Abstract
BackgroundBecause they represent the earliest divergences of the Chlorophyta, the morphologically diverse unicellular green algae making up the prasinophytes hold the key to understanding the nature of the first viridiplants and the evolutionary patterns that accompanied the radiation of chlorophytes. Nuclear-encoded 18S rDNA phylogenies unveiled nine prasinophyte clades (clades I through IX) but their branching order is still uncertain. We present here the newly sequenced chloroplast genomes of Nephroselmis astigmatica (clade III) and of five picoplanktonic species from clade VI (Prasinococcus sp. CCMP 1194, Prasinophyceae sp. MBIC 106222 and Prasinoderma coloniale) and clade VII (Picocystis salinarum and Prasinophyceae sp. CCMP 1205). These chloroplast DNAs (cpDNAs) were compared with those of the six previously sampled prasinophytes (clades I, II, III and V) in order to gain information both on the relationships among prasinophyte lineages and on chloroplast genome evolution.ResultsVarying from 64.3 to 85.6 kb in size and encoding 100 to 115 conserved genes, the cpDNAs of the newly investigated picoplanktonic species are substantially smaller than those observed for larger-size prasinophytes, are economically packed and contain a reduced gene content. Although the Nephroselmis and Picocystis cpDNAs feature a large inverted repeat encoding the rRNA operon, gene partitioning among the single copy regions is remarkably different. Unexpectedly, we found that all three species from clade VI (Prasinococcales) harbor chloroplast genes not previously documented for chlorophytes (ndhJ, rbcR, rpl21, rps15, rps16 and ycf66) and that Picocystis contains a trans-spliced group II intron. The phylogenies inferred from cpDNA-encoded proteins are essentially congruent with 18S rDNA trees, resolving with robust support all six examined prasinophyte lineages, with the exception of the Pycnococcaceae.ConclusionsOur results underscore the high variability in genome architecture among prasinophyte lineages, highlighting the strong pressure to maintain a small and compact chloroplast genome in picoplanktonic species. The unique set of six chloroplast genes found in the Prasinococcales supports the ancestral status of this lineage within the prasinophytes. The widely diverging traits uncovered for the clade-VII members (Picocystis and Prasinophyceae sp. CCMP 1205) are consistent with their resolution as separate lineages in the chloroplast phylogeny.
Highlights
Because they represent the earliest divergences of the Chlorophyta, the morphologically diverse unicellular green algae making up the prasinophytes hold the key to understanding the nature of the first viridiplants and the evolutionary patterns that accompanied the radiation of chlorophytes
Pairwise genome comparisons revealed that numerous genes form conserved clusters (Figures 1, 2 and 3), gene order is substantially scrambled in all three sampled lineages and multiple ancestral clusters are disrupted in clades VI and VII (Figure 5)
They are congruent with the branching order of prasinophyte lineages in nuclear-encoded small subunit (SSU) rDNA trees, even though the two clade-VII members analyzed, Picocystis and Prasinophyceae sp
Summary
Because they represent the earliest divergences of the Chlorophyta, the morphologically diverse unicellular green algae making up the prasinophytes hold the key to understanding the nature of the first viridiplants and the evolutionary patterns that accompanied the radiation of chlorophytes. Sister to the Chlorophyta is the Streptophyta, which comprises freshwater green algae, the so-called charophytes, and all their land plant relatives Given their basal positions, prasinophytes hold the key to understanding the nature of the last common ancestor of all green plants and the origin of the core chlorophytes (i.e. the Pedinophyceae, Chlorodendrophyceae, Trebouxiophyceae, Ulvophyceae and Chlorophyceae). Prasinophytes exhibit considerable diversity with respect to cell shape and size, flagella number and behavior, mitotic and cytokinetic mechanisms, and biochemical features such as accessory pigments and storage products [2,5,6,7,8] They include the smallest free-living eukaryote known to date (Ostreococcus tauri with an average size of 0.8 μm [9,10]). Others lack scales, and in some cases, both flagella and scales are absent (e.g., Ostreococcus)
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