Plant and Soil

, Volume 384, Issue 1–2, pp 79–92 | Cite as

Nutrient interactions and arbuscular mycorrhizas: a meta-analysis of a mycorrhiza-defective mutant and wild-type tomato genotype pair

Regular Article

Abstract

Background and aims

Arbuscular mycorrhizas (AM) enhance plant uptake of a range of mineral nutrients from the soil. Interactions between nutrients in the soil and plant, are complex, and can be affected by AM. Using a mycorrhiza-defective mutant tomato genotype (rmc) and its wild-type (76R), provides a novel method to study AM functioning.

Methods

We present a meta-analysis comparing tissue nutrient concentration (P, Zn, K, Ca, Cu, Mg, Mn, S, B, Na, Fe), biomass and mycorrhizal colonisation data between the 76R and rmc genotypes, across a number of studies that have used this pair of tomato genotypes. Particular attention is paid to interactions between soil P or soil Zn, with tissue nutrients.

Results

For most nutrients, the difference in concentration between genotypes was significantly affected either by soil P, soil Zn, or both. When soil P was deficient, AM were particularly beneficial in terms of uptake of not only P, but other nutrients as well.

Conclusions

Colonisation by AMF significantly affects the uptake of many soil macro- and micro-nutrients. Furthermore, the soil P and Zn status also influences the difference in nutrient concentrations between mycorrhizal and non-mycorrhizal plants. The interactions identified by this meta-analysis provide a basis for future research in this area.

Keywords

Arbuscular mycorrhizas (AM) Micro-nutrients Macro-nutrients Nutrient interactions Phosphorus (P) Zinc (Zn) 76R, rmc Solanum lycopersicum (tomato) 

Notes

Acknowledgments

The authors wish to thank members of Cavlab, particularly Dr. Michael Rose for advice on the meta-analysis. We also gratefully acknowledge Prof. Sally Smith and A/Prof. Susan Barker for continued access to the rmc and 76R genotypes of tomato. We also thank Prof. Sally Smith for valuable discussions, and two anonymous reviewers for their helpful comments on an earlier version of this manuscript. TRC also wishes to acknowledge the Australian Research Council for financial support (FT120100463).

Supplementary material

11104_2014_2140_MOESM1_ESM.docx (92 kb)
ESM 1 (DOCX 92 kb)

