Arbuscular mycorrhizas are beneficial under both deficient and toxic soil zinc conditions

Abstract

Background and aims

Arbuscular mycorrhizas (AM) play different roles in plant Zn nutrition depending on whether the soil is Zn-deficient (AM enhancement of plant Zn uptake) or Zn-toxic (AM protection of plant from excessive Zn uptake). In addition, soil P concentration modifies the response of AM to soil Zn conditions. We undertook a glasshouse experiment to study the interactive effects of P and Zn on AM colonisation, plant growth and nutrition, focusing on the two extremes of soil Zn concentration—deficient and toxic.

Methods

We used a mycorrhiza-defective tomato (Solanum lycopersicum) genotype (rmc) and compared it to its wild-type counterpart (76R). Plants were grown in pots amended with five soil P addition treatments, and two soil Zn addition treatments.

Results

The mycorrhizal genotype generally thrived better than the non-mycorrhizal genotype, in terms of biomass and tissue P and Zn concentrations. This was especially true under low soil Zn and P conditions, however there was evidence of the ‘protective effect’ of mycorrhizas when soil was Zn-contaminated. Above- and below-ground allocation of biomass, P and Zn were significantly affected by AM colonisation, and toxic soil Zn conditions.

Conclusions

The relationship between soil Zn and soil P was highly interactive, and heavily influenced AM colonisation, plant growth, and plant nutrition.

This is a preview of subscription content, access via your institution.

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

References

  1. 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.1365-313X.1998.00252.x

    Article  CAS  Google Scholar 

  2. Bi YL, Li XL, Christie P (2003) Influence of early stages of arbuscular mycorrhiza on uptake of zinc and phosphorus by red clover from a low-phosphorus soil amended with zinc and phosphorus. Chemosphere 50(6):831–837. doi:10.1016/s0045-6535(02)00227-8

    PubMed  Article  CAS  Google Scholar 

  3. Bolan NS (1991) A critical review on the role of mycorrhizal fungi in the uptake of phosphorus by plants. Plant Soil 134(2):189–207. doi:10.1007/bf00012037

    Article  CAS  Google Scholar 

  4. Bolan NS, Robson AD, Barrow NJ (1984) Increasing phosphorus supply can increase the infection of plant roots by vesicular-arbuscular mycorrhizal fungi. Soil Biol Biochem 16(4):419–420. doi:10.1016/0038-0717(84)90043-9

    Article  CAS  Google Scholar 

  5. Bradley R, Burt AJ, Read DJ (1981) Mycorrhizal infection and resistance to heavy metal toxicity in Calluna vulgaris. Nature 292(5821):335–337. doi:10.1038/292335a0

    Article  CAS  Google Scholar 

  6. Brown MT, Wilkins DA (1985) Zinc tolerance of mycorrhizal Betula. New Phytol 99(1):101–106

    Article  CAS  Google Scholar 

  7. Burleigh SH, Kristensen BK, Bechmann IE (2003) A plasma membrane zinc transporter from Medicago truncatula is up-regulated in roots by Zn fertilization, yet down-regulated by arbuscular mycorrhizal colonization. Plant MolBiol 52(5):1077–1088. doi:10.1023/a:1025479701246

    CAS  Google Scholar 

  8. 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. J Agric Food Chem 60(19):4946–4956. doi:10.1021/jf2047288

    PubMed  Article  CAS  Google Scholar 

  9. Cakmak I, Marschner H (1986) Mechanism of phosphorus induced zinc deficiency in cotton. I. Zinc deficiency-enhanced uptake rate of phosphorus. Physiol Plant 68(3):483–490. doi:10.1111/j.1399-3054.1986.tb03386.x

    Article  CAS  Google Scholar 

  10. Cardoso IM, Kuyper TW (2006) Mycorrhizas and tropical soil fertility. Agric Ecosyst Environ 116(1–2):72–84. doi:10.1016/j.agee.2006.03.011

    Article  Google Scholar 

  11. Cavagnaro TR (2008) The role of arbuscular mycorrhizas in improving plant zinc nutrition under low soil zinc concentrations: a review. Plant Soil 304(1–2):315–325. doi:10.1007/s11104-008-9559-7

