More evidence for co-option in the evolution of soma

One of the reasons Volvox was developed as a model organism was that it has the minimum number of cell types something with cellular differentiation can have: two. This property focuses investigations of cellular differentiation in a way that an organism with many cell types could not. In describing their move from studying avian and mammalian models to studying Volvox, Marilyn and David Kirk said,

The thing that appealed to us most about V. carteri – in addition to the genetic accessibility that Starr (1970) had already demonstrated – was the fact that it presented the germ-soma dichotomy in such a clear and simple form. Each asexual adult (or “spheroid”) of V. carteri contains only two cell types: small, biflagellate somatic cells, and large asexual reproductive cells, called gonidia (figure 1). The somatic cells are mortal; once they have provided the organism with motility for a few days they die. The gonidia, in contrast, are potentially immortal; each mature gonidium acts as a stem cell, dividing to produce a juvenile organism containing a new cohort of gonidia and somatic cells. No one has ever found a way to make wild-type somatic cells divide, but the only way to prevent gonidia from dividing is by withholding energy or poisoning them. Who could ask for a clearer presentation of one of the central issues of developmental biology: how are cells with extremely different phenotypes produced from the progeny of a single cell?

Kirk & Kirk 2004 Fig. 1

Figure 1 from Kirk & Kirk 2004. A young adult spheroid of V. carteri consists of thousands of small, biflagellate somatic cells that are embedded at the surface of a transparent sphere of extracellular matrix, and about 16 large asexual reproductive cells, called gonidia, that are located just internal to the somatic cells.

In Volvox carteri, somatic cell determination is controlled by regA, a transcription factor that expressed in small cells and suppresses genes involved in chloroplast biogenesis. regA is part of a cluster of genes generated by gene duplication, the reg cluster.

Although regA is present in several distantly related species of Volvox (Volvox is polyphyletic), it is absent from unicellular Chlamydomonas and the simple, undifferentiated colonies of Gonium. What’s not known is whether the reg clusters in various Volvox species descend from a single duplication event near the base of the volvocine tree or from independent duplication events in different lineages. A recent paper from Zach Grochau-Wright and colleagues addresses this question.

By sequencing reg genes from a variety of volvocine species, Grochau-Wright and colleagues were able to reconstruct the evolutionary history of this cluster of genes. They chose a handful of species representing the major branches of the volvocine phylogeny and representing different grades of organization:

Figure 1 from Grochau-Wright et al. 2017. Species phylogeny and micrographs of exemplar species of volvocine algae. (a) Bayesian species tree, consistent with previously published species trees. Colour of species without (Chlamydomonas reinhardtii, red; Gonium pectorale, orange) and with the reg cluster (undifferentiated Pandorina morum, Platydorina caudata, Yamagishiella unicocca and Eudorina elegans UTEX 1212, green; soma-differentiated Pleodorina californica, blue) corresponds to other figures, Volvox (germ- and soma-differentiated) species for which the reg cluster has been previously sequenced are shown in black, and species in grey are not included in this analysis. Inferred origin of the reg cluster is denoted. See Fig. 5 for maximum-likelihood and Bayesian support values. (b) C. reinhardtii (scale bar, 10 μm); (c) G. pectorale (10μm); (d) Pla. caudata (25 μm); (e) V. ferrisii (50 μm); (f) Pan. morum (10 μm); (g) Y. unicocca (20 μm); (h) E. elegans UTEX 1212 (10 μm); (i) V. carteri f. nagariensis (50 μm); (j) Ple. californica (25 μm).

The reg cluster was found in all examined species of the family Volvocaceae, including those without cellular differentiation (see Fig. 1A above). Furthermore, the order of the genes within the cluster was the same for all of these species. The most likely explanation for these observations is that the reg cluster was present in the most recent common ancestor of the Volvocaceae. It could have been even earlier; since Astrephomene (a genus with soma and sister to Gonium) was not included in this study, it’s possible that the reg cluster was present in the ancestor of the Volvocaceae and Goniaceae and lost from Gonium. Either way, though, the ancestor in which the reg cluster originated was almost certainly undifferentiated, indicating that the full complement of reg genes was present before cellular differentiation. Whatever the reg genes were doing in this undifferentiated ancestor, they (or at least regA) were co-opted for their role in determining somatic cell fate.

One thing that would help to make sense of these results would be to find out whether or not reg genes are actually involved in cellular differentiation across its various origins. The role of regA in determining somatic cell fate is beyond question in Volvox carteri, but only in Volvox carteri. Since cellular differentiation has evolved several times in the volvocine algae, it remains possible that the genetic basis of this differentiation is completely different in the other species. It’s a sign of the rapid advances in DNA sequencing technology that we now know much more about what genes are present in these other species than we do about the functions of their genes.


Stable links:

Grochau-Wright Z. I., E. R. Hanschen, P. J. Ferris, T. Hamaji, H. Nozaki, B. J. S. C. Olson, R. E. Michod. Genetic basis for soma is present in undifferentiated volvocine green algae. Journal of Evolutionary Biology 30: 1205-1218. doi: 10.1111/jeb.13100.

Kirk, M.M. and Kirk, D.L. 2004. Exploring germ-soma differentiation in Volvox. J. Biosci., 29: 143–152. doi: 10.1007/BF02703412

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