Register      Login
Crop and Pasture Science Crop and Pasture Science Society
Plant sciences, sustainable farming systems and food quality
RESEARCH FRONT

Sequential zinc and iron biofortification of bread-wheat grains: from controlled to uncontrolled environments

Fernando C. Lidon A F , Ana S. Almeida B , Ana R. Costa B , Ana S. Bagulho B , Paula Scotti-Campos B , José N. Semedo B , Benvindo Maçãs B , José Coutinho B , Nuno Pinheiro B , Conceição Gomes B , António E. Leitão A C , Isabel P. Pais B , Maria M. Silva D , Fernando H. Reboredo A , Maria F. Pessoa A and José C. Ramalho A C E
+ Author Affiliations
- Author Affiliations

A GeoBioTec, DCT, Faculdade de Ciências e Tecnologia, Universidade Nova de Lisboa (FCT/UNL), 2829-516 Caparica, Portugal.

B Unidade de Biotecnologia e Recursos Genéticos, Instituto Nacional de Investigação Agrária e Veterinária, I.P. (INIAV), Apartado 6, 7350-591 Elvas/Quinta do Marquês, Av. República, 2784-505 Oeiras, Portugal.

C Grupo Interações Planta-Ambiente and Biodiversidade (Plant Stress and Biodiversity), Centro de Ambiente, Agricultura e Desenvolvimento (BioTrop), Instituto de Investigação Científica Tropical, I.P. (IICT), Av. República, Quinta do Marquês, 2784-505 Oeiras, Portugal.

D ESE Almeida Garrett, Grupo Univ. Lusófona, COFAC, Largo do Sequeiro no. 7, Lisbon, Portugal.

E Instituto Superior de Agronomia, Universidade de Lisboa, Tapada da Ajuda, 1349-017 Lisbon, Portugal.

F Corresponding author. Email: fjl@fct.unl.pt

Crop and Pasture Science 66(11) 1097-1104 https://doi.org/10.1071/CP14270
Submitted: 19 September 2014  Accepted: 19 January 2015   Published: 14 August 2015

Abstract

The development of knowledge on bread wheat (Triticum aestivum L.) biofortification in zinc (Zn) and iron (Fe), related to its potential agronomical use and the nutritional and technological implications, is becoming important to strategies for improving human nutrition. In this context, we studied the accumulation of Zn and Fe in grains, considering potential uptake and translocation kinetics, photoassimilate production and deposition, and related yields, in grains of cv. Roxo produced under controlled-environment conditions and used thereafter in field trials. The metabolic plasticity of this wheat genotype grown under controlled-environment conditions allowed a 10- and 4-fold enhancement in accumulation of Zn and Fe in the grains after nutrient supplementation with a 5-fold concentrated Hoagland solution (5S), after two generations. Moreover, when these seeds were sown under field conditions and the resulting plants supplemented with or without Zn and Fe, the accumulation of these nutrients decreased within the next two generations. Such field seeds obtained without further Zn and Fe supplementation (with nitrogen only; F3(S) and F4(S)) maintained enhanced levels of Zn (~400%) and Fe (40–50%) compared with the initial seeds. If Zn and Fe supplement was given to the plants germinated from F2(5S), the subsequent F3(5S) and F4(5S) seeds maintained the Zn increase (~400%), whereas a further enhancement was observed for Fe, to 75% and 89%, respectively. Toxic limits were not reached for photosynthetic functioning. Even under the highest Zn and Fe supplement dose given to the F3(5S) plants, there was only a slight effect on photosystem II photochemical performance; in fact, enhanced net photosynthesis values were observed. In conclusion, within this experimental design, Zn and Fe biofortification can be obtained without toxicity effects on photosynthetic performance and with negligible modifications to grain texture and nutritional value (protein quality and contents as well as fatty acids).

Additional keywords: bread wheat, biofortification, iron, photoassimilates, zinc.


References

Aciksoz SB, Yazici A, Ozturk L, Cakmak I (2011) Biofortification of wheat with iron through soil and foliar application of nitrogen and iron fertilizers. Plant and Soil 349, 215–225.
Biofortification of wheat with iron through soil and foliar application of nitrogen and iron fertilizers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFKntLnJ&md5=1365a61a5433c0e107514a89f77636cbCAS |

Assunção AGL, Schat H, Aarts MGM (2010) Regulation of the adaptation to zinc deficiency in plants. Plant Signaling & Behavior 5, 1553–1555.
Regulation of the adaptation to zinc deficiency in plants.Crossref | GoogleScholarGoogle Scholar |

