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

Abstract

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.

Mg-Protoporphyrin IX and Heme ControlHEMA, the Gene Encoding the First Specific Step of Tetrapyrrole Biosynthesis, inChlamydomonas reinhardtii

“…These two tetrapyrroles, whose synthesis is assumed to take place in plastids (MgProto) and in plastids as well as mitochondria (heme), are proposed to act as organellar signals in controlling HEMA expression. This gene, whose product catalyzes the first and rate-limiting step of the pathway, thus occupies a special position, since none of the other tetrapyrrole biosynthesis genes tested were found to be regulated by MgProto (54) or heme (Z. Vasileuskaya and C. F. Beck, unpublished data).…”

“…2B). We have shown previously that Mg-porphyrins may regulate the expression of nuclear genes in C. reinhardtii (24,54). Here we first analyzed the effect of a feeding of MgProto to cells kept in the dark.…”

Defects in the Cytochrome b6/f Complex Prevent Light-Induced Expression of Nuclear Genes Involved in Chlorophyll Biosynthesis

“…The light-mediated activation of HEMA1 and, to a minor degree that of GSA, was impaired by chloroplast-damaging treatments such as the application of the phytoene desaturase-inhibitor norflurazon, by far-red light pretreatment, or by inhibitors of plastid protein synthesis (Kumar et al, 1996;McCormac and Terry, 2004). In contrast, the C. reinhardtii HEMA gene is induced by the feeding of MgProtoporphyrin IX (Vasileuskaya et al, 2005), which also activates expression of three nuclear HSP70 genes (Kropat et al, 1997;Vasileuskaya et al, 2004). It could be hypothesized that lack of light induction in cytb 6 /f mutants is related to a defect in the accumulation of Mg-protoporphyrin IX, or its release from the chloroplast.…”

“…A number of Chlamydomonas reinhardtii genes involved in chlorophyll biosynthesis (HEMA, GSA, ALAD, CPXI, CHLD, CHLH1, CHLI1, and CTH1) have been shown to be induced in dark-adapted cultures by a shift from dark to light of a moderate fluence rate (40 mEÁm 22 Ás 21 ; Vasileuskaya et al, 2004). The expression of five of these nuclear genes was analyzed at the RNA level in those mutants that either lacked the cytb 6 /f complex or possessed strongly reduced levels.…”

Implication of chlorophyll biosynthesis on chloroplast-to-nucleus retrograde signaling

“…HEMA gene and genes encoding HSP70 proteins were also induced in Chlamydomonas after treatment with MgProto and MgProtoMe in darkness. 13,14 The Arabidopsis genome contains several HSP70 genes encoding cytoplasmic HSP70 proteins, but it is intriguing to note that the upregulated genes in ntrc (At3g12580 and At3g09440) encode cytoplasmic proteins that are the closest homologues to the single cytoplasmic HSP70A gene in Chlamydomonas. 21 (iv) The pale green ntrc leaves have higher number of cells per area than wild type Arabidopsis and significantly reduced cell size with low number of chloroplasts, 17 suggesting that the plastidial and nuclear divisions are uncoupled in ntrc plants.…”