Plant and Soil

, Volume 390, Issue 1–2, pp 157–166 | Cite as

How important is the mycorrhizal pathway for plant Zn uptake?

  • Stephanie J. Watts-Williams
  • F. Andrew Smith
  • Michael J. McLaughlin
  • Antonio F. Patti
  • Timothy R. CavagnaroEmail author
Regular Article



Formation of arbuscular mycorrhizas can enhance plant uptake of immobile nutrients such as zinc (Zn) and phosphorus (P). Enhancement of Zn uptake by arbuscular mycorrhizal (AM) fungi on Zn-deficient soils has been studied previously, however, the quantity of Zn that is contributed by the AM pathway of uptake to the plant has not previously been reported for soil of any Zn status.


We grew a mycorrhiza-defective mutant tomato (Solanum lycopersicum L.) genotype (rmc) and its mycorrhizal wild-type progenitor (76R) in pots containing a hyphal compartment (HC) accessible only by the external hyphae of AM fungi, and containing the radioisotope 65Zn. This was repeated at three soil Zn concentrations, ranging from low to high. We estimated the amount of Zn delivered via both the AM and direct (root) pathways.


Up to 24 % of Zn in the shoots of the AM plants was delivered via the AM pathway at the lowest soil Zn treatment. This decreased significantly, to 8 %, as soil Zn concentration increased. No 65Zn was detected in the tissues of the non-mycorrhizal genotype.


The relative contribution to shoot Zn by the AM pathway of uptake was highest when soil Zn was low, and decreased with increasing soil Zn concentration.


Arbuscular mycorrhizal (AM) uptake Arbuscular mycorrhizas Phosphorus Plant nutrition Tomato (Solanum lycopersicum L.) Zinc 



The authors gratefully acknowledge Rebecca Stonor, Gillian Cozens, Bogumila Tomczak and Jessica Mackay for their excellent technical assistance. We would also like to thank Prof. Sally Smith and Prof. Iver Jakobsen for valuable discussions. TRC acknowledges the ARC for funding his research via the award of a Future Fellowship (FT120100463). SJWW wishes to acknowledge support received from the Monash University Postgraduate Publications Award.


