Abstract
BackgroundPlastid replacements through secondary endosymbioses include massive transfer of genes from the endosymbiont to the host nucleus and require a new targeting system to enable transport of the plastid-targeted proteins across 3-4 plastid membranes. The dinoflagellates are the only eukaryotic lineage that has been shown to have undergone several plastid replacement events, and this group is thus highly relevant for studying the processes involved in plastid evolution. In this study, we analyzed the phylogenetic origin and N-terminal extensions of plastid-targeted proteins from Lepidodinium chlorophorum, a member of the only dinoflagellate genus that harbors a green secondary plastid rather than the red algal-derived, peridinin-containing plastid usually found in photosynthetic dinoflagellates.ResultsWe sequenced 4,746 randomly picked clones from a L. chlorophorum cDNA library. 22 of the assembled genes were identified as genes encoding proteins functioning in plastids. Some of these were of green algal origin. This confirms that genes have been transferred from the plastid to the host nucleus of L. chlorophorum and indicates that the plastid is fully integrated as an organelle in the host. Other nuclear-encoded plastid-targeted protein genes, however, are clearly not of green algal origin, but have been derived from a number of different algal groups, including dinoflagellates, streptophytes, heterokonts, and red algae. The characteristics of N-terminal plastid-targeting peptides of all of these genes are substantially different from those found in peridinin-containing dinoflagellates and green algae.ConclusionsL. chlorophorum expresses plastid-targeted proteins with a range of different origins, which probably arose through endosymbiotic gene transfer (EGT) and horizontal gene transfer (HGT). The N-terminal extension of the genes is different from the extensions found in green alga and other dinoflagellates (peridinin- and haptophyte plastids). These modifications have likely enabled the mosaic proteome of L. chlorophorum.
Highlights
Plastid replacements through secondary endosymbioses include massive transfer of genes from the endosymbiont to the host nucleus and require a new targeting system to enable transport of the plastid-targeted proteins across 3-4 plastid membranes
The exact number of secondary endosymbiotic events involving red algae remains controversial [8,9,10,11,12], with theories ranging from a single uptake in the common ancestor of all algal lineages harboring secondary plastids derived from a red alga to serial independent uptakes of red algal plastids or transfer of red algaderived plastids between algal groups [4,8,13,14]
L. chlorophorum contains a true plastid with a phylogenetically hybrid plastid proteome The genus Lepidodinium is the only known dinoflagellate lineage that possesses a secondary plastid of green algal origin rather than the red algal derived peridinincontaining plastid found in most photosynthetic dinoflagellates [22,23,24,37]
Summary
Plastid replacements through secondary endosymbioses include massive transfer of genes from the endosymbiont to the host nucleus and require a new targeting system to enable transport of the plastid-targeted proteins across 3-4 plastid membranes. We analyzed the phylogenetic origin and N-terminal extensions of plastid-targeted proteins from Lepidodinium chlorophorum, a member of the only dinoflagellate genus that harbors a green secondary plastid rather than the red algal-derived, peridinin-containing plastid usually found in photosynthetic dinoflagellates. An ancient primary endosymbiosis gave rise to photosynthethic organelles in members of the Viridiplantae, rhodophytes (red algae) and glaucophytes [1,2,3,4,5] Such primary plastids (bound by two membranes) were subsequently spread to other protist lineages through a series of eukaryote-eukaryote secondary and. Green plastids of secondary origin are known to be found in three distinct algal lineages: the chlorarachniophytes, the photosynthetic euglenids and in the dinoflagellate genus Lepidodinium. The distant evolutionary relationships between the chlorarachniophyte, euglenid and dinoflagellate host lineages indicate that their plastids originate from three distinct endoymbiotic events [7,18,25,26]
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