References

  1. Abdel Latef AAH, Chaoxing H (2011) Effect of arbuscular mycorrhizal fungi on growth, mineral nutrition, antioxidant enzymes activity and fruit yield of tomato grown under salinity stress. Scientia Horticulturae 127(3):228–233. doi: 10.1016/j.scienta.2010.09.020 CrossRefGoogle Scholar
  2. Al-Karaki GN (2006) Nursery inoculation of tomato with arbuscular mycorrhizal fungi and subsequent performance under irrigation with saline water. Scientia Horticulturae 109(1):1–7. doi: 10.1016/j.scienta.2006.02.019 CrossRefGoogle Scholar
  3. Al-Karaki GN, Hammad R (2001) Mycorrhizal influence on fruit yield and mineral content of tomato grown under salt stress. J Plant Nutr 24(8):1311–1323. doi: 10.1081/PLN-100106983 CrossRefGoogle Scholar
  4. Al-Karaki GN, Hammad R, Rusan M (2001) Response of two tomato cultivars differing in salt tolerance to inoculation with mycorrhizal fungi under salt stress. Mycorrhiza 11(1):43–47CrossRefGoogle Scholar
  5. Alloway BJ (2008) Zinc in soils and crop nutrition. International Zinc Association and International Fertilizer Industry Association, Brussels, Belgium and Paris, FranceGoogle Scholar
  6. Arines J, VilariÑO A, Sainz M (1989) Effect of different inocula of vesicular-arbuscular mycorrhizal fungi on manganese content and concentration in red clover (Trifolium pratense L.) plants. New Phytologist 112(2):215–219. doi: 10.1111/j.1469-8137.1989.tb02376.x CrossRefGoogle Scholar
  7. Asghari HR, Cavagnaro TR (2011) Arbuscular mycorrhizas enhance plant interception of leached nutrients. Functional Plant Biology 38(3):219–226. doi: 10.1071/fp10180 CrossRefGoogle Scholar
  8. Asghari HR, Cavagnaro TR (2012) Arbuscular Mycorrhizas Reduce Nitrogen Loss via Leaching. Plos One 7(1):151–155. doi: 10.1371/journal.pone.0029825 CrossRefGoogle Scholar
  9. 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 Journal 15(6):791–797. doi: 10.1046/j.1365-313×.1998.00252.× CrossRefGoogle Scholar
  10. Bolan NS (1991) A critical review on the role of mycorrhizal fungi in the uptake of phosphorus by plants. Plant and Soil 134(2):189–207. doi: 10.1007/bf00012037 CrossRefGoogle Scholar
  11. Broadley M, Brown P, Cakmak I, Rengel Z, Zhao F (2012) Chapter 7 - Function of Nutrients: Micronutrients. In: Marschner P (ed) Marschner's Mineral Nutrition of Higher Plants, 3rd edn. Academic, San Diego, pp 191–248CrossRefGoogle Scholar
  12. Bryla DR, Koide RT (1998) Mycorrhizal response of two tomato genotypes relates to their ability to acquire and utilize phosphorus. Annals of Botany 82(6):849–857CrossRefGoogle Scholar
  13. Burkert B, Robson A (1994) Zn-65 uptake in subterranean clover (Trifolium-subterraneum l) by 3 vesicular-arbuscular mycorrhizal fungi in a root-free sandy soil. Soil Biol Biochem 26(9):1117–1124. doi: 10.1016/0038-0717(94)90133-3 CrossRefGoogle Scholar
  14. Burns AE, Gleadow RM, Zacarias AM, Cuambe CE, Miller RE, Cavagnaro TR (2012) Variations in the Chemical Composition of Cassava (Manihot esculenta Crantz) Leaves and Roots As Affected by Genotypic and Environmental Variation. Journal of Agricultural and Food Chemistry 60(19):4946–4956. doi: 10.1021/jf2047288 PubMedCrossRefGoogle Scholar
  15. Cardoso IM, Kuyper TW (2006) Mycorrhizas and tropical soil fertility. Agriculture, ecosystems & environment 116(1):72–84CrossRefGoogle Scholar
  16. Cavagnaro TR, Martin AW (2011) Arbuscular mycorrhizas in southeastern Australian processing tomato farm soils. Plant and Soil 340(1–2):327–336. doi: 10.1007/s11104-010-0603-z
