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The dual symbiosis between arbuscular mycorrhiza and nitrogen fixing bacteria benefits the growth and nutrition of the woody invasive legume Acacia cyclops under nutrient limiting conditions

Abstract

Background and aims

Acacia cyclops is an invasive species within Mediterranean ecosystems, characteristically low in soil nutrients. Thus associations with nitrogen-fixing bacteria (NFB) and arbuscular mycorrhiza (AM) may provide an advantage to these legumes. This study investigated the role of AM and NFB in the growth and nutritional physiology of A. cyclops.

Methods

Seedlings were inoculated with naturally occurring NFB, Glomus mosseae or both, and grown under glasshouse conditions for 5 months. Plants were cultivated in sand and supplied with a 20 % strength nutrient solution. Xylem sap nutrients, photosynthetic rates, biomass and chemical compositions, were recorded.

Results

The dual inoculation decreased the colonization of both symbionts, compared to a single symbiosis with either symbiont. Despite low colonization levels, the dual symbiosis increased host biomass and relative growth rates. This was associated with increased photosynthetic rates and enhanced nutrition. Additionally, dual symbiotic plants had enhanced N and P acquisition and utilization rates. Xylem sap analysis showed higher levels of NH +4 being exported from the roots to the shoots in the dual symbiotic plants compared with other treatments.

Conclusions

These findings suggest the dual symbiosis is an important factor in the growth and development of A. cyclops under nutrient limiting conditions.

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References

  1. Bell TL, Pate JS (1995) Nitrogen and phosphorus nutrition in Mycorrhizal Epacridaceae of South-west Australia. Ann Bot 77:389–397

    Article  Google Scholar 

  2. Brown MS, Bethlenfalvay GJ (1988) The Glycine-Glomus-Rhizobium Symbiosis VII. Photosynthetic nutrient-use efficiency in nodulated, mycorrhizal soybeans. Plant Physiol 86:491–496

    Article  Google Scholar 

  3. Brundrett M, Melville L, Peterson L (Eds.) (1994) Practical methods in mycorrhiza research. Mycologue Publications, Guelph

  4. Carvalho LM, Antunes PM, Martins-Loucao AM, Klironomos JN (2010) Disturbance influences the outcome of plant-soil biota interactions in invasive the Acacia longifolia and native species. Oikos 119:1172–1180

    Article  Google Scholar 

  5. Catford JG, Staehelin C, Lerat S, Piché Y, Vierheilig H (2003) Suppression of arbuscular mycorrhizal colonization and nodulation in split-root systems of alfalfa after pre-inoculation and treatment with Nod factors. J Exp Bot 54:1481–1487

    PubMed  Article  CAS  Google Scholar 

  6. Chalk PM, Souza RDF, Urquiaga S, Alves BJR, Boddey RM (2006) The role of arbuscular mycorrhiza in legume symbiotic performance. Soil Biol Biochem 38:2944–2951

    Article  CAS  Google Scholar 

  7. Chaturvedi C, Singh R (1989) Response of chickpea (Cicer arietinum L.) to inoculation with Rhizobium and VA mycorrhiza. Proc Indian Nat Sci Acad Sec B 59:443–446

    Google Scholar 

  8. Constable JVH, Bassirirad H, Lussenhop J, Ayalsew Z (2001) Influence of elevated CO2 and mycorrhiza on nitrogen acquisition: contrasting responses in Pinus taeda and Liquidambar styraciflua. Tree Physiol 21:83–91

    PubMed  Article  CAS  Google Scholar 

  9. Cramer MD, Richards MB (1999) The effect of rhizosphere dissolved inorganic carbon on the growth of tomato seedlings. J Exp Bot 50:79–87

    CAS  Google Scholar 

  10. Epo WDB (1991) Effect of nitrogen nutrition on photosynthesis and growth in C4Panicum species. Plant Cell Environ 14:295–301

    Article  Google Scholar 

  11. Fitter AH (1991) Costs and benefits of mycorrhiza: implications for functioning under natural conditions. Experientia 47:350–355

    Article  Google Scholar 

  12. Govindarajulu M, Pfeffer PE, Hairu J, Abubaker J, Douds DD, Allen JW, Bucking H, Lammers PJ, Shachar-Hill Y (2005) Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature 435(9):819–823

    PubMed  Article  CAS  Google Scholar 

  13. Hewitt EJ (1966) Sand and water culture methods used in the study of plant nutrition, 2nd edn. Commonwealth Bureau of Horticultural Technology and Communication. No. 221, Commonwealth Agricultural Bureau: Farnham Royal, England

