A new paper by Shota Yamashita and colleagues explores the genetic basis for soma in one of the most mysterious volvocine algae, Astrephomene gubernaculifera. By combining whole genome sequencing with cell-type specific transcriptomics, they have shown that the gene or genes controlling germ/soma differentiation in Astrephomene are different from those in Volvox carteri, but the resulting cell-type specific differences in gene expression are similar between the two.
Astrephomene represents one of several independent origins of somatic cells within the volvocine algae:
The only species for which the genetic basis of soma is well understood is Volvox carteri, and one of the biggest open questions about the volvocine algae is the degree to which that genetic basis is similar across the other origins of soma, including that of Astrephomene. Zach Grochau-Wright and colleagues previously showed that transcription factor genes in the reg cluster, one of which controls somatic differentiation in Volvox carteri, are present in other species in the family Volvocaceae, including some that do not have somatic cells. However, that alone doesn’t tell us if those genes are actually involved in soma determination in, for example, Volvox globator and Pleodorina starrii.
In the new paper, Yamashita and colleagues sequenced the genome of Astrephomene gubernaculifera and analyzed patterns of gene expression between somatic cells and reproductive cells. They found that the Astrephomene genome does not contain reg-cluster genes at all. However, they did find that three other transcription factors were overexpressed in somatic cells compared to reproductive cells. Furthermore, the differences in gene expression between somatic and reproductive cells that they found in Astrephomene are similar to those that Gavriel Matt and Jim Umen found in Volvox carteri:
Among the genes involved in motility, many of the genes encoding flagella components belonged to somatic genes…The most obvious difference in gene expression in A. gubernaculifera between somatic and reproductive cells was observed in photosynthetic genes. Almost all of the genes encoding core subunits of photosynthetic complexes on the thylakoid membranes exhibited higher expression in reproductive cells…
Among carbon metabolism genes, almost all genes in the Calvin-Benson–Bassham cycle were reproductive genes in A. gubernaculifera. Moreover, more than half of fatty acid biosynthesis genes and half of amino acid biosynthesis genes were reproductive genes. These anabolic pathways were also upregulated in gonidia of V. carteri. In addition, genes involved in acetate metabolism were reproductive in A. gubernaculifera…In A. gubernaculifera, genes involved in both metabolic pathways, including enzymes for acetyl-CoA synthesis from acetate (ACK2, PAT1, and ACS1 for TCA cycle, ACS2 and ACS3 for glyoxylate cycle) and downstream TCA and glyoxylate cycles, were mainly upregulated in reproductive cells. By contrast, glyoxylate cycle genes, along with upstream fatty acid degradation, are upregulated in the somatic cells of V. carteri.
Somatic genes and reproductive genes, in this context, are shorthand for genes significantly upregulated in one cell type relative to the other.
So what does all of this mean? It means that the mechanism of somatic cell determination is similar between Astrephomene and Volvox carteri at the level of gene expression, but it differs in the particular gene(s) that cause cell-type specific gene expression. Furthermore, the soma-specific three transcription factors the authors identified are candidates for controlling these differences.
There is still much to be done before we have a complete picture of the evolution of soma in the volvocine algae. For example, confirming that one or more of the soma-specific transcription factors identified by Yamashita et al. actually control somatic differentiation in Astrephomene will likely require a forward genetics approach; there is no bioinformatic shortcut for this. And that will still leave identifying the genetic bases for soma in the other Volvox and Pleodorina lineages. The new paper by Yamashita and colleagues is a big step in the right direction.