  17. Cavagnaro TR, Gao LL, Smith FA, Smith SE (2001) Morphology of arbuscular mycorrhizas is influenced by fungal identity. New Phytol 151(2):469–475. doi: 10.1046/j.0028-646x.2001.00191.x
  18. 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(2):485–494. doi: 10.1046/j.1469-8137.2004.00967.x
  19. 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 and Soil 282(1–2):209–225. doi: 10.1007/s11104-005-5847-7 CrossRefGoogle Scholar
  20. Cavagnaro TR, Sokolow SK, Jackson LE (2007) Mycorrhizal effects on growth and nutrition of tomato under elevated atmospheric carbon dioxide. Funct Plant Biol 34(8):730–736. doi: 10.1071/fp06340
  21. 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(3):228–235. doi: 10.1071/fp07281
  22. Cavagnaro TR, Dickson S, Smith FA (2010) Arbuscular mycorrhizas modify plant responses to soil zinc addition. Plant and Soil 329(1–2):307–313. doi: 10.1007/s11104-009-0158-z CrossRefGoogle Scholar
  23. Cavagnaro TR, Barrios-Masias FH, Jackson LE (2012) Arbuscular mycorrhizas and their role in plant growth, nitrogen interception and soil gas efflux in an organic production system. Plant and Soil 353(1–2):181–194. doi: 10.1007/s11104-011-1021-6 CrossRefGoogle Scholar
  24. Cayton MTC, Reyes ED, Neue HU (1985) Effect of zinc fertilization on the mineral nutrition of rices differing in tolerance to zinc deficiency. Plant and Soil 87(3):319–327. doi: 10.1007/bf02181899 CrossRefGoogle Scholar
  25. Chen BD, Li XL, Tao HQ, Christie P, Wong MH (2003) The role of arbuscular mycorrhiza in zinc uptake by red clover growing in a calcareous soil spiked with various quantities of zinc. Chemosphere 50(6):839–846. doi: 10.1016/s0045-6535(02)00228-x PubMedCrossRefGoogle Scholar
  26. Chen BD, Shen H, Li XL, Feng G, Christie P (2004) Effects of EDTA application and arbuscular mycorrhizal colonization on growth and zinc uptake by maize (Zea mays L.) in soil experimentally contaminated with zinc. Plant and Soil 261(1–2):219–229. doi: 10.1023/B:PLSO.0000035538.09222.ff CrossRefGoogle Scholar
  27. Christie P, Li XL, Chen BD (2004) Arbuscular mycorrhiza can depress translocation of zinc to shoots of host plants in soils moderately polluted with zinc. Plant and Soil 261(1–2):209–217. doi: 10.1023/B:PLSO.0000035542.79345.1b CrossRefGoogle Scholar
  28. Clark RB, Zeto SK (2000) Mineral acquisition by arbuscular mycorrhizal plants. J Plant Nutr 23(7):867–902. doi: 10.1080/01904160009382068 CrossRefGoogle Scholar
  29. Cooper KM, Tinker PB (1978) Translocation and transfer of nutrients in vesicular-arbuscular mycorrhizas. 2. Uptake and translocation of phosphorus, zinc and sulfur. New Phytologist 81(1):43. doi: 10.1111/j.1469-8137.1978.tb01602.x CrossRefGoogle Scholar
  30. Diaz G, AzconAguilar C, Honrubia M (1996) Influence of arbuscular mycorrhizae on heavy metal (Zn and Pb) uptake and growth of Lygeum spartum and Anthyllis cytisoides. Plant and Soil 180(2):241–249. doi: 10.1007/bf00015307 CrossRefGoogle Scholar
  31. Egger M, Smith GD, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315(7109):629–634. doi: 10.1136/bmj.315.7109.629 PubMedCrossRefPubMedCentralGoogle Scholar
  32. Epstein E, Bloom AJ (2005) Mineral nutrition of plants: principles and perspectives, 2nd edn. Sinauer Associates, MAGoogle Scholar
  33. Fageria V (2001) Nutrient interactions in crop plants. J Plant Nutr 24(8):1269–1290CrossRefGoogle Scholar
