, Volume 76, Issue 3, pp 221–228 | Cite as

Role of acid phosphatase in the tolerance of the rhizobial symbiosis with legumes to phosphorus deficiency

  • Mohamed LazaliEmail author
  • Jean Jacques Drevon


Phosphorus (P) deficiency initiates a myriad of transcriptional, biochemical and physiological responses stimulating either the root’s extracellular abilities to acquire soil P in the rhizosphere or optimize its intracellular use efficiency and allocation through all plant organs. Enhancing activity of acid phosphatase (APase) to acquire and remobilize Pi from organic P compounds is one important strategy for improving plant P nutrition. The release of APase to the rhizosphere is a typical and almost universal P-starvation response in higher plants. However, relatively little is known about the functions of intracellular APase in legume nodules. The aim of this review was to track the enzyme activity along with the intra-nodular localization of APase, and its contribution in the rhizobial symbiosis tolerance to P-deficiency. Our findings have revealed that expression of APase and phytases genes and activities of the corresponding enzymes were positively correlated with increases both of the P use efficiency for N2 fixation and nodule O2 permeability in the rhizobial symbiosis with legumes. The induced enzyme activity and the marked transcripts localization of APase and phytase in nodule cortex would control nodule respiration and contribute to adaptation of nodulated legumes to low-P availability. Thus, the increase of APase and phytase activities in legume nodules supports a physiological role of these enzymes in the regulation of nitrogenase activity in connection with the nodule-P status, and opens up a new scenario for a better understanding of the regulation of N2 fixation in legumes.


Legumes Acid phosphatases Phytase Nodule respiration Phosphorus 



Acid phosphatase


International Center of Tropical Agriculture






Inorganic phosphate


Phosphorus use efficiency


Recombinant inbred line


Symbiotic nitrogen fixation



This work was supported by the Great Federative Project FABATROPIMED, financed by Agropolis Foundation of Montpellier under the reference ID 1001-009.


