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Absorption of foliar applied Zn is decreased in Zn deficient sunflower (Helianthus annuus) due to changes in leaf properties

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Abstract

Aims

Despite the importance of foliar Zn fertilisation, it remains unclear how the Zn status of the plant itself influences the efficacy of foliar applied Zn, with this forming the focus of the present study.

Methods

Sunflower (Helianthus annuus) was grown in nutrient solutions with either 0.5 (sufficient) or 0 μM Zn (deficient) to relate the absorption of foliar applied Zn to leaf properties. The distribution and speciation of Zn within the leaf were examined in situ using synchrotron-based X-ray fluorescence microscopy and X-ray absorption spectroscopy.

Results

Zinc deficiency decreased foliar absorption of Zn as ZnSO4 by 50–66% compared to Zn sufficient sunflower, despite μ-XRF analysis showing the pattern of Zn absorption was similar for both plants. Rather, Zn deficiency decreased the leaf trichome density and likely altered the adaxial leaf surface composition and structure, with these presumably being the main causes for the reduced Zn absorption. The Zn status of the plant also influenced the speciation of the absorbed Zn, with 37–53% as Zn phytate in Zn sufficient leaves but 55% as Zn phosphate in Zn deficient leaves.

Conclusions

Zinc status of the plants influenced leaf surface properties, with Zn deficiency leading to decreased absorption of foliar applied Zn.

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Abbreviations

ICP-MS:

Inductively coupled plasma mass spectrometry

ICP-OES:

Inductively coupled plasma optical emission spectroscopy

LCF:

Linear combination fitting

XAS:

Synchrotron-based X-ray absorption spectroscopy

XANES:

K-edge X-ray absorption near edge structure spectra

YFELs:

Youngest fully-expanded leaves

μ-XRF:

Synchrotron-based X-ray fluorescence microscopy

References

  • Alloway B (2009) Soil factors associated with zinc deficiency in crops and humans. Environ Geochem Health 31:537–548

    Article  CAS  Google Scholar 

  • Álvarez-Fernández A, Díaz-Benito P, Abadía A, López-Millán A-F, Abadía J (2014) Metal species involved in long distance metal transport in plants. Front Plant Sci 5:105

    Article  Google Scholar 

  • Bashir K, Ishimaru Y, Nishizawa NK (2012) Molecular mechanisms of zinc uptake and translocation in rice. Plant Soil 361:189–201

    Article  CAS  Google Scholar 

  • Blamey FPC, Hernandez-Soriano MC, Cheng M, Tang C, Paterson DJ, Lombi E, Wang WH, Scheckel KG, Kopittke PM (2015) Synchrotron-based techniques shed light on mechanisms of plant sensitivity and tolerance to high manganese in the root environment. Plant Physiol 169:2006–2020

    PubMed  PubMed Central  Google Scholar 

  • Cakmak I (2008) Enrichment of cereal grains with zinc: agronomic or genetic biofortification? Plant Soil 302:1–17

    Article  CAS  Google Scholar 

  • Cakmak I, Kutman U (2018) Agronomic biofortification of cereals with zinc: a review. Eur J Soil Sci 69:172–180

    Article  Google Scholar 

  • Cakmak I, Kalayci M, Kaya Y, Torun AA, Aydin N, Wang Y, Arisoy Z, Erdem H, Yazici A, Gokmen O, Ozturk L, Horst WJ (2010) Biofortification and localization of zinc in wheat grain. J Agric Food Chem 58:9092–9102. https://doi.org/10.1021/jf101197h

    Article  CAS  PubMed  Google Scholar 

  • DeRosa MC, Monreal C, Schnitzer M, Walsh R, Sultan Y (2010) Nanotechnology in fertilizers. Nat Nanotechnol 5:91–91

    Article  CAS  Google Scholar 

  • Drissi S, Houssa AA, Bamouh A, Benbella M (2015) Corn silage (Zea mays L.) response to zinc foliar spray concentration when grown on sandy soil. J Agric Sci 7:68–79