Becker R (2007) ‘Fatty acids in foods and their health implications.’ 3rd edn (Ed. Ching Kuang Chow) pp. 303–316. (CRC Press: Boca Raton, FL, USA)

Bekiaroglou P, Karataglis S (2002) The effect of lead and zinc on Mentha spicata. Journal of Agronomy & Crop Science 188, 201–205.
The effect of lead and zinc on Mentha spicata.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xlt1KitLw%3D&md5=fa7a2226c7efbdb09a67c1eb644d4867CAS |

Bertrand M, Poirier I (2005) Photosynthetic organisms and excess of metals. Photosynthetica 43, 345–353.
Photosynthetic organisms and excess of metals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVylu77L&md5=9429815c0c936cb7fa9bfbd442caff16CAS |

Bouis HE, Welch RM (2010) Biofortification—A sustainable agricultural strategy for reducing micronutrient malnutrition in the global south. Crop Science 50, S-20–S-32.
Biofortification—A sustainable agricultural strategy for reducing micronutrient malnutrition in the global south.Crossref | GoogleScholarGoogle Scholar |

Brennan RF (2005) Zinc application and its availability to plants. PhD Dissertation, School of Environmental Science, Division of Science and Engineering, Murdoch University, Perth, WA, Australia.

Broadley MR, White PJ, Hammond JP, Zelko I, Lux A (2007) Zinc in plants. New Phytologist 173, 677–702.
Zinc in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjvFGgsL8%3D&md5=b8e3fb5f7694848234b0aca631692697CAS | 17286818PubMed |

Cakmak I (2010) Biofortification of cereals with zinc and iron through fertilization strategy. In ‘Soil solutions for a changing world. Proceedings 19th World Congress of Soil Science’. 1–6 August, Brisbane, Qld. pp. 4–6. (International Union of Soil Sciences) Available at: http://r4d.dfid.gov.uk/PDF/Outputs/Misc_Crop/Cakmak-1165.pdf

Cakmak I, Torun A, Millet E, Feldman M, Fahima T, Korol A, Nevo E, Braun HJ, Özkan H (2004) Triticum dicoccoides an important genetic resource for increasing zinc and iron concentration in modern cultivated wheat. Soil Science and Plant Nutrition 50, 1047–1054.
Triticum dicoccoides an important genetic resource for increasing zinc and iron concentration in modern cultivated wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjslSksw%3D%3D&md5=7db3cb14c5fcf3cbb3882ea90031699dCAS |

Cherif J, Derbel N, Nakkach M, von Bergmann H, Jemal F, Ben Lakhdar Z (2010) Analysis of in vivo chlorophyll fluorescence spectra to monitor physiological state of tomato plants growing under zinc stress. Journal of Photochemistry and Photobiology. B, Biology 101, 332–339.
Analysis of in vivo chlorophyll fluorescence spectra to monitor physiological state of tomato plants growing under zinc stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlenu7jM&md5=cb648b4e8192c0fd7ee36c1c49db3963CAS | 20829059PubMed |

Dhir B, Sharmila P, Pardha Sarad P (2008) Photosynthetic performance of Salvinia natans exposed to chromium and zinc rich wastewater. Brazilian Journal of Plant Physiology 20, 61–70.
Photosynthetic performance of Salvinia natans exposed to chromium and zinc rich wastewater.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXptFygu7c%3D&md5=0fbb73b632c8d86511860fe3555c09c4CAS |

Di Baccio D, Kopriva S, Sebastiani L, Rennenberg H (2005) Does glutathione metabolism have a role in the defence of poplar against zinc excess? New Phytologist 167, 73–80.
Does glutathione metabolism have a role in the defence of poplar against zinc excess?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmtl2nsbg%3D&md5=30e8b8ae5f3c10f31c58e9ff4835c3e3CAS | 15948831PubMed |

Dick JW, Quick JS (1983) A modified screening test for rapid estimation of gluten strength in early-generation durum wheat breeding lines. Cereal Chemistry 60, 315–318.

