Plant and Soil

, Volume 353, Issue 1–2, pp 181–194 | Cite as

Arbuscular mycorrhizas and their role in plant growth, nitrogen interception and soil gas efflux in an organic production system

  • T. R. Cavagnaro
  • F. H. Barrios-Masias
  • L. E. Jackson
Regular Article

Abstract

Background and aims

Roots and mycorrhizas play an important role in not only plant nutrient acquisition, but also ecosystem nutrient cycling.

Methods

A field experiment was undertaken in which the role of arbuscular mycorrhizas (AM) in the growth and nutrient acquisition of tomato plants was investigated. A mycorrhiza defective mutant of tomato (Solanum lycopersicum L.) (named rmc) and its mycorrhizal wild type progenitor (named 76R) were used to control for the formation of AM. The role of roots and AM in soil N cycling was studied by injecting a 15N-labelled nitrate solution into surface soil at different distances from the 76R and rmc genotypes of tomato, or in plant free soil. The impacts of mycorrhizal and non-mycorrhizal root systems on soil greenhouse gas (CO2 and 14+15N2O and 15N2O) emissions, relative to root free soils, were also studied.

Results

The formation of AM significantly enhanced plant growth and nutrient acquisition, including interception of recently applied NO3. Whereas roots caused a small but significant decrease in 15N2O emissions from soils at 23 h after labeling, compared to the root-free treatment, arbuscular mycorrhizal fungi (AMF) had little effect on N2O emissions. In contrast soil CO2 emissions were higher in plots containing mycorrhizal root systems, where root biomass was also greater.

Conclusions

Taken together, these data indicate that roots and AMF have an important role to play in plant nutrient acquisition and ecosystem N cycling.

Keywords

Arbuscular mycorrhizas Carbon dioxide Nitrogen Nitrous oxide Nutrient cycling Plant nutrition Tomato mutant 

