Subcellular dynamics studies of iron reveal how tissue-specific distribution patterns are established in developing wheat grains.

Yongfang Wan,Peter R Shewry,Janneke Balk,James M Connorton,Eudri Venter,Katie L Moore,Sadia Sheraz,Shailender K Verma,Qing Xiong,Joshua Waites

doi:10.1111/nph.17440

Abstract

Understanding the mechanisms of iron trafficking in plants is key to enhancing the nutritional quality of crops. Because it is difficult to image iron in transit, we currently have an incomplete picture of the route(s) of iron translocation in developing seeds and how the tissue-specific distribution is established. We have used a novel approach, combining iron-57 (57 Fe) isotope labelling and nanoscale secondary ion mass spectrometry (NanoSIMS), to visualize iron translocation between tissues and within cells in immature wheat grain, Triticum aestivum. This enabled us to track the main route of iron transport from maternal tissues to the embryo through the different cell types. Further evidence for this route was provided by genetically diverting iron into storage vacuoles, with confirmation provided by histological staining and transmission electron microscopy energy dispersive X-ray spectroscopy (TEM-EDS). Almost all iron in both control and transgenic grains was found in intracellular bodies, indicating symplastic rather than apoplastic transport. Furthermore, a new type of iron body, highly enriched in 57 Fe, was observed in aleurone cells and may represent iron being delivered to phytate globoids. Correlation of the 57 Fe enrichment profiles obtained by NanoSIMS with tissue-specific gene expression provides an updated model of iron homeostasis in cereal grains with relevance for future biofortification strategies.

Highlights

As widely consumed staple crops, cereals are important sources of mineral micronutrients, including iron and zinc which are essential for human health
Our results revealed that the major route of iron is from the nucellar transfer cells through a zone of endosperm cells between the crease and the embryo, but that this pathway is disrupted by overexpression of TaVIT2
To select one line for detailed study, we chose line 22-19 based on a representative pattern of iron staining in handdissected grain and a consistent > two-fold increase in the iron concentration in the white flour fraction

Summary

Introduction

As widely consumed staple crops, cereals are important sources of mineral micronutrients, including iron and zinc which are essential for human health. Deficiencies in these minerals affect large parts of the global population (WHO, 2013, 2015). Iron and zinc are unevenly distributed in the grain, accumulating at high concentrations in the embryo (germ) and outer layers (bran), which are removed during polishing or milling. By contrast, both minerals are low in the starchy endosperm which constitutes about 70% of the grain and is preferentially consumed in human diets (as white wheat flour and polished rice, for example). Attempts to biofortify cereal grains are focussing on increasing the total amounts of iron and zinc, changing their distribution and reducing phytic acid levels (Vasconcelos et al, 2017; Cominelli et al, 2020)

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