Transcriptional integration of the responses to iron availability in Arabidopsis by the bHLH factor ILR3

Abstract

Summary Iron (Fe) homeostasis is crucial for all living organisms. In mammals, an integrated posttranscriptional mechanism couples the regulation of both Fe deficiency and Fe excess responses. Whether in plants an integrated control mechanism involving common players regulates responses both to deficiency and to excess is still to be determined. In this study, molecular, genetic and biochemical approaches were used to investigate transcriptional responses to both Fe deficiency and excess. A transcriptional activator of responses to Fe shortage in Arabidopsis, called bHLH105/ILR3, was found to also negatively regulate the expression of ferritin genes, which are markers of the plant's response to Fe excess. Further investigations revealed that ILR3 repressed the expression of several structural genes that function in the control of Fe homeostasis. ILR3 interacts directly with the promoter of its target genes, and repressive activity was conferred by its dimerisation with bHLH47/PYE. Last, this study highlighted that important facets of plant growth in response to Fe deficiency or excess rely on ILR3 activity. Altogether, the data presented herein support that ILR3 is at the centre of the transcriptional regulatory network that controls Fe homeostasis in Arabidopsis, in which it acts as both transcriptional activator and repressor.

Iron acquisition strategies in land plants: not so different after all

“…AtIMA3 has the longest Asp stretch of all the eight Arabidopsis genes (6xAsp), suggesting that it is also the closest to the ancestral gene. Interestingly, in Arabidopsis IMA target genes include bHLH105 (ILR3)‐regulated genes (Tissot et al ., ), suggesting that the molecular mechanism of IMAs is related to the post‐transcriptional regulation of group IVc bHLH proteins.…”

Oryza sativa POSITIVE REGULATOR OF IRON DEFICIENCY RESPONSE 2 (OsPRI2) and OsPRI3 are involved in the maintenance of Fe homeostasis

“…Moreover, POPEYE (PYE) maintains Fe homeostasis by negatively regulating the expression of the Fe homeostasis genes ZIF1 , FRO3 , and NAS4 (Long et al, ). bHLH105/ILR3 was recently demonstrated to act as a negative regulator of Fe homeostasis by the interaction with PYE (Gao, Robe, Gaymard, Izquierdo, & Dubos, ; Tissot et al, ) Additionally, bHLH38/39/100/101 and PYE expression levels are upregulated by Fe‐deficiency (Long et al, ; Wang et al, ) in a process that depends on the upstream positive regulators bHLH34/104/105/115 (Li et al, ; Liang et al, ; Zhang et al, ). Fe deficiency responsive signaling is similar across non‐graminaceous plants, including soybean, tomato and apple (Li et al, ; Ling, Bauer, Bereczky, Keller, & Ganal, ; Zhao, Ren, Wang, Wang, et al, ; Zhao, Ren, Wang, Yao, et al, ).…”

bHLH11 inhibits bHLH IVc proteins by recruiting the TOPLESS/TOPLESS-RELATED corepressors in Arabidopsis

“…PYE and bHLH11 are negative regulators of Fe homeostasis (Long et al 2010; Tanabe et al 2019). bHLH105/ILR3 also functions as a negative regulator when it interacts with PYE (Tissot et al 2019). In contrast, bHLH121 is required for activation of numerous Fe deficiency responsive genes (Kim et al 2019; Gao et al 2020; Lei et al 2020).…”

“…In contrast, bHLH121 is required for activation of numerous Fe deficiency responsive genes (Kim et al 2019; Gao et al 2020; Lei et al 2020). Moreover, both bHLH 121 and PYE interact with bHLH IVc to regulate Fe homeostasis in Arabidopisis (Long et al 2010; Selote et al 2015; Kim et al 2019; Tissot et al 2019; Gao et al 2020; Lei et al 2020). There is also a similar Fe deficiency response signaling network in rice (Ogo et al 2007; Kobayashi 2013, 2019; Zhang et al 2017, 2020; Wang et al 2020; Li et al 2020).…”