Organellar phylogenomics inform systematics in the green algal family Hydrodictyaceae (Chlorophyceae) and provide clues to the complex evolutionary history of plastid genomes in the green algal tree of life

Abstract

PREMISE OF THE STUDY:Phylogenomic analyses across the green algae are resolving relationships at the class, order, and family levels and highlighting dynamic patterns of evolution in organellar genomes. Here we present a within-family phylogenomic study to resolve genera and species relationships in the family Hydrodictyaceae (Chlorophyceae), for which poor resolution in previous phylogenetic studies, along with divergent morphological traits, have precluded taxonomic revisions. METHODS:Complete plastome sequences and mitochondrial protein-coding gene sequences were acquired from representatives of the Hydrodictyaceae using next-generation sequencing methods. Plastomes were characterized, and gene order and content were compared with plastomes spanning the Sphaeropleales. Single-gene and concatenated-gene phylogenetic analyses of plastid and mitochondrial genes were performed. KEY RESULTS:The Hydrodictyaceae contain the largest sphaeroplealean plastomes thus far fully sequenced. Conservation of plastome gene order within Hydrodictyaceae is striking compared with more dynamic patterns revealed across Sphaeropleales. Phylogenetic analyses resolve Hydrodictyon sister to a monophyletic Pediastrum, though the morphologically distinct P. angulosum and P. duplex continue to be polyphyletic. Analyses of plastid data supported the neochloridacean genus Chlorotetraëdron as sister to Hydrodictyaceae, while conflicting signal was found in the mitochondrial data. CONCLUSIONS:A phylogenomic approach resolved within-family relationships not obtainable with previous phylogenetic analyses. Denser taxon sampling across Sphaeropleales is necessary to capture patterns in plastome evolution, and further taxa and studies are needed to fully resolve the sister lineage to Hydrodictyaceae and polyphyly of Pediastrum angulosum and P. duplex.

Order, please! Uncertainty in the ordinal-level classification of Chlorophyceae

“…S1–S5). Most recently this issue received extensive attention in McManus et al (2018), who expanded the taxon sampling in Hydrodictyaceae to 14 species in five genera, but still recovered conflicting relationships between Hydrodictyaceae and Neochloridaceae in different single-gene and concatenated analyses. Expanding the sampling of Neochloridaceae, especially to include the genus Tetraedron , is the next logical step in the effort to resolve this systematic problem.…”

“…Expanding the sampling of Neochloridaceae, especially to include the genus Tetraedron , is the next logical step in the effort to resolve this systematic problem. However, given the varying signal from individual chloroplast and mitochondrial genes reported in McManus et al (2018), it is possible that another confounding factor needs to be considered, such as horizontal gene transfer or insufficient model complexity in analyses. For the scope of our study, positioning of the two families is a minor issue, but the results of McManus et al (2018) exemplify that increased taxon sampling may not always be a sufficient solution to all phylogenetic conflict; adding species helped within Hydrodictyaceae but did nothing to resolve the relationships among closely related families.…”

“…In the last decade, chloroplast genome data have been used to recover robust phylogenies of green algae, leveraging the availability of 50+ genes evolving at a range of rates. The taxon sampling of chloroplast phylogenomic studies is also gradually improving, not only to include representatives of additional major lineages, but also strengthening the sampling within orders, families, and genera (e.g., Turmel et al, 2008; Lemieux, Otis & Turmel, 2014; Lemieux et al, 2015; Fučíková, Lewis & Lewis, 2016; McManus et al, 2018). Chloroplast genome-scale data thus appear particularly promising, as they balance a multi-gene approach with dense taxon representation, and especially as high-throughput sequencing becomes easier and more affordable, and bioinformatic tools for processing large data sets become more accessible.…”

Sequencing the Plastid Genome of Giant Ragweed (Ambrosia trifida, Asteraceae) From a Herbarium Specimen

“…Staats et al (2011) showed that it is also possible to use genome skimming to analyze DNA that is otherwise too degraded for PCR-based approaches, thus offering the possibility to include rare and extinct species from natural history collections in phylogenetic analyses. Several phylogenomic studies have explored the potential of herbarium specimens of different ages (Staats et al, 2013; Besnard et al, 2014; Aubriot et al, 2018; McManus et al, 2018; Zeng et al, 2018). For example, the entire nuclear genome of a 43-year-old Arabidopsis thaliana (L.) Heynh.…”

Using and navigating the plant tree of life

“…McManus et al. () used organellar phylogenomics to clarify relationships and identify conserved plastome gene order within the chlorophytic algal family Hydrodictyaceae, noting that this conservation contrasts with the dynamic plastome evolution characteristic of Sphaeropleales. Outside of Viridiplantae , Parks et al.…”