Advertisement

Mycorrhiza

pp 1–13 | Cite as

Arbuscular mycorrhizal fungal inoculation and soil zinc fertilisation affect the productivity and the bioavailability of zinc and iron in durum wheat

  • Binh T. T. Tran
  • Timothy R. Cavagnaro
  • Stephanie J. Watts-WilliamsEmail author
Original Article

Abstract

There is a growing recognition of the role of arbuscular mycorrhizal fungi (AMF) in food security, specifically the potential for AMF to enhance the yield and mineral nutrition—including phosphorus, zinc (Zn), and iron (Fe)—of food crops. However, the bioavailability of Zn and Fe for humans in the grain of cereal crops can be overestimated by failing to consider the abundance of phytic acid (PA). This is because PA can chelate the micronutrients, making them difficult to absorb. In order to understand the effect of an AM fungus and soil Zn concentration on the productivity and nutritional quality of food parts, this study examined the growth and nutritional responses of durum wheat, with and without inoculation with Rhizophagus irregularis, at five soil Zn concentrations. Growth and nutrient responses of the plants to soil Zn amendment was stronger than responses to AMF. However, the protective effect of AMF under soil Zn toxicity conditions was observed as reduced Zn concentration in the mycorrhizal durum wheat grain at Zn50. Here, AMF inoculation increased the concentration of PA in durum wheat grain but had no effect on the concentration of Zn and Fe; this consequently reduced the predicted bioavailability of grain Zn and Fe, which could lead to a decrease in nutritional quality of the grain. This research suggests that in soil with low (available) phosphorus and Zn concentrations, AMF may reduce the food quality of durum wheat because of an increase in PA concentration, and thus, a decrease in the bioavailability of Zn and Fe.

Keywords

Rhizophagus irregularis Biofortification Plant nutrition Micronutrient bioavailability Phytic acid 

Notes

Acknowledgments

The authors would like to thank Professor Mike McLaughlin and Ms. Bogumila Tomczak for access to the ICP-AES, and Ms. Andrea Ramirez Sepulveda and Ms. Cuc Tran for technical assistance. We also thank the anonymous reviewers and the editor of this manuscript for valuable feedback.

Funding information

BTTT acknowledges the Vied-Adelaide University joint scholarship. SJWW acknowledges the University of Adelaide Ramsay Fellowship and the Australian Research Council Centre of Excellence in Plant Energy Biology for support (Grant number CE140100008).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

572_2019_911_MOESM1_ESM.docx (26 kb)
ESM 1 (DOCX 25.6 kb)

