Potential Implications of Interactions between Fe and S on Cereal Fe Biofortification

Abstract

Iron (Fe) and sulfur (S) are two essential elements for plants, whose interrelation is indispensable for numerous physiological processes. In particular, Fe homeostasis in cereal species is profoundly connected to S nutrition because phytosiderophores, which are the metal chelators required for Fe uptake and translocation in cereals, are derived from a S-containing amino acid, methionine. To date, various biotechnological cereal Fe biofortification strategies involving modulation of genes underlying Fe homeostasis have been reported. Meanwhile, the resultant Fe-biofortified crops have been minimally characterized from the perspective of interaction between Fe and S, in spite of the significance of the crosstalk between the two elements in cereals. Here, we intend to highlight the relevance of Fe and S interrelation in cereal Fe homeostasis and illustrate the potential implications it has to offer for future cereal Fe biofortification studies.

Keywords: Fe and S interaction; Fe biofortification; Strategy I; Strategy II; cereals; nicotianamine; phytosiderophores.

Figure 1

Overview of the connection between sulfur (S) nutrition and iron (Fe) nutrition in cereals plants. Black arrows indicate enzymatic synthetic reactions, unless otherwise indicated. Blue arrows signify promotional effects between biological processes, whereas red bars with flat ends indicate suppressive effects between biological agents and processes. Arrows and bars with dotted lines indicate relationships between biological processes/agents that are hypothetically pronounced in Fe-biofortified crops. Hydrogen sulfide (H₂S) is hypothesized to regulate nicotianamine (NA)/phytosiderophores (PS) synthesis via unknown biological mechanisms or agents. Abbreviations are as follows: APS: ADENOSINE PHOSPHOSULFATE; APSR: APS REDUCTASE; ATPS: ATP SULFURYLASE; CBL: CYSTATHIONINE β-LYASE; CGS: CYSTATHIONINE γ-SYNTHASE; Cys: cysteine; DMA: deoxymugineic acid; DMAS: DMA SYNTHASE; Glu: glutamate; Gly: glycine; GS: GLUTATHIONE SYNTHETASE; GSH: glutathione; Met: methionine; MS: Met synthase; MT: METALLOTHIONEIN; NAAT: NA AMINOTRANSFERASE; NAS: NA SYNTHASE; OAS: O-acetylserine; OAS-TL: OAS (THIOL) LYASE; PC; phytochelatin; PCS: PC synthase; ROS: reactive oxygen species; S²⁻: sulfide; SAM: S-adenosyl methionine; SAMS: SAM SYNTHASE; Ser: serine; SO₃²⁻: sulfite; SO₄²⁻: sulfate; SULTR: SULFATE TRANSPORTER; Zn: zinc; γ-EC: glutamylcysteine; γ-ECS: γ-EC SYNTHETASE.

Figure 2

Graphical summary of important cereal iron (Fe) biofortification strategies. Proteins surrounded with blue squares are those whose modulation leads to increase in grain Fe concentration. Blue underlines indicate the molecules whose genes are up-regulated in rice lines overaccumulating nicotianamine (NA) or overexpressing NA SYNTHASE (NAS). Red underscores refer to the complexes whose amount is putatively increased in NAS-overexpressing lines. Black arrows indicate the movement of molecules unless otherwise noted, whereas green arrows signify synthetic enzymatic reactions. In the inset for Fe homeostasis regulation, blue arrows and red bars with flat ends indicate promotional and suppressive effects between molecular agents and/or processes, respectively. In the same inset, black arrows pointing to the bin indicate proteasomic degradation of proteins. Abbreviations are as follows: AtNRAMP3: NATURAL RESISTANCE-ASSOCIATED MACROPHAGE PROTEIN 3 from Arabidopsis thaliana; bHLH156: BASIC HELIX-LOOP-HELIX 156; DMA: deoxymugineic acid; DMAS: DMA SYNTHASE; FER: FERRITIN; HRZ: HEMERYTHRIN MOTIF-CONTAINING REALLY INTERESTING NEW GENE- AND ZINC-FINGER PROTEIN; IBP1: IDEF1-BINDING PROTEIN 1; IDEF1: IRON DEFICIENCY-RESPONSIVE ELEMENT-BINDING FACTOR 1; IRO2/3: IRON-RELATED TRANSCRIPTION FACTOR 2/3; IRT1: IRON-REGULATED TRANSPORTER 1; PRI: POSITIVE REGULATOR OF IRON DEFICIENCY RESPONSE; TOM1: TRANSPORTER OF MUGENEIC ACID 1; VIT: VACUOLAR IRON TRANSPORTER; YSL2/15: YELLOW STRIPE-1 LIKE 2/15.

Figure 3

Schematic representation of the occurrence of rice sulfide toxicity as affected by water management practice and soil sulfur (S) availability. (A) In upland conditions, the majority of S in soil exists in oxidized forms (SO₄²⁻) due to high availability of oxygen in the soil. (B) Prolonged submergence leads to S reduction in deep soil, where anerobic condition prevails. (C) S abundance in the soil can further promote sulfide (S²⁻) occurrence, leading to higher risk of sulfide toxicity in rice, ultimately resulting in yield loss.

Figure 4

Proposed hypothetical effect of NICOTIANAMINE SYNTHASE (NAS) overexpression on Fe plaque accumulation and susceptibility to sulfide toxicity. (A) In non-transgenic (NT) rice plants, a portion of the oxygen (O₂) supplied for the roots via aerenchyma diffuses to oxidize the rhizosphere (radial oxygen loss; ROL), where iron (Fe) accumulates as ferric oxides as Fe plaque. Protocatechuic acid (PCA) secreted from PHENOLICS EFFLUX ZERO2 (PEZ2) and possibly deoxymugineic acid (DMA) secreted from TRANSPORTER OF MUGENEIC ACID 1 (TOM1) contribute to solubilization of Fe plaque. Sulfide (S²⁻) can also react with Fe to form FeS. (B) PEZ1-overexpressing plants reported by Ishimaru et al. (2011) accumulated less Fe on their roots. This was likely due to increased secretion of phenolics to the rhizosphere through PEZ1. (C) NAS overexpression leads to increased DMA synthesis as well as upregulation of TOM1, leading to enhanced secretion of DMA into the rhizosphere. If DMA contributes to Fe plaque solubilization and forms stronger complex with Fe(III) than phenolics do, NAS overexpression might result in significant reduction of Fe plaque. This might have implications for buffering sulfide toxicity; however, this needs further research.