Five genetic loci were identified in a genetic screen for mutants affected in chloroplast-to-nucleus signaling in Arabidopsis (Susek et al., 1993). Four of them are involved in the tetrapyrrole biosynthetic pathway: gun2 and gun3 in heme catabolism, gun4 and gun5 in chlorophyll synthesis (Larkin et al., 2003; Mochizuki et al., 2001; Susek et al., 1993). The GUN4 protein was previously uncharacterized. This protein binds protoporphyrin IX and Mg-protoporphyrin IX and facilitates the release of the product from the catalytic site of the ChlH subunit of the Mg-chelatase (Davison et al., 2005; Larkin et al., 2003; Verdecia et al., 2005).
We have identified and characterized a gun4 mutant of Chlamydomonas reinhardtii and shown that in the absence of the GUN4 protein, Chlamydomonas accumulates 50-60% of chlorophyll compared to wild type. This result was somehow surprising, given the fact that in Arabidopsis and Synechocystis the absence of GUN4 causes a drastic reduction in chlorophyll content, with a maximum accumulation of 25 % of the wild type measured in Synechocystis under dim light (Larkin et al., 2003; Peter and Grimm, 2009; Sobotka et al., 2008). In spite of the relatively high level of chlorophyll accumulation in the Chlamydomonas gun4 mutant, its photoautotrophic growth is severely impaired We have shown that under conditions in which the photoxidative damage is not severe (dim light) the mutant can grow, but at a rate which is significantly lower compared to the wild type. Analysis of the photosynthetic apparatus revealed that the antenna systems of PSII and PSI are reduced to 40% and 20% of wild type levels, respectively. Surprisingly the ratio of functional PSI over functional PSII is five fold
131 higher in gun4 than in the wild type, despite a greater reduction of the PSI antenna system compared to PSII. Indeed in the mutant, PSII appears to be disconnected from the photosynthetic electron transport chain as revealed by the measurement of the redox state of the reaction center of PSI (P700) in the presence or absence of DCMU. Treatment with DCMU does not affect the oxidation state of P700 in the mutant, whereas in the wild type it blocks the linear electron flow from PSII, thus causing an oxidation of the PSI reaction center. The impairment in linear electron flow may be responsible for the reduced photoautotrophic growth of the mutant. In fact the electrons pumped to the stromal side by PSI seem to be used to re-reduce the reaction center of PSI in the gun4 mutant. This would lead to a decreased availability of reducing power for the metabolic reactions in the chloroplast. Moreover, consequences of the reduced functionality of PSII are a reduction in the water splitting reaction and a more oxidized state of the PQ pool. These two events would lead to a decrease of the proton concentration in the lumen of the thylakoids and thus to a reduction in ATP synthesis. Taken together the reduction of ATP synthesis and of NADPH strongly supports the hypothesis that the photoautotrophic growth is reduced due to the block in photosynthetic linear electron flow.
As mentioned earlier, GUN4 was found in a genetic screen for mutants impaired in chloroplast retrograde signaling (Susek et al., 1993). We found an increase in the expression of LhcII-4 and Lhcb-4 genes compared to the wild type, but interestingly the mutant is still able to downregulate the expression of the two genes in high light. This result suggests that one retrograde signal is affected in the gun4 mutant, but another is still able to repress the expression of the photosynthetic genes upon light stress. In this respect, it is interesting to note that despite a drastic reduction in the antenna size of PSI, we have observed an increase in its activity compared to PSII. It is possible that a constant oxidized state of the PQ pool is interpreted by the cell as a signal to reduce the activity of PSI. This would be achieved in the long term by a reduction in the concentration of LHCI, the antenna system of PSI. The redox
132
state of the PQ pool, hence the photosynthetic activity, seems to be an important regulatory chloroplast-to-nucleus signal in the gun4 mutant in Chlamydomonas.
We are particularly interested in analyzing the in vivo functions of GUN4 not related to the reaction catalyzed by the Mg-chelatase. For this purpose, we prepared mutant versions of the protein with single amino acid substitutions. The mutations were designed on the basis of the analysis of the Synechocystis GUN4 published by Verdecia and colleagues (Verdecia et al., 2005). We examined mutations which affect porphyrin binding in vitro. This analysis revealed that some of these mutations do not have the same effect as GUN4 of Synechocystis. Similar differences have been obtained also by Adhikari and colleagues with the Arabidosis GUN4 (Adhikari et al., 2009) and can be explained assuming some diversity in the positioning of the amino acids in proteins from different species. Nevertheless, we are currently screening transformants for clones expressing other mutant versions of the Chlamydomonas protein and we hope that their analysis will help in understanding the role of GUN4 in photoprotection and in retrograde signaling.
133
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