References

  1. Augé RM (2000) Stomatal behavior of arbuscular mycorrhizal plants. In: Kapulnik Y, Douds DD (eds) Arbuscular mycorrhizas: physiology and function. Springer, Dordrecht, pp 201–237.  https://doi.org/10.1007/978-94-017-0776-3_10 CrossRefGoogle Scholar
  2. Azcon R, Ambrosano E, Charest C (2003) Nutrient acquisition in mycorrhizal lettuce plants under different phosphorus and nitrogen concentration. Plant Sci 165:1137–1145.  https://doi.org/10.1016/s0168-9452(03)00322-4 CrossRefGoogle Scholar
  3. Baon JB, Smith SE, Alston AM (1993) Mycorrhizal responses of barley cultivars differing in P efficiency. Plant Soil 157:97–105CrossRefGoogle Scholar
  4. Baslam M, Garmendia I, Goicoechea N (2011a) Arbuscular mycorrhizal fungi (AMF) improved growth and nutritional quality of greenhouse-grown lettuce. J Agric Food Chem 59:5504–5515.  https://doi.org/10.1021/jf200501c CrossRefGoogle Scholar
  5. Baslam M, Pascual I, Sánchez-Díaz M, Erro J, García-Mina JM, Goicoechea N (2011b) Improvement of nutritional quality of greenhouse-grown lettuce by arbuscular mycorrhizal fungi is conditioned by the source of phosphorus nutrition. J Agric Food Chem 59:11129–11140CrossRefGoogle Scholar
  6. Baum C, El-Tohamy W, Gruda N (2015) Increasing the productivity and product quality of vegetable crops using arbuscular mycorrhizal fungi: a review. Sci Hortic 187:131–141CrossRefGoogle Scholar
  7. Berruti A, Lumini E, Balestrini R, Bianciotto V (2016) Arbuscular mycorrhizal fungi as natural biofertilizers: let’s benefit from past successes. Front Microbiol 6:1559CrossRefGoogle Scholar
  8. Bowles TM, Barrios-Masias FH, Carlisle EA, Cavagnaro TR, Jackson LE (2016) Effects of arbuscular mycorrhizae on tomato yield, nutrient uptake, water relations, and soil carbon dynamics under deficit irrigation in field conditions. Sci Total Environ 566:1223–1234CrossRefGoogle Scholar
  9. Bowles TM, Jackson LE, Loeher M, Cavagnaro TR (2017) Ecological intensification and arbuscular mycorrhizas: a meta-analysis of tillage and cover crop effects. J Appl Ecol 54:1785–1793CrossRefGoogle Scholar
  10. Cakmak I (2009) Biofortification of cereal grains with zinc by applying zinc fertilizers. Biozoom 1:2–7Google Scholar
  11. Cavagnaro TR (2008) The role of arbuscular mycorrhizas in improving plant zinc nutrition under low soil zinc concentrations: a review. Plant Soil 304:315–325CrossRefGoogle Scholar
  12. Cavagnaro TR, Dickson S, Smith FA (2010) Arbuscular mycorrhizas modify plant responses to soil zinc addition. Plant Soil 329:307–313.  https://doi.org/10.1007/s11104-009-0158-z CrossRefGoogle Scholar
  13. Chaney RL (1993) Zinc phytotoxicity. In: Robson AD (ed) Zinc in soils and plants. Kluwer Academic, Dordrecht, pp 135–150.  https://doi.org/10.1007/978-94-011-0878-2_10 CrossRefGoogle Scholar
  14. 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.  https://doi.org/10.1016/S0045-6535(02)00228-X CrossRefGoogle Scholar
  15. Coccina A, Cavagnaro TR, Pellegrino E, Ercoli L, McLaughlin MJ, Watts-Williams SJ (2019) The mycorrhizal pathway of zinc uptake contributes to zinc accumulation in barley and wheat grain. BMC Plant Biol 19:133CrossRefGoogle Scholar
  16. Dutt S, Sharma SD, Kumar P (2013) Arbuscular mycorrhizas and Zn fertilization modify growth and physiological behavior of apricot (Prunus armeniaca L.). Sci Hortic 155:97–104.  https://doi.org/10.1016/j.scienta.2013.03.012 CrossRefGoogle Scholar
  17. Ercoli L, Schussler A, Arduini I, Pellegrino E (2017) Strong increase of durum wheat iron and zinc content by field-inoculation with arbuscular mycorrhizal fungi at different soil nitrogen availabilities. Plant Soil 419:153–167.  https://doi.org/10.1007/s11104-017-3319-5 CrossRefGoogle Scholar
  18. FAO (2013) The state of food and agriculture. Food and Agriculture Organization, RomeGoogle Scholar
  19. FAO (2018) The state of food security and nutrition in the world 2018. Building climate resilience for food security and nutrition. Food and Agriculture Organization, RomeGoogle Scholar
  20. FAO, WHO (2011) Working document for information and use in discussions related to contaminants and toxins in the GSCTFF, CF/5 INF/1. vol 5. The Hague, The NetherlandsGoogle Scholar
