Studying the embryonic nervous system of the cricket Gryllus bimaculatus has suggested that a gene once considered exclusive to the germ line, may actually have its origins in somatic development.
Some animals – including Drosophila – employ a maternal inheritance mode of germ cell specification that is likely derived with respect to the ancestral mechanism for specifying germ cells in animals. In Drosophila, a gene called oskar encodes a maternal protein necessary and sufficient for germ cell fate. Oskar protein nucleates assembly of cytoplasmic granules containing germ line determinant molecules. For decades after its initial discovery, oskar‘s evolutionary origin was unknown, and it was thought to exist only in “higher” insects and to be exclusive and indispensable to the germ line. We have found that oskar is actually present in all groups of insects, is dispensable for the germ line outside of higher insects, and is at least 500 million years old, born from fusion of eukaryotic and prokaryotic sequences. Using our cricket (Gryllus bimaculatus) model system, we revealed a novel role for oskar in embryonic neurogenesis.
The movie above shows the crystal structure of the native LOTUS domain (+HgCl2) of D. melanogaster Oskar protein, showing a novel dimerization interface for this domain type that generates a beta sheet. Structure solved by John Srouji in collaboration with Andrés Leschziner.
Our current and ongoing work in this area now addresses several key questions:
(1) How did a protein operating in the soma, potentially in the nervous system, evolve interactions with pre-existing germ line molecules to acquire a germ line role?
(2) How did oskar, a gene with no known relatives in animal genomes, first evolve?
(3) What are the molecular mechanisms and biophysical properties of oskar that underlie its role in D. melanogaster germ line development?
By applying Hidden Markov Models to »1500 arthropod genomes and transcriptomes, we discovered over 300 previously undescribed oskar orthologs, giving us the phylogenetic power needed to answer some of these questions for the first time. By comparing the biophysical properties of Oskar between insects where it plays a germ line role versus a neural role, we provided strong evidence that the evolution of two key molecular features displayed by Drosophila Oskar protein – namely, dimerization via its LOTUS domain and physical interaction with the conserved germ line helicase Vasa – were key to Oskar’s evolutionary transformation into a germ plasm nucleator, and therefore to the emergence of inheritance-based germ cell specification in higher insects. We have also suggested an unexpected solution to the mystery of oskar’s evolutionary origin: our cross-kingdom phylogenetic analysis shows that part of its sequence is bacterial in origin. Our work thus suggests that gene birth processes previously considered to have negligible impact on development, including horizontal gene transfer, can in fact contribute new genes that are able to integrate into pre-existing regulatory modules and re-shape the evolution of developmental programs.
- 2020 Cool Paper: our work on oskar origins!
- An Interview with Alan Alda: How oskar the gene invented sex
- And the Oskar goes to: germ-soma differentiation in insects
- Creativity springs from unusual pairings
- Horizontal helper: Evidence suggests part of key gene needed for insect reproduction came from bacterial genomes
- oskar Reveals Missing Link in Co-optive Evolution
- Solving a biological mystery: researchers find gene related to germ cell formation older than thought