The gene complement for proteolysis in the cyanobacterium Synechocystis sp. PCC 6803 and Arabidopsis thaliana chloroplasts

Abstract

A set of 62 genes that encode the entire peptidase complement of Synechocystis sp. PCC 6803 has been identified in the genome database of that cyanobacterium. Sequence comparisons with the Arabidopsis genome uncovered the presumably homologous chloroplast components inherited from their cyanobacterial ancestor. A systematic gene disruption approach was chosen to individually inactivate, by customary transformation strategies, the majority of the cyanobacterial genes encoding peptidase subunits that are related to chloroplast enzymes. This allowed classification of the peptidases that are required for cell viability or are involved in specific stress responses. The comparative analysis between Synechocystis and Arabidopsis chloroplast peptidases showed that: (1) homologous enzymes that arose by gene duplications in cyanobacteria are functionally diverse and frequently do not complement each other, (2) the chloroplast appears to house a number of distinct peptidase polypeptide chains of cyanobacterial origin (49) which is comparable with a cyanobacterial cell (62) and (3) the peptidase complement in plastids results from a combination of the loss of some cyanobacterial peptidases and the gain or diversification of subclasses of peptidases. This reorganization in the pattern of proteolytic enzymes may reflect distinct environmental and physiological changes between prokaryotic and organellar systems.

Coordinated Regulation and Complex Formation of YELLOW VARIEGATED1 and YELLOW VARIEGATED2, Chloroplastic FtsH Metalloproteases Involved in the Repair Cycle of Photosystem II in Arabidopsis Thylakoid Membranes

“…Later, the product of FtsH1 cDNA, when expressed as a soluble fusion protein, was shown to participate in vitro in the degradation of photodamaged D1 protein of the photosystem (PS) II reaction center (Lindahl et al, 2000). A notable observation is that, in contrast to other organisms such as yeast and humans, higher plants contain an extraordinary number of FtsH homologs (Adam et al, 2001;Ogura and Wilkinson, 2001;Sokolenko et al, 2002). This implies that a full understanding of FtsH func-tions in chloroplasts requires the consideration of gene redundancy.…”

“…Observations in unicellular organisms and higher plants indicate that protease activities are crucial for plastid viability and homeostasis (Adam, 2000;Adam and Clarke, 2002). Furthermore, various kinds of plastidic proteases have been identified by their homology with known prokaryotic proteases and by progress in genome projects (Adam et al, 2001;Sokolenko et al, 2002). However, their precise function in the degradation of specific chloroplast proteins remains poorly understood.…”

A single recessive mutation in the proteolytic machinery of Arabidopsis chloroplasts impairs photoprotection and photosynthesis upon cold stress

“…One possible explanation is that the products of other genes compensate for the affected one. This view is supported by the fact that known chloroplast proteases occur in plant genomes in multiple isomers: ClpC is encoded by two closely related genes, ClpP is found in six copies, FtsH appears to have 12 isomers and DegP has 14 Adam and Clarke 2002;Sokolenko et al 2002). How many of these are indeed found within chloroplasts is not yet clear.…”

Quality control of Photosystem II: The molecular basis for the action of FtsH protease and the dynamics of the thylakoid membranes

“…This bidirectionality in the processive digestion makes it possible for FtsH to promptly degrade unnecessary membrane proteins. FtsH genes exist not only in bacteria but also in photosynthetic organisms, such as cyanobacteria and higher plants [67][68][69]. An FtsH homolog in higher plants was first found by an immunological analysis with an antibody against E. coli FtsH protease, which was shown to cross-react with a protein in spinach thylakoid membranes [70].…”

“…PCC6803, where four genes slr1390, slr0228, slr1604 and sll1463 were found to be homologous to the bacterial FtsH (FtsH1, 2, 3 and 4) [45,69,72]. Of the four homologs, FtsH1 and 3 are required for cell viability while FtsH2 and 4 are not essential for the survival of the cyanobacterium [68,69]. Further studies, however, showed that a mutant lacking the FtsH2 is sensitive to light stress compared with the wild-type protein, and the photodamaged D1 protein was found to accumulate in the mutant thylakoids.…”