The large ribosomal protein gene cluster of a cryptomonad plastid: Gene organization, sequence and evolutionary implications

Abstract

The complete sequence of the major ribosomal protein gene cluster of the plastid genome of the cryptomonad alga Guillardia theta (formerly Cryptomonas Φ) is presented. The ribosomal protein genes (corresponding to the SIO, spc, alpha and L13/S9 operons of E. coli are found upstream of the previously reported plastid str operon, and transcribed in the same orientation. The genes are very tightly packed with as little as two nucleotides between the rpll4 and rpl24 genes. The gene arrangement is very similar to that reported for the rhodophyte alga, Porphyra purpurea, and the chromophyte diatom, Odontella sinensis, indicating a close evolutionary relationship between these groups of algae. Northern analysis indicates that the 29 genes1 are arranged as one operon and are transcribed as a single mRNA that is subsequently processed into smaller transcripts.

The Origin of Red Algae and Cryptomonad Nucleomorphs: A Comparative Phylogeny Based on Small and Large Subunit rRNA Sequences ofPalmaria palmata, Gracilaria verrucosa,and theGuillardia thetaNucleomorph

“…Based on nucleomorph small subunit (SSU) rRNA data, Douglas et al (1991) suggested that cryptophyte plastids probably originate from a primitive red alga, as was confirmed in other SSU rRNA analyses (Maier et al, 1991;Cavalier-Smith et al, 1994;Ragan and Gutell, 1995;Van de Peer et al, 1996a). This agrees with studies based on sequences and organization of plastid genes, which indicate a relationship between rhodophyte and chromophyte plastids (Morden et al, 1992;Bhattacharya and Medlin, 1995;Van de Peer et al, 1996a;Wang et al, 1997). It is also consistent with the fact that starch is present in the cytoplasm of red algae as well as in the periplastid space of cryptomonads (McFadden, 1993).…”

The Plastid Genome of the Cryptophyte Alga, Guillardia theta: Complete Sequence and Conserved Synteny Groups Confirm Its Common Ancestry with Red Algae

“…There is considerable evidence for polycistronic transcription of genes for related functions, not only from the presence of gene clusters on plastid genomes, but also from transcription studies (Douglas and Murphy 1994;Löffelhardt et al 1997;Wang et al 1997). Putative promoters similar to the canonical prokaryotic-type promoter sequences have been reported upstream of many G. theta plastid genes (Douglas et al 1990;Douglas and Turner 1991;Douglas and Murphy 1994;Wang et al 1997) and inspection of sequences upstream of polycistronic transcripts known from cyanobacteria and other plastids (see Löffelhardt et al 1997) have revealed several more putative promoters.…”

“…However, problems encountered with substitutional bias caused by the relatively high A+T content of plastid genes (Lockhart et al 1992), as well as varying mutational rates of different plastid genes or different sites within genes (Van De Peer et al 1996) and the possibility of lateral gene transfers (Delwiche and Palmer 1996), have yielded conflicting results that may not reflect the true evolution of these lineages. Comparisons of gene order, on the other hand, offer a means of determining relationships among plastids that are not affected by these phenomena (Kowallik 1989(Kowallik , 1997Wang et al 1997).…”

“…Intergenic spacers are very short, no introns have been detected, and several genes overlap, all resulting in a very compact genome. In addition, large clusters of genes (such as those for the ribosomal proteins) are organized into single transcriptional units (Wang et al 1997), again resulting in an economically organized genome. The cryptophyte plastid genome is almost completely comprised of clusters of genes that are found on the rhodophyte Porphyra purpurea, confirming its common ancestry with red algae.…”

The Structure and Gene Repertoire of an Ancient Red Algal Plastid Genome

“…O. sinensis, a diatom, is derived from a secondary endosymbiosis event (Kowallik et al 1995;Wang et al 1997), which may have caused major changes in gene content and organization compared to other members of the red lineage. A comparison of these three genomes revealed that there exist large regions of conserved order (Douglas 1998).…”