru R, Stankevi R et al (2016) The effects of extruded lupins (Lupinus Spp.), Faba Beans (Vicia Faba) and Peas (Pisum Sativum) on the ruminal fluid parameters in dairy. Vetir Zootech 73:88–94
Lazali M, Zaman-Allah M, Amenc L et al (2013) A phytase gene is overexpressed in root nodules cortex of Phaseolus vulgaris-rhizobia symbiosis under phosphorus deficiency. Planta 238:317–324. https://doi.org/10.1007/s00425-013-1893-1
Lei X, Porres JM, Mullaney EJ, Brinch-Pedersen H (2007) Phytase : source, structure and application. Structure 29:505–529
Li Z, Rui J, Li X et al (2017) Bacterial community succession and metabolite changes during doubanjiang-meju fermentation, a Chinese traditional fermented broad bean (Vicia faba L.) paste. Food Chem 218:534–542. https://doi.org/10.1016/j.foodchem.2016.09.104
Limpens E, Bisseling T (2003) Signaling in symbiosis. Curr Opin Plant Biol 6:343–350. https://doi.org/10.1016/S1369-5266(03)00068-2
Liu S, Zhu Y, Wu F et al (2016) Characterization of plant-derived carbon and phosphorus in lakes by sequential fractionation and NMR spectroscopy. Sci Total Environ 566–567:1398–1409. https://doi.org/10.1016/j.scitotenv.2016.05.214
Magadlela A, Kleinert A, Dreyer LL, 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. https://doi.org/10.1071/BT13264
Maistry PM, Muasya AM, Valentine AJ, Chimphango SBM (2015) Balanced allocation of organic acids and biomass for phosphorus and nitrogen demand in the fynbos legume Podalyria calyptrata. J Plant Physiol 174:16–25. https://doi.org/10.1016/j.jplph.2014.10.005
Mandri B, Drevon J-J, Bargaz A et al (2012) Interactions between common bean genotypes and rhizobia strains isolated from moroccan soils for growth, phosphatase and phytase activities under phosphorus deficiency conditions. J Plant Nutr 35:1477–1490. https://doi.org/10.1080/01904167.2012.689908
Mehra P, Pandey BP, Giri J (2017) Improvement of phosphate acquisition and utilization by a secretory purple acid phosphatase (OsPAP21b) in rice. Plant Biotechnol J. https://doi.org/10.1111/ijlh.12426
Multari S, Stewart D, Russell WR (2015) Potential of fava bean as future protein supply to partially replace meat intake in the human diet. Compr Rev Food Sci Food Saf 14:511–522. https://doi.org/10.1111/1541-4337.12146
Nasto MK, Osborne BB, Lekberg Y et al (2017) Nutrient acquisition, soil phosphorus partitioning and competition among trees in a lowland tropical rain forest. New Phytol. https://doi.org/10.1111/nph.14494
Plante AF (2007) Soil biogeochemical cycling of inorganic nutrients and metals. In: Paul EA (ed) Soil microbiology, ecology and biochemistry, 3rd edn. Elsevier Inc., Burlington, MA 01803, USA, pp 389–432
Ramaekers L, Remans R, Rao IM et al (2010) Strategies for improving phosphorus acquisition efficiency of crop plants. Field Crop Res 117:169–176. https://doi.org/10.1016/j.fcr.2010.03.001
Rizzello CG, Verni M, Koivula H et al (2017) Influence of fermented faba bean flour on the nutritional, technological and sensory quality of fortified pasta. Food Funct. https://doi.org/10.1039/C6FO01808D
Schulze J, Drevon JJ (2005) P-deficiency increases the O2 uptake per N2 reduced in alfalfa. J Exp Bot 56:1779–1784. https://doi.org/10.1093/jxb/eri166
Secco D, Bouain N, Rouached A et al (2017) Critical reviews in biotechnology phosphate, phytate and phytases in plants: from fundamental knowledge gained in Arabidopsis to potential biotechnological applications in wheat. Crit Rev Biotechnol. https://doi.org/10.1080/07388551.2016.1268089
Sulieman S, Tran LSP (2015) Phosphorus homeostasis in legume nodules as an adaptive strategy to phosphorus deficiency. Plant Sci 239:36–43. https://doi.org/10.1016/j.plantsci.2015.06.018
Sulieman S, Van Ha C, Schulze J, Tran LSP (2013) Growth and nodulation of symbiotic Medicago truncatula at different levels of phosphorus availability. J Exp Bot 64:2701–2712. https://doi.org/10.1093/jxb/ert122
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. https://doi.org/10.1016/j.jplph.2013.09.001
Tsai Y-C, Greco TM, Boonmee A et al (2012) Functional proteomics establishes the interaction of SIRT7 with chromatin remodeling complexes and expands its role in regulation of RNA polymerase I transcription. Mol Cell Proteom 11:M111.015156–M111.015156. https://doi.org/10.1074/mcp.m111.015156
Turner WL, Plaxton WC (2003) Purification and characterization of pyrophosphate- and ATP-dependent phosphofructokinases from banana fruit. Planta 217:113–121. https://doi.org/10.1007/s00425-002-0962-7
Vadez V, Drevon JJ (2001) Genotypic variability in phosphorus use efficiency for symbiotic N2 fixation in common bean (Phaseolus vulgaris). Agronomie 21:691–699
Valentine AJ, Kleinert A, Benedito VA (2017) Adaptive strategies for nitrogen metabolism in phosphate deficient legume nodules. Plant Sci 256:46–52. https://doi.org/10.1016/j.plantsci.2016.12.010
Vance CP, Uhde-Stone C, Allan DL (2003) Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. New Phytol 157:423–447. https://doi.org/10.1046/j.1469-8137.2003.00695.x
Vardien W, Mesjasz-Przybylowicz J, Przybylowicz WJ et al (2014) Nodules from Fynbos legume Virgilia divaricata have high functional plasticity under variable P supply levels. J Plant Physiol 171:1732–1739. https://doi.org/10.1016/j.jplph.2014.08.005
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. https://doi.org/10.1016/j.jplph.2015.12.002
Acknowledgements
This work was supported by the Great Federative FABATROPIMED Project under the reference ID 1001-009 and the AVERROES scholarship programme of the EU for the internship of Bouchra MAKOUDI in Montpellier. We also thank the Moroccan Centre National pour la Recherche Scientifique et Technique (CNRST) for their ministerial fellowship (2011–2015).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by M. H. Walter.
Rights and permissions
About this article
Cite this article
Makoudi, B., Kabbadj, A., Mouradi, M. et al. Phosphorus deficiency increases nodule phytase activity of faba bean–rhizobia symbiosis. Acta Physiol Plant 40, 63 (2018). https://doi.org/10.1007/s11738-018-2619-6
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11738-018-2619-6