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

    PubMed  Article  Google Scholar 

  15. Jia Y, Gray VM, Straker CJ (2004) The influence of Rhizobium and arbuscular mycorrhizal fungi on nitrogen and phosphorous accumulation by Vicia faba. Ann Bot 94:251–258

    PubMed  Article  CAS  Google Scholar 

  16. Kaschuk G, Kuyper TW, Leffelaar PA, Hungaria M, Giller KE (2009) Are the rates of photosynthesis stimulated by the carbon sink strength of rhizobial and arbuscular mycorrhizal symbioses? Soil Biol Biochem 41:1233–1244

    Article  CAS  Google Scholar 

  17. Lima JD, Da Matta FM, Mosquim PR (2008) Growth attributes, xylem sap composition, and photosynthesis in common bean as affected by nitrogen and phosphorus deficiency. J Plant Nutr 23(7):937–947

    Google Scholar 

  18. Marchante HS, Marchante E, Buscardo E, Maia J, Freitas H (2003) Recovery potential of dune ecosystems invaded by an exotic Acacia species (Acacia longifolia). Weed Tech 18:1427–1433

    Article  Google Scholar 

  19. Marchante E, Kjoller A, Struwe S, Freitas H (2009) Soil recovery after removal of N2-fixing invasive Acacia longifolia: consequences for ecosystem recovery. Biol Invasions 11:813–823

    Article  Google Scholar 

  20. Marschner H, Dell B (1994) Nutrient uptake in mycorrhizal symbiosis. Plant Soil 59:89–102

    Google Scholar 

  21. Mortimer PE, Pérez-Fernández MA, Valentine AJ (2008) The role of arbuscular mycorrhizal colonization in the carbon and nutrient economy of the tripartite symbiosis with nodulated Phaseolus vulgaris. Soil Biol Biochem 40:1019–1027

    Article  CAS  Google Scholar 

  22. Mortimer PE, Pérez-Fernández MA, Valentine AJ (2009) Arbuscular mycorrhiza affect the N and C economy of nodulated Phaseolus vulgaris (L.) during NH +4 nutrition. Soil Biol Biochem 41:2115–2121

    Article  CAS  Google Scholar 

  23. Mortimer PE, Pérez-Fernández MA, Valentine AJ (2012) Arbuscular mycorrhiza maintains nodule function during external NH +4 supply in Phaseolus vulgaris (L.). Mycorrhiza 22:237–245

    PubMed  Article  CAS  Google Scholar 

  24. Murphy J, Riley JP (1962) A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta 27:31–36

    Article  CAS  Google Scholar 

  25. Nielson KL, Amram E, Lynch JP (2001) The effect of phosphorous availability on the carbon economy of contrasting common bean (Phaseolus vulgaris L.) genotypes. J Exp Bot 52:329–339

    Article  Google Scholar 

  26. Pacovsky RS, Fuller G, Stafford AE, Paul EA (1986) Nutrient and growth interactions in soybeans colonized with Glomus fasciculatum and Rhizobium japonicum. Plant Soil 92:37–45

    Article  Google Scholar 

  27. Pearson JN, Abbott LK, Jasper DA (1993) Mediation of competition between two colonizing VA mycorrhizal fungi by the host plant. New Phytol 123:93–98

    Article  Google Scholar 

  28. Peoples MB, Pate JS, Atkins CA, Bergensen FJ (1986) Nitrogen nutrition and xylem sap composition of Peanut (Arachis hypogaea L. cv Virginia Bunch). Plant Physiol 82:946–951

    PubMed  Article  CAS  Google Scholar 

  29. Possel M, Hewitt CN (2009) Gas exchange and photosynthetic performance of the tropical tree Acacia nigrescens when grown in different CO2 concentrations. Planta 229:837–846

    Article  Google Scholar 

  30. Reinhart KO, Callaway RM (2006) Soil biota and invasive plants. New Phytol 170:445–457

    PubMed  Article  Google Scholar 

  31. Richardson DM, Van Wilgen BW (2004) Invasive alien plants in South Africa: how well do we understand the ecological impacts? SA J Sci 100:45–52

    Google Scholar 

  32. Richardson DM, van Wilgen BW, Higgins SI, Trinder-Smiths TH, Cowling RM, McKellt DH (1996) Current and future threats to plant biodiversity on the Cape Peninsula, South Africa. Biodivers Conserv 5:607–647