Erenoglu EB, Kutman UB, Ceylan Y, Yildiz B, Cakmak I (2011) Improved nitrogen nutrition enhances root uptake, root-to-shoot translocation and remobilization of Zinc (65Zn) in wheat. New Phytologist 189, 438–448.
Improved nitrogen nutrition enhances root uptake, root-to-shoot translocation and remobilization of Zinc (65Zn) in wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlChtLk%3D&md5=f986ad0a639bed7677b4f6df6c8c4921CAS | 21029104PubMed |

Galliard T, Gallagher DM (1988) The effects of wheat bran particle size and storage period on bran flavor and baking quality of bran/flour contents. Journal of Cereal Science 8, 147–154.
The effects of wheat bran particle size and storage period on bran flavor and baking quality of bran/flour contents.Crossref | GoogleScholarGoogle Scholar |

Hendrickson B, Forster BJ, Pogson WS, Chow A (2005) Simple chlorophyll fluorescence parameter that correlates with the rate coefficient of photoinactivation of photosystem II. Photosynthesis Research 84, 43–49.
Simple chlorophyll fluorescence parameter that correlates with the rate coefficient of photoinactivation of photosystem II.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXms1yiu70%3D&md5=c4cf17e92f28fdb6f5cf7824d373acafCAS |

Inkpen J, Quackenbush FW (1969) Extractable and “bound” fatty acids. Cereal Chemistry 46, 580–587.

IPQ (1993) ‘NP 519. Cereais e derivados Determinação do teor de cinza a 900°C.’ (Instituto Português da Qualidade: Lisbon, Portugal)

ISO (2008) ‘ISO 27971. Determination of alveograph properties of dough at constant hydration from commercial or test flours and test milling methodology.’ (International Organization for Standardization: Geneva, Switzerland)

ISO (2013) ‘ISO 20483. Cereals and pulses—Determination of the nitrogen content and calculation of the crude protein content—Kjeldahl method.’ (International Organization for Standardization: Geneva, Switzerland)

Ivanov YV, Savochkin YV, Kuznetsov VV (2011) Scots pine as a model plant for studying the mechanisms of conifers adaptation to heavy metal action: 1. Effects of continuous zinc presence on morphometric and physiological characteristics of developing pine seedlings. Russian Journal of Plant Physiology: a Comprehensive Russian Journal on Modern Phytophysiology 58, 871–878.
Scots pine as a model plant for studying the mechanisms of conifers adaptation to heavy metal action: 1. Effects of continuous zinc presence on morphometric and physiological characteristics of developing pine seedlings.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVGis7nL&md5=937383b6993f90262d74dbdf2b8eb73dCAS |

Kabata-Pendias A, Pendias H (2001) ‘Trace elements in soils and plants.’ (CRC Press: Boca Raton, FL, USA)

Khudsar T, Mahmooduzzafar M, Iqbal I, Sairam RK (2004) Zinc-induced changes in morpho-physiological and biochemical parameters in Artemisia annua. Biologia Plantarum 48, 255–260.
Zinc-induced changes in morpho-physiological and biochemical parameters in Artemisia annua.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXptVeltb4%3D&md5=afb56443161b7a21bf1a05486be834e9CAS |

Kochian LV (1993) Zinc absorption from hydroponic solution by plant roots In ‘Zinc in soils and plants’. (Ed. DA Robson) pp. 45–58. (Kluwer Academic Publishers: Dordrecht, the Netherlands)

Küpper H, Šetlík I, Spiller M, Küpper F, Prášil O (2002) Heavy metal-induced inhibition of photosynthesis: Targets of in vivo heavy metal chlorophyll formation. Journal of Phycology 38, 429–441.
Heavy metal-induced inhibition of photosynthesis: Targets of in vivo heavy metal chlorophyll formation.Crossref | GoogleScholarGoogle Scholar |

Kutman UB, Yildiz B, Ozturk L, Cakmak I (2010) Biofortification of durum wheat with zinc through soil and foliar applications of nitrogen. Cereal Chemistry 87, 1–9.
Biofortification of durum wheat with zinc through soil and foliar applications of nitrogen.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht1Cit7w%3D&md5=159485669488f2832058698c205ab1bcCAS |

Lidon FC, Henriques FS (1992) Effects of copper on the nitrate to ammonia reduction mechanism in rice plants. Photosynthetica 26, 371–380.

Lidon FC, Henriques FS (1998) Role of rice shoot vacuoles in copper toxicity regulation. Environmental and Experimental Botany 39, 197–202.
Role of rice shoot vacuoles in copper toxicity regulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXkvVWit7w%3D&md5=8048bfe3078f1e2228246dd99f5e55a9CAS |

Marschner H (1995) ‘Mineral nutrition of higher plants.’ 2nd edn (Academic Press: San Diego, CA, USA)

Martins LD, Tomaz MA, Lidon FC, DaMatta FM, Ramalho JC (2014) Combined effects of elevated [CO2] and high temperature on leaf mineral balance in Coffea spp. plants. Climatic Change 126, 365–379.
Combined effects of elevated [CO2] and high temperature on leaf mineral balance in Coffea spp. plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhsVCqu7rK&md5=2805d209b4f4500ad392ed789d3f848cCAS |

