A tale of two metals: Biofortification of rice grains with iron and zinc

Abstract

Iron (Fe) and zinc (Zn) are essential micronutrients needed by virtually all living organisms, including plants and humans, for proper growth and development. Due to its capacity to easily exchange electrons, Fe is important for electron transport in mitochondria and chloroplasts. Fe is also necessary for chlorophyll synthesis. Zn is a cofactor for several proteins, including Zn-finger transcription factors and redox metabolism enzymes such as copper/Zn superoxide dismutases. In humans, Fe participates in oxygen transport, electron transport, and cell division whereas Zn is involved in nucleic acid metabolism, apoptosis, immunity, and reproduction. Rice (Oryza sativa L.) is one of the major staple food crops, feeding over half of the world’s population. However, Fe and Zn concentrations are low in rice grains, especially in the endosperm, which is consumed as white rice. Populations relying heavily on rice and other cereals are prone to Fe and Zn deficiency. One of the most cost-effective solutions to this problem is biofortification, which increases the nutritional value of crops, mainly in their edible organs, without yield reductions. In recent years, several approaches were applied to enhance the accumulation of Fe and Zn in rice seeds, especially in the endosperm. Here, we summarize these attempts involving transgenics and mutant lines, which resulted in Fe and/or Zn biofortification in rice grains. We review rice plant manipulations using ferritin genes, metal transporters, changes in the nicotianamine/phytosiderophore pathway (including biosynthetic genes and transporters), regulators of Fe deficiency responses, and other mutants/overexpressing lines used in gene characterization that resulted in Fe/Zn concentration changes in seeds. This review also discusses research gaps and proposes possible future directions that could be important to increase the concentration and bioavailability of Fe and Zn in rice seeds without the accumulation of deleterious elements. We also emphasize the need for a better understanding of metal homeostasis in rice, the importance of evaluating yield components of plants containing transgenes/mutations under field conditions, and the potential of identifying genes that can be manipulated by gene editing and other nontransgenic approaches.

Concomitant Activation of OsNAS2 and OsNAS3 Contributes to the Enhanced Accumulation of Iron and Zinc in Rice

“…For proper growth and development of plants and humans, iron (Fe) and zinc (Zn) are essential micronutrients and accumulate in edible parts of crops that are primary sources of micronutrients for humans [ 1 ]. In plants, Fe is required for electron transfer reactions in mitochondria, chlorophyll biosynthesis, and photosynthesis [ 2 , 3 ]. Zn is a structurally important component for almost 10% of all plant proteins; affects protein–protein interactions in plant cells; and is required as a cofactor for the functional activity of various enzymes such as Cu/Zn superoxide dismutases, carbonic anhydrase, and alkaline phosphatase [ 4 , 5 ].…”

“…Fe and Zn content in rice grains is low, as in other cereal crops such as maize and wheat, and populations that depend on these grains as a staple food experience hidden hunger [ 2 , 9 , 10 ]. As a result, the prevalence of Fe deficiency anemia (IDA) is believed to be above 33% worldwide, while up to 20% may have zinc deficiency [ 2 ].…”

“…Fe and Zn content in rice grains is low, as in other cereal crops such as maize and wheat, and populations that depend on these grains as a staple food experience hidden hunger [ 2 , 9 , 10 ]. As a result, the prevalence of Fe deficiency anemia (IDA) is believed to be above 33% worldwide, while up to 20% may have zinc deficiency [ 2 ]. Biofortification, which uses several strategies such as agronomic practices, traditional plant breeding, and modern biotechnology, is a practical and sustainable method to generate nutritionally enhanced food crops with increased bioavailability to the human population [ 11 ].…”

“…Biofortification, which uses several strategies such as agronomic practices, traditional plant breeding, and modern biotechnology, is a practical and sustainable method to generate nutritionally enhanced food crops with increased bioavailability to the human population [ 11 ]. Transgenic approaches are being used for increasing Fe and Zn concentrations in rice grains, utilizing different genes under the control of constitutive or tissue-specific promoters, either a single gene alone or multiple genes together, which are involved in different regulatory pathways including metal-homeostasis-related genes, metal transporters, the MA pathway, and others [ 2 ].…”

Luxury Zinc Supply Prevents the Depression of Grain Nitrogen Concentrations in Rice (Oryza sativa L.) Typically Induced by Elevated CO2

“…Rice ( Oryza sativa L.; Poales, Poaceae) is the most important staple crop throughout Asia, Latin America, and Africa [ 1 ]; it accounts for about 50–80% of the daily calorie intake of over half of the world population [ 2 , 3 ]. However, rice fails to meet the minimum daily intake requirements of zinc (Zn) [ 4 , 5 ]), iron (Fe) [ 6 , 7 ], and protein [ 8 ]. Rice productivity is generally expected to rise with the rising atmospheric concentration of carbon dioxide ([CO 2 ]) [ 9 , 10 ], and through breeding for increased yield—both factors that decrease the concentrations of essential elements, such as Zn and protein (N) in the grain [ 11 , 12 , 13 , 14 ].…”