    Article  CAS  Google Scholar 

  12. Cavagnaro TR, Martin AW (2011) Arbuscular mycorrhizas in southeastern Australian processing tomato farm soils. Plant Soil 340(1–2):327–336. doi:10.1007/s11104-010-0603-z

    Article  CAS  Google Scholar 

  13. Cavagnaro TR, Smith FA, Lorimer MF, Haskard KA, Ayling SM, Smith SE (2001) Quantitative development of Paris-type arbuscular mycorrhizas formed between Asphodelus fistulosus and Glomus coronatum. New Phytol 149(1):105–113. doi:10.1046/j.1469-8137.2001.00001.x

    Article  Google Scholar 

  14. Cavagnaro TR, Smith FA, Ayling SM, Smith SE (2003) Growth and phosphorus nutrition of a Paris-type arbuscular mycorrhizal symbiosis. New Phytol 157(1):127–134. doi:10.1046/j.1469-8137.2003.00654.x

    Article  Google Scholar 

  15. Cavagnaro TR, Dickson S, Smith FA (2010) Arbuscular mycorrhizas modify plant responses to soil zinc addition. Plant Soil 329(1–2):307–313. doi:10.1007/s11104-009-0158-z

    Article  CAS  Google Scholar 

  16. 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

    PubMed  Article  CAS  Google Scholar 

  17. 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 Soil 261(1–2):219–229. doi:10.1023/B:PLSO.0000035538.09222.ff

    Article  CAS  Google Scholar 

  18. 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(1–2):209–217. doi:10.1023/B:PLSO.0000035542.79345.1b

    Article  CAS  Google Scholar 

  19. Clark RB, Zeto SK (2000) Mineral acquisition by arbuscular mycorrhizal plants. J Plant Nutr 23(7):867–902. doi:10.1080/01904160009382068

    Article  CAS  Google Scholar 

  20. 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 Soil 180(2):241–249. doi:10.1007/bf00015307

    Article  CAS  Google Scholar 

  21. Dueck TA, Visser P, Ernst WHO, Schat H (1986) Vesicular-arbuscular mycorrhizae decrease zinc-toxicity to grasses growing in zinc-polluted soil. Soil Biol Biochem 18(3):331–333. doi:10.1016/0038-0717(86)90070-2

    Article  Google Scholar 

  22. Facelli E, Smith SE, Facelli JM, Christophersen HM, Smith FA (2010) Underground friends or enemies: model plants help to unravel direct and indirect effects of arbuscular mycorrhizal fungi on plant competition. New Phytol 185(4):1050–1061. doi:10.1111/j.1469-8137.2009.03162.x

    PubMed  Article  Google Scholar 

  23. Fomina M, Charnock J, Bowen AD, Gadd GM (2007) X-ray absorption spectroscopy (XAS) of toxic metal mineral transformations by fungi. Environ Microbiol 9(2):308–321. doi:10.1111/j.1462-2920.2006.01139.x

    PubMed  Article  CAS  Google Scholar 

  24. Fredeen AL, Rao IM, Terry N (1989) Influence of phosphorus nutrition on growth and carbon partitioning in Glycine max. Plant Physiol 89(1):225–230. doi:10.1104/pp.89.1.225

    PubMed  Article  CAS  Google Scholar 

  25. Gildon A, Tinker PB (1983) 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 Phytol 95(2):247–261. doi:10.1111/j.1469-8137.1983.tb03491.x

    Article  CAS  Google Scholar 

  26. Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol 84(3):489–500

    Article  Google Scholar 

  27. Gonzalez-Guerrero M, Azcon-Aguilar C, Mooney M, Valderas A, MacDiarmid CW, Eide DJ, Ferrol N (2005) Characterization of a Glomus intraradices gene encoding a putative Zn transporter of the cation diffusion facilitator family. Fungal Genet Biol 42(2):130–140. doi:10.1016/j.fgb.2004.10.007

    PubMed  Article  CAS  Google Scholar 

  28. Gonzalez-Guerrero M, Melville LH, Ferrol N, Lott JNA, Azcon-Aguilar C, Peterson RL (2008) Ultrastructural localization of heavy metals in the extraradical mycelium and spores of the arbuscular mycorrhizal fungus Glomus intraradices. Can J Microbiol 54(2):103–110. doi:10.1139/w07-119

