Glutathione plays an essential role in nitric oxide‐mediated iron‐deficiency signaling and iron‐deficiency tolerance in Arabidopsis

Abstract

Summary Iron (Fe) deficiency is a common agricultural problem that affects both the productivity and nutritional quality of plants. Thus, identifying the key factors involved in the tolerance of Fe deficiency is important. In the present study, the zir1 mutant, which is glutathione deficient, was found to be more sensitive to Fe deficiency than the wild type, and grew poorly in alkaline soil. Other glutathione‐deficient mutants also showed various degrees of sensitivity to Fe‐limited conditions. Interestingly, we found that the glutathione level was increased under Fe deficiency in the wild type. By contrast, blocking glutathione biosynthesis led to increased physiological sensitivity to Fe deficiency. On the other hand, overexpressing glutathione enhanced the tolerance to Fe deficiency. Under Fe‐limited conditions, glutathione‐deficient mutants, zir1, pad2 and cad2 accumulated lower levels of Fe than the wild type. The key genes involved in Fe uptake, including IRT1, FRO2 and FIT, are expressed at low levels in zir1; however, a split‐root experiment suggested that the systemic signals that govern the expression of Fe uptake‐related genes are still active in zir1. Furthermore, we found that zir1 had a lower accumulation of nitric oxide (NO) and NO reservoir S‐nitrosoglutathione (GSNO). Although NO is a signaling molecule involved in the induction of Fe uptake‐related genes during Fe deficiency, the NO‐mediated induction of Fe‐uptake genes is dependent on glutathione supply in the zir1 mutant. These results provide direct evidence that glutathione plays an essential role in Fe‐deficiency tolerance and NO‐mediated Fe‐deficiency signaling in Arabidopsis.

S‐Nitrosoglutathione works downstream of nitric oxide to mediate iron‐deficiency signaling in Arabidopsis

“…A previous study has demonstrated that critical GSH levels were involved in NO‐mediated Fe‐starvation signaling and are required for tolerance to Fe deficiency (Shanmugam et al ., ). We speculated that, according to Figures , and S4, GSNO may act downstream of NO to regulate FIT but not lb bHLH genes.…”

“…Under Fe starvation, both NO and GSH levels are increased, so as to activate the Fe‐deficiency response (Chen et al ., ; Garcia et al ., ; Shanmugam et al ., ). Our data indicated that NO is immediately induced upon exposure to Fe deficiency (Figure b) whereas GSH level is increased during 5 day Fe starvation (Shanmugam et al ., ), such an increase cannot be observed after 6 h Fe deficiency (Figure c). R7 enhanced both NO and GSH levels in roots under Fe deficiency (Figures and S7).…”

Glutathione foliar fertilisation prevents lime‐induced iron chlorosis in soil grownMedicago scutellata

“…An effect of GSH applied via roots on preserving cell redox homeostasis has been previously reported in Arabidopsis ( Ramírez et al., ). Several studies support that glutathione plays an essential role in Fe‐deficiency tolerance and NO‐mediated Fe‐deficiency signalling in plants ( Ramírez et al., , ; Koen et al., ; Shanmugam et al., , ). Data are also in line with previous studies on GSH in different abiotic stresses in other plant species ( Chen et al., , ; Hussain et al., ; Akram et al., ; Bela et al., ; Cao et al., ).…”

Ascorbate Alleviates Fe Deficiency-Induced Stress in Cotton (Gossypium hirsutum) by Modulating ABA Levels

“…Recent evidence suggests the existence of a role for ascorbate (ASC) and glutathione (GSH) in adaption to Fe deficiency (Ramirez et al, 2013; Shanmugam et al, 2015). In animals, ASC is involved in iron accumulation by astrocytes, an important contributor to iron homoeostasis in the mammalian brain (Lane et al, 2010).…”

“…In higher plants, ASC and GSH treatments can alleviate Fe deficiency-induced chlorosis and restore chlorophyll content in Fe-deficient Arabidopsis seedlings (Ramirez et al, 2013). Recently, a study indicated that the decrease in GSH concentrations in the GSH biosynthesis pathway mutant zir1 significantly reduces plant tolerance to Fe deficiency and alkaline soils, while transgenic ZIR1 overexpressors exhibit increases in GSH content and enhanced tolerance to Fe deficiency (Shanmugam et al, 2015). However, the underlying molecular basis for ASC or GSH effects on Fe deficiency, including links with plant hormone signaling systems, are not well-understood.…”