Plastid phylogenomics with broad taxon sampling further elucidates the distinct evolutionary origins and timing of secondary green plastids

Abstract

Secondary plastids derived from green algae occur in chlorarachniophytes, photosynthetic euglenophytes, and the dinoflagellate genus Lepidodinium. Recent advances in understanding the origin of these plastids have been made, but analyses suffer from relatively sparse taxon sampling within the green algal groups to which they are related. In this study we aim to derive new insights into the identity of the plastid donors, and when in geological time the independent endosymbiosis events occurred. We use newly sequenced green algal chloroplast genomes from carefully chosen lineages potentially related to chlorarachniophyte and Lepidodinium plastids, combined with recently published chloroplast genomes, to present taxon-rich phylogenetic analyses to further pinpoint plastid origins. We integrate phylogenies with fossil information and relaxed molecular clock analyses. Our results indicate that the chlorarachniophyte plastid may originate from a precusor of siphonous green algae or a closely related lineage, whereas the Lepidodinium plastid originated from a pedinophyte. The euglenophyte plastid putatively originated from a lineage of prasinophytes within the order Pyramimonadales. Our molecular clock analyses narrow in on the likely timing of the secondary endosymbiosis events, suggesting that the event leading to Lepidodinium likely occurred more recently than those leading to the chlorarachniophyte and photosynthetic euglenophyte lineages.

Figure 1

RAxML phylogenetic analysis inferred from an amino acid alignment of 64 plastid genes from streptophytes, green algae, photosynthetic euglenophytes, the “green” dinoflagellate Lepidodinium chlorophorum, and chlorarachniophytes. The dataset was partitioned by gene according to the best-fit model assigned by PartitionFinder. Thick branches have full ML bootstrap support. Coloured vertical bars to the right of the phylogeny are labelled: S, Streptophytes; P, prasinophytes; CC, core Chlorophyta. Branch lengths are proportional to the number of substitution per site.

Figure 2

Chronogram of streptophytes, green algae, photosynthetic euglenophytes, the “green” dinoflagellate Lepidodinium chlorophorum, and chlorarachniophytes. Node ages were inferred using Bayesian inference assuming a relaxed molecular clock and a set of node age constraints derived from the fossil record as well as node age estimates from previous studies (see Supporting Information File 1). Values at nodes indicate average node ages and grey bars at selected nodes represent 95% confidence intervals. Coloured vertical bars to the right of the phylogeny are labelled: S, Streptophyta; P, prasinophytes; CC, core Chlorophyta. “S/C split” = divergence of the Streptophyta and Chlorophyta. “CC split” = divergence of the prasinophytes and core Chlorophyta. Timeline abbreviations: Camb., Cambrian; Ord., Ordovician; Sil., Silurian; Dev., Devonian; Carb., Carboniferous; Perm., Permian; Tri., Triassic; Jur., Jurassic.