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Phytosiderophores determine thresholds for iron and zinc accumulation in biofortified rice endosperm while inhibiting the accumulation of cadmium.

ABSTRACT: Nicotianamine (NA) and 2'-deoxymugenic acid (DMA) are metal-chelating ligands that promote the accumulation of metals in rice endosperm, but it is unclear how these phytosiderophores regulate the levels of different metals and limit their accumulation. In this study, transgenic rice plants producing high levels of NA and DMA accumulated up to 4-fold more iron (Fe) and 2-fold more zinc (Zn) in the endosperm compared with wild-type plants. The distribution of Fe and Zn in vegetative tissues suggested that both metals are sequestered as a buffering mechanism to avoid overloading the seeds. The buffering mechanism involves the modulation of genes encoding metal transporters in the roots and aboveground vegetative tissues. As well as accumulating more Fe and Zn, the endosperm of the transgenic plants accumulated less cadmium (Cd), suggesting that higher levels of Fe and Zn competitively inhibit Cd accumulation. Our data show that although there is a strict upper limit for Fe (~22.5 µg g-1 dry weight) and Zn (~84 µg g-1 dry weight) accumulation in the endosperm, the careful selection of strategies to increase endosperm loading with essential minerals can also limit the accumulation of toxic metals such as Cd, thus further increasing the nutritional value of rice.

SUBMITTER: Banakar R

PROVIDER: S-EPMC5853871 | biostudies-literature | 2017 Oct

REPOSITORIES: biostudies-literature

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Phytosiderophores determine thresholds for iron and zinc accumulation in biofortified rice endosperm while inhibiting the accumulation of cadmium.

Banakar Raviraj R Alvarez Fernandez Ana A Díaz-Benito Pablo P Abadia Javier J Capell Teresa T Christou Paul P

Journal of experimental botany 20171001 17

Nicotianamine (NA) and 2'-deoxymugenic acid (DMA) are metal-chelating ligands that promote the accumulation of metals in rice endosperm, but it is unclear how these phytosiderophores regulate the levels of different metals and limit their accumulation. In this study, transgenic rice plants producing high levels of NA and DMA accumulated up to 4-fold more iron (Fe) and 2-fold more zinc (Zn) in the endosperm compared with wild-type plants. The distribution of Fe and Zn in vegetative tissues sugges ...[more]

PMID: 29048564

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Project description:Zinc malnutrition is a major issue in developing countries where polished rice is a staple food. With the existing significant genetic variability for high zinc in polished rice, the development of biofortified rice varieties was targeted in India with support from HarvestPlus, Department of Biotechnology, and Indian Council of Agricultural Research of Government of India. Indian Institute of Rice Research (IIRR) facilitates rice varietal release through All India Coordinated Rice Improvement Project (AICRIP) and also supports rice biofortification program in India. Various germplasm sets of several national institutions were characterized at IIRR for their zinc content in brown rice using energy-dispersive X-ray fluorescence spectroscopy indicating the range of zinc to be 7.3 to 52.7 mg/kg. Evaluation of different mapping populations involving wild germplasm, landraces, and varieties for their zinc content showed the feasibility of favorable recombination of high zinc content and yield. Ninety-nine genotypes from germplasm and 344 lines from mapping populations showed zinc content of ≥28 mg/kg in polished rice meeting the target zinc content set by HarvestPlus. Through AICRIP biofortification trial constituted since 2013, 170 test entries were nominated by various national institutions until 2017, and four biofortified rice varieties were released. Only the test entry with target zinc content, yield, and quality parameters is promoted to the next year; thus, each test entry is evaluated for 3 years across 17 to 27 locations for their performance. Multilocation studies of two mapping populations and AICRIP biofortification trials indicated the zinc content to be highly influenced by environment. The bioavailability of a released biofortified rice variety, viz., DRR Dhan 45 was found to twice that of control IR64. The technology efficacy of the four released varieties developed through conventional breeding ranged from 48 to 75% with zinc intake of 38 to be 47% and 46 to 57% of the RDA for male and female, respectively. The observations from the characterization of germplasm and mapping populations for zinc content and development of national evaluation system for the release of biofortified rice varieties have been discussed in the context of the five criteria set by biofortification program.

Project description:Biofortification of rice (Oryza sativa L.) with micronutrients is widely recognized as a sustainable strategy to alleviate human iron (Fe) and zinc (Zn) deficiencies in developing countries where rice is the staple food. Constitutive overexpression of the rice nicotianamine synthase (OsNAS) genes has been successfully implemented to increase Fe and Zn concentrations in unpolished and polished rice grain. Intensive research is now needed to couple this high-micronutrient trait with high grain yields. We investigated associations of increased grain Fe and Zn concentrations with agro-morphological traits of backcross twice second filial (BC2F2) transgenic progeny carrying OsNAS1 or OsNAS2 overexpression constructs under indica/japonica and japonica/japonica genetic backgrounds. Thirteen agro-morphological traits were evaluated in BC2F2 transgenic progeny grown under hydroponic conditions. Concentrations of eight mineral nutrients (Fe, Zn, copper, manganese, calcium, magnesium, potassium, and phosphorus) in roots, stems/sheaths, non-flag leaves, flag leaves, panicles, and grain were also determined. A distance-based linear model (DistLM) was utilized to extract plant tissue nutrient predictors accounting for the largest variation in agro-morphological traits differing between transgenic and non-transgenic progeny. Overall, the BC2F2 transgenic progeny contained up to 148% higher Fe and 336% higher Zn concentrations in unpolished grain compared to non-transgenic progeny. However, unpolished grain concentrations surpassing 23 ?g Fe g-1 and 40 ?g Zn g-1 in BC2F2indica/japonica progeny, and 36 ?g Fe g-1 and 56 ?g Zn g1 in BC2F2japonica/japonica progeny, were associated with significant reductions in grain yield. DistLM analyses identified grain-Zn and panicle-magnesium as the primary nutrient predictors associated with grain yield reductions in the indica/japonica and japonica/japonica background, respectively. We subsequently produced polished grain from high-yield BC2F2 transgenic progeny carrying either the OsNAS1 or OsNAS2 overexpression constructs. The OsNAS2 overexpressing progeny had higher percentages of Fe and Zn in polished rice grain compared to the OsNAS1 overexpressing progeny. Results from this study demonstrate that genetic background has a major effect on the development of Fe and Zn biofortified rice. Moreover, our study shows that high-yielding rice lines with Fe and Zn biofortified polished grain can be developed by OsNAS2 overexpression and monitoring for Zn overaccumulation in the grain.

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Phytosiderophores determine thresholds for iron and zinc accumulation in biofortified rice endosperm while inhibiting the accumulation of cadmium.

Publications

Phytosiderophores determine thresholds for iron and zinc accumulation in biofortified rice endosperm while inhibiting the accumulation of cadmium.

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