Abstract
BackgroundHeterokont algae, together with cryptophytes, haptophytes and some alveolates, possess red-algal derived plastids. The chromalveolate hypothesis proposes that the red-algal derived plastids of all four groups have a monophyletic origin resulting from a single secondary endosymbiotic event. However, due to incongruence between nuclear and plastid phylogenies, this controversial hypothesis remains under debate. Large-scale genomic analyses have shown to be a powerful tool for phylogenetic reconstruction but insufficient sequence data have been available for red-algal derived plastid genomes.ResultsThe chloroplast genomes of two brown algae, Ectocarpus siliculosus and Fucus vesiculosus, have been fully sequenced. These species represent two distinct orders of the Phaeophyceae, which is a major group within the heterokont lineage. The sizes of the circular plastid genomes are 139,954 and 124,986 base pairs, respectively, the size difference being due principally to the presence of longer inverted repeat and intergenic regions in E. siliculosus. Gene contents of the two plastids are similar with 139-148 protein-coding genes, 28-31 tRNA genes, and 3 ribosomal RNA genes. The two genomes also exhibit very similar rearrangements compared to other sequenced plastid genomes. The tRNA-Leu gene of E. siliculosus lacks an intron, in contrast to the F. vesiculosus and other heterokont plastid homologues, suggesting its recent loss in the Ectocarpales. Most of the brown algal plastid genes are shared with other red-algal derived plastid genomes, but a few are absent from raphidophyte or diatom plastid genomes. One of these regions is most similar to an apicomplexan nuclear sequence. The phylogenetic relationship between heterokonts, cryptophytes and haptophytes (collectively referred to as chromists) plastids was investigated using several datasets of concatenated proteins from two cyanobacterial genomes and 18 plastid genomes, including most of the available red algal and chromist plastid genomes.ConclusionThe phylogenetic studies using concatenated plastid proteins still do not resolve the question of the monophyly of all chromist plastids. However, these results support both the monophyly of heterokont plastids and that of cryptophyte and haptophyte plastids, in agreement with nuclear phylogenies.
Highlights
Heterokont algae, together with cryptophytes, haptophytes and some alveolates, possess red-algal derived plastids
Structure and gene content of the phaeophyte plastid genomes The plastid genomes of E. siliculosus and F. vesiculosus are 139,954 and 124,986 base pairs in size, respectively, and both contain two inverted repeat regions (IR)
These IRs divide the circular molecules into large (LSC) and small single copy (SSC) regions (Figure 1 and see general features of the two plastid genomes in additional file 1, Table S1)
Summary
Heterokont algae, together with cryptophytes, haptophytes and some alveolates, possess red-algal derived plastids. Chlorophyll c-containing plastids have been shown to be derived from an ancestral red alga via a secondary endosymbiotic process that took place around one billion years ago [11,12] This type of plastid is found in Cryptophyta, Haptophyta, Heterokonta ( called stramenopiles) and Dinophyceae algae [3,4]. During diversification of the four extant chromalveolates lineages, photosynthetic capacity and/or the plastid organelle would have been independently lost several times in different eukaryotic lineages, such as oomycetes (non-photosynthetic heterokonts), apicomplexa or ciliates (non-photosynthetic alveolates) According to this so-called "chromalveolate" hypothesis, plastid and nuclear genomes have similar evolutionary histories and one would expect monophyly of chromalveolate lineages in both nuclear and plastid phylogenies. This hypothesis has been extensively debated over the last ten years (for recent references, [5,6,15,16,17]), in part because of incongruence between plastid and nuclear phylogenies [9]
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