  21. Field KJ, Cameron DD, Leake JR, Tille S, Bidartondo MI, Beerling DJ (2012) Contrasting arbuscular mycorrhizal responses of vascular and non-vascular plants to a simulated palaeozoic CO2 decline. Nat Commun 3:835CrossRefGoogle Scholar
  22. Frassinetti S, Bronzetti GL, Caltavuturo L, Cini M, Della Croce C (2006) The role of zinc in life: a review. J Environ Pathol Toxicol Oncol 25:597–610CrossRefGoogle Scholar
  23. FSANZ ANZFS (2003) The 20th Australian total diet survey. Food Standards Australia New ZealandGoogle Scholar
  24. Garg N, Chandel S (2011) Effect of mycorrhizal inoculation on growth, nitrogen fixation, and nutrient uptake in Cicer arietinum (L.) under salt stress. Turk J Agric For 35:205–214.  https://doi.org/10.3906/tar-0908-12 Google Scholar
  25. Gibson RS (2006) Zinc: the missing link in combating micronutrient malnutrition in developing countries. Proc Nutr Soc 65:51–60CrossRefGoogle Scholar
  26. Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol 84:489–500.  https://doi.org/10.1111/j.1469-8137.1980.tb04556.x CrossRefGoogle Scholar
  27. Giovannetti M, Avio L, Barale R, Ceccarelli N, Cristofani R, Iezzi A, Mignolli F, Picciarelli P, Pinto B, Reali D, Sbrana C, Scarpato R (2012) Nutraceutical value and safety of tomato fruits produced by mycorrhizal plants. Br J Nutr 107:242–251CrossRefGoogle Scholar
  28. Glahn RP, Wortley GM, South PK, Miller DD (2002) Inhibition of iron uptake by phytic acid, tannic acid, and ZnCl2: studies using an in vitro digestion/Caco-2 cell model. J Agric Food Chem 50:390–395CrossRefGoogle Scholar
  29. Goicoechea N, Antolín MC (2017) Increased nutritional value in food crops. Microb Biotechnol 10:1004–1007CrossRefGoogle Scholar
  30. Goicoechea N, Bettoni MM, Fuertes-Mendizabal T, González-Murua C, Aranjuelo I (2016) Durum wheat quality traits affected by mycorrhizal inoculation, water availability and atmospheric CO2 concentration. Crop Pasture Sci 67:147–155CrossRefGoogle Scholar
  31. Harikumar VS (2017) A new method of propagation of arbuscular mycorrhizal fungi in field cropped sesame (Sesamum indicum L.). Symbiosis:1–4.  https://doi.org/10.1007/s13199-017-0482-7
  32. Hídvégi M, Lásztity R (2002) Phytic acid content of cereals and legumes and interaction with proteins. Period Polytech 46:59–64Google Scholar
  33. Hurrell R, Egli I (2010) Iron bioavailability and dietary reference values. Am J Clin Nutr 91:1461S–1467SCrossRefGoogle Scholar
  34. Johnson NC, Graham JH, Smith FA (1997) Functioning of mycorrhizal associations along the mutualism–parasitism continuum. New Phytol 135:575–585.  https://doi.org/10.1046/j.1469-8137.1997.00729.x CrossRefGoogle Scholar
  35. Johnson NC, Wilson GWT, Wilson JA, Miller RM, Bowker MA (2015) Mycorrhizal phenotypes and the law of the minimum. New Phytol 205:1473–1484.  https://doi.org/10.1111/nph.13172 CrossRefGoogle Scholar
  36. Jung MC, Thornton L (1997) Environmental contamination and seasonal variation of metals in soils, plants and waters in the paddy fields around a Pb-Zn mine in Korea. Sci Total Environ 198:105–121.  https://doi.org/10.1016/S0048-9697(97)05434-X CrossRefGoogle Scholar
  37. Konieczny A, Kowalska I (2017) Effect of arbuscular mycorrhizal fungi on the content of zinc in lettuce grown at two phosphorus levels and an elevated zinc level in a nutrient solution. J Elem 22:761–772.  https://doi.org/10.5601/jelem.2016.21.4.1335 Google Scholar
  38. Lehmann A, Rillig MC (2015) Arbuscular mycorrhizal contribution to copper, manganese and iron nutrient concentrations in crops–a meta-analysis. Soil Biol Biochem 81:147–158CrossRefGoogle Scholar
  39. Lehmann A, Veresoglou SD, Leifheit EF, Rillig MC (2014) Arbuscular mycorrhizal influence on zinc nutrition in crop plants–a meta-analysis. Soil Biol Biochem 69:123–131CrossRefGoogle Scholar
  40. Lewis JD, Koide RT (1990) Phosphorus supply, mycorrhizal infection and plant offspring vigour. Funct Ecol 4:695–702.  https://doi.org/10.2307/2389738 CrossRefGoogle Scholar
  41. Li H, Smith SE, Holloway RE, Zhu Y, Smith FA (2006) Arbuscular mycorrhizal fungi contribute to phosphorus uptake by wheat grown in a phosphorus-fixing soil even in the absence of positive growth responses. New Phytol 172:536–543CrossRefGoogle Scholar
