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.
MeSH Terms
Cloning, Molecular
Evolution, Molecular
Gene Expression Regulation
Genes/genetics
Models, Genetic
Molecular Sequence Data
Phylogeny
Plant Proteins/genetics
Plastids/genetics
RNA, Messenger/analysis
Rhodophyta/genetics
SEC Translocation Channels
Sequence Analysis, DNA
Sequence Homology, Amino Acid
Chemicals
Plant Proteins
RNA, Messenger
SEC Translocation Channels
SecY protein, Cyanidium caldarium
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Vogel H
Institute for Plant Physiology, Justus-Liebig University, Giessen, Germany.
Fischer S
Valentin K
References (22)
22 references, click to expand
-
Unusual organization of a ribosomal protein operon in the plastid genome of Cryptomonas phi: evolutionary considerations.
Curr Genet. 1991 Apr;19(4):289-94
PMID: 1868578
-
Studies with Cyanidium caldarium, an anomalously pigmented chlorophyte.
Arch Mikrobiol. 1959;32(3):270-7
PMID: 13628094
-
SecA is plastid-encoded in a red alga: implications for the evolution of plastid genomes and the thylakoid protein import apparatus.
Mol Gen Genet. 1993 Jan;236(2-3):245-50
PMID: 8437571
-
A High-Resolution Gene Map of the Chloroplast Genome of the Red Alga Porphyra purpurea.
Plant Cell. 1993 Apr;5(4):465-475
PMID: 12271072
-
Identification of a chloroplast-encoded secA gene homologue in a chromophytic alga: possible role in chloroplast protein translocation.
Curr Genet. 1992 Nov;22(5):421-7
PMID: 1423730
-
The SecY protein family: comparative analysis and phylogenetic relationships.
Mol Phylogenet Evol. 1994 Sep;3(3):187-91
PMID: 7820283
-
Isolation and characterization of a cDNA encoding the SecA protein from spinach chloroplasts. Evidence for azide resistance of Sec-dependent protein translocation across thylakoid membranes in spinach.
J Biol Chem. 1995 Aug 4;270(31):18341-6
PMID: 7629156
-
The enzymology of protein translocation across the Escherichia coli plasma membrane.
Annu Rev Biochem. 1991;60:101-24
PMID: 1831965
-
The spc ribosomal protein operon of Escherichia coli: sequence and cotranscription of the ribosomal protein genes and a protein export gene.
Nucleic Acids Res. 1983 May 11;11(9):2599-616
PMID: 6222285
-
Rubisco genes indicate a close phylogenetic relation between the plastids of Chromophyta and Rhodophyta.
Plant Mol Biol. 1990 Oct;15(4):575-84
PMID: 2102375
-
Genetic analysis of protein export in Escherichia coli.
Annu Rev Genet. 1990;24:215-48
PMID: 2088168
-
Structure of the Rubisco operon from the unicellular red alga Cyanidium caldarium: evidence for a polyphyletic origin of the plastids.
Mol Gen Genet. 1990 Jul;222(2-3):425-30
PMID: 2274041
-
Cloning and characterization of the secY gene from the cyanobacterium Synechococcus PCC7942.
Biochim Biophys Acta. 1992 Nov 15;1171(1):113-6
PMID: 1420358
-
A secY homologue is found in the plastid genome of Cryptomonas phi.
FEBS Lett. 1992 Feb 17;298(1):93-6
PMID: 1544427
-
Identification of the SecA protein homolog in pea chloroplasts and its possible involvement in thylakoidal protein transport.
J Biol Chem. 1994 Dec 16;269(50):31338-41
PMID: 7989297
-
Characterisation of a chloroplast-encoded secY homologue and atpH from a chromophytic alga. Evidence for a novel chloroplast genome organisation.
FEBS Lett. 1992 Jun 15;304(2-3):119-23
PMID: 1618309
-
Characterization and mutagenesis of sulfur-regulated genes in a cyanobacterium: evidence for function in sulfate transport.
J Bacteriol. 1991 May;173(9):2739-50
PMID: 1708375
-
CLUSTAL V: improved software for multiple sequence alignment.
Comput Appl Biosci. 1992 Apr;8(2):189-91
PMID: 1591615
-
Biogenesis of prokaryotic pores.
Experientia. 1990 Feb 15;46(2):174-80
PMID: 1689256
-
SecA homolog in protein transport within chloroplasts: evidence for endosymbiont-derived sorting.
Science. 1994 Nov 4;266(5186):796-8
PMID: 7973633
-
SecY, an integral subunit of the bacterial preprotein translocase, is encoded by a plastid genome.
J Biol Chem. 1993 Apr 5;268(10 ):7514-9
PMID: 8463282
-
A SecY homolog in Arabidopsis thaliana. Sequence of a full-length cDNA clone and import of the precursor protein into chloroplasts.
J Biol Chem. 1995 Jul 28;270(30):17664-7
PMID: 7629062