Distinctive architecture of the chloroplast genome in the chlorophycean green alga Stigeoclonium helveticum
The chloroplast genome has experienced many architectural changes during the evolution of chlorophyte green algae, with the class Chlorophyceae displaying the lowest degree of ancestral traits. We have previously shown that the completely sequenced chloroplast DNAs (cpDNAs) of Chamydomonas reinhardtii (Chlamydomonadales) and Scenedesmus obliquus (Sphaeropleales) are highly scrambled in gene order relative to one another. Here, we report the complete cpDNA sequence of Stigeoclonium helveticum (Chaetophorales), a member of a third chlorophycean lineage. This genome, which encodes 97 genes and contains 21 introns (including four putatively trans-spliced group II introns inserted at novel sites), is remarkably rich in derived features and extremely rearranged relative to its chlorophycean counterparts. At 223,902 bp, Stigeoclonium cpDNA is the largest chloroplast genome sequenced thus far, and in contrast to those of Chlamydomonas and Scenedesmus, features no large inverted repeat. Interestingly, the pattern of gene distribution between the DNA strands and the bias in base composition along each strand suggest that the Stigeoclonium genome replicates bidirectionally from a single origin. Unlike most known trans-spliced group II introns, those of Stigeoclonium exhibit breaks in domains I and II. By placing our comparative genome analyses in a phylogenetic framework, we inferred an evolutionary scenario of the mutational events that led to changes in genome architecture in the Chlorophyceae.
KeywordsChlorophyta Plastid genome evolution Gene order Origin of replication Group II introns Repeated sequences
We thank Jean-François Pombert and Jean-Charles de Cambiaire for their help with the sequence analyses and for critical reading of the manuscript. This work was supported by a grant from the Natural Sciences and Engineering Research Council of Canada (to C.L. and M.T.).
- Friedl T (1997) The evolution of the green algae. Plant Syst Evol 11(Suppl):87–101Google Scholar
- Heinhorst S, Cannon GC (1993) DNA replication in chloroplasts. J Cell Sci 104:1–9Google Scholar
- Kunnimalaiyaan M, Nielsen BL (1997) Chloroplast DNA replication: mechanism, enzymes and replication origins. J Plant Biochem Biotechnol 6:1–7Google Scholar
- Mattox KR, Stewart KD (1984) Classification of the green algae: a concept based on comparative cytology. In: Irvine DEG, John DM (eds) The systematics of the green algae. Academic, London, pp 29–72Google Scholar
- Palmer JD (1991) Plastid chromosomes: structure and evolution. In: Bogorad L, Vasil I (eds) The molecular biology of plastids. Cell culture and somatic cell genetics of plants. Academic, San Diego, pp 5–53Google Scholar
- Pombert JF, Otis C, Lemieux C, Turmel M (2004) The complete mitochondrial DNA sequence of the green alga Pseudendoclonium akinetum (Ulvophyceae) highlights distinctive evolutionary trends in the Chlorophyta and suggests a sister-group relationship between the Ulvophyceae and Chlorophyceae. Mol Biol Evol 21:922–935PubMedCrossRefGoogle Scholar
- Turmel M, Otis C, Lemieux C (2002) The chloroplast and mitochondrial genome sequences of the charophyte Chaetosphaeridium globosum: insights into the timing of the events that restructured organelle DNAs within the green algal lineage that led to land plants. Proc Natl Acad Sci USA 99:11275–11280PubMedCrossRefGoogle Scholar
- Volfovsky N, Haas BJ, Salzberg SL (2001) A clustering method for repeat analysis in DNA sequences. Genome Biol 2:Research0027Google Scholar
- Wakasugi T, Nagai T, Kapoor M, Sugita M, Ito M, Ito S, Tsudzuki J, Nakashima K, Tsudzuki T, Suzuki Y, Hamada A, Ohta T, Inamura A, Yoshinaga K, Sugiura M (1997) Complete nucleotide sequence of the chloroplast genome from the green alga Chlorella vulgaris: the existence of genes possibly involved in chloroplast division. Proc Natl Acad Sci USA 94:5967–5972PubMedCrossRefGoogle Scholar