  42. Ma X, Wanqing L, Li J, Wu F (2019) Arbuscular mycorrhizal fungi increase both concentrations and bioavilability of Zn in wheat (Triticum aestivum L) grain on Zn-spiked soils. Appl Soil Ecol 135:91–97.  https://doi.org/10.1016/j.apsoil.2018.11.007 CrossRefGoogle Scholar
  43. Maenz DD, Engele-Schaan CM, Newkirk RW, Classen HL (1999) The effect of minerals and mineral chelators on the formation of phytase-resistant and phytase-susceptible forms of phytic acid in solution and in a slurry of canola meal. Anim Feed Sci Technol 81:177–192CrossRefGoogle Scholar
  44. Magallanes-López AM et al (2017) Variability in iron, zinc and phytic acid content in a worldwide collection of commercial durum wheat cultivars and the effect of reduced irrigation on these traits. Food Chem 237:499–505 https://ac.els-cdn.com/S0308814617309123/1-s2.0-S0308814617309123-main.pdf?_tid=a6e89be1-5b41-4a19-b5f7-144547a42ce6&acdnat=1542766111_1d7f59593b21876f66481b31b7229cc1 CrossRefGoogle Scholar
  45. Miller RO (1998) Microwave digestion of plant tissue in a closed vessel. In: Kalra YP (ed) Handbook and reference methods for plant analysis. CRC Press, New York, pp 69–74Google Scholar
  46. Mnasri M, Janouskova M, Rydlova J, Abdelly C, Ghnaya T (2017) Comparison of arbuscular mycorrhizal fungal effects on the heavy metal uptake of a host and a non-host plant species in contact with extraradical mycelial network. Chemosphere 171:476–484.  https://doi.org/10.1016/j.chemosphere.2016.12.093 CrossRefGoogle Scholar
  47. Pellegrino E, Öpik M, Bonari E, Ercoli L (2015) Responses of wheat to arbuscular mycorrhizal fungi: a meta-analysis of field studies from 1975 to 2013. Soil Biol Biochem 84:210–217CrossRefGoogle Scholar
  48. Peverill K, Sparrow L, Reuter D (1999) Soil analysis: an interpretation manual. CSIRO publishingGoogle Scholar
  49. Porcel R, Aroca R, Ruiz-Lozano JM (2012) Salinity stress alleviation using arbuscular mycorrhizal fungi. A review. Agron Sustain Dev 32:181–200CrossRefGoogle Scholar
  50. Reddy NR (2001) Occurrence, distribution, content, and dietary intake of phytate. In: Food Phytates. CRC Press, pp 41–68Google Scholar
  51. Rillig MC et al. (2019) Why farmers should manage the arbuscular mycorrhizal symbiosis: a response to Ryan & Graham (2018) ‘little evidence that farmers should consider abundance or diversity of arbuscular mycorrhizal fungi when managing crops’. New Phytol in press  https://doi.org/10.1111/nph.15602
  52. Rouphael Y, Cardarelli M, Di Mattia E, Tullio M, Rea E, Colla G (2010) Enhancement of alkalinity tolerance in two cucumber genotypes inoculated with an arbuscular mycorrhizal biofertilizer containing Glomus intraradices. Biol Fertil Soils 46:499–509CrossRefGoogle Scholar
  53. Ryan MH, Graham JH (2018) Little evidence that farmers should consider abundance or diversity of arbuscular mycorrhizal fungi when managing crops. New Phytol 220:1092–1107CrossRefGoogle Scholar
  54. Ryan MH, McInerney JK, Record IR, Angus JF (2008) Zinc bioavailability in wheat grain in relation to phosphorus fertiliser, crop sequence and mycorrhizal fungi. J Sci Food Agric 88:1208–1216.  https://doi.org/10.1002/jsfa.3200 CrossRefGoogle Scholar
  55. Smith SE, Read DJ (2008) Mycorrhizas in agriculture, horticulture and forestry. In: Smith SE, Read D (eds) Mycorrhizal symbiosis, 3rd edn. Academic Press, Oxford, pp 611–636.  https://doi.org/10.1016/B978-012370526-6.50019-2 CrossRefGoogle Scholar
  56. Subramanian KS, Balakrishnan N, Senthil N (2013) Mycorrhizal symbiosis to increase the grain micronutrient content in maize. Agron sustain dev 7:900 http://www.cropj.com/subramanian_7_7_2013_900_910.pdf
  57. Takkar PN, Mann MS (1978) Toxic levels of soil and plant zinc for maize and wheat. Plant Soil 49:667–669.  https://doi.org/10.1007/BF02183293 CrossRefGoogle Scholar
  58. Tawaraya K (2003) Arbuscular mycorrhizal dependency of different plant species and cultivars. Soil Sci Plant Nutr 49:655–668CrossRefGoogle Scholar
  59. Thirkell TJ, Charters MD, Elliott AJ, Sait SM, Field KJ (2017) Are mycorrhizal fungi our sustainable saviours? Considerations for achieving food security. J Ecol 105:921–929CrossRefGoogle Scholar
  60. Torres N, Antolín MC, Goicoechea N (2018) Arbuscular mycorrhizal symbiosis as a promising resource for improving berry quality in grapevines under changing environments. Front Plant Sci 9:897CrossRefGoogle Scholar
