Arabidopsis genomes uncoupled 5 ( GUN5 ) mutant reveals the involvement of Mg-chelatase H subunit in plastid-to-nucleus signal transduction

Abstract

A plastid-derived signal plays an important role in the coordinated expression of both nuclear-and chloroplast-localized genes that encode photosynthesis-related proteins. Arabidopsis GUN (genomes uncoupled) loci have been identified as components of plastid-to-nucleus signal transduction. Unlike wild-type plants, gun mutants have nuclear Lhcb1 expression in the absence of chloroplast development. We observed a synergistic phenotype in some gun double-mutant combinations, suggesting there are at least two independent pathways in plastid-to-nucleus signal transduction. There is a reduction of chlorophyll accumulation in gun4 and gun5 mutant plants, and a gun4gun5 double mutant shows an albino phenotype. We cloned the GUN5 gene, which encodes the ChlH subunit of Mg-chelatase. We also show that gun2 and gun3 are alleles of the known photomorphogenic mutants, hy1 and hy2, which are required for phytochromobilin synthesis from heme. These findings suggest that certain perturbations of the tetrapyrrole biosynthetic pathway generate a signal from chloroplasts that causes transcriptional repression of nuclear genes encoding plastid-localized proteins. The comparison of mutant phenotypes of gun5 and another Mg-chelatase subunit (ChlI) mutant suggests a specific function for ChlH protein in the plastid-signaling pathway.A number of components required for plastid structure and development are encoded by the nuclear genome. There is a considerable body of evidence that suggests that the proper and timely expression of these genes depends in part on the functional state of the chloroplast. For example, nuclear mutations that result in developmentally arrested chloroplasts also result in the reduced expression of nuclear-localized photosynthetic genes (1). These results tie the functional state of the chloroplast to nuclear function and suggest that the chloroplast signals the nucleus in a retrograde fashion (2).Such retrograde signaling between chloroplast and nucleus has been studied primarily by using carotenoid-deficient plants induced either by mutations or by carotenoid biosynthesis inhibitors such as Norflurazon (Nf; refs. 3 and 4). Carotenoids prevent the production of reactive oxygen species by excited triplet states of chlorophyll. Carotenoid-deficient plants thus suffer a rapid photooxidation of most chloroplast components under intense light. Although most nuclear-encoded cytoplasmic enzymes are present at normal levels in photooxidatively damaged plants, a small set of nuclear-encoded chloroplast enzymes is absent (3, 4). Accordingly, it was hypothesized that plastids send an unknown signal(s) to the nucleus that regulates the expression of a small subset of nuclear-localized photosynthetic genes (2, 5).The molecular nature of the plastid signal(s) and the mechanism by which it is relayed to the nucleus remain ambiguous. Although both plastid transcription and translation are necessary for the production of the plastid signal (4, 6), the plastid signal is not a direct translational product of a plastid gene. Lig...

Plastid Proteome Assembly without Toc159: Photosynthetic Protein Import and Accumulation of N-Acetylated Plastid Precursor Proteins

“…The assembly and maintenance of the chloroplast proteome are highly regulated processes and involve not only the organellar import machinery but also multiple anterograde and retrograde signaling events that affect the transcription of nuclear-and chloroplast-encoded genes (Mochizuki et al, 2001(Mochizuki et al, , 2008Strand et al, 2003;Larkin et al, 2003;Koussevitzky et al, 2007;Moulin et al, 2008;Kakizaki et al, 2009). Similar transcript patterns observed under different environmental conditions or genetic modifications identified key regulators that affect entire sets of plastid proteins and biochemical networks (Richly et al, 2003;Biehl et al, 2005).…”

Genomics-based dissection of the cross-talk of chloroplasts with the nucleus and mitochondria in Arabidopsis

“…In Chlamydomonas, intermediates in the chlorophyll biosynthetic pathway modulate the accumulation of transcripts of several nuclear chloroplast genes (Johanningmeier and Howell, 1984;Kropat et al, 1997). Arabidopsis mutants that do not react to norflurazoninduced photo-oxidative damage by repression of Lhcb transcription (genomes uncoupled 1 -5: gun1 -5) were affected in genes encoding proteins involved in tetrapyrrole metabolism: the products of GUN2/HY1 and GUN3/HY2 contribute to heme degradation in the ''Fe branch'' of tetrapyrrole biosynthesis (Mochizuki et al, 2001), GUN5 encodes the CHL H subunit of the Mg-chelatase (Mochizuki et al, 2001), and GUN4 binds product and substrate of Mgchelatase, and activates Mg-chelatase (Larkin et al, 2003).…”

“…GUN5 was originally suggested to act as a sensor (Mochizuki et al, 2001), but the idea was recently revised in favour of the tetrapyrrole intermediate Mg-protoporphyrin IX, a proposed signalling molecule between chloroplast and nucleus (Strand et al, 2003; Fig. 1).…”

Oxygen Deficiency Responsive Gene Expression in Chlamydomonas reinhardtii through a Copper-Sensing Signal Transduction Pathway

“…The modulation of cofactor biosynthetic pathways through changes in Cpx1 and Crd1 expression might also serve to signal oxygen status to the nucleus. This is precedented by the heme-dependent O 2 -sensing system in S. cerevisiae (Zhang and Hach, 1999) and by the Mg-protoporphyrin IX-dependent plastid-to-nucleus signaling system in C. reinhardtii and plants (Kropat et al, 1997;Mochizuki et al, 2001).…”