Green Algal Models for Multicellularity

The repeated evolution of multicellularity across the tree of life has profoundly affected the ecology and evolution of nearly all life on Earth. Many of these origins were in different groups of photosynthetic eukaryotes, or algae. Here, we review the evolution and genetics of multicellularity in several groups of green algae, which include the closest relatives of land plants. These include millimeter-scale, motile spheroids of up to 50,000 cells in the volvocine algae; decimeter-scale seaweeds in the genus Ulva (sea lettuce); and very plantlike, meter-scale freshwater algae in the genus Chara (stoneworts). We also describe algae in the genus Caulerpa, which are giant, multinucleate, morphologically complex single cells. In each case, we review the life cycle, phylogeny, and genetics of traits relevant to the evolution of multicellularity, and genetic and genomic resources available for the group in question. Finally, we suggest routes toward developing these groups as model organisms for the evolution of multicellularity. Expected final online publication date for the Annual Review of Genetics, Volume 55 is November 2021. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

Phylotranscriptomics points to multiple independent origins of multicellularity and cellular differentiation in the volvocine algae

Background The volvocine algae, which include the single-celled species Chlamydomonas reinhardtii and the colonial species Volvox carteri, serve as a model in which to study the evolution of multicellularity and cellular differentiation. Studies reconstructing the history of this group have by and large relied on datasets of one to a few genes for phylogenetic inference and ancestral character state reconstruction. As a result, volvocine phylogenies lack concordance depending on the number and/or type of genes (i.e., chloroplast vs nuclear) chosen for phylogenetic inference. While multiple studies suggest that multicellularity evolved only once in the volvocine algae, that each of its three colonial families is monophyletic, and that there have been at least three independent origins of cellular differentiation in the group, other studies call into question one or more of these conclusions. An accurate assessment of the evolutionary history of the volvocine algae requires inference of a more robust phylogeny. Results We performed RNA sequencing (RNA-seq) on 55 strains representing 47 volvocine algal species and obtained similar data from curated databases on 13 additional strains. We then compiled a dataset consisting of transcripts for 40 single-copy, protein-coding, nuclear genes and subjected the predicted amino acid sequences of these genes to maximum likelihood, Bayesian inference, and coalescent-based analyses. These analyses show that multicellularity independently evolved at least twice in the volvocine algae and that the colonial family Goniaceae is not monophyletic. Our data further indicate that cellular differentiation arose independently at least four, and possibly as many as six times, within the volvocine algae. Conclusions Altogether, our results demonstrate that multicellularity and cellular differentiation are evolutionarily labile in the volvocine algae, affirming the importance of this group as a model system for the study of major transitions in the history of life.

Phylotranscriptomics points to multiple independent origins of multicellularity and cellular differentiation in the volvocine algae

The volvocine algae, which include the single-celled speciesChlamydomonas reinhardtiiand the colonial speciesVolvox carteri, serve as a model in which to study the evolution of multicellularity and cellular differentiation. Studies reconstructing the evolutionary history of this group have often relied on datasets of one to a few genes for phylogenetic inference and ancestral character state reconstruction. These studies suggest that multicellularity evolved only once in the volvocine algae, that each of its three colonial families is monophyletic, and that there have been at least three independent origins of cellular differentiation in the group. We performed RNA-Seq on 55 strains representing 47 volvocine algal species and obtained similar data from curated databases on 13 additional strains. We compiled a dataset consisting of transcripts for 40 single-copy, protein-coding, nuclear genes, then subjected the predicted amino acid sequences of these genes to maximum likelihood, Bayesian inference, and coalescent-based analyses. These analyses show that multicellularity independently evolved at least twice in the volvocine algae and that the colonial family Goniaceae is not monophyletic. Our data further indicate that cellular differentiation independently arose at least four and possibly as many as six times within the group. Altogether, these results show how multicellularity and cellular differentiation are evolutionarily labile in the volvocine algae, affirming their importance for the study of major transitions in the history of life.