  61. Tran BTT, Watts-Williams SJ, Cavagnaro TR (2019) Impact of an arbuscular mycorrhizal fungus forming arbuscular mycorrhizas on the growth and nutrition of fifteen crop and pasture plant species. Funct Plant Biol 46:732–742CrossRefGoogle Scholar
  62. van der Heijden MGA (2003) Arbuscular mycorrhizal fungi as a determinant of plant diversity: in search of underlying mechanisms and general principles. In: van der Heijden MGA, Sanders IR (eds) Mycorrhizal ecology. Springer, Berlin, Heidelberg, pp 243–265.  https://doi.org/10.1007/978-3-540-38364-2_10 CrossRefGoogle Scholar
  63. Vierheilig H, Coughlan AP, Wyss U, Piché Y (1998) Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Appl Environ Microbiol 64:5004–5007Google Scholar
  64. Walder F, van der Heijden MGA (2015) Regulation of resource exchange in the arbuscular mycorrhizal symbiosis. Nat Plants 1:15159.  https://doi.org/10.1038/nplants.2015.159 CrossRefGoogle Scholar
  65. Wang Y-y et al (2014) Improved yield and Zn accumulation for rice grain by Zn fertilization and optimized water management. J Zhejiang Univ Sci B 15:365–374CrossRefGoogle Scholar
  66. Watts-Williams SJ, Cavagnaro TR (2018) Arbuscular mycorrhizal fungi increase grain zinc concentration and modify the expression of root ZIP transporter genes in a modern barley (Hordeum vulgare) cultivar. Plant Sci 274:163–170.  https://doi.org/10.1016/j.plantsci.2018.05.015 CrossRefGoogle Scholar
  67. Watts-Williams SJ, Patti AF, Cavagnaro TR (2013) Arbuscular mycorrhizas are beneficial under both deficient and toxic soil zinc conditions. Plant Soil 371:299–312CrossRefGoogle Scholar
  68. Watts-Williams SJ, Smith FA, McLaughlin MJ, Patti AF, Cavagnaro TR (2015) How important is the mycorrhizal pathway for plant Zn uptake? Plant Soil 390:157–166.  https://doi.org/10.1007/s11104-014-2374-4 CrossRefGoogle Scholar
  69. Watts-Williams SJ, Tyerman SD, Cavagnaro TR (2017) The dual benefit of arbuscular mycorrhizal fungi under soil zinc deficiency and toxicity: linking plant physiology and gene expression. Plant Soil 420:375–388.  https://doi.org/10.1007/s11104-017-3409-4 CrossRefGoogle Scholar
  70. Watts-Williams SJ, Cavagnaro TR, Tyerman SD (2019) Variable effects of arbuscular mycorrhizal fungal inoculation on physiological and molecular measures of root and stomatal conductance of diverse Medicago truncatula accessions. Plant. Cell Environ:285–294.  https://doi.org/10.1111/pce.13369
  71. White PJ, Broadley MR (2009) Biofortification of crops with seven mineral elements often lacking in human diets–iron, zinc, copper, calcium, magnesium, selenium and iodine. New Phytol 182:49–84CrossRefGoogle Scholar
  72. WHO (1996) Trace-element bioavailability and interactions. World Health Organisation, GenevaGoogle Scholar
  73. Wise A (1995) Phytate and zinc bioavailability. Int J Food Sci Nutr 46:53–63CrossRefGoogle Scholar
  74. Wood RJ, Zheng JJ (1997) High dietary calcium intakes reduce zinc absorption and balance in humans. Am J Clin Nutr 65:1803–1809CrossRefGoogle Scholar
  75. Yu Y, Luo L, Yang K, Zhang S (2011) Influence of mycorrhizal inoculation on the accumulation and speciation of selenium in maize growing in selenite and selenate spiked soils. Pedobiologia 54:267–272CrossRefGoogle Scholar
  76. Zhang W, Liu D, Liu Y, Cui Z, Chen X, Zou C (2016) Zinc uptake and accumulation in winter wheat relative to changes in root morphology and mycorrhizal colonization following varying phosphorus application on calcareous soil. Field Crops Res 197:74–82CrossRefGoogle Scholar
  77. Zhang S, Lehmann A, Zheng W, You Z, Rillig MC (2019) Arbuscular mycorrhizal fungi increase grain yields: a meta-analysis. New Phytol 222:543–555.  https://doi.org/10.1111/nph.15570 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.The School of Agriculture, Food and Wine, and the Waite Research InstituteThe University of AdelaideGlen OsmondAustralia
  2. 2.Faculty of Agriculture and ForestryTaynguyen UniversityBuon Ma Thuot CityVietnam
  3. 3.Australian Research Council Centre of Excellence in Plant Energy BiologyThe University of AdelaideGlen OsmondAustralia

Personalised recommendations