Abstract

Iron-sulfur (Fe-S) clusters are evolutionarily ancient ubiquitous protein cofactors which have mostly catalytic functions but can also have structural roles. In Arabidopsis thaliana, we presently know a total of 124 Fe-S metalloproteins that are encoded in the genome. Fe-S clusters are highly sensitive to oxidation. Therefore, we hypothesized that Fe-S cluster protein biogenesis is adjusted following the daily rhythms in metabolism driven by photosynthesis at the whole-plant, organ, cellular and sub-cellular levels. It had been concluded previously that little such regulation occurs at the transcript level among the genes functioning in Fe-S cluster assembly. As an initial step toward testing our hypothesis, we thus addressed the diel time course of the translation state of relevant transcripts based on publicly available genome-wide microarray data. This analysis can answer whether the translation of the pool of transcripts of a given gene is temporarily either enhanced or suppressed, and when during the day. Thirty-three percent of the transcripts with functions in Fe-S cluster assembly exhibited significant changes in translation state over a diurnal time course, compared to 26% of all detected transcripts. These transcripts comprised functions in all three steps of cluster assembly including persulfide formation, Fe-S cluster formation and Fe-S cluster transfer to target apoproteins. The number of Fe-S cluster carrier/transfer functions contributed more than half of these transcripts, which reached maxima in translation state either during the night or the end of the night. Similarly, translation state of mitochondrial frataxin and ferredoxin, which are thought to contribute Fe and electrons during cluster formation, peaked during the night. By contrast, translation state of chloroplast SUFE2 in persulfide formation and cytosolic Fe-S cluster formation scaffold protein NBP35 reached maxima in translation state during the day. Among the transcripts encoding target Fe-S cluster-utilizing proteins, 19% exhibited diurnal variation in translation state. Day-time maxima of translation state were most common among these transcripts, with none of the maxima during the night (ZT18). We conclude that diurnal regulation of translation state is important in metalloprotein biogenesis. Future models of Fe-S protein biogenesis require more comprehensive data and will have to accommodate diurnal dynamics.

Highlights

  • Across all groups of biological organisms, proteins that can bind one or several iron-sulfur (Fe-S) cluster cofactors in vivo (Fe-S proteins) fulfill central cellular biochemical functions

  • Fe-S cluster assembly Fe-S cluster use All functions aTranscript levels detected as present in all ribosome-associated fractions at all four time points (Missra et al, 2015). bNumber counts for transcripts exhibiting significant diurnal variation in translation state (TL) according to Missra et al (2015)

  • 13 transcripts encode Fe-S cluster-utilizing proteins (Figure 3B) and 10 transcripts encode Fe-S proteins that are involved in cluster assembly and Fe-S protein biogenesis (Figure 3A)

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Summary

Introduction

Across all groups of biological organisms, proteins that can bind one or several iron-sulfur (Fe-S) cluster cofactors in vivo (Fe-S proteins) fulfill central cellular biochemical functions. Several types exist of protein-bound Fe-S clusters, based on chemical structures and oxidation states. Cubane [4Fe–4S] and rhombic [2Fe–2S] are the most widespread Fe– S clusters, containing ferrous or ferric Fe( + II) or (+III) and sulfide S(−II) (Lill, 2009; Balk and Schaedler, 2014). Disruption of Fe-S protein biogenesis has been associated with serious diseases in human and animals (Lill, 2009; Wachnowsky et al, 2017). Frataxin is thought to function as the iron donor for the mitochondrial Isu scaffold protein complex in Fe-S cluster assembly in human. Depletion of frataxin causes the neurodegenerative disease Friedreich’s ataxia, attributed to defective Fe–S protein activity and iron accumulation (Campuzano et al, 1996; Rötig et al, 1997)

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