    Google Scholar 

  • Eichert T, Fernández V (2012) Uptake and release of elements by leaves and other aerial plant parts. Marschner's Mineral Nutrition of Higher Plants (Third Edition). Elsevier

  • Eichert T, Goldbach HE (2008) Equivalent pore radii of hydrophilic foliar uptake routes in stomatous and astomatous leaf surfaces–further evidence for a stomatal pathway. Physiol Plant 132:491–502

    Article  CAS  Google Scholar 

  • Erenoglu B, Nikolic M, Römheld V, Cakmak I (2002) Uptake and transport of foliar applied zinc (65Zn) in bread and durum wheat cultivars differing in zinc efficiency. Plant Soil 241:251–257

    Article  CAS  Google Scholar 

  • Fernández V, Eichert T (2009) Uptake of hydrophilic solutes through plant leaves: current state of knowledge and perspectives of foliar fertilization. Crit Rev Plant Sci 28:36–68

    Article  Google Scholar 

  • Fernández V, Eichert T, Del Río V, López-Casado G, Heredia-Guerrero JA, Abadía A, Heredia A, Abadía J (2008) Leaf structural changes associated with iron deficiency chlorosis in field-grown pear and peach: physiological implications. Plant Soil 311:161–172

    Article  Google Scholar 

  • Fernández V, Khayet M, Montero-Prado P, Heredia-Guerrero JA, Liakopoulos G, Karabourniotis G, Del Rio V, Domínguez E, Tacchini I, Nerín C (2011) New insights into the properties of pubescent surfaces: peach fruit as a model. Plant Physiol 156:2098–2108

    Article  Google Scholar 

  • Fernández V, Sotiropoulos T, Brown P (2013) Foliar fertilization: scientific principles and field practices. International Fertilizer Industry Association (IFA), Paris, France

    Google Scholar 

  • Fernández V, Guzmán P, Peirce CA, McBeath TM, Khayet M, McLaughlin MJ (2014a) Effect of wheat phosphorus status on leaf surface properties and permeability to foliar-applied phosphorus. Plant Soil 384:7–20

    Article  Google Scholar 

  • Fernández V, Sancho-Knapik D, Guzmán P, Peguero-Pina JJ, Gil L, Karabourniotis G, Khayet M, Fasseas C, Heredia-Guerrero JA, Heredia A (2014b) Wettability, polarity, and water absorption of holm oak leaves: effect of leaf side and age. Plant Physiol 166:168–180

    Article  Google Scholar 

  • Fernández V, Guzmán-Delgado P, Graça J, Santos S, Gil L (2016) Cuticle structure in relation to chemical composition: re-assessing the prevailing model. Front Plant Sci 7:427

    PubMed  PubMed Central  Google Scholar 

  • Fernández V, Bahamonde HA, Javier Peguero-Pina J, Gil-Pelegrín E, Sancho-Knapik D, Gil L, Goldbach HE, Eichert T (2017) Physico-chemical properties of plant cuticles and their functional and ecological significance. J Exp Bot 68:5293–5306

    Article  Google Scholar 

  • Gupta N, Ram H, Kumar B (2016) Mechanism of zinc absorption in plants: uptake, transport, translocation and accumulation. Rev Environ Sci Biotechno 15:89–109

    Article  CAS  Google Scholar 

  • Guzmán P, Fernández V, Graça J, Cabral V, Kayali N, Khayet M, Gil L (2014) Chemical and structural analysis of Eucalyptus globulus and E. camaldulensis leaf cuticles: a lipidized cell wall region. Front Plant Sci 5:481

    Article  Google Scholar 

  • Hadrami A (2011) Understanding deliquescence. Farming. Online: http://agadvance.com/issues/jun-jul-2011/understanding-deliquescence.aspx

  • Heredia-Guerrero JA, Benitez JJ, Dominguez E, Bayer IS, Cingolani R, Athanassiou A, Heredia A (2014) Infrared and Raman spectroscopic features of plant cuticles: a review. Front Plant Sci 5:305