    PubMed  Article  CAS  Google Scholar 

  29. 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(2):341–350. doi:10.1046/j.1469-8137.2003.00826.x

    Article  CAS  Google Scholar 

  30. Impa SM, Johnson-Beebout S (2012) Mitigating zinc deficiency and achieving high grain Zn in rice through integration of soil chemistry and plant physiology research. Plant and Soil:1-39. doi:10.1007/s11104-012-1315-3

  31. Kafkas S, Ortas I (2009) Various mycorrhizal fungi enhance dry weights, P and Zn uptake of four Pistacia species. J Plant Nutr 32(1):146–159. doi:10.1080/01904160802609005

    Article  CAS  Google Scholar 

  32. Kizilgoz I, Sakin E (2010) The effects of increased phosphorus application on shoot dry matter, shoot P and Zn concentrations in wheat (Triticum durum L.) and maize (Zea mays L.) grown in a calcareous soil. Afr J Biotechnol 9(36):5893–5896

    CAS  Google Scholar 

  33. Koide R (2010) Mycorrhizal symbiosis and plant reproduction. In: Koltai H, Kapulnik Y (eds) Arbuscular mycorrhizas: physiology and function. Springer, Netherlands, pp 297–320

    Google Scholar 

  34. Larue JH, McClellan WD, Peacock WL (1975) Mycorrhizal fungi and peach nursery nutrition. Calif Agric 29(5):7

    Google Scholar 

  35. 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 Soil 278(1–2):361–370. doi:10.1007/s11104-005-0373-1

    Article  CAS  Google Scholar 

  36. Leyval C, Berthelin J, Schontz D, Weissenhorn I, Morel JL (1991) Influence of endomycorrhizas on maize uptake of Pb, Cu, Zn and Cd applied as mineral salts or sewage sludge. In: Farmer JG (ed) Heavy metals in the environment. CEP Consultants Ltd., Edinburgh

    Google Scholar 

  37. 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(2):201–207. doi:10.1016/s0045-6535(00)00126-0

    PubMed  Article  CAS  Google Scholar 

  38. 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

    Article  CAS  Google Scholar 

  39. Lu XH, Koide RT (1994) The effects of mycorrhizal infection on components of plant growth and reproduction. New Phytol 128(2):211–218. doi:10.1111/j.1469-8137.1994.tb04004.x

    Article  CAS  Google Scholar 

  40. Marschner H, Dell B (1994) Nutrient uptake in mycorrhizal symbiosis. Plant Soil 159(1):89–102

    CAS  Google Scholar 

  41. 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

    Article  Google Scholar 

  42. Nord EA, Shea K, Lynch JP (2011) Optimizing reproductive phenology in a two-resource world: a dynamic allocation model of plant growth predicts later reproduction in phosphorus-limited plants. Ann Bot. doi:10.1093/aob/mcr143

  43. Ortas I (2012) Do maize and pepper plants depend on mycorrhizae in terms of phosphorus and zinc uptake? J Plant Nutr 35(11):1639–1656. doi:10.1080/01904167.2012.698346

    Article  CAS  Google Scholar 

  44. 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

    Article  CAS  Google Scholar 

  45. Pawlowska TE, Blaszkowski J, Ruhling A (1996) The mycorrhizal status of plants colonizing a calamine spoil mound in southern Poland. Mycorrhiza 6(6):499–505

    Article  Google Scholar 

  46. 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

    Article  Google Scholar 

  47. 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(2):445–453. doi:10.1111/j.1469-8137.2005.01523.x

    PubMed  Article  CAS  Google Scholar 

  48. Ryan MH, Angus JF (2003) Arbuscular mycorrhizae in wheat and field pea crops on a low P soil: increased Zn-uptake but no increase in P-uptake or yield. Plant Soil 250(2):225–239. doi:10.1023/a:1022839930134

    Article  CAS  Google Scholar 

  49. Scheublin TR, Van Logtestijn RSP, Van Der Heijden MGA (2007) Presence and identity of arbuscular mycorrhizal fungi influence competitive interactions between plant species. J Ecol 95(4):631–638. doi:10.1111/j.1365-2745.2007.01244.x

    Article  CAS  Google Scholar 

  50. Shetty KG, Hetrick BAD, Figge DAH, Schwab AP (1994) Effects of mycorrhizae and other soil microbes on revegetation of heavy metal contaminated mine spoil. Environ Pollut 86(2):181–188. doi:10.1016/0269-7491(94)90189-9