References

  1. Ames RN, Reid CPP, Porter L, Cambardella C (1983) Hyphal uptake and transport of nitrogen from two 15N-labelled sources by Glomus mosseae, a vesicular arbuscular mycorrhizal fungus. New Phytol 95:381–396CrossRefGoogle Scholar
  2. Asghari HR, Cavagnaro TR (2011) Arbuscular mycorrhizas enhance plant interception of leached nutrients. Funct Plant Biol 38:219–226CrossRefGoogle Scholar
  3. Barker SJ, Stummer B, Gao L, Dispain I, O'Connor PJ, Smith SE (1998) A mutant in Lycopersicon esculentum Mill. with highly reduced VA mycorrhizal colonization, isolation and preliminary characterisation. Plant J 15:791–797CrossRefGoogle Scholar
  4. Burger M, Jackson LE (2003) Plant and microbial nitrogen use and turnover: rapid conversion of nitrate to ammonium in soil with roots. Plant Soil 266:289–301CrossRefGoogle Scholar
  5. Burger M, Jackson LE, Lundquist EJ, Louie DT, Miller RL, Rolston DR, Scow KM (2005) Microbial responses and nitrous oxide emissions during rewetting and drying of agricultural soil under organic and conventional management. Biol Fertil Soils 42:109–118CrossRefGoogle Scholar
  6. Cardoso IM, Kuyper TW (2006) Mycorrhizas and tropical soil fertility. Agr Ecosyst Environ 116:72–84CrossRefGoogle Scholar
  7. Cavagnaro TR (2008) The role of arbuscular mycorrhzas in improving plant zinc nutrition under low soil zinc concentrations: a review. Plant Soil 304:315–325CrossRefGoogle Scholar
  8. Cavagnaro TR, Jackson LE, Six J, Ferris H, Goyal S, Asami D, Scow KM (2006) Arbuscular mycorrhizas, microbial communities, nutrient availability, and soil aggregates in organic tomato production. Plant Soil 282:209–225CrossRefGoogle Scholar
  9. Cavagnaro TR, Langley AJ, Jackson LE, Smukler SM, Koch GW (2008) Growth, nutrition, and soil respiration of a mycorrhiza-defective tomato mutant and its mycorrhizal wild-type progenitor. Funct Plant Biol 35:228–235CrossRefGoogle Scholar
  10. Cavagnaro TR, Martin AW (2011) Arbuscular mycorrhizas in southeastern Australian processing tomato farm soils. Plant Soil 340:327–336CrossRefGoogle Scholar
  11. Cavagnaro TR, Smith FA, Hay G, Carne-Cavagnaro VL, Smith SE (2004) Inoculum type does not affect overall resistance of an arbuscular mycorrhiza-defective tomato mutant to colonisation but inoculation does change competitive interactions with wild-type tomato. New Phytol 161:485–494CrossRefGoogle Scholar
  12. David-Schwartz BH, Smadar W, Levy AA, Galili G, Kapulnik Y (2001) Identification of a novel genetically controlled step in mycorrhizal colonization: plant resistance to infection by fungal spores but not extra-radical hyphae. Plant J 27:561–569PubMedCrossRefGoogle Scholar
  13. Drinkwater LE, Letourneau DK, Workneh F, van Bruggen AHC, Shennan C (1995) Fundamental differences between conventional and organic tomato agroecosystems in California. Ecol Appl 5:1098–1112CrossRefGoogle Scholar
  14. Facelli E, Facelli JM (2002) Soil phosphorus heterogeneity and mycorrhizal symbiosis regulate plant intra-specific competition and size distribution. Oecologia 133:54–61CrossRefGoogle Scholar
  15. Forster JC (ed) (1995) Soil nitrogen. Methods in applied soil microbiology and biochemistry. Academic, San DiegoGoogle Scholar
  16. Gao L-L (2002) Control of arbuscular mycorrhizal colonisation. Studies of a mycorrhiza-defective tomato mutant. Adelaide University, AdeliadeGoogle Scholar
  17. Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular-arbuscular mycorrhizal infection in roots. New Phytol 84:489–500CrossRefGoogle Scholar
  18. Hadas A, Doane TA, Kramer AW, van Kessel C, Horwath WR (2002) Modelling the turnover of 15N-labelled fertilizer and cover crop in soil and its recovery by maize. Eur J Soil Sci 53:541–552CrossRefGoogle Scholar
  19. Hodge A, Campbell CD, Fitter AH (2001) An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material. Nature 413:297–299PubMedCrossRefGoogle Scholar
  20. Hodge A, Fitter AH (2010) Substantial nitrogen acquisition by arbuscular mycorrhizal fungi from organic material has implications for N cycling. Proc Natl Acad Sci U S A 107:13754–13759PubMedCrossRefGoogle Scholar
  21. Jackson L, Burger M, Cavagnaro T (2008) Roots, nitrogen transformations, and ecosystem services. Annu Rev Plant Biol 59:341–363PubMedCrossRefGoogle Scholar
  22. Jackson LE, Miller D, Smith SE (2002) Arbuscular mycorrhizal colonization and growth of wild and cultivated lettuce in response to nitrogen and phosphorus. Sci Hortic-Amsterdam 94:205–218CrossRefGoogle Scholar
  23. Johnson NC, Graham JH, Smith FA (1997) Functioning of mycorrhizal associations along the mutualism-parasitism continuum. New Phytol 135:575–586CrossRefGoogle Scholar
  24. Kayaa C, Tunab AL, Dikilitasc M, Ashrafd M, Koskeroglub S, Gunerie M (2009) Supplementary phosphorus can alleviate boron toxicity in tomato. Sci Hortic-Amsterdam 121:284–288CrossRefGoogle Scholar
