Diurnal Dynamics in the Biogenesis of Iron-Sulfur Cluster and other Metalloproteins of Plants in Dependence on Cluster Assembly

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The genome of the genetic model plant Arabidopsis thaliana encodes more than 100 proteins that require iron-sulfur (FeS) cluster cofactors for their biological function, for example in photosynthesis, respiration and nucleic acid metabolism. Plants possess three cellular pathways of FeS cluster assembly in chloroplasts, mitochondria and the cytosol, respectively. As sessile organisms, they must efficiently protect the biogenesis of FeS proteins under fluctuating and non-optimal environmental conditions, for example in the presence of reactive oxygen species or an excess of interfering metals. To examine how this is accomplished, we analyze the diurnal dynamics in the biogenesis of FeS-dependent and other metalloproteins in different cellular compartments by using genome-wide translatome sequencing (ribo-seq) as a proxy. This is combined with an analysis of the diurnal dynamics of metal and low-molecular-weight chelator concentrations, sub-cellular metal distribution and enzyme activities of major molybdenum cofactor(Moco-) and FeS-dependent proteins. We compare wild-type plants with plants exhibiting defects in each of the three FeS cluster assembly pathways to reveal a possible dependence on, and regulatory roles of, subcellular FeS cluster assembly for metal homeostasis and metalloprotein biosynthesis. Our results can serve as a basis for future strategies to optimize bioenergy production and agricultural fertilization schemes.