  1. Alloway BJ (2008) Zinc in soils and crop nutrition. International Zinc Association and International Fertilizer Industry Association, BrusselsGoogle Scholar
  2. 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 15:791–797. doi: 10.1046/j.1365-313X.1998.00252.x CrossRefGoogle Scholar
  3. Bürkert 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 26:1117–1124. doi: 10.1016/0038-0717(94)90133-3 CrossRefGoogle Scholar
  4. Cakmak I (2002) Plant nutrition research: priorities to meet human needs for food in sustainable ways. Plant Soil 247:3–24. doi: 10.1023/a:1021194511492 CrossRefGoogle Scholar
  5. Cavagnaro TR (2008) The role of arbuscular mycorrhizas in improving plant zinc nutrition under low soil zinc concentrations: a review. Plant Soil 304:315–325. doi: 10.1007/s11104-008-9559-7 CrossRefGoogle Scholar
  6. Cavagnaro TR (2014) Impacts of compost application on the formation and functioning of arbuscular mycorrhizas. Soil Biol Biochem 78. doi: 10.1016/j.soilbio.2014.07.007
  7. Cavagnaro TR, Gao LL, Smith FA, Smith SE (2001) Morphology of arbuscular mycorrhizas is influenced by fungal identity. New Phytol 151:469–475. doi: 10.1046/j.0028-646x.2001.00191.x CrossRefGoogle Scholar
  8. 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 Phytologist 161: 485–494. doi: 10.1046/j.1469-8137.2004.00967.x.
  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 35:228–235. doi: 10.1071/fp07281 CrossRefGoogle Scholar
  10. Cavagnaro TR, Dickson S, Smith FA (2010) Arbuscular mycorrhizas modify plant responses to soil zinc addition. Plant Soil 329:307–313. doi: 10.1007/s11104-009-0158-z CrossRefGoogle Scholar
  11. 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 50:839–846. doi: 10.1016/s0045-6535(02)00228-x CrossRefPubMedGoogle Scholar
  12. 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 Soil 261:209–217. doi: 10.1023/B:PLSO.0000035542.79345.1b CrossRefGoogle Scholar
  13. Graham RD, Welch RM (1997) A strategy for breeding staple-food crops with high micronutrient density. Natl Research Council Canada, OttawaCrossRefGoogle Scholar
  14. Grønlund M, Albrechtsen M, Johansen IE, Hammer EC, Nielsen TH, Jakobsen I (2013) The interplay between P uptake pathways in mycorrhizal peas: a combined physiological and gene-silencing approach. Physiol Plant 149:234–248. doi: 10.1111/ppl.12030 CrossRefPubMedGoogle Scholar
  15. Hacisalihoglu G, Kochian LV (2003) How do some plants tolerate low levels of soil zinc? Mechanisms of zinc efficiency in crop plants. New Phytol 159:341–350. doi: 10.1046/j.1469-8137.2003.00826.x CrossRefGoogle Scholar
  16. Jakobsen I, Abbott LK, Robson AD (1992) External hyphae of vesicular—arbuscular mycorrhizal fungi associated with Trifolium subterraneum L 2. Hyphal transport of 32P over defined distances. New Phytol 120:509–516. doi: 10.1111/j.1469-8137.1992.tb01800.x CrossRefGoogle Scholar
  17. 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 23:481–488. doi: 10.1051/agro:2003013 CrossRefGoogle Scholar
  18. Johansen A, Jakobsen I, Jensen ES (1992) Hyphal transport of N-15-labeled nitrogen by a vesicular-arbuscular mycorrhizal fungus and its effect on depletion of inorganic soil-N. New Phytol 122:281–288. doi: 10.1111/j.1469-8137.1992.tb04232.x CrossRefGoogle Scholar
  19. 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 Phytol 124:61–68. doi: 10.1111/j.1469-8137.1993.tb03797.x CrossRefGoogle Scholar
  20. Johnson NC, Graham JH, Smith FA (1997) Functioning of mycorrhizal associations along the mutualism-parasitism continuum. New Phytol 135:575–586. doi: 10.1046/j.1469-8137.1997.00729.x CrossRefGoogle Scholar
  21. Joner EJ, Jakobsen I (1994) Contribution by 2 arbuscular mycorrhizal fungi to P-uptake by cucumber (Cucumis-sativus L) from P-32 labeled organic-matter during mineralization in soil. Plant Soil 163:203–209. doi: 10.1007/bf00007969 CrossRefGoogle Scholar
  22. Jung MC, Thornton I (1996) Heavy metal contamination of soils and plants in the vicinity of a lead-zinc mine, Korea. Appl Geochem 11:53–59CrossRefGoogle Scholar
  23. Kothari SK, Marschner H, Römheld V (1991) Contribution of the VA mycorrhizal hyphae in acquisition of phosphorus and zinc by maize grown in a calcareous soil. Plant Soil 131:177–185. doi: 10.1007/bf00009447 CrossRefGoogle Scholar
  24. 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 43:976–980CrossRefGoogle Scholar
  25. Li XL, Christie P (2001) Changes in soil solution Zn and pH and uptake of Zn by arbuscular mycorrhizal red clover in Zn-contaminated soil. Chemosphere 42:201–207. doi: 10.1016/s0045-6535(00)00126-0 CrossRefPubMedGoogle Scholar
  26. Lindsay W, Norvell WA (1978) Development of a DTPA soil test for zinc, iron, manganese, and copper. Soil Sci Soc Am J 42:421–428CrossRefGoogle Scholar
  27. Lingua G, Franchin C, Todeschini V, Castiglione S, Biondi S, Burlando B, Parravicini V, Torrigiani P, Berta G (2008) Arbuscular mycorrhizal fungi differentially affect the response to high zinc concentrations of two registered poplar clones. Environ Pollut 153:137–147CrossRefPubMedGoogle Scholar
  28. 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 9:331–336. doi: 10.1007/s005720050277 CrossRefGoogle Scholar