  1. 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 169:1084–1089CrossRefGoogle Scholar
  2. 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 51:1289–1297PubMedGoogle Scholar
  3. Al-Niemi TS, Kahn ML, McDermott TR (1998) Phosphorus uptake by bean nodules. Plant Soil 198:71–78CrossRefGoogle Scholar
  4. 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 312:129–138CrossRefGoogle Scholar
  5. Bargaz A, Ghoulam C, Faghire M, Attar HA, Drevon JJ (2011) The nodule conductance to O2 diffusion increases with high phosphorus content in the Phaseolus vulgaris-rhizobia symbiosis. Symbiosis 53:157–164jCrossRefGoogle Scholar
  6. Bargaz A, Ghoulam C, Amenc L, Lazali M, Faghire M, Drevon JJ (2012) Phosphoenol pyruvate phosphatase is induced in the root nodule cortex of Phaseolus vulgaris under phosphorus deficiency. J Exp Bot 63:4723–4730CrossRefGoogle Scholar
  7. Bargaz A, Lazali M, Amenc M, 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 238:107–119CrossRefGoogle Scholar
  8. Bargaz A, Zaman-Allah M, Farissi M, Lazali M, Drevon JJ, Maougal RT, Carlsson G (2015) Physiological and molecular aspects of tolerance to environmental constraints in grain and forage legumes. Int J Mol Sci 16:18976–19008CrossRefGoogle Scholar
  9. Dalton DA, Joyner SL, Becana M, Iturbe-Ormaetxe I, Chatfield JM (1998) Antioxidant defenses in the peripheral cell layers of legume root nodules. Plant Physiol 116:37–43CrossRefGoogle Scholar
  10. Drevon JJ, Abadie J, Alkama N, Andriamananjara A, Amenc L, Bargaz A, Carlsson G, Lazali M, Ghoulam C, Ounane SM (2015) Phosphorus use efficiency for N2 fixation in the rhizobial symbiosis with legumes. In: de Bruijn FJ (ed) Biological nitrogen fixation. John Wiley & Sons, Inc, Hoboken, USA, pp 455–464CrossRefGoogle Scholar
  11. Duff SMG, Sarath G, Plaxton WC (1994) The role of acid phosphatase in plant phosphorus metabolism. Physiol Plant 90:791–800CrossRefGoogle Scholar
  12. Gálvez S, Hirsch AM, Wycoff KL, Hunt S, Layzell DB, Kondorosi A, Crespi M (2000) Oxygen regulation of a nodule-located carbonic anhydrase in alfalfa. Plant Physiol 124:1059–1068CrossRefGoogle Scholar
  13. Garcia NAT, Olivera M, Iribarne C, Lluch C (2004) Partial purification and characterization of a non-specific acid phosphatase in leaves and root nodules of Phaseolus vulgaris. Plant Physiol Biochem 42:585–591CrossRefGoogle Scholar
  14. George TS, Richardson AE (2008) Potential and limitations to improving crops for enhanced phosphorus utilization. In: White PJ, Hammond JP (eds) The ecophysiology of plant-phosphorus interactions. Springer, Dordrecht, pp 247–270CrossRefGoogle Scholar
  15. Greiner R, Lim BL, Cheng C, Carlsson NG (2007) Pathway of phytate dephosphorylation by beta-propeller phytases of different origins. Can J Microbiol 53:488–495CrossRefGoogle Scholar
  16. Huang H, Shi P, Wang Y, Luo H, Shao N, Wang G, Yang P, Yao B (2009) Diversity of beta-propeller phytase genes in the intestinal contents of grass carp provides insight into the release of major phosphorus from phytate in nature. Appl Environ Microbiol 75:1508–1516CrossRefGoogle Scholar
  17. Hunt S, Layzell DB (1993) Gas exchange of legume nodules and the regulation of nitrogenase activity. Annu Rev Plant Physiol Plant Mol Biol 44:483–511CrossRefGoogle Scholar
  18. Jebara M, Drevon JJ (2001) Genotypic variation in nodule conductance to the oxygen diffusion in common bean (Phaseolus vulgaris L.). Agron 21:667–674CrossRefGoogle Scholar
  19. Jebara M, Aouani ME, Payre H, Drevon JJ (2005) Nodule conductance varied among common bean (Phaseolus vulgaris) genotypes under phosphorus deficiency. J Plant Physiol 162:309–315CrossRefGoogle Scholar
  20. Kouas S, Louche J, Debez A, Plassard C, Drevon JJ, Abdelly C (2009) Effect of phosphorus deficiency on acid phosphatase and phytase activities in common bean (Phaseolus vulgaris L.) under symbiotic nitrogen fixation. Symbiosis 47:141–149CrossRefGoogle Scholar