Gene loss during the transition to multicellularity

SummaryMulticellular evolution is a major transition associated with momentous diversification of multiple lineages and increased developmental complexity. The volvocine algae comprise a valuable system for the study of this transition, as they span from unicellular to undifferentiated and differentiated multicellular morphologies despite their genomes being highly similar, suggesting multicellular evolution requires few genetic changes to undergo dramatic shifts in developmental complexity. Here, the evolutionary dynamics of five volvocine genomes were examined, where a gradual loss of genes was observed in parallel to the co-option of a few key genes. Protein complexes in the five species exhibited a high degree of novel interactions, suggesting that gene loss promotes evolutionary novelty. This finding was supported by gene network modeling, where gene loss outpaces gene gain in generating novel stable network states. These results suggest developmental complexity may be driven by gene loss rather than gene gain.

Comparative genomics of Chlamydomonas

Despite its fundamental role as a model organism in plant sciences, the green alga Chlamydomonas reinhardtii entirely lacks genomic resources for any closely related species, obstructing its development as a study system in several fields. We present highly contiguous and well-annotated genome assemblies for the two closest known relatives of the species, Chlamydomonas incerta and Chlamydomonas schloesseri, and a third more distantly related species, Edaphochlamys debaryana. We find the three Chlamydomonas genomes to be highly syntenous with similar gene contents, although the 129.2 Mb C. incerta and 130.2 Mb C. schloesseri assemblies are more repeat-rich than the 111.1 Mb C. reinhardtii genome. We identify the major centromeric repeat in C. reinhardtii as an L1 LINE transposable element homologous to Zepp (the centromeric repeat in Coccomyxa subellipsoidea) and infer that centromere locations and structure are likely conserved in C. incerta and C. schloesseri. We report extensive rearrangements, but limited gene turnover, between the minus mating-type loci of the Chlamydomonas species, potentially representing the early stages of mating-type haplotype reformation. We produce an 8-species whole-genome alignment of unicellular and multicellular volvocine algae and identify evolutionarily conserved elements in the C. reinhardtii genome. We find that short introns (<~100 bp) are extensively overlapped by conserved elements, and likely represent an important functional class of regulatory sequence in C. reinhardtii. In summary, these novel resources enable comparative genomics analyses to be performed for C. reinhardtii, significantly developing the analytical toolkit for this important model system.

Phylogenetic Analysis and Substitution Rate Estimation of Colonial Volvocine Algae Based on Mitochondrial Genomes

We sequenced the mitochondrial genome of six colonial volvocine algae, namely: Pandorina morum, Pandorina colemaniae, Volvulina compacta, Colemanosphaera angeleri, Colemanosphaera charkowiensi, and Yamagishiella unicocca. Previous studies have typically reconstructed the phylogenetic relationship between colonial volvocine algae based on chloroplast or nuclear genes. Here, we explore the validity of phylogenetic analysis based on mitochondrial protein-coding genes. We found phylogenetic incongruence of the genera Yamagishiella and Colemanosphaera. In Yamagishiella, the stochastic error and linkage group formed by the mitochondrial protein-coding genes prevent phylogenetic analyses from reflecting the true relationship. In Colemanosphaera, a different reconstruction approach revealed a different phylogenetic relationship. This incongruence may be because of the influence of biological factors, such as incomplete lineage sorting or horizontal gene transfer. We also analyzed the substitution rates in the mitochondrial and chloroplast genomes between colonial volvocine algae. Our results showed that all volvocine species showed significantly higher substitution rates for the mitochondrial genome compared with the chloroplast genome. The nonsynonymous substitution (dN)/synonymous substitution (dS) ratio is similar in the genomes of both organelles in most volvocine species, suggesting that the two counterparts are under a similar selection pressure. We also identified a few chloroplast protein-coding genes that showed high dN/dS ratios in some species, resulting in a significant dN/dS ratio difference between the mitochondrial and chloroplast genomes.

Problems of species and the features of geographical distribution in colonial volvocine algae (Chlorophyta)

More than ten new species of colonial volvocine algae were described in world literature during recent years. In present review, the published data on taxonomy, geographical distribution and the species problem in this group of algae, mainly from the genera Gonium, Pandorina, Eudorina, and Volvox, are critically discussed. There are both cosmopolitan volvocalean species and species with local or disjunct distribution. On the other hand, the description of new cryptic taxa in some genera of the colonial family Volvocaceae, such as Pandorina and Volvox, complicates the preparation of a comprehensive review on their geography.