Skip to main content
Log in

How important is the mycorrhizal pathway for plant Zn uptake?

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Introduction

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.

Methods

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.

Results

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.

Conclusions

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Alloway BJ (2008) Zinc in soils and crop nutrition. International Zinc Association and International Fertilizer Industry Association, Brussels

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Cavagnaro TR (2014) Impacts of compost application on the formation and functioning of arbuscular mycorrhizas. Soil Biol Biochem 78. doi: http://dx.doi.org/10.1016/j.soilbio.2014.07.007

  • 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

    Article  Google Scholar 

  • 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.

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Graham RD, Welch RM (1997) A strategy for breeding staple-food crops with high micronutrient density. Natl Research Council Canada, Ottawa

    Book  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Jung MC, Thornton I (1996) Heavy metal contamination of soils and plants in the vicinity of a lead-zinc mine, Korea. Appl Geochem 11:53–59

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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 43:976–980

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Lindsay W, Norvell WA (1978) Development of a DTPA soil test for zinc, iron, manganese, and copper. Soil Sci Soc Am J 42:421–428

    Article  CAS  Google Scholar 

  • 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 153:137–147

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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 32:229–240

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Rhodes LH, Gerdemann JW (1978b) Influence of phosphorus nutrition on sulfur uptake by vesicular-arbuscular mycorrhizae of onion. Soil Biol Biochem 10:361–364

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Schweiger PF, Jakobsen I (1999) Direct measurement of arbuscular mycorrhizal phosphorus uptake into field-grown winter wheat. Agron J 91:998–1002

    Article  Google Scholar 

  • Sinaj S, Dubois A, Frossard E (2004) Soil isotopically exchangeable zinc: a comparison between E and L values. Plant Soil 261:17–28

    Article  CAS  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic Press, New York

    Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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 10:151–164

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

  • 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

    Article  CAS  Google Scholar 

  • Wilkinson H, Loneragan J, Quirk J (1968) The movement of zinc to plant roots. Soil Sci Soc Am J 32:831–833

    Article  Google Scholar 

  • 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 18:131–146

    Article  CAS  Google Scholar 

  • 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 27:1331–1354

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Timothy R. Cavagnaro.

Additional information

Responsible Editor: Peter Christie.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Watts-Williams, S.J., Smith, F.A., McLaughlin, M.J. et al. How important is the mycorrhizal pathway for plant Zn uptake?. Plant Soil 390, 157–166 (2015). https://doi.org/10.1007/s11104-014-2374-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-014-2374-4

Keywords

Navigation