    Article  Google Scholar 

  • Joy EJ, Stein AJ, Young SD, Ander EL, Watts MJ, Broadley MR (2015) Zinc-enriched fertilisers as a potential public health intervention in Africa. Plant Soil 389:1–24

    Article  CAS  Google Scholar 

  • Khan GA, Bouraine S, Wege S, Li Y, De Carbonnel M, Berthomieu P, Poirier Y, Rouached H (2014) Coordination between zinc and phosphate homeostasis involves the transcription factor PHR1, the phosphate exporter PHO1, and its homologue PHO1; H3 in Arabidopsis. J Exp Bot 65:871–884

    Article  CAS  Google Scholar 

  • Kopittke PM, Menzies NW, de Jonge MD, McKenna BA, Donner E, Webb RI, Paterson DJ, Howard DL, Ryan CG, Glover CJ (2011) In situ distribution and speciation of toxic copper, nickel, and zinc in hydrated roots of cowpea. Plant Physiol 156:663–673

    Article  CAS  Google Scholar 

  • Lei L (2018) A seesaw between Pi and Zn. Nat Plants 4:190–190

    Article  CAS  Google Scholar 

  • Li C, Wang P, Menzies NW, Lombi E, Kopittke PM (2017) Effects of changes in leaf properties mediated by methyl jasmonate (MeJA) on foliar absorption of Zn, Mn and Fe. Ann Bot 120:405–415

    Article  Google Scholar 

  • Li C, Wang P, Lombi E, Cheng M, Tang C, Howard DL, Menzies NW, Kopittke PM (2018a) Absorption of foliar-applied Zn fertilizers by trichomes in soybean and tomato. J Exp Bot 69:2717–2729

    Article  Google Scholar 

  • Li C, Wang P, Van der Ent A, Jiang H, Read TL, Lombi E, Cheng M, Tang C, de Jonge MD, Menzies NW, Kopittke PM (2018b) Absorption of foliar-applied Zn in sunflower (Helianthus annuus): importance of the cuticle, stomata, and trichomes. Ann Bot. https://doi.org/10.1093/aob/mcy135

  • Nishiyama R, Kato M, Nagata S, Yanagisawa S, Yoneyama T (2012) Identification of Zn–nicotianamine and Fe-2′-deoxymugineic acid in the phloem sap from rice plants. Plant Cell Physiol 53:381–390

    Article  CAS  Google Scholar 

  • Paterson D, De Jonge M, Howard D, Lewis W, McKinlay J, Starritt A, Kusel M, Ryan C, Kirkham R, Moorhead G (2011) The X-ray fluorescence microscopy beamline at the Australian Synchrotron. The 10th International Conference on X-ray Microscopy. AIP Publishing

  • Popp C, Burghardt M, Friedmann A, Riederer M (2005) Characterization of hydrophilic and lipophilic pathways of Hedera helix L. cuticular membranes: permeation of water and uncharged organic compounds. J Exp Bot 56:2797–2806

    Article  CAS  Google Scholar 

  • Ravel B, Newville M (2005) ATHENA, ARTEMIS, HEPHAESTUS: data analysis for X-ray absorption spectroscopy using IFEFFIT. J Synchrotron Radiat 12:537–541. https://doi.org/10.1107/S0909049505012719

    Article  CAS  Google Scholar 

  • Reuter D, Edwards D, Wilhelm N (1997) Temperate and tropical crops. In: ‘Plant analysis: an interpretation manual’.(Eds DJ Reuter, JB Robinson). CSIRO Publishing, Melbourne, pp 83–284

    Google Scholar 

  • Ryan C (2000) Quantitative trace element imaging using PIXE and the nuclear microprobe. Int J Imaging Syst Technol 11:219–230

    Article  Google Scholar 

  • Ryan C, Jamieson D (1993) Dynamic analysis: on-line quantitative PIXE microanalysis and its use in overlap-resolved elemental mapping. Nucl Instrum Methods Phys Res B 77:203–214