    PubMed  Article  CAS  Google Scholar 

  51. Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic, New York

    Google Scholar 

  52. Timmer LW, Leyden RF (1980) The relationship of mycorrhizal infection to phosphorus-induced copper deficiency in sour orange seedlings. New Phytol 85(1):15. doi:10.1111/j.1469-8137.1980.tb04443.x

    Article  CAS  Google Scholar 

  53. Tinker PB, Nye PH (2000) Solute movement in the rhizosphere. Oxford University Press, Oxford

    Google Scholar 

  54. van der Heijden MGA, Wiemken A, Sanders IR (2003) Different arbuscular mycorrhizal fungi alter coexistence and resource distribution between co-occurring plant. New Phytol 157(3):569–578. doi:10.1046/j.1469-8137.2003.00688.x

    Article  Google Scholar 

  55. Veresoglou SD, Menexes G, Rillig MC (2012) Do arbuscular mycorrhizal fungi affect the allometric partition of host plant biomass to shoots and roots? A meta-analysis of studies from 1990 to 2010. Mycorrhiza 22(3):227–235. doi:10.1007/s00572-011-0398-7

    PubMed  Article  Google Scholar 

  56. Wasserman JL, Mineo L, Majumdar SK, Vantyne C (1987) Detection of heavy metals in oak mycorrhizae of northeastern Pennsylvania forests, using x-ray microanalysis. Can J Bot-Rev Can Bot 65(12):2622–2627

    Article  CAS  Google Scholar 

  57. Watts-Williams S, Cavagnaro T (2012) Arbuscular mycorrhizas modify tomato responses to soil zinc and phosphorus addition. Biol Fertil Soils 48(3):285–294. doi:10.1007/s00374-011-0621-x

    Article  CAS  Google Scholar 

  58. Weissenhorn I, Leyval C (1995) Root colonization of maize by a Cd-sensitive and a Cd-tolerant Glomus mosseae and cadmium uptake in sand culture. Plant Soil 175(2):233–238. doi:10.1007/bf00011359

    Article  CAS  Google Scholar 

  59. Weissenhorn I, Leyval C, Berthelin J (1993) Cd-tolerant arbuscular mycorrhizal (AM) fungi from heavy-metal polluted soils. Plant Soil 157(2):247–256. doi:10.1007/bf00011053

    Article  CAS  Google Scholar 

  60. Yun W, Pratt ST, Miller RM, Cai Z, Hunter DB, Jarstfer AG, Kemner KM, Lai B, Lee HR, Legnini DG, Rodrigues W, Smith CI (1998) X-ray imaging and microspectroscopy of plants and fungi. J Synchrot Radiation 5:1390–1395. doi:10.1107/s0909049598007225

    Article  CAS  Google Scholar 

  61. Zar JH (2007) Biostatistical Analysis (5th Edition). Prentice-Hall, Inc.,

  62. Zhu YG, Smith SE, Smith FA (2001) Zinc (Zn)-phosphorus (P) interactions in two cultivars of spring wheat (Triticum aestivum L.) differing in P uptake efficiency. Ann Bot 88(5):941–945. doi:10.1006/anbo.2001.1522

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors wish to thank Dr Michael Rose and other members of the ‘Cav-Lab’ for valuable discussions. We also gratefully acknowledge Dr Susan Barker and Prof. Sally Smith for continued access to the rmc and 76R genotypes of tomato. This research was in part funded by the Monash University, School of Biological Sciences. TRC also wishes to acknowledge the Australian Research Council and the Monash Research Accelerator program for financial support.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Stephanie J. Watts-Williams.

Additional information

Responsible Editor: Peter Christie.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Watts-Williams, S.J., Patti, A.F. & Cavagnaro, T.R. Arbuscular mycorrhizas are beneficial under both deficient and toxic soil zinc conditions. Plant Soil 371, 299–312 (2013). https://doi.org/10.1007/s11104-013-1670-8

Download citation

Keywords

  • Arbuscular mycorrhizas (AM)
  • Zinc
  • Phosphorus
  • Mycorrhiza defective tomato mutant (rmc)
  • Solanum lycopersicum (Tomato)