Metabolic engineering of bread wheat improves grain iron concentration and bioavailability

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Summary

Bread wheat ( Triticum aestivum L.) is cultivated on more land than any other crop and produces a fifth of the calories consumed by humans. Wheat endosperm is rich in starch yet contains low concentrations of dietary iron (Fe) and zinc (Zn). Biofortification is a micronutrient intervention aimed at increasing the density and bioavailability of essential vitamins and minerals in staple crops; Fe biofortification of wheat has proved challenging. In this study we employed constitutive expression ( CE) of the rice ( Oryza sativa L.) nicotianamine synthase 2 ( Os NAS2 ) gene in bread wheat to up‐regulate biosynthesis of two low molecular weight metal chelators – nicotianamine ( NA) and 2′‐deoxymugineic acid ( DMA) – that play key roles in metal transport and nutrition. The CE‐ Os NAS2 plants accumulated higher concentrations of grain Fe, Zn, NA and DMA and synchrotron X‐ray fluorescence microscopy ( XFM) revealed enhanced localization of Fe and Zn in endosperm and crease tissues, respectively. Iron bioavailability was increased in white flour milled from field‐grown CE‐ Os NAS2 grain and positively correlated with NA and DMA concentrations.

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Increasing CO2 threatens human nutrition.

Samuel Myers, Antonella Zanobetti, Itai Kloog … (2014)

Dietary deficiencies of zinc and iron are a substantial global public health problem. An estimated two billion people suffer these deficiencies, causing a loss of 63 million life-years annually. Most of these people depend on C3 grains and legumes as their primary dietary source of zinc and iron. Here we report that C3 grains and legumes have lower concentrations of zinc and iron when grown under field conditions at the elevated atmospheric CO2 concentration predicted for the middle of this century. C3 crops other than legumes also have lower concentrations of protein, whereas C4 crops seem to be less affected. Differences between cultivars of a single crop suggest that breeding for decreased sensitivity to atmospheric CO2 concentration could partly address these new challenges to global health.

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Wheat.

P. Shewry (2009)

Wheat is the dominant crop in temperate countries being used for human food and livestock feed. Its success depends partly on its adaptability and high yield potential but also on the gluten protein fraction which confers the viscoelastic properties that allow dough to be processed into bread, pasta, noodles, and other food products. Wheat also contributes essential amino acids, minerals, and vitamins, and beneficial phytochemicals and dietary fibre components to the human diet, and these are particularly enriched in whole-grain products. However, wheat products are also known or suggested to be responsible for a number of adverse reactions in humans, including intolerances (notably coeliac disease) and allergies (respiratory and food). Current and future concerns include sustaining wheat production and quality with reduced inputs of agrochemicals and developing lines with enhanced quality for specific end-uses, notably for biofuels and human nutrition.

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Constitutive Overexpression of the OsNAS Gene Family Reveals Single-Gene Strategies for Effective Iron- and Zinc-Biofortification of Rice Endosperm

Alexander Johnson, Bianca Kyriacou, Damien L. Callahan … (2011)

Background Rice is the primary source of food for billions of people in developing countries, yet the commonly consumed polished grain contains insufficient levels of the key micronutrients iron (Fe), zinc (Zn) and Vitamin A to meet daily dietary requirements. Experts estimate that a rice-based diet should contain 14.5 µg g−1 Fe in endosperm, the main constituent of polished grain, but breeding programs have failed to achieve even half of that value. Transgenic efforts to increase the Fe concentration of rice endosperm include expression of ferritin genes, nicotianamine synthase genes (NAS) or ferritin in conjunction with NAS genes, with results ranging from two-fold increases via single-gene approaches to six-fold increases via multi-gene approaches, yet no approach has reported 14.5 µg g−1 Fe in endosperm. Methodology/Principal Findings Three populations of rice were generated to constitutively overexpress OsNAS1, OsNAS2 or OsNAS3, respectively. Nicotianamine, Fe and Zn concentrations were significantly increased in unpolished grain of all three of the overexpression populations, relative to controls, with the highest concentrations in the OsNAS2 and OsNAS3 overexpression populations. Selected lines from each population had at least 10 µg g−1 Fe in polished grain and two OsNAS2 overexpression lines had 14 and 19 µg g−1 Fe in polished grain, representing up to four-fold increases in Fe concentration. Two-fold increases of Zn concentration were also observed in the OsNAS2 population. Synchrotron X-ray fluorescence spectroscopy demonstrated that OsNAS2 overexpression leads to significant enrichment of Fe and Zn in phosphorus-free regions of rice endosperm. Conclusions The OsNAS genes, particularly OsNAS2, show enormous potential for Fe and Zn biofortification of rice endosperm. The results demonstrate that rice cultivars overexpressing single rice OsNAS genes could provide a sustainable and genetically simple solution to Fe and Zn deficiency disorders affecting billions of people throughout the world.

