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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.

SUBMITTER: Jackson C

PROVIDER: S-EPMC5784168 | biostudies-literature | 2018 Jan

REPOSITORIES: biostudies-literature

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

Jackson Christopher C Knoll Andrew H AH Chan Cheong Xin CX Verbruggen Heroen H

Scientific reports 20180124 1

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. ...[more]

PMID: 29367699

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Project description:BACKGROUND:Heterokont 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. RESULTS:The 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. CONCLUSION:The 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.

Project description:Background and aimsPhylogenetic relationships within tribe Shoreeae, containing the main elements of tropical forests in Southeast Asia, present a long-standing problem in the systematics of Dipterocarpaceae. Sequencing whole plastomes using next-generation sequencing- (NGS) based genome skimming is increasingly employed for investigating phylogenetic relationships of plants. Here, the usefulness of complete plastid genome sequences in resolving phylogenetic relationships within Shoreeae is evaluated.MethodsA pipeline to obtain alignments of whole plastid genome sequences across individuals with different amounts of available data is presented. In total, 48 individuals, representing 37 species and four genera of the ecologically and economically important tribe Shoreeae sensu Ashton, were investigated. Phylogenetic trees were reconstructed using maximum parsimony, maximum likelihood and Bayesian inference.Key resultsHere, the first fully sequenced plastid genomes for the tribe Shoreeae are presented. Their size, GC content and gene order are comparable with those of other members of Malvales. Phylogenomic analyses demonstrate that whole plastid genomes are useful for inferring phylogenetic relationships among genera and groups of Shorea (Shoreeae) but fail to provide well-supported phylogenetic relationships among some of the most closely related species. Discordance in placement of Parashorea was observed between phylogenetic trees obtained from plastome analyses and those obtained from nuclear single nucleotide polymorphism (SNP) data sets identified in restriction-site associated sequencing (RADseq).ConclusionsPhylogenomic analyses of the entire plastid genomes are useful for inferring phylogenetic relationships at lower taxonomic levels, but are not sufficient for detailed phylogenetic reconstructions of closely related species groups in Shoreeae. Discordance in placement of Parashorea was further investigated for evidence of ancient hybridization.

Dataset Information

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

Publications

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

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