    Article  Google Scholar 

  33. Rodriguez-Echeverria S, Crisostomo JA, Nabais C, Freitas H (2008) Belowground mutualist and the invasive ability of Acacia longifolia in coastal dunes in Portugal. Biol Invasions 11:651–661

    Article  Google Scholar 

  34. Rosen H (1957) A modified ninhydrin colorimetric analysis for amino acids. Arch Biochem Biophys 67(1):10–15

    PubMed  Article  CAS  Google Scholar 

  35. Solorzano L (1969) Determination of ammonia in natural waters by the phenolhypochlorite method. Limnol Oceanog 14:799–801

    Article  CAS  Google Scholar 

  36. Stock WD, Wienand KT, Baker AC (1995) Impacts of invading N2-fixing Acacia species on patterns of nutrient cycling in two Cape ecosystems: evidence from soil incubation studies and 15 N natural abundance values. Oecologia 101:375–382

    Article  Google Scholar 

  37. Tang C, Hisinger 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(1):131–138

    Article  CAS  Google Scholar 

  38. Toro M, Azcon R, Barea JM (1998) The use of isotopic dilution techniques to evaluate the interactive effects of Rhizobium genotype, mycorrhizal fungi, phosphate-solubilizing rhizobacteria and rock phosphate on nitrogen and phosphorus acquisition by Medicago sativa. New Phytol 138:265–273

    Article  CAS  Google Scholar 

  39. Toussaint JP, St-Arnaud M, Charest C (2004) Nitrogen transfer and assimilation between the arbuscular mycorrhizal fungus Glomus intraradices Schenck & Smith and Ri T-DNA roots of Daucus carota L. in an in vitro compartmented system. Can J Microbiol 50(4):251–260

    PubMed  Article  CAS  Google Scholar 

  40. Vadez V, Lasso JH, Beck DP, Drevon JJ (1999) Variability of N2-fixation in common bean (Phaseolus vulgaris L.) under P deficiency is related to P use efficiency. Euphytica 106:231–242

    Article  Google Scholar 

  41. Valentine AJ, Kleinert A (2006) Respiratory metabolism of root-zone CO2 in mycorrhizal plants with NH +4 and NO 3 nutrition. Symbiosis 41(3):119–126

    CAS  Google Scholar 

  42. Vitousek PM, Walker LR, Whiteaker LD, Muller-Dombois D, Matson PA (1987) Biological invasions by Myrica faya alters ecosystem development in Hawaii. Science 238:802–804

    PubMed  Article  CAS  Google Scholar 

  43. Vogels GD, van der Drift C (1970) Differential analysis of glyoxylate derivatives. Anal Biochem 33:143–157

    PubMed  Article  CAS  Google Scholar 

  44. Winter HC, Powell GK, Dekker EE (1981) 4-Methyleneglutamine in peanut plants: dynamics of formation, levels, and turnover in relation to other free amino acids. Plant Physiol 68:588–593

    PubMed  Article  CAS  Google Scholar 

  45. Witowski ETF (1989) Effects of nutrients on the distribution of dry mass, nitrogen and phosphorus in seedlings of Protea repens (L.) L. (Proteaceae). New Phytol 112:481–487

    Article  Google Scholar 

  46. Witowski ETF (1991) Effects of invasive alien acacias on nutrient cycling in the coastal lowlands of the Cape Fynbos. J App Ecol 28:1–15

    Article  Google Scholar 

  47. Wright DP, Read DJ, Scholes JD (1998) Mycorrhizal sink strength influences whole plant carbon balance of Trifolium repens L. Plant Cell Environ 21:881–891

    Article  Google Scholar 

  48. Yu H, Ong BL (2003) Effect of radiation quality on growth and photosynthesis of Acacia magnum seedlings. Photosynthetica 41:349–355

    Article  CAS  Google Scholar 

  49. Zar JH (1999) Biostatistical analysis, 4th edn. Prentice-Hall, Upper Saddle River

    Google Scholar 

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Correspondence to Peter E. Mortimer.

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Responsible Editor: Hans Lambers.

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Mortimer, P.E., Le Roux, M.R., Pérez-Fernández, M.A. et al. The dual symbiosis between arbuscular mycorrhiza and nitrogen fixing bacteria benefits the growth and nutrition of the woody invasive legume Acacia cyclops under nutrient limiting conditions. Plant Soil 366, 229–241 (2013). https://doi.org/10.1007/s11104-012-1421-2

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Keywords

  • Arbuscular mycorrhiza
  • Nitrogen fixing bacteria
  • Dual symbiosis
  • P and N nutrition
  • Xylem sap
  • Invasive species
  • Acacia cyclops