Iron-Nicotianamine Transporters Are Required for Proper Long Distance Iron Signaling

Abstract

The mechanisms of root iron uptake and the transcriptional networks that control root-level regulation of iron uptake have been well studied, but the mechanisms by which shoots signal iron status to the roots remain opaque. Here, we characterize an Arabidopsis (Arabidopsis thaliana) double mutant, yellow stripe1-like yellow stripe3-like (ysl1ysl3), which has lost the ability to properly regulate iron deficiency-influenced gene expression in both roots and shoots. In spite of markedly low tissue levels of iron, the double mutant does not up-and down-regulate iron deficiency-induced and -repressed genes. We have used grafting experiments to show that wild-type roots grafted to ysl1ysl3 shoots do not initiate iron deficiency-induced gene expression, indicating that the ysl1ysl3 shoots fail to send an appropriate long-distance signal of shoot iron status to the roots. We present a model to explain how impaired iron localization in leaf veins results in incorrect signals of iron sufficiency being sent to roots and affecting gene expression there. Improved understanding of the mechanism of long-distance iron signaling will allow improved strategies for the engineering of staple crops to accumulate additional bioavailable iron in edible parts, thus improving the iron nutrition of the billions of people worldwide whose inadequate diet causes iron deficiency anemia.

An effective antioxidant defense provides protection against zinc deficiency‐induced oxidative stress in Zn‐efficient maize plants

“…GSH and AA have been reported to protect Arabidopsis plants against detrimental effects of Fe deficiency by increasing tissue Fe concentration (Ramirez et al, 2013). Both Zn and Fe probably share certain common mechanism of their uptake and translocation in plants as Zn deficiency is reported to induce FRO4 (ferric chelate reductase), ZIP1 (zinc transporter), ZIP4 (metal transporter), and ZIP5 (metal transporter; Wintz et al, 2003), NAS2, NAS3, and NAS4 (encode nicotianamine synthases; van de Mortel et al, 2006) and Fe deficiency is reported to induce FRO2 (ferric chelate reductase; Le et al, 2016), IRT1 (Ivanov et al, 2014;Le et al, 2016;Kumar et al, 2017), IRT2 (Fe transporter genes; Wintz et al, 2003) and ZAT12 (zinc finger of Arabidopsis thaliana) transcripts (Le et al, 2016).…”

Micrografting device for testing environmental conditions for grafting and systemic signaling in Arabidopsis

“…A double-knockout mutant of two YSL members, ysl1ysl3 , showed a weak Fe-deficiency response even under Fe-starvation conditions, the phenotype of which is opposite to the opt3 and nas4x-2 mutants. Kumar et al (2017) indicated that the weak deficiency phenotype of ysl1ysl3 mutant could be explained by the restriction of Fe distribution within leaf veins. The weak Fe-deficiency response of a ysl1ysl3 mutant was rescued by grafting onto WT shoots but not WT roots, demonstrating that YSL1 and YSL3 in shoots, the expression of which is strongly detected in the xylem parenchyma and the phloem, respectively, are required for the Fe-deficiency response in roots.…”

“…The restoration of the nas4x-2 root phenotype by WT shoot grafting emphasized the contribution of Fe–NA transport via shoot phloem tissues to systemic Fe distribution. Previous studies already showed that the Fe status is regulated both locally and systemically (Jeong et al , 2017, Kumar et al , 2017). With regard to local regulation, the amount of available Fe in the root apoplast affects the expression of IRT1 and FERRIC REDUCTION OXIGENASE2 , encoding a ferric chelate reductase (Vert et al , 2003).…”

“…With regard to local regulation, the amount of available Fe in the root apoplast affects the expression of IRT1 and FERRIC REDUCTION OXIGENASE2 , encoding a ferric chelate reductase (Vert et al , 2003). Recently, Kumar et al (2017) conducted micrografting experiments using a mutant of Fe–NA transporters called Yellow Stripe1-Like (YSL) family. A double-knockout mutant of two YSL members, ysl1ysl3 , showed a weak Fe-deficiency response even under Fe-starvation conditions, the phenotype of which is opposite to the opt3 and nas4x-2 mutants.…”

“…Like phytohormones, macro-and micronutrients also have each specific form for long-distance transport (Maathuis, 2009, Hänsch and Mendel, 2009). As an instance, iron (Fe) homeostasis is regulated in a systemic manner, where Fe makes conjugates with metal chelators such as citrate (Ci) and nicotianamine (NA) and distributed to entire body via the vascular tissues together with the action of transporters (Maas et al , 1988, Durrett et al , 2007, Gayomba et al , 2015, Kumar et al , 2017). In Arabidopsis harboring a mutation in Oligopeptide Transporter 3 ( OPT3 ), which mediates uptake of Fe into phloem and regulates shoot-to-root Fe redistribution, shoot-to-root Fe transport was disrupted, causing accumulation of Fe in shoots (Zhai et al , 2014).…”