  21. Latati M, Bargaz A, Belarbi B, Lazali M, Benlahrech S, Tellah S, Kaci G, Drevon JJ, Ounane SM (2016) The intercropping common bean with maize improves the rhizobial efficiency, resource use and grain yield under low phosphorus availability. Eur J Agron 72:80–90CrossRefGoogle Scholar
  22. Lazali M, Bargaz A (2017) Examples of belowground mechanisms enabling legumes to mitigate phosphorus deficiency. In: Sulieman S, Tran LSP (eds) Legume nitrogen fixation in soils with low phosphorus availability. Springer International Publishing, Switzerland, pp 135–152Google Scholar
  23. Lazali M, Drevon JJ (2014) The nodule conductance to O2 diffusion increases with phytase activity in N2-fixing Phaseolus vulgaris L. Plant Physiol Biochem 80:53–59CrossRefGoogle Scholar
  24. Lazali M, Zaman-Allah M, Amenc L, Ounane G, Abadie J, Drevon JJ (2013) A phytase gene is over-expressed in root nodules cortex of Phaseolus vulgaris-rhizobia symbiosis under phosphorus deficiency. Planta 238:317–324CrossRefGoogle Scholar
  25. Lazali M, Louadj L, Ounane G, Abadie J, Amenc L, Bargaz A, Lullien-Pellerin V, Drevon JJ (2014a) Localization of phytase transcripts in germinating seeds of the common bean (Phaseolus vulgaris L.). Planta 240:471–478CrossRefGoogle Scholar
  26. Lazali M, Bargaz A, Carlsson G, Ounane SM, Drevon JJ (2014b) Discrimination against 15N among recombinant inbred lines of Phaseolus vulgaris L. contrasting in phosphorus use efficiency for nitrogen fixation. J Plant Physiol 171:199–204CrossRefGoogle Scholar
  27. Lazali M, Bargaz A, Brahimi S, Amenc L, Abadie J, Drevon JJ (2016a) Expression of a phosphate-starvation inducible fructose-1,6-bisphosphatase gene in common bean nodules correlates with phosphorus use efficiency. J Plant Physiol 205:48–56CrossRefGoogle Scholar
  28. Lazali M, Brahimi S, Merabet C, Latati M, Benadis C, Maougal RT, Blavet D, Drevon JJ, Ounane SM (2016b) Nodular diagnosis of contrasting recombinant inbred lines of Phaseolus vulgaris in multi-local field tests under Mediterranean climate. Eur J Soil Biol 73:100–107CrossRefGoogle Scholar
  29. Lazali M, Blavet D, Pernot C, Desclaux D, Drevon JJ (2017) Efficiency of phosphorus use for dinitrogen fixation varies between common bean genotypes under phosphorus limitation. Agron J 109:283–290CrossRefGoogle Scholar
  30. Lei XG, Weaver JD, Mullaney E, Ullah AH, Azain MJ (2013) Phytase, a new life for an “old” enzyme. Annu Rev Anim Biosci 1:283–309CrossRefGoogle Scholar
  31. 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 109:275–285CrossRefGoogle Scholar
  32. Liang C, Tian J, Lam HM, Lim BL, Yan X, Liao H (2010) Biochemical and molecular characterization of PvPAP3: a novel purple acid phosphatase isolated from common bean enhancing extracellular ATP utilization. Plant Physiol 152:854–865CrossRefGoogle Scholar
  33. Minchin FR, James EK, Becana M (2008) Oxygen diffusion, production of reactive oxygen and nitrogen species, and antioxidants in legume nodules. In: Dilworth MJ, James EK, Sprent JI, Newton WE (eds) Nitrogen-fixing leguminous symbioses. Springer, Dordrecht, pp 321–362Google Scholar
  34. Molina C, Zaman-Allah M, Khan F, Fatnassi N, Horres R, Rotter B, Steinhauer D, Amenc L, Drevon JJ, Winter P, Kahl G (2011) The salt responsive transcriptome of chickpea roots and nodules via deepSuperSAGE. BMC Plant Biol 11:31CrossRefGoogle Scholar
  35. Penheiter AR, Duff SMG, Sarath G (1997) Soybean root nodule acid phosphatase. Plant Physiol 114:597–604CrossRefGoogle Scholar
  36. Plaxton WC, Tran HT (2011) Metabolic adaptations of phosphate-starved plants. Plant Physiol 156:1006–1015CrossRefGoogle Scholar
  37. Raghothama KG (1999) Phosphate acquisition. Annu Rev Plant Physiol Plant Mol Biol 50:665–693CrossRefGoogle Scholar
