3.5 ǀ Sensing of plant Fe status
Until now, the mechanisms of Fe sensing in plants have mostly been investigated under Fe deficient conditions rather than under Fe excess. In both rice and Arabidopsis (Arabidopsis thaliana ), a group of proteins containing the hemerythrin motif are involved in sensing Fe deficiency. In rice, Hemerythrin motif-containing RING- and zinc-finger protein 1/2 (OsHRZ1/2), directly bind to Fe and functions as a molecular sensor for Fe status (Kobayashi et al., 2013). OsHRZ1/2 proteins negatively affect Fe deficiency responses, and knockdown of these proteins renders plants less susceptible to Fe deficiency, probably by destabilizing a basic helix-loop-helix (bHLH) transcription factor OsPRI1 (Zhang et al., 2017). Likewise, a homologue of OsHRZ1/2 in Arabidopsis, BRUTUS, negatively affects the stability of PRI1 homologues (Arabidopsis bHLH105/115) and Fe deficiency responses (Selote et al., 2015), indicating that the Fe sensing mechanisms via the hemerythrin motif-containing proteins are conserved among higher plant species.
A recent study showed that knockdown of OsHRZ2 leads to susceptibility to Fe excess stress in rice. The OsHRZ2-knockdown plants were associated with greater growth retardation, leaf bronzing and shoot Fe concentrations compared with the wild-type plants under Fe excess condition (Aung, Kobayashi, Masuda & Nishizawa, 2018b). Correspondingly, the expression of Fe deficiency-inducible genes associated with Fe uptake, such as OsNAS1/2, mugineic acid transporter OsTOM1, and Yellow Stripe-Like 15 (OsYSL15) that encodes a Fe transporter, were higher in the OsHRZ2 knockdown plants than the wild-type under the Fe excess (Aung et al., 2018b). Therefore, OsHRZ2, and probably OsHRZ1 as well, are at least partly involved in sensing excess Fe, and precise sensing of Fe status by these proteins is likely to be important for tolerance. Other components involved in sensing Fe status have been elucidated, such as the Fe-binding, graminaceous species-specific transcription factor iron deficiency-responsive elements factor 1 (IDEF1) (Kobayashi et al., 2007, 2012) and short peptides IRON MAN (IMA) that are ubiquitously found in flowering plant lineage (Grillet et al., 2018; Kobayashi, Nagano & Nishizawa, 2021). IDEF1 is classified into the ABI3/VP1 transcription factor family which binds to Fe2+ ion via its His-Asp repeats and Pro-rich regions (Kobayashi et al., 2012), and the overexpression of rice homologue (OsIDEF1) which leads to enhanced tolerance to Fe deficiency (Kobayashi et al., 2007). Overexpression of Fe deficiency-inducible IMA homologues in rice (OsIMA1/2) enhances the expression of many Fe deficiency-inducible Fe uptake-related genes in roots (Kobayashi et al., 2021). In Arabidopsis, IMA1-overexpression lines hyperaccumulate Fe and exhibit foliar necrotic symptoms under the standard Fe conditions, indicating Fe toxicity (Grillet et al., 2018). It remains to be clarified whether these Fe sensing mechanisms are functional under the Fe excess condition and linked with the tolerance in rice.
A recent GWAS based study on root shortening induced by excess Fe and a subsequent mutant study revealed that S-nitrosoglutathione reductase (GSNOR) is involved in sensing Fe status at the root tip (Li et al., 2019). GSNOR alleviates Fe-dependent production of nitric oxide and hydrogen peroxide, and resultant inhibition of root meristem growth. Naturally occurring polymorphism in the promoter region of GSNOR gene was associated with its expression level, and the allele of GSNOR that yielded higher expression conferred tolerance. Consistently, the knockout of rice homologues of GSNOR led to higher susceptibility to Fe excess, in terms of root elongation (Li et al., 2019). It remains to be determined if naturally occurring alleles of GSNOR in rice could be used to increase the tolerance of currently grown rice cultivars and enhance biomass production and grain yield.