Transcriptional integration of plant responses to iron availability

Abstract

Iron is one of the most important micronutrient for plant growth and development. It functions as the enzyme cofactor or component of electron transport chains in various vital metabolic processes, including photosynthesis, respiration and amino acid biosynthesis. For maintaining iron homeostasis, and therefore preventing any deficiency or excess that could be detrimental, plants have evolved complex transcriptional regulatory networks to tightly control iron uptake, translocation, assimilation and storage. Such regulatory networks are composed of various transcription factors among them members from the basic helix-loop-helix (bHLH) family play an essential role. Here, we first review recent advances in understanding the roles of bHLH transcription factors involved in the regulatory cascade controlling iron homeostasis in the model plant Arabidopsis, extending it to rice and other plant species. The importance of other classes of transcription factors will also be discussed. Secondly, we elaborate on the posttranslational mechanisms involved in the regulation of these regulatory networks. Finally, we give some perspectives on future research that should be conducted in order to precisely depict how plants control the homeostasis of this micronutrient.

Basic Helix-Loop-Helix (bHLH) Transcription Factors Regulate a Wide Range of Functions in Arabidopsis

“…In the case of FIT, its function is required to regulate Fe uptake responses; bHLH47 (POPEYE, PYE) is another bHLH transcription factor that plays a major role in the Fe homeostasis. PYE interacts with bHLH104, bHLH105 and bHLH115 to bind to the promoters of several Fe response genes and repress their activity [60][61][62]123]. Interestingly, the bHLH104, bHLH105 and bHLH115 protein levels are posttranslationally controlled by BRUTUS (BTS), a hemerythrin E3 ligase, via the proteosomal degradation to negatively regulate the bHLH protein stability [61,124].…”

IRONMAN Tunes Responses to Iron Deficiency in Concert with Environmental pH

“…In Arabidopsis, all Fe deficiency responses are regulated by a complex cascade of regulatory processes that orchestrate a subtle balance of promotive and repressive trans -acting factors in concert with post-translational control of central regulatory nodes (Rodrígues-Celma et al, 2019; Schwarz and Bauer, 2020; Spielmann and Vert, 2020; Gao and Dubos, 2020). Overexpression of IMA1-IMA3 was shown to induce large parts of the Fe deficiency response in Arabidopsis (Grillet et al, 2018; Hirayama et al, 2018; this study), but the exact position of IMA peptides in the regulatory network governing cellular Fe homeostasis has not yet been defined.…”

The iron will of the research community: advances in iron nutrition and interactions in lockdown times

“…The main actors belong to the basic helix–loop–helix (bHLH) family of transcription factors, a gene family that has been exploited by plants to the full to regulate different processes, not just iron. Interestingly, in the last 2–3 years, a coherent framework is emerging that is central to orchestrating the transcriptional iron deficiency response in both dicot and monocot plants, as detailed in two of the reviews published in this issue ( Gao and Dubos, 2021 ; Riaz and Guerinot, 2021 ). The bHLH transcription factors not only regulate each other’s transcriptional activity but also integrate other signals.…”

“…On the other hand, very little is known about evolutionary differences in the mechanisms of iron acquisition and homeostasis in the green lineage. In this respect, a lot is to be learned from iron homeostasis mechanisms in algae, which have to deal with constantly changing environmental conditions and extreme fluctuations in the abundance of iron ( Gao et al , 2021 ).…”