Mazliak P (1983) Plant membrane lipids: changes and alterations during aging and senescence In ‘Postharvest physiology and crop preservation’. (Ed. M Lieberman) pp. 123–140. (Plenum Press: New York)

Megahad OA, Kinawy OSE (2002) Studies on the extraction of wheat germ oil by commercial hexane. Grasas y Aceites 53, 414–418.
Studies on the extraction of wheat germ oil by commercial hexane.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjsVarsLg%3D&md5=1ae236c64ea94e536f45094c078b075eCAS |

Ramalho JC, Fortunato AS, Goulao LF, Lidon FC (2013) Cold-induced changes in mineral content in Coffea spp. Identification of descriptors for tolerance assessment. Biologia Plantarum 57, 495–506.
Cold-induced changes in mineral content in Coffea spp. Identification of descriptors for tolerance assessment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtV2rsrvM&md5=e3c9930aa5f4c467558823035712866bCAS |

Sagardoy R, Vázquez S, Florez-Sarasa ID, Albacete A, Ribas-Carbó M, Flexas J, Abadía J, Morales F (2010) Stomatal and mesophyll conductances to CO2 are the main limitations to photosynthesis in sugar beet (Beta vulgaris) plants grown with excess zinc. New Phytologist 187, 145–158.
Stomatal and mesophyll conductances to CO2 are the main limitations to photosynthesis in sugar beet (Beta vulgaris) plants grown with excess zinc.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXptV2ntrw%3D&md5=90af2196eda3a96f8c7745600435f1d4CAS | 20374501PubMed |

Schreiber U (2004) Pulse-amplitude-modulation (PAM) fluorometry and saturation pulse method: an overview. In ‘Chlorophyll a fluorescence: a signature of photosynthesis’. (Eds GC Papageorgiou, Govindjee) pp. 279–319. (Springer: Dordrecht, the Netherlands)

Scotti-Campos P, Pais IP, Partelli FL, Batista-Santos P, Ramalho JC (2014) Phospholipids profile in chloroplasts of Coffea spp. genotypes differing in cold acclimation ability. Journal of Plant Physiology 171, 243–249.
Phospholipids profile in chloroplasts of Coffea spp. genotypes differing in cold acclimation ability.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtlCntLzJ&md5=c0eee8279129f73c9e4ec62e423e62c1CAS | 23988560PubMed |

Sgarbieri VC (1987) ‘Alimentação e Nutrição—Fator de saúde e desenvolvimento.’ (Almed Editora e Livraria Ltda: São Paulo)

Singh G, Bhati M (2003) Mineral toxicity and physiological functions in tree seedlings irrigated with effluents of varying chemistry in sandy soil of dry region. Journal of Environmental Sciences 21, 45–63.

Symeonidis L, Karataglis S (1992) The effect of lead and zinc on plant growth and chlorophyll content of Holcus lanataus L. Journal of Agronomy & Crop Science 168, 108–112.
The effect of lead and zinc on plant growth and chlorophyll content of Holcus lanataus L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XitV2hu7o%3D&md5=7329d5622b3024c01b83f86d74287b94CAS |

Tsonev T, Lidon FJC (2012) Zinc in plants—An overview. Emirates Journal of Food and Agriculture 24, 322–333.

Vassilev A, Lidon FC, Matos MC, Ramalho JC, Yordanov I (2002) Photosynthetic performance and some nutrients content in Cd and Cu-treated barley (Hordeum vulgare L). Journal of Plant Nutrition 25, 2343–2360.
Photosynthetic performance and some nutrients content in Cd and Cu-treated barley (Hordeum vulgare L).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnslGntLw%3D&md5=ea7dcd8c2be9655d8ba63de49c2fe1e4CAS |

von Wettstein D, Gough S, Kannangara CG (1995) Chlorophyll biosynthesis. The Plant Cell 7, 1039–1057.
Chlorophyll biosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXnt1Sgt7o%3D&md5=2e699c5424f6ce37816a211d5c026abeCAS | 12242396PubMed |

White PJ (2012) Long-distance transport in the xylem and phloem. In ‘Marschner’s mineral nutrition of higher plants’. 3rd edn (Ed. P Marschner) pp. 49–70. (Academic Press: London)

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 Phytologist 182, 49–84.
Biofortification of crops with seven mineral elements often lacking in human diets – iron, zinc, copper, calcium, magnesium, selenium and iodine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXksVKhtbw%3D&md5=bc00d739e8f944c687ed9fe0c40fb43eCAS | 19192191PubMed |