  25. Kuzyakov Y, Domanski G (2002) Model for rhizodeposition and CO2 efflux from planted soil and its validation by 14C pulse labeling of ryegrass. Plant Soil 239:87–102CrossRefGoogle Scholar
  26. Langley JA, Hungate BA (2003) Mycorrhizal controls in belowground litter quality. Ecology 84:2302–2312CrossRefGoogle Scholar
  27. Marschner H, Dell B (1994) Nutrient uptake in mycorrhizal symbiosis. Plant Soil 159:89–102Google Scholar
  28. Miranda KM, Espey MG, Wink DA (2001) A rapid, simple spectrophotometric method for simultaneous detection of nitrate and nitrite. Nitric Oxide 5:62–71PubMedCrossRefGoogle Scholar
  29. Pang PC, Paul EA (1980) Effects of vesicular arbuscular mycorrhiza on 14C and 15N distribution in nodulated faba beans. Can J Soil Soc 60:241–250CrossRefGoogle Scholar
  30. Pearson JN, Jakobsen I (1993) Symbiotic exchange of carbon and phosphorus between cucumber and three arbuscular mycorrhizal fungi. New Phytol 124:481–488CrossRefGoogle Scholar
  31. Peng S, Eissenstat DM, Graham JH, Williams K, Hodge NC (1993) Growth depression in mycorrhizal citrus at high-phosphorus supply. Plant Physiol 101:1063–1071PubMedGoogle Scholar
  32. Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:158–161CrossRefGoogle Scholar
  33. Poulsen KH, Nagy R, Gao L-L, Smith SE, Bucher M, Smith FA, Jakobsen I (2005) Physiological and molecular evidence for Pi uptake via the symbiotic pathway in a reduced mycorrhizal colonization mutant in tomato associated with a compatible fungus. New Phytol 168:445–453PubMedCrossRefGoogle Scholar
  34. Reynolds HL, Hartley AE, Vogelsang KM, Bever JD, Schultz PA (2005) Arbuscular mycorrhizal fungi do not enhance nitrogen acquisition and growth of old-field perennials under lownitrogen supply in glasshouse culture. New Phytol 167:869–880PubMedCrossRefGoogle Scholar
  35. Rillig MC, Ramsey PW, Gannon JE, Mummey DL, Gadkar V, Kapulnik Y (2008) Suitability of mycorrhiza-defective mutant/wildtype plant pairs (Solanum lycopersicum L. cv Micro-Tom) to address questions in mycorrhizal soil ecology. Plant Soil 308:267–275CrossRefGoogle Scholar
  36. Rochette P, Angers DA (1999) Soil surface carbon dioxide fluxes induced by spring, summer, and fall moldboard plowing in a sandy loam. Soil Sci Soc Am J 63:621–628CrossRefGoogle Scholar
  37. Rolston DE (1986) Gas flux. In: Klute A (ed) Methods of soil analysis: part 1. Physical and mineralogical methods. Agron. Monogr. 9. SSSA, Madison, pp 383–411Google Scholar
  38. Ruzicka DR, Barrios-Masias FH, Hausmann NT, Jackson LE, Schachtman DP (2010) Tomato root transcriptome response to a nitrogen-enriched soil patch. BMC Plant Biol 10:75–94PubMedCrossRefGoogle Scholar
  39. Ruzicka DR, Hausmann NT, Barrios-Masias FH, Jackson LE, Schachtman DP (2011) Transcriptomic and metabolic responses of mycorrhizal roots to nitrogen patches under field conditions. Plant Soil, Online FirstGoogle Scholar
  40. Sah RN, Miller RO (1992) Spontaneous reaction for acid dissolution of biological tissues in closed vessels. Anal Chem 64:230–233PubMedCrossRefGoogle Scholar
  41. Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press Ltd., CambridgeGoogle Scholar
  42. Smukler SM, Sánchez-Moreno S, Fonte JJ, Ferris H, Klonsky K, O’Geen AT, Scow KM, Steenwerth KL, Jackson LE (2010) Biodiversity and multiple ecosystem functions in an organic farmscape. Agr Ecosyst Environ 139:80–97CrossRefGoogle Scholar
  43. Tanaka Y, Yano K (2005) Nitrogen delivery to maize via mycorrhizal hyphae depends on the form of N supplied. Plant Cell Environ 28:1247–1254CrossRefGoogle Scholar
  44. Tibbett M (2000) Roots, foraging and the exploitation of soil nutrient patches: the role of mycorrhizal symbiosis. Funct Ecol 14:397–399CrossRefGoogle Scholar
  45. Valentine AJ, Kleinert A (2007) Phosphate deficiency affects respiratory metabolism of dark CO2 fixation in mycorrhizal roots. Mycorrhiza 17:137–143PubMedCrossRefGoogle Scholar
  46. Vance ED, Brookes PD, Jenkinson DS (1987) An extraction method to estimate soil microbial biomass C. Soil Biol Biochem 19:703–707CrossRefGoogle Scholar
  47. Zar JH (1999) Biostatistical analysis, 4th edn. Prentice Hall, New JerseyGoogle Scholar
  48. Zhu YG, Miller RM (2003) Carbon cycling by arbuscular mycorrhizal fungi in soil-plant systems. Trends Plant Sci 8:407–409PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • T. R. Cavagnaro
    • 1
    • 2
  • F. H. Barrios-Masias
    • 3
  • L. E. Jackson
    • 3
  1. 1.School of Biological SciencesMonash UniversityClaytonAustralia
  2. 2.Australian Centre for BiodiversityMonash UniversityClaytonAustralia
  3. 3.Department of Land, Air and Water ResourcesUniversity of California DavisDavisUSA

Personalised recommendations