  29. McLaughlin MJ, Lancaster P, Sale P, Uren N, Peverill K (1994) Comparison of cation/anion exchange resin methods for multi-element testing of acidic soils. Soil Res 32:229–240CrossRefGoogle Scholar
  30. Mehravaran H, Mozafar A, Frossard E (2000) Uptake and partitioning of 32P and 65Zn by white clover as affected by eleven isolates of mycorrhizal fungi. J Plant Nutr 23:1385–1395. doi: 10.1080/01904160009382109 CrossRefGoogle Scholar
  31. Pearson JN, Jakobsen I (1993) The relative contribution of hyphae and roots to phosphorus uptake by arbuscular mycorrhizal plants, measured by dual labelling with 32P and 33P. New Phytol 124:489–494. doi: 10.1111/j.1469-8137.1993.tb03840.x CrossRefGoogle Scholar
  32. 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 Phytol 168:445–453. doi: 10.1111/j.1469-8137.2005.01523.x CrossRefPubMedGoogle Scholar
  33. Rhodes LH, Gerdemann JW (1978a) Hyphal translocation and uptake of sulfur by vesicular-arbuscular mycorrhizae of onion. Soil Biol Biochem 10:355–360. doi: 10.1016/0038-0717(78)90057-3 CrossRefGoogle Scholar
  34. Rhodes LH, Gerdemann JW (1978b) Influence of phosphorus nutrition on sulfur uptake by vesicular-arbuscular mycorrhizae of onion. Soil Biol Biochem 10:361–364CrossRefGoogle Scholar
  35. Rhodes LH, Gerdemann JW (1978c) Translocation of calcium and phosphate by external hyphae of vesicular-arbuscular mycorrhizae. Soil Sci 126:125–126. doi: 10.1097/00010694-197808000-00009 CrossRefGoogle Scholar
  36. Schweiger PF, Jakobsen I (1999) Direct measurement of arbuscular mycorrhizal phosphorus uptake into field-grown winter wheat. Agron J 91:998–1002CrossRefGoogle Scholar
  37. Sinaj S, Dubois A, Frossard E (2004) Soil isotopically exchangeable zinc: a comparison between E and L values. Plant Soil 261:17–28CrossRefGoogle Scholar
  38. Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic Press, New YorkGoogle Scholar
  39. Smith SE, Smith FA, Jakobsen I (2003) Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses. Plant Physiol 133:16–20. doi: 10.1104/pp. 103.024380 CrossRefPubMedCentralPubMedGoogle Scholar
  40. Smith SE, Smith FA, Jakobsen I (2004) Functional diversity in arbuscular mycorrhizal (AM) symbioses: the contribution of the mycorrhizal P uptake pathway is not correlated with mycorrhizal responses in growth or total P uptake. New Phytol 162:511–524. doi: 10.1111/j.1469-8137.2004.01039.x CrossRefGoogle Scholar
  41. Thingstrup I, Kahiluoto H, Jakobsen I (2000) Phosphate transport by hyphae of field communities of arbuscular mycorrhizal fungi at two levels of P fertilization. Plant Soil 221:181–187. doi: 10.1023/a:1004721626216 CrossRefGoogle Scholar
  42. Tiller K, Honeysett J, De VM (1972) Soil zinc and its uptake by plants. I. Isotopic exchange equilibria and the application of tracer techniques. II. Soil chemistry in relation to prediction of availability. Soil Res 10:151–164CrossRefGoogle Scholar
  43. Watts-Williams SJ, Cavagnaro TR (2012) Arbuscular mycorrhizas modify tomato responses to soil zinc and phosphorus addition. Biol Fertil Soils 48:285–294. doi: 10.1007/s00374-011-0621-x CrossRefGoogle Scholar
  44. Watts-Williams SJ, Cavagnaro TR (2014) Nutrient interactions and arbuscular mycorrhizas: a meta-analysis of a mycorrhiza-defective mutant and wild-type tomato genotype pair. Plant Soil 384:79–92. doi: 10.1007/s11104-014-2140-7 CrossRefGoogle Scholar
  45. Watts-Williams SJ, Patti AF, Cavagnaro TR (2013) Arbuscular mycorrhizas are beneficial under both deficient and toxic soil zinc conditions. Plant Soil 371:299–312. doi:  10.1007/s11104-013-1670-8
  46. Watts-Williams SJ, Turney TW, Patti AF, Cavagnaro TR (2014) Uptake of zinc and phosphorus by plants is affected by zinc fertiliser material and arbuscular mycorrhizas. Plant Soil 376:165–175. doi: 10.1007/s11104-013-1967-7 CrossRefGoogle Scholar
  47. Wilkinson H, Loneragan J, Quirk J (1968) The movement of zinc to plant roots. Soil Sci Soc Am J 32:831–833CrossRefGoogle Scholar
  48. Zarcinas B, Cartwright B, Spouncer L (1987) Nitric acid digestion and multi‐element analysis of plant material by inductively coupled plasma spectrometry. C Soil Sci Plant Anal 18:131–146CrossRefGoogle Scholar
  49. Zarcinas BA, McLaughlin MJ, Smart MK (1996) The effect of acid digestion technique on the performance of nebulization systems used in inductively coupled plasma spectrometry. C Soil Sci Plant Anal 27:1331–1354CrossRefGoogle Scholar
  50. Zhu YG, Christie P, Laidlaw AS (2001) Uptake of Zn by arbuscular mycorrhizal white clover from Zn-contaminated soil. Chemosphere 42:193–199. doi: 10.1016/s0045-6535(00)00125-9 CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • Stephanie J. Watts-Williams
    • 1
  • F. Andrew Smith
    • 2
  • Michael J. McLaughlin
    • 2
    • 3
  • Antonio F. Patti
    • 4
  • Timothy R. Cavagnaro
    • 2
    Email author
  1. 1.School of Biological SciencesMonash UniversityClaytonAustralia
  2. 2.School of Agriculture, Food and WineThe University of AdelaideGlen OsmondAustralia
  3. 3.CSIRO, Land and Water Flagship, PMB 2Glen OsmondAustralia
  4. 4.School of ChemistryMonash UniversityClaytonAustralia

Personalised recommendations