Abstract
Plastids possess a bacteria-like sec apparatus that is involved in protein import into the thylakoid lumen. We have analyzed one of the genes essential for this process, secY. A secY gene from the unicellular red alga Cyanidium caldarium was found to be transcriptionally active, demonstrating for the first time that secY is functional in a plastid. Unlike the situation seen in bacteria the C. caldarium gene is transcribed monocistronically, despite the fact that it is part of a large ribosomal gene cluster that resembles bacterial spc operons. A molecular phylogeny is presented for 8 plastid-encoded secY genes, four of which have not been published yet. In this analysis plastid secY genes fall into two classes. One of these, comprising of genes from multicellular red algae and Cryptophyta, clusters in a neighbour-joining tree with a cyanobacterial counterpart. Separated from the aforesaid are secY genes from Chromophyta, Glaucocystophyta and a unicellular red alga. All plastid and cyanobacterial sequences are located on the same branch, separated from bacterial homologues. We postulate that the two classes of secY genes are paralogous, i.e. their gene products are involved in different protein translocation processes. Based on this assumption a model for the evolution of the plastid sec apparatus is presented.
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References
Allen MB: Studies with Cyanidium caldarium, an anomalously pigmented chlorophyte. Arch Mikrobiol 32: 270–277 (1959).
Berghofer J, Karnauchov I, Herrmann RG, Klösgen RB: Isolation and characterization of a CDNA encoding the SecA protein from spinach chloroplasts. Evidence for azide resistance of secdependent protein translocation across thylakoid membranes in spinach. J Biol Chem 270: 18341–18346 (1995).
Ceretti DP, Dean D, Davis GR, Bedwell DM, Nomura M: The spc ribosomal protein operon of Escherichia coli: Sequence and cotranscripion of the ribosomal protein genes and a protein export gene. Nucl Acids Res 11: 2599–2616 (1983).
Davis LC, Dibner MD, Battey JF: Basic Methods in Molecular Biology. Elsevier Science Publishers, Amsterdam (1986).
Douglas SE: Unusual organization of a ribosomal protein operon in the plastid genome of Cryptomonas Φ. Curr Genet, 19: 289–294 (1991).
Douglas SE: A secY homologue is found in the plastid genome of Cryptomonas Φ. FEBS Lett 298: 93–96 (1992).
Higgins DG, Bleasby AJ, Fuchs R: CLUSTAL V: improved software for multiple sequence alignments. Comp Anal Biol Sci (CABIOS) 8: 189–191 (1992).
Flachmann R, Michalowski CB, Löffelhardt W, Bohnert HJ: Sec Y, an integral subunit of the bacterial preprotein translocase, is encoded by a plastid genome. J Biol Chem 268: 7514–7519 (1993).
Laidler V, Chaddock AM, Knott TG, Walker D, Robinson C: A secY homolog in Arabidopsis thaliana. Sequence of a full-length cDNA clone and import of the precursor protein into chloroplasts. J Biol Chem 270: 17664–17667 (1995).
Laudenbach DE, Grossmann AR: Characterization of sulfurregulated genes in a Cyanobacterium: evidence for function in sulfate transport. J Bact 173: 2739–2750 (1991).
Merola A, Astaldo R, Deluca P, Gombarella R, Musaccio A, Taddei R: Revision of Cyanidium caldarium. Three species of acidophilic algae. Giorn Bot Ital 115: 189–195 (1981).
Nakai M, Tanaka A, Omata T, Endo T: Cloning and characterization of the secY gene from the cyanobacterium Synechococcus PCC7942. Biochim Biophys Acta 1171: 113–116 (1992).
Nakai M, Goto A, Nohara T, Sugita D, Endo T: Identification of the SecA protein homolog in pea chloroplasts and its possible involvement in thylakoid protein transport. J Biol Chem 269: 31338–31341 (1994).
Nikaido H, Reid J: Biogenesis of procaryotic pores. Experientia 46: 174–180 (1990).
Ohyama K, Fukuzawa H, Kochi T, Shirai H, Sano T, Sano S, Umesono K, Shiki Y, Takeushi M, Chang Z, Aota SI, Inokuchi H, Ozeki H: Chloroplast gene organization deduced from the complete sequence of liverworth Marchantia polymorpha chloroplast DNA. Nature 322: 572–574 (1985).
Reith M, Munholland J: A high-resolution gene map of the chloroplast genome of the red alga Porphyra umbilicalis. Plant Cell 5: 465–475 (1994).
Rensing SA, Maier UG: The secY protein family: comparative analysis and phylogenetic relationships. Mol Phylogen Evol 3: 187–191 (1994).
Sambrook J, Fritsch EF, Maniatis T: Molecular Cloning: A Laboratory Manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY (1989).
Scaramuzzi CD, Stokes HW, Hiller RG: Characterization of a chloroplast-encoded secY homologue and atpH homologue from a chromophytic alga: evidence for a novel chloroplast genome organization. FEBS Lett 304: 119–123 (1992).
Scaramuzzi CD, Hiller RG, Stokes HW: Identification of a chloroplast-encoded secA homologue in a chromophytic alga: possible role in chloroplast protein translocation. Curr Genet 22: 421–427 (1992).
Schatz PJ, Beckwith J: Genetic analysis of protein export in Escherichia coli. Annu Rev Genet 24: 215–248 (1990).
Valentin K, Zetsche K: Structure of the Rubisco operon from the unicellular red alga Cyanidium caldarium: evidence for a polyphyletic origin of the plastids. Mol Gen Genet 222: 425–439 (1990).
Valentin K, Zetsche K: Rubisco genes indicate a close phylogenetic relation between the plastids of Chromophyta and Rhodophyta. Plant Mol Biol 15: 575–584 (1990).
Valentin K, Cattolico RA, Zetsche K: Phylogenetic origin of the plastids. In: Lewin RA (ed), Origins of Plastids, pp. 193–221. Chapman and Hall, New York/London (1992).
Valentin K: SecA is plastid-encoded in a red alga: implications for the evolution of plastid genomes and the thylakoid protein import apparatus. Mol Gen Genet 236: 245–250 (1993).
Wickner W, Driessen AJM, Hartl FU: The enzymology of protein translocation across the Escherichia coli plasma membrane. Annu Rev Biochem 60: 101–124 (1991).
Yuan J, Henry R, McCaffery M, Cline K: SecA homolog in protein transport within chloroplasts: evidence for endosymbiont-derived sorting. Science 266: 796–298 (1994).
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Vogel, H., Fischer, S. & Valentin, K. A model for the evolution of the plastid sec apparatus inferred from secY gene phylogeny. Plant Mol Biol 32, 685–692 (1996). https://doi.org/10.1007/BF00020209
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DOI: https://doi.org/10.1007/BF00020209