  34. Foy CD, Chaney RL, White MC (1978) The Physiology of Metal Toxicity in Plants. Annual Review of Plant Physiology 29(1):511–566. doi: 10.1146/annurev.pp.29.060178.002455 CrossRefGoogle Scholar
  35. Gao LL, Delp G, Smith SE (2001) Colonization patterns in a mycorrhiza-defective mutant tomato vary with different arbuscular-mycorrhizal fungi. New Phytologist 151(2):477–491. doi: 10.1046/j.0028-646x.2001.00193.x CrossRefGoogle Scholar
  36. Gianinazzi S, Gollotte A, Binet MN, van Tuinen D, Redecker D, Wipf D (2010) Agroecology: the key role of arbuscular mycorrhizas in ecosystem services. Mycorrhiza 20(8):519–530. doi: 10.1007/s00572-010-0333-3 PubMedCrossRefGoogle Scholar
  37. Gildon A, Tinker PB (1983a) Interactions of vesicular arbuscular mycorrhizal infection and heavy metals in plants. 1. The effects of heavy metals on the development of vesicular-arbuscular mycorrhizas. New Phytologist 95(2):247–261. doi: 10.1111/j.1469-8137.1983.tb03491.x CrossRefGoogle Scholar
  38. Gildon A, Tinker PB (1983b) Interactions of vesicular arbuscular mycorrhizal infections and heavy-metals in plants. 2. The effects of infection on uptake of copper. New Phytologist 95(2):263–268. doi: 10.1111/j.1469-8137.1983.tb03492.x CrossRefGoogle Scholar
  39. Giri B, Mukerji KG (2004) Mycorrhizal inoculant alleviates salt stress in Sesbania aegyptiaca and Sesbania grandiflora under field conditions: evidence for reduced sodium and improved magnesium uptake. Mycorrhiza 14(5):307–312. doi: 10.1007/s00572-003-0274-1 PubMedCrossRefGoogle Scholar
  40. Graham RD, Welch RM, Grunes DL, Cary EE, Norvell WA (1987) Effect of Zinc Deficiency on the Accumulation of Boron and Other Mineral Nutrients in Barley. Soil Sci Soc Am J 51(3):652–657. doi: 10.2136/sssaj1987.03615995005100030018x CrossRefGoogle Scholar
  41. Grewal HS, Graham RD, Stangoulis J (1998) Zinc-boron interaction effects in oilseed rape. J Plant Nutr 21(10):2231–2243CrossRefGoogle Scholar
  42. Hallett PD, Feeney DS, Bengough AG, Rillig MC, Scrimgeour CM, Young IM (2009) Disentangling the impact of AM fungi versus roots on soil structure and water transport. Plant and Soil 314(1–2):183–196. doi: 10.1007/s11104-008-9717-y
  43. Higgins JPT, Thompson SG (2002) Quantifying heterogeneity in a meta-analysis. Statistics in Medicine 21(11):1539–1558. doi: 10.1002/sim.1186 PubMedCrossRefGoogle Scholar
  44. Higgins JP, Thompson SG, Deeks JJ, Altman DG (2003) Measuring inconsistency in meta-analyses. BMJ: British Medical Journal 327(7414):557PubMedCrossRefPubMedCentralGoogle Scholar
  45. Hildebrandt U, Regvar M, Bothe H (2007) Arbuscular mycorrhiza and heavy metal tolerance. Phytochemistry 68(1):139–146PubMedCrossRefGoogle Scholar
  46. Hosseini SM, Maftoun M, Karimian N, Ronaghi A, Emam Y (2007) Effect of Zinc x Boron Interaction on Plant Growth and Tissue Nutrient Concentration of Corn. J Plant Nutr 30(5):773–781. doi: 10.1080/01904160701289974 CrossRefGoogle Scholar
  47. Jansa J, Mozafar A, Frossard E (2003) Long-distance transport of P and Zn through the hyphae of an arbuscular mycorrhizal fungus in symbiosis with maize. Agronomie 23(5–6):481–488. doi: 10.1051/agro:2003013 CrossRefGoogle Scholar
  48. Johansen A, Jakobsen I, Jensen ES (1993) External hyphae of vesicular-arbuscular mycorrhizal fungi associated with Trifolium-subterraneum l. 3. Hyphal transport of P-32 and N-15. New Phytologist 124(1):61–68. doi: 10.1111/j.1469-8137.1993.tb03797.x CrossRefGoogle Scholar