    Article  Google Scholar 

  • Sadeghzadeh B (2013) A review of zinc nutrition and plant breeding. J. Soil Sci Plant Nutr 13:905–927

    Google Scholar 

  • Schönherr J (1976) Water permeability of isolated cuticular membranes: the effect of pH and cations on diffusion, hydrodynamic permeability and size of polar pores in the cutin matrix. Planta 128:113–126

    Article  Google Scholar 

  • Schönherr J (2006) Characterization of aqueous pores in plant cuticles and permeation of ionic solutes. J Exp Bot 57:2471–2491

    Article  Google Scholar 

  • Schreiber L, Schönherr J (2009) Water and solute permeability of plant cuticles. Springer

  • Shaff JE, Schultz BA, Craft EJ, Clark RT, Kochian LV (2010) GEOCHEM-EZ: a chemical speciation program with greater power and flexibility. Plant Soil 330:207–214

    Article  CAS  Google Scholar 

  • Sillanpaa M (1990) Micronutrient assessment at the country level: an international study. FAO Soils Bulletin No. 63. FAO, Rome

  • Soltangheisi A, Ishak CF, Musa HM, Zakikhani H, Rahman ZA (2013) Phosphorus and zinc uptake and their interaction effect on dry matter and chlorophyll content of sweet corn (Zea mays var. saccharata). J Agron 12:187–192

    Article  CAS  Google Scholar 

  • Velu G, Ortiz-Monasterio I, Cakmak I, Hao Y, Singh R (2014) Biofortification strategies to increase grain zinc and iron concentrations in wheat. J Cereal Sci 59:365–372

    Article  CAS  Google Scholar 

  • Vu DT, Huang L, V Nguyen A, Du Y, Xu Z, A Hampton M, Li P, Rudolph V (2013) Quantitative methods for estimating foliar uptake of zinc from suspension-based Zn chemicals. J Plant Nutr Soil Sci 176:764–775

    CAS  Google Scholar 

  • Wang P, Lombi E, Zhao F-J, Kopittke PM (2016) Nanotechnology: a new opportunity in plant sciences. Trends Plant Sci 21:699–712

    Article  CAS  Google Scholar 

  • Will S, Eichert T, Fernández V, Möhring J, Müller T, Römheld V (2011) Absorption and mobility of foliar-applied boron in soybean as affected by plant boron status and application as a polyol complex. Plant Soil 344:283–293

    Article  CAS  Google Scholar 

  • Woodward RP (1999) Contact angle measurements using the drop shape method. First Ten Angstroms Inc, Portsmouth, VA 66: 1–8

  • Zhang T, Sun H, Lv Z, Cui L, Mao H, Kopittke PM (2018) Using synchrotron-based approaches to examine the foliar application of ZnSO4 and ZnO nanoparticles for field-grown winter wheat. J Agric Food Chem 66:2572–2579

    Article  CAS  Google Scholar 

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Acknowledgements

The authors acknowledge use of the facilities and technical assistance of both the Queensland Brain Institute and the Australian Microscopy & Microanalysis Research Facility at the Centre for Microscopy and Microanalysis, The University of Queensland. Suggestions from Dr. Bernhard Wehr also thanked. Parts of the research were undertaken on the XFM and XAS beamlines at the Australian Synchrotron, part of Australian Nuclear Science and Technology Organisation (ANSTO). This work was supported by Sonic Essentials, as well as by the Australian Research Council (ARC) through the Linkage Projects funding scheme (LP130100741). Support was also provided to Peter Kopittke by the ARC Future Fellowship funding scheme (FT120100277) and to Cui Li through the China Scholarship Council and The University of Queensland International Scholarship award.

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Correspondence to Cui Li.

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Responsible Editor: Michael A. Grusak.

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Li, C., Wang, P., Lombi, E. et al. Absorption of foliar applied Zn is decreased in Zn deficient sunflower (Helianthus annuus) due to changes in leaf properties. Plant Soil 433, 309–322 (2018). https://doi.org/10.1007/s11104-018-3841-0

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