Mg-protoporphyrin IX and heme control HEMA, the gene encoding the first specific step of tetrapyrrole biosynthesis, in Chlamydomonas reinhardtii.

HEMA encodes glutamyl-tRNA reductase (GluTR), which catalyzes the first step specific for tetrapyrrole biosynthesis in plants, archaea, and most eubacteria. In higher plants, GluTR is feedback inhibited by heme and intermediates of chlorophyll biosynthesis. It plays a key role in controlling flux through the tetrapyrrole biosynthetic pathway. This enzyme, which in Chlamydomonas reinhardtii is encoded by a single gene (HEMA), exhibits homology to GluTRs of higher plants and cyanobacteria. HEMA mRNA accumulation was inducible not only by light but also by treatment of dark-adapted cells with Mg-protoporphyrin IX (MgProto) or hemin. The specificity of these tetrapyrroles as inducers was demonstrated by the absence of induction observed upon the feeding of protoporphyrin IX, the precursor of both heme and MgProto, or chlorophyllide. The HEMA mRNA accumulation following treatment of cells with light and hemin was accompanied by increased amounts of GluTR. However, the feeding of MgProto did not suggest a role for Mg-tetrapyrroles in posttranscriptional regulation. The induction by light but not that by the tetrapyrroles was prevented by inhibition of cytoplasmic protein synthesis. Since MgProto is synthesized exclusively in plastids and heme is synthesized in plastids and mitochondria, the data suggest a role of these compounds as organellar signals that control expression of the nuclear HEMA gene.

Involvement of tetrapyrroles in inter-organellar signaling in plants and algae.

For the assembly of a functional chloroplast, the coordinated expression of genes distributed between nucleus and chloroplasts is a prerequisite. While the nucleus plays an undisputed dominant role in controling biogenesis and functioning of chloroplasts, plastidic signals appear to control the expression of a subset of nuclear genes; the majority of which encodes chloroplast constituents. Tetrapyrrole biosynthesis intermediates are attractive candidates for one type of plastidic signal ever since an involvement of Mg-porphyrins in signaling from chloroplast to nucleus was first demonstrated in Chlamydomonas reinhardtii. Since then, Mg-protoporphyrin IX has been shown to exert a regulatory function on nuclear genes in higher plants as well. Here we review evidence for the role played by tetrapyrroles in inter-organellar communication. We also report on a screening for nuclear genes that may be subject to regulation by tetrapyrroles. This revealed that (i) >HEMA, the gene encoding the first enzyme specific for porphyrin biosynthesis is induced by Mg-protoporphyrin IX, (ii) several nuclear HSP70 genes are regulated by tetrapyrroles. Members of the gene family induced by the feeding of Mg-rotoporphyrin IX encode chaperones located in either the chloroplast or the cytosol. These results point to an important role of Mg-tetrapyrroles as plastidic signal in controling the initial step of porphyrin biosynthesis, and the synthesis of chaperones involved in protein folding in cytosol/stroma, protein transport into organelles, and the stress response.