  49. Juniper S, Abbott L (1993) Vesicular-arbuscular mycorrhizas and soil salinity. Mycorrhiza 4(2):45–57. doi: 10.1007/BF00204058 CrossRefGoogle Scholar
  50. Kothari SK, Marschner H, Romheld V (1991a) Contribution of the VA mycorrhizal hyphae in acquisition of phosphorus and zinc by maize grown in a calcareous soil. Plant and Soil 131(2):177–185. doi: 10.1007/bf00009447 CrossRefGoogle Scholar
  51. Kothari SK, Marschner H, Romheld V (1991b) Effect of a Vesicular-Arbuscular Mycorrhizal Fungus and Rhizosphere Micro- Organisms on Manganese Reduction in the Rhizosphere and Manganese Concentrations in Maize (Zea mays L.). New Phytologist 117(4):649–655. doi: 10.1111/j.1469-8137.1991.tb00969.x CrossRefGoogle Scholar
  52. Lambert D, Weidensaul T (1991) Element uptake by mycorrhizal soybean from sewage-sludge-treated soil. Soil Sci Soc Am J 55(2):393–398CrossRefGoogle Scholar
  53. Lambert DH, Baker DE, Cole H (1979) Role of mycorrhizae in the interactions of phosphorus with zinc, copper, and other elements. Soil Sci Soc Am J 43(5):976–980CrossRefGoogle Scholar
  54. Lee YJ, George E (2005) Contribution of mycorrhizal hyphae to the uptake of metal cations by cucumber plants at two levels of phosphorus supply. Plant and Soil 278(1–2):361–370. doi: 10.1007/s11104-005-0373-1 CrossRefGoogle Scholar
  55. Li XL, Marschner H, George E (1991) Acquisition of phosphorus and copper by VA-mycorrhizal hyphae and root-to-shoot transport in white clover. Plant and Soil 136(1):49–57. doi: 10.1007/bf02465219 CrossRefGoogle Scholar
  56. Liu A, Hamel C, Hamilton RI, Ma BL, Smith DL (2000) Acquisition of Cu, Zn, Mn and Fe by mycorrhizal maize (Zea mays L.) grown in soil at different P and micronutrient levels. Mycorrhiza 9(6):331–336. doi: 10.1007/s005720050277 CrossRefGoogle Scholar
  57. Loneragan JF, Webb MJ (1993) Interactions Between Zinc and Other Nutrients Affecting the Growth of Plants, vol 55. Zinc in Soils and Plants. Kluwer Academic Publ, DordrechtGoogle Scholar
  58. Loneragan JF, Grove TS, Robson AD, Snowball K (1979) Phosphorus Toxicity as a Factor in Zinc-Phosphorus Interactions in Plants. Soil Sci Soc Am J 43(5):966–972CrossRefGoogle Scholar
  59. Manjarrez M, Smith FA, Marschner P, Smith SE (2008) Is cortical root colonization required for carbon transfer to arbuscular mycorrhizal fungi? Evidence from colonization phenotypes and spore production in the reduced mycorrhizal colonization (rmc) mutant of tomato. Botany 86(9):1009–1019. doi: 10.1139/b08-043 CrossRefGoogle Scholar
  60. Manjarrez M, Wallwork M, Smith SE, Smith FA, Dickson S (2009) Different arbuscular mycorrhizal fungi induce differences in cellular responses and fungal activity in a mycorrhiza-defective mutant of tomato (rmc). Funct Plant Biol 36(1):86–96. doi: 10.1071/fp08032
  61. Manjarrez M, Christophersen HM, Smith SE, Smith FA (2010) Cortical colonisation is not an absolute requirement for phosphorus transfer to plants in arbuscular mycorrhizas formed by Scutellospora calospora in a tomato mutant: evidence from physiology and gene expression. Funct Plant Biol 37(12):1132–1142Google Scholar
  62. Marschner P (2012) Chapter 15 - Rhizosphere Biology. In: Marschner P (ed) Marschner's Mineral Nutrition of Higher Plants, 3rd edn. Academic, San Diego, pp 369–388CrossRefGoogle Scholar
  63. Marschner H, Dell B (1994) Nutrient uptake in mycorrhizal symbiosis. Plant and Soil 159(1):89–102Google Scholar