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Author and article information

Contributors

Alexander A. T. Johnson:

ORCID: https://orcid.org/0000-0002-1209-6447

johnsa@unimelb.edu.au

Journal

Journal ID (nlm-ta): Plant Biotechnol J

Journal ID (iso-abbrev): Plant Biotechnol. J

Journal ID (doi): 10.1111/(ISSN)1467-7652

Journal ID (publisher-id): PBI

Title: Plant Biotechnology Journal

Publisher: John Wiley and Sons Inc. (Hoboken )

ISSN (Print): 1467-7644

ISSN (Electronic): 1467-7652

Publication date (Electronic): 25 January 2019

Publication date (Print): August 2019

Volume: 17

Issue: 8 ( doiID: 10.1111/pbi.2019.17.issue-8 )

Pages: 1514-1526

Affiliations

[ ¹ ] School of BioSciences The University of Melbourne Melbourne VIC Australia

[ ² ] School of Life and Environmental Sciences Deakin University Burwood VIC Australia

[ ³ ] Robert W. Holley Center for Agriculture and Health USDA‐ARS Ithaca NY USA

[ ⁴ ] Future Industries Institute University of South Australia Mawson Lakes SA Australia

[ ⁵ ]Present address: Institute for Applied Ecology University of Canberra Canberra ACT 2617 Australia

Author notes

[*] [* ] Correspondence (Tel +61 3 8344 3969; fax +61 3 9347 5460; email: johnsa@ 123456unimelb.edu.au )

[†]

These authors contributed equally to this work.

Author information

Alexander A. T. Johnson https://orcid.org/0000-0002-1209-6447

Article

Publisher ID: PBI13074

DOI: 10.1111/pbi.13074

PMC ID: 6662306

PubMed ID: 30623558

SO-VID: 51033e73-4fd7-4fce-994a-3a96f81abf98

License:

This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

History

Date received : 09 July 2018

Date revision received : 13 December 2018

Date accepted : 17 December 2018

Page count

Figures: 6, Tables: 1, Pages: 13, Words: 8303

Funding

Funded by: HarvestPlus Challenge program

Custom metadata

source-schema-version-number 2.0

component-id pbi13074

cover-date August 2019

details-of-publishers-convertor Converter:WILEY_ML3GV2_TO_NLMPMC version:5.6.6.2 mode:remove_FC converted:29.07.2019

ScienceOpen disciplines: Biotechnology

Keywords: nicotianamine,2′‐deoxymugineic acid,biofortification,zinc,caco‐2,x‐ray fluorescence microscopy

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ScienceOpen disciplines: Biotechnology

Keywords: nicotianamine, 2′‐deoxymugineic acid, biofortification, zinc, caco‐2, x‐ray fluorescence microscopy

Metabolic engineering of bread wheat improves grain iron concentration and bioavailability

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Most cited references 40

Increasing CO2 threatens human nutrition.

Wheat.

Constitutive Overexpression of the OsNAS Gene Family Reveals Single-Gene Strategies for Effective Iron- and Zinc-Biofortification of Rice Endosperm

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