Thompson, Elinor Patsy; (2003) Proteins involved in the maintenance of the photosynthetic apparatus in cyanobacteria and plants. Doctoral thesis (Ph.D), UCL (University College London).

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Abstract

Plant and algal chloroplasts evolved following symbiosis of a cyanobacterium-like photosynthetic prokaryote with the eukaryotic host. Although most genes have been transferred from the organelle genome to the nucleus the function of plastid proteins is often retained. It can be helpful therefore to complement the study of a plant gene by examining its role in a cyanobacterium or vice versa. Two genes were investigated in this way. First was the predicted product of open-reading frame (ORF) slr0575 in Synechocystis sp. PCC 6803, a possible equivalent to the Arabidopsis thaliana protein Ape-1 (At5g38660). Similar genes are conserved in various photosynthetic organisms, suggestive of a continued function. ape-1 mutant plants have deficient regulation of light harvesting and therefore the role of slr0575 deletion mutants was explored under different light conditions. Although an equivalent role was not identified in the cyanobacterium, there is evidence that the response to high light is perturbed in a Synechocystis insertional inactivation mutant of slr0575. Second, a family of ATP-dependent metalloproteases encoded within the genomes of both Synechogstis and A. thaliana was investigated. The nucleic acid sequences for these are similar to the Escherichia coli ftsH but inactivation of homologous genes in the plant and cyanobacterium showed that they have important roles in photosynthesis. Using a chlorophyll biosynthesis double-mutant and light- or nutrient-deprivation experiments, the effect of inactivating ftsH genes on the turnover and assembly of the photosynthetic apparatus was monitored. This work showed that in Synechocystis, the product of the ORF slr0228 is needed in order to degrade photosystem II (PSII) not only after light-induced damage, as previously suggested, but under non-photoinhibitory conditions. Assays of dark-grown heterotrophic cells suggested that the PSII composition of cyanobacterial thylakoid membranes is regulated when photosynthesis is prevented, in the absence of light, and that the slr0228-encoded FtsH is vital for that PSII turnover process. Likewise, in Arabidopsis, the Var2 FtsH is necessary for turnover of PSII D1 protein damaged by high light, and it may also have a role in the turnover of the photosynthetic apparatus during senescence. Preliminary studies showed that Var2-2 mutant seedlings allowed to partially senesce were unable to remove PSII, much of their response to dark conditions being quite different to that of Co10 wild-type (WT) seedlings. The effect of inactivating these FtsH proteins extends to photosystem I (PSI). The accumulation of PSI and pigments in slr0228- Synechocystis after degradation of the photosynthetic apparatus was delayed, with a lag phase of 1-3 days compared with regreening WT. The function of slr0228 in PSI assembly may also involve trimer formation: cultures of slr0228- cells in trimer-favouring light conditions grow very poorly and lose PSI and chlorophyll. Unlike slr0228- Synechocystis, var2- A. thaliana is not deficient in PSI but a delay in the return of pigment after etiolation requires more study. The role of these proteins in the maintenance of the photosynthetic apparatus was established and appears to be conserved, in general, between the plant and cyanobacterium. Secondary effects of mutation upon carotenoid and fatty acid content in both A. thaliana and Synechocystis were also evident, suggesting that the numerous roles of proteases and chaperones in photosynthesis merit further investigation.

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