  64. Marschner P, Timonen S (2005) Interactions between plant species and mycorrhizal colonization on the bacterial community composition in the rhizosphere. Appl Soil Ecol 28(1):23–36. doi: 10.1016/j.apsoil.2004.06.007
  65. Meier S, Azcon R, Cartes P, Borie F, Cornejo P (2011) Alleviation of Cu toxicity in Oenothera picensis by copper-adapted arbuscular mycorrhizal fungi and treated agrowaste residue. Applied Soil Ecology 48(2):117–124CrossRefGoogle Scholar
  66. Merrild MP, Ambus P, Rosendahl S, Jakobsen I (2013) Common arbuscular mycorrhizal networks amplify competition for phosphorus between seedlings and established plants. New Phytologist 200(1):229–240. doi: 10.1111/nph.12351 PubMedCrossRefGoogle Scholar
  67. Miller RE, Gleadow RM, Cavagnaro TR (2014) Age versus stage: does ontogeny modify the effect of phosphorus and arbuscular mycorrhizas on above- and below-ground defence in forage sorghum? Plant. Cell & Environment 37(4):929–942. doi: 10.1111/pce.12209 CrossRefGoogle Scholar
  68. Nakagawa S, Santos EA (2012) Methodological issues and advances in biological meta-analysis. Evol Ecol 26(5):1253–1274. doi: 10.1007/s10682-012-9555-5 CrossRefGoogle Scholar
  69. Ortas I, Ortakci D, Kaya Z, Cinar A, Onelge N (2002) Mycorrhizal dependency of sour orange in relation to phosphorus and zinc nutrition. J Plant Nutr 25(6):1263–1279. doi: 10.1081/pln-120004387 CrossRefGoogle Scholar
  70. Peverill KI, Sparrow LA, Reuter DJ (1999) Soil Analysis: An Interpretation Manual. CSIRO PublishingGoogle Scholar
  71. Plenchette C, Fortin J, Furlan V (1983) Growth responses of several plant species to mycorrhizae in a soil of moderate P-fertility. Plant and Soil 70(2):199–209CrossRefGoogle Scholar
  72. Poulsen KH, Nagy R, Gao LL, 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 Phytologist 168(2):445–453. doi: 10.1111/j.1469-8137.2005.01523.x PubMedCrossRefGoogle Scholar
  73. Reuter DJ, Robinson JB (1997) Plant analysis: an interpretation manual, 2nd edn. CSIRO Publishing, MelbourneGoogle Scholar
  74. Rhodes LH, Gerdemann JW (1975) Phosphate Uptake Zones of Mycorrhizal and Non-Mycorrhizal Onions. New Phytologist 75(3):555–561. doi: 10.2307/2431598 CrossRefGoogle Scholar
  75. Rhodes LH, Gerdemann JW (1978a) Hyphal translocation and uptake of sulfur by vesicular-arbuscular mycorrhizae of onion. Soil Biol Biochem 10(5):355–360. doi: 10.1016/0038-0717(78)90057-3 CrossRefGoogle Scholar
  76. Rhodes LH, Gerdemann JW (1978b) Translocation of calcium and phosphate by external hyphae of vesicular-arbuscular mycorrhizae. Soil Science 126(2):125–126. doi: 10.1097/00010694-197808000-00009 CrossRefGoogle Scholar
  77. 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 and Soil 308(1–2):267–275. doi: 10.1007/s11104-008-9629-x CrossRefGoogle Scholar
  78. Robson AD, Pitman MG (1983) Interactions between nutrients in higher plants. Encyclopedia Plant Physiology New Series, vol 15A. Springer, BerlinGoogle Scholar
  79. Rose MT, Patti AF, Little KR, Brown AL, Jackson WR, Cavagnaro TR (2014) Chapter Two - A Meta-Analysis and Review of Plant-Growth Response to Humic Substances: Practical Implications for Agriculture. In: Donald LS (ed) Advances in Agronomy, vol Volume 124. Academic Press, pp 37-89Google Scholar
  80. Ruzicka DR, Hausmann NT, Barrios-Masias FH, Jackson LE, Schachtman DP (2012) Transcriptomic and metabolic responses of mycorrhizal roots to nitrogen patches under field conditions. Plant and Soil 350(1–2):145–162. doi: 10.1007/s11104-011-0890-z