  38. Ribet J, Drevon JJ (1995) Increase in permeability to oxygen and in oxygen uptake of soybean nodules under limiting phosphorus nutrition. Physiol Plant 94:298–304CrossRefGoogle Scholar
  39. Richardson AE, Hocking PJ, Simpson RJ, George TS (2009) Plant mechanisms to optimize access to soil phosphorus. Crop Pasture Sci 60:124–143CrossRefGoogle Scholar
  40. Robinson WD, Park J, Tran HT, Del Vecchio HA, Ying S, Zins J, Patel K, McKnight TD, Plaxton WC (2012) The secreted purple acid phosphatase isozymes AtPAP12 and AtPAP26 play a pivotal role in extracellular phosphate scavenging by Arabidopsis thaliana. J Exp Bot 63:6531–6542CrossRefGoogle Scholar
  41. Schulze J, Drevon JJ (2005) P-deficiency increases the O2 uptake per N2 reduced in alfalfa. J Exp Bot 56:1779–1784CrossRefGoogle Scholar
  42. Serraj R, Roy G, Drevon JJ (1994) Salt stress induces a decrease in the oxygen uptake of soybean nodules and in their conductance to oxygen diffusion. Physiol Plant 91:161–168CrossRefGoogle Scholar
  43. Serraj R, Fleurat-Lessard P, Jaillard B, Drevon JJ (1995) Structural changes in the inner cortex cells of soybean root nodules are induced by short-term exposure to high salt or oxygen concentrations. Plant Cell Environ 18:455–462CrossRefGoogle Scholar
  44. Simpson RJ, Oberson A, Culvenor RA, Ryan MH, Veneklaas EJ, Lambers H, Lynch JP, Ryan PR, Delhaize E, Smith FA, Smith SE, Harvey PR, Richardson AE (2011) Strategies and agronomic interventions to improve the phosphorus use efficiency of farming systems. Plant Soil 349:89–120CrossRefGoogle Scholar
  45. Streeter JG (1980) Carbohydrates in soybean nodules. II. Distribution of compounds in seedlings during the onset of nitrogen fixation. Plant Physiol 66:471–476CrossRefGoogle Scholar
  46. Sulieman S, Tran LSP (2015) Phosphorus homeostasis in legume nodules as an adaptive strategy to phosphorus deficiency. Plant Sci 239:36–43CrossRefGoogle Scholar
  47. Tian J, Wang XR, Tong YP, Chen XP, Liao H (2012) Bioengineering and management for efficient phosphorus utilization in crops and pastures. Curr Opin Biotech 23:866–871CrossRefGoogle Scholar
  48. 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 34:871–878Google Scholar
  49. Vance CP, Uhde-Stone C, Allan DL (2003) Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. New Phytol 157:423–447CrossRefGoogle Scholar
  50. Vecchio HA, Ying S, Park J, Knowles VL, Kanno S, Tanoi K, She YM, Plaxton WC (2014) The cell wall-targeted purple acid phosphatase AtPAP25 is critical for acclimation of Arabidopsis thaliana to nutritional phosphorus deprivation. Plant J 80:569–581CrossRefGoogle Scholar
  51. Veneklaas EJ, Lambers H, Bragg J, Finnegan PM, Lovelock CE, Plaxton WC, Price CA, Scheible WR, Shane MW, White PJ, Raven JA (2012) Opportunities for improving phosphorus- use efficiency in crop plants. New Phytol 195:306–320CrossRefGoogle Scholar
  52. Wang XR, Yan XL, Liao H (2010) Genetic improvement for phosphorus efficiency in soybean: a radical approach. Ann Bot 106:215–222CrossRefGoogle Scholar
  53. Wang LS, Li Z, Qian WQ, Guo WL, Guo X, Huang LL, Wang H, Zhu HF, Wu JW, Wang DW, Liu D (2011) The Arabidopsis purple acid phosphatase AtPAP10 is predominantly associated with the root surface and plays an important role in plant tolerance to phosphate limitation. Plant Physiol 157:1283–1299CrossRefGoogle Scholar
  54. Witty JF, Minchin FR (1998) Hydrogen measurements provide direct evidence for a variable physical barrier to gas diffusion in legume nodules. J Exp Bot 49:1015–1020CrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Laboratoire de recherche ERP, Faculté des Sciences de la Nature et de la Vie & des Sciences de la TerreUniversité Djilali Bounaama de Khemis MilianaKhemis MilianaAlgeria
  2. 2.UMR Ecologie Fonctionnelle & Biogéochimie des Sols et Agroécosystèmes, INRA-IRD-CIRAD-SupAgroInstitut National de la Recherche AgronomiqueMontpellierFrance

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