Evolution and Cytological Diversification of the Green Seaweeds (Ulvophyceae)

Abstract

The Ulvophyceae, one of the four classes of the Chlorophyta, is of particular evolutionary interest because it features an unrivaled morphological and cytological diversity. Morphological types range from unicells and simple multicellular filaments to sheet-like and complex corticated thalli. Cytological layouts range from typical small cells containing a single nucleus and chloroplast to giant cells containing millions of nuclei and chloroplasts. In order to understand the evolution of these morphological and cytological types, the present paper aims to assess whether the Ulvophyceae are monophyletic and elucidate the ancient relationships among its orders. Our approach consists of phylogenetic analyses (maximum likelihood and Bayesian inference) of seven nuclear genes, small subunit nuclear ribosomal DNA and two plastid markers with carefully chosen partitioning strategies, and models of sequence evolution. We introduce a procedure for fast site removal (site stripping) targeted at improving phylogenetic signal in a particular epoch of interest and evaluate the specificity of fast site removal to retain signal about ancient relationships. From our phylogenetic analyses, we conclude that the ancestral ulvophyte likely was a unicellular uninucleate organism and that macroscopic growth was achieved independently in various lineages involving radically different mechanisms: either by evolving multicellularity with coupled mitosis and cytokinesis (Ulvales-Ulotrichales and Trentepohliales), by obtaining a multinucleate siphonocladous organization where every nucleus provides for its own cytoplasmic domain (Cladophorales and Blastophysa), or by developing a siphonous organization characterized by either one macronucleus or millions of small nuclei and cytoplasmic streaming (Bryopsidales and Dasycladales). We compare different evolutionary scenarios giving rise to siphonous and siphonocladous cytologies and argue that these did not necessarily evolve from a multicellular or even multinucleate state but instead could have evolved independently from a unicellular ancestor.

New phylogenetic hypotheses for the core Chlorophyta based on chloroplast sequence data

“…The increase in support observed in our genome-scale analysis (compared to the 7-and 8-gene analyses) suggests that sequencing additional chloroplast genomes would be a reasonable strategy (Figures 2-4). Considering the discordance between our results and those of the nuclear gene-analyses of Cocquyt et al (2010), complementing this chloroplast-based approach with transcriptome sequencing to obtain nuclear gene data would be a useful exercise. There is a possibility that the organellar phylogeny is legitimately discordant with the nuclear phylogeny, although introgression at such a high taxonomic level would be extraordinary.…”

“…To date, systematic studies have often focused on within-class relationships, ignoring the possibility that lineages from other classes may be interspersed between their focal taxa (Cocquyt et al, 2010;Neustupa et al, 2013a,b;Fučíková et al, 2014b). This limited focus is in part due to the very different nature of the groups-Trebouxiophyceae are mostly terrestrial unicells and Ulvophyceae are mostly marine seaweeds-with each requiring different sampling and culturing procedures not commonly found within individual research groups.…”

“…The first was Cocquyt et al (2010), which focused mainly on relationships within Ulvophyceae and used a similar site-removal approach to phylogenetic inference as the present study. In addition to a very different gene selection (2 plastid genes, 18S, and 7 nuclear protein-coding genes), differences in taxon sampling is a plausible explanation for the contradicting findings, as Cocquyt et al (2010) only included Chlorellales (here shown to form a separate clade from the remaining trebouxiophytes) to represent Trebouxiophyceae and did not include either of the genera identified as most problematic in our study: Choricystis and Oltmannsiellopsis. The second notable case is Ruhfel et al (2014), which focused primarily on land plants and used a genome-scale chloroplast data set to infer the phylogeny of Viridiplantae.…”

“…Most single and multigene phylogenies have provided weak or no support for monophyly of the class, but have instead supported two clades: one containing Oltmannsiellopsidales, Ulvales and Ulotrichales, the other consisting of Trentepohliales, Bryopsidales, Dasycladales and Cladophorales (e.g., Watanabe and Nakayama, 2007;Cocquyt et al, 2009;Lü et al, 2011). The earliest study providing stronger support for a monophyletic Ulvophyceae was based on phylogenetic analysis of eight nuclear and two plastid genes (Cocquyt et al, 2010). Analyses of these data also resulted in good resolution and support for most nodes in the phylogeny of the class.…”

Green Algae and the Origins of Multicellularity in the Plant Kingdom

“…Moreover, some green algae are both multicellular and coenocytic (termed siphonocladous) because they are composed of multiple cells, each of which contains multiple nuclei (e.g., Cladophora). Cytoplasmic continuity and developmental patterning in coenocytic macroscopic algae are beyond the scope of this review, but are covered in other recent reviews (Baluška et al 2004;Cocquyt et al 2010;.…”