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

• Published in: The Plant journal : for cell and molecular biology Vol. 84; no. 3; pp. 464 - 477
• Main Authors: Shanmugam, Varanavasiappan, Wang, Yi‐Wen, Tsednee, Munkhtsetseg, Karunakaran, Krithika, Yeh, Kuo‐Chen
• Format: Journal Article
• Language: English
• Published: England Blackwell Publishing Ltd 01-11-2015
• Subjects: Arabidopsis - drug effects; Arabidopsis - physiology; Arabidopsis Proteins - genetics; Arabidopsis thaliana; Basic Helix-Loop-Helix Transcription Factors - genetics; Botany; Buthionine Sulfoximine - pharmacology; Cation Transport Proteins - genetics; Enzymes; Fe deficiency; Fe‐deficiency signaling; FMN Reductase - genetics; Gene Expression Regulation, Plant; Genetics; Glutamate-Cysteine Ligase - antagonists & inhibitors; Glutamate-Cysteine Ligase - genetics; Glutamate-Cysteine Ligase - metabolism; glutathione; Glutathione - metabolism; Glutathione - pharmacology; Iron - metabolism; Iron - pharmacology; Mutation; nitric oxide; Nitric Oxide - metabolism; Plant Roots - genetics; Plant Roots - metabolism; Plant Shoots - genetics; Plant Shoots - metabolism; Plants, Genetically Modified; S-Nitrosoglutathione - metabolism; Signal Transduction; S‐nitrosoglutathione; Arabidopsis thaliana; nitric oxide; Fe-deficiency signaling; S-nitrosoglutathione; glutathione; Fe deficiency
• ISSN: 0960-7412; 1365-313X
• DOI: 10.1111/tpj.13011

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.
Significance Statement
Identifying factors involved in tolerance to iron deficiency is important for maintaining the productivity and nutritional quality of plants. Here we characterized a mutant in GSH1, a gene encoding a key enzyme in the glutathione synthesis pathway and showed that glutathione levels correlate with tolerance to iron deficiency.