The evolution of multicellularity in the volvocine algae appears to have happened primarily through co-option of existing genes for new functions. For example, the initial transition from a unicellular life cycle to a simple multicellular one involved the retinoblastoma gene, as Hanschen and colleagues elegantly demonstrated (see “The evolution of undifferentiated multicellularity: the Gonium genome“). A Volvox gene involved in cellular differentiation, regA, was likely co-opted from an ancestral role in environmental sensing, and a similar origin appears to explain the use of cyclic AMP for the signaling that causes multicellular aggregation in cellular slime molds (see “Volvox 2015: evolution“).
Some of the changes leading to complex multicellularity, though, clearly did involve new genes. Two gene families involved in building the extracellular matrix that makes up most of a Volvox colony, the pherophorins and metalloproteinases, have undergone multiple duplication events leading to greatly expanded gene families (see “Heads I win; tails you lose: Evolution News & Views on Gonium, part 2“). One mechanism by which genes are duplicated is retroposition, in which a messenger RNA is reverse transcribed into DNA and inserted into the genome:
Fig S1A from Jakalski et al. 2016. Basic mechanism of retroposition. DNA is transcribed into a pre-mRNA by RNA polymerase, introns are spliced out, and a poly(A) tail is added to the 3′ end, resulting in a mature messenger RNA. The mRNA is then reverse-transcribed to DNA and inserted into a new genomic location.
Marcin Jąkalski and colleagues recently analyzed the Chlamydomonas and Volvox genomes looking for retrogenes (the article is open access). By searching the Volvox and Chlamydomonas genomes, they found 141 genes that looked as if they could have originated through retroposition (retrogenes). Potential retrogenes were identified by their lack of introns (because these are spliced out after transcription) and, in some cases, by the presence of a poly(A) tail.
Phylogenetic reconstruction of gene families including predicted retrogenes allowed the authors to infer evolutionary events leading to their emergence:
Fig. 2 from Jakalski et al. 2016. The inferred evolutionary events leading to the emergence of the identified retrogene candidates. The numbers in boxes that are projected on the phylogeny of the three studied green algae represent the estimated count of evolutionary events based on the composition of the retrogene-containing gene clusters, the inferred phylogenetic trees of the retrogene-containing homologous gene families, and the analyzed synteny.
They inferred 52 retroposition events in the most recent common ancestor of Volvox and Chlamy, as well as 22 lineage-specific events in Volvox and 6 in Chlamydomonas.
The authors find that the Volvox lineage
…contains significantly larger number of retrogenes, while having a smaller number of genes encoded by its genome compared to the unicellular Chlamydomonas…indicating possible contributions of retrogenes to the morphological differences in the two algae. Nevertheless, none of the genes thought to contribute to the observed morphological differences was found among our retrogene set…We found only two families of retrogenes that underwent expansion, namely the iron/manganese superoxide dismutase…and small nuclear ribonucleoprotein SmE family, both of them identified in the Volvox lineage. These results suggest that the gene family expansions described by Prochnik et al. were generally independent of retroposition events and that retroposition could be one of the probable molecular mechanisms contributing to the evolution of multicellularity in the green algae. [emphasis added]
All of that makes sense to me until the last bit. Volvox has more retrogenes than Chlamydomonas, but none of them have been identified as contributors to the morphological differences between the two, and the two gene family expansions that are thought to contribute to these differences don’t appear to result from retroposition. Nothing about that suggests to me that retroposition contributed to the evolution of multicellularity. There’s no reason it couldn’t have; the methods used in the study surely didn’t identify all of the retrogenes, and lots of the ones they did detect have unknown functions. But the evidence they did find doesn’t suggest anything of the sort. Retroposition contributing to multicellularity sounds to me like what the authors wanted to find rather than what they did find.
They continue with a subtle bit of question-begging:
…functional information about retrogenes and their parental genes in the green algae is still far from being comprehensive and, therefore, we could not clearly demonstrate the contribution of retroposition to the evolution of multicellularity in this lineage. [emphasis added]
Again, it’s entirely possible that retrogenes contributed to multicellularity. But this quote implies that incomplete information is the cause (“therefore”) of the failure to demonstrate a contribution, ignoring the possibility that no such contribution occurred.
To resolve this issue, genome-wide gene expression and functional analyses would be necessary. The current results are only first estimate of the evolutionary history of retrogene origination in green algae, yet we believe that presented study will provide a good foundation for any future investigation of the retrogene repertoire in this lineage…
Yes, and I hope we can look forward to such an analysis. In spite of my quibbles, this is a good start. Another nice addition would be the inclusion of Gonium and, eventually, other volvocine genomes. The Gonium genome was published in April, only two months before this paper was submitted to Biology Direct, so it may be that the authors had already spent six months analyzing data and didn’t want to start over, or it may be that the paper was already in review at a different journal when the Gonium genome came out.
Stable links:
Hanschen, E. R., T. N. Marriage, P. J. Ferris, T. Hamaji, A. Toyoda, A. Fujiyama, R. Neme, H. Noguchi, Y. Minakuchi, M. Suzuki, H. Kawai-Toyooka, D. R. Smith, V. Luria, A. Karger, M. W. Kirschner, H. Sparks, J. Anderson, R. Bakaric, P. M. Durand, R. E. Michod, H. Nozaki, and B. J. S. C. Olson. 2016. The Gonium pectorale genome demostrates co-option of cell cycle regulation during the evolution of multicellularity. Nature Communications 7:11370.
Jąkalski, M., K. Takeshita, M. Deblieck, K. O. Koyanagi, I. Makałowska, H. Watanabe, and W. Makałowski. 2016. Comparative genomic analysis of retrogene repertoire in two green algae Volvox carteri and Chlamydomonas reinhardtii. Biology Direct 11:35.
Prochnik, S. E., J. Umen, A. M. Nedelcu, A. Hallmann, S. M. Miller, I. Nishii, P. J. Ferris, A. Kuo, T. Mitros, L. K. Fritz-Laylin, U. Hellsten, J. Chapman, O. Simakov, S. A. Rensing, A. Terry, J. Pangilinan, V. Kapitonov, J. Jurka, A. Salamov, H. Shapiro, J. Schmutz, J. Grimwood, E. Lindquist, S. Lucas, I. V. Grigoriev, R. Schmitt, D. L. Kirk, and D. S. Rokhsar. 2010. Genomic analysis of organismal complexity in the multicellular green alga Volvox carteri. Science 329:223–226.
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