SKB1/PRMT5‐mediated histone H4R3 dimethylation of Ib subgroup bHLH genes negatively regulates iron homeostasis in Arabidopsis thaliana

Abstract

These authors contributed equally to this work. SUMMARYHistone modifications play critical roles in the perception of environmental cues by plants. Here, we report that Shk1 binding protein 1 (SKB1/AtPRMT5), which catalyzes the symmetric dimethylation of histone H4R3 (H4R3sme2), is involved in iron homeostasis in Arabidopsis. The SKB1 lesion mutant exhibited higher iron accumulation in shoots and greater tolerance to iron deficiency than the wild type. The expression of SKB1 was not affected by iron, but the level of H4R3sme2 mediated by SKB1 was related to iron status in plants. We showed by chromatin immunoprecipitation (ChIP) and genome-wide ChIP-seq that SKB1 associated with the chromatin of the Ib subgroup bHLH genes (AtbHLH38, AtbHLH39, AtbHLH100 and AtbHLH101), and symmetrically dimethylated histone H4R3. The quantity of SKB1 that associated with chromatin of the Ib subgroup bHLH genes and the level of H4R3sme2 corresponded to the iron status of plants (higher with increased iron supply and lower when iron was removed). We conclude that SKB1-mediated H4R3sme2 regulates iron homeostasis in Arabidopsis in the context of increasing or decreasing expression of Ib subgroup bHLH genes. Iron deficiency may cause an increase in the disassociation of SKB1 from chromatin of the bHLH genes and a decrease in the level of H4R3sme2, thereby elevating their transcription and enhancing iron uptake. Our findings provide new insight into the molecular mechanisms of iron homeostasis in strategy I plants.

Nutrient stress-induced chromatin changes in plants

“…In 2011, Widiez et al characterized the high nitrogen-insensitive 9-1 (hni9) mutant that is impaired in the systemic feedback repression of the root nitrate transporter NRT2.1 by high N supply, revealing that HNI9/AtIWS1 was a key factor in the deposition of trimethylated lysine 27 of histone H3 (H3K27me3) at the NRT2.1 locus in response to high N supply [25]. More recently, it has been shown that symmetric dimethylation of histone H4R3 (H4R3sme2) was involved in iron homeostasis [26 ]. Indeed, mutation in the Arabidopsis Protein Arginine MethylTransferase 5 (PRMT5, also referred to as SKB1), involved in catalyzing histone H4R3 symmetric dimethylation, resulted in mutant plants having higher iron accumulation in shoots and greater tolerance to iron deficiency than wild type plants.…”

“…Indeed, mutation in the Arabidopsis Protein Arginine MethylTransferase 5 (PRMT5, also referred to as SKB1), involved in catalyzing histone H4R3 symmetric dimethylation, resulted in mutant plants having higher iron accumulation in shoots and greater tolerance to iron deficiency than wild type plants. Mutation in PRMT5 also affected the expression of several Ib subgroup bHLH genes [26 ], which are required for the regulation of iron uptake and homeostasis in Arabidopsis [27] and iron-uptake processes [26 ]. The involvement of trimethylated lysine 4 of histone H3 (H3K4me3) in response to nutrient stress was also reported in a study aimed at identifying genes involved in root hair elongation in Arabidopsis specifically under phosphate starvation, revealing the alfin-like 6 (AL6) gene [28,29].…”

The bHLH Transcription Factor bHLH104 Interacts with IAA-LEUCINE RESISTANT3 and Modulates Iron Homeostasis in Arabidopsis

“…Recently, the lesion mutant of SHK1 BINDING PROTEIN1, which mediates symmetric histone dimethylation, was found to accumulate high levels of Fe in shoots and exhibit tolerance to Fe deficiency. This reveals that epigenetic control is involved in Fe homeostasis (Fan et al, 2014). By coexpression analysis of PYE, Long et al (2010) found the E3 ligase BRUTUS (BTS) as a putative negative regulator of Fe absorption.…”

GENERAL CONTROL NONREPRESSED PROTEIN5-Mediated Histone Acetylation of FERRIC REDUCTASE DEFECTIVE3 Contributes to Iron Homeostasis in Arabidopsis

“…Recent studies have highlighted transcriptional responses to iron deficiency (Buckhout et al, 2009;Yang and Finnegan, 2010) and that the regulation of gene expression is accomplished by epigenetic mechanisms that modulate chromatin structure. Fan et al (2014) reported that histone H4R3 dimethylation negatively regulated iron homeostasis by affecting several Ib subgroup bHLH genes and the iron-uptake processes. Here, our data show that histone acetylation is also important for iron distribution.…”

“…For example, Shk1 binding protein1 (SKB1), which catalyzes the symmetric dimethylation of histone 4 arginine 3 (H4R3), is involved in iron homeostasis in Arabidopsis. Histone H4R3 dimethylation negatively regulates iron homeostasis by affecting several Ib subgroup bHLH genes and iron-uptake processes (Fan et al, 2014).…”