  81. Shen H, Christie P, Li X (2006) Uptake of zinc, cadmium and phosphorus by arbuscular mycorrhizal maize (Zea mays L.) from a low available phosphorus calcareous soil spiked with zinc and cadmium. Environmental Geochemistry and Health 28(1–2):111–119. doi: 10.1007/s10653-005-9020-2 PubMedCrossRefGoogle Scholar
  82. Smith SE, Read DJ (2008) Mycorrhizal Symbiosis, 3rd edn. Academic, New YorkGoogle Scholar
  83. Smith SE, Smith FA, Jakobsen I (2003) Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses. Plant Physiol 133(1):16–20. doi: 10.1104/pp. 103.024380 PubMedCrossRefPubMedCentralGoogle Scholar
  84. Sonmez O, Aydemir S, Kaya C (2009) Mitigation effects of mycorrhiza on boron toxicity in wheat (Triticum durum) plants. New Zealand Journal of Crop and Horticultural Science 37(2):99–104CrossRefGoogle Scholar
  85. Subramanian K, Santhanakrishnan P, Balasubramanian P (2006) Responses of field grown tomato plants to arbuscular mycorrhizal fungal colonization under varying intensities of drought stress. Scientia horticulturae 107(3):245–253CrossRefGoogle Scholar
  86. Schwarz D, Welter S, George E, Franken P, Lehmann K, Weckwerth W, Doelle S, Worm M (2011) Impact of arbuscular mycorrhizal fungi on the allergenic potential of tomato. Mycorrhiza 21(5):341–349. doi: 10.1007/s00572-010-0345-z
  87. Tang J-L, Liu JLY (2000) Misleading funnel plot for detection of bias in meta-analysis. Journal of Clinical Epidemiology 53(5):477–484PubMedCrossRefGoogle Scholar
  88. Thompson SG, Higgins JPT (2002) How should meta-regression analyses be undertaken and interpreted? Statistics in Medicine 21(11):1559–1573. doi: 10.1002/sim.1187 PubMedCrossRefGoogle Scholar
  89. Veresoglou SD, Chen B, Rillig MC (2012) Arbuscular mycorrhiza and soil nitrogen cycling. Soil Biology and Biochemistry 46:53–62CrossRefGoogle Scholar
  90. Viechtbauer W (2010) Conducting meta-analyses in R with the metafor package. Journal of Statistical Software 36(3):1–48Google Scholar
  91. Warnock RE (1970) Micronutrient Uptake and Mobility Within Corn Plants (Zea mays L.) in Relation to Phosphorus-induced Zinc Deficiency1. Soil Sci Soc Am J 34(5):765–769. doi: 10.2136/sssaj1970.03615995003400050028× CrossRefGoogle Scholar
  92. Watts-Williams S, Cavagnaro T (2012) Arbuscular mycorrhizas modify tomato responses to soil zinc and phosphorus addition. Biology and Fertility of Soils 48(3):285–294. doi: 10.1007/s00374-011-0621-× CrossRefGoogle Scholar
  93. Watts-Williams S, Patti A, Cavagnaro T (2013) Arbuscular mycorrhizas are beneficial under both deficient and toxic soil zinc conditions. Plant and Soil 371(1–2):299–312. doi: 10.1007/s11104-013-1670-8 CrossRefGoogle Scholar
  94. Watts-Williams S, Turney T, Patti A, Cavagnaro T (2014) Uptake of zinc and phosphorus by plants is affected by zinc fertiliser material and arbuscular mycorrhizas. Plant and Soil 1–11. doi: 10.1007/s11104-013-1967-7
  95. Zhu YG, Christie P, Laidlaw AS (2001) Uptake of Zn by arbuscular mycorrhizal white clover from Zn-contaminated soil. Chemosphere 42(2):193–199. doi: 10.1016/s0045-6535(00)00125-9 PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  1. 1.School of Biological SciencesMonash UniversityClayton, MelbourneAustralia
  2. 2.School of Agriculture, Food and WineThe University of AdelaideAdelaideAustralia

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