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The Phylogenetic Origin of Coincided with the
Origin of Maternally Provisioned Germ Plasm and Pole Cells at the Base of the
Holometabola


The establishment of the germline is a critical, yet surprisingly evolutionarily

labile, event in the development of sexually reproducing animals. In the fly

Drosophila, germ cells acquire their fate early during

development through the inheritance of the germ plasm, a specialized maternal

cytoplasm localized at the posterior pole of the oocyte. The gene

oskar (osk) is both necessary and

sufficient for assembling this substance. Both maternal germ plasm and

oskar are evolutionary novelties within the insects, as the

germline is specified by zygotic induction in basally branching insects, and

osk has until now only been detected in dipterans. In order

to understand the origin of these evolutionary novelties, we used comparative

genomics, parental RNAi, and gene expression analyses in multiple insect

species. We have found that the origin of osk and its role in

specifying the germline coincided with the innovation of maternal germ plasm and

pole cells at the base of the holometabolous insects and that losses of

osk are correlated with changes in germline determination

strategies within the Holometabola. Our results indicate that the invention of

the novel gene osk was a key innovation that allowed the

transition from the ancestral late zygotic mode of germline induction to a

maternally controlled establishment of the germline found in many holometabolous

insect species. We propose that the ancestral role of osk was

to connect an upstream network ancestrally involved in mRNA localization and

translational control to a downstream regulatory network ancestrally involved in

executing the germ cell program.


Vyšlo v časopise: The Phylogenetic Origin of Coincided with the Origin of Maternally Provisioned Germ Plasm and Pole Cells at the Base of the Holometabola. PLoS Genet 7(4): e32767. doi:10.1371/journal.pgen.1002029
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002029

Souhrn

The establishment of the germline is a critical, yet surprisingly evolutionarily

labile, event in the development of sexually reproducing animals. In the fly

Drosophila, germ cells acquire their fate early during

development through the inheritance of the germ plasm, a specialized maternal

cytoplasm localized at the posterior pole of the oocyte. The gene

oskar (osk) is both necessary and

sufficient for assembling this substance. Both maternal germ plasm and

oskar are evolutionary novelties within the insects, as the

germline is specified by zygotic induction in basally branching insects, and

osk has until now only been detected in dipterans. In order

to understand the origin of these evolutionary novelties, we used comparative

genomics, parental RNAi, and gene expression analyses in multiple insect

species. We have found that the origin of osk and its role in

specifying the germline coincided with the innovation of maternal germ plasm and

pole cells at the base of the holometabolous insects and that losses of

osk are correlated with changes in germline determination

strategies within the Holometabola. Our results indicate that the invention of

the novel gene osk was a key innovation that allowed the

transition from the ancestral late zygotic mode of germline induction to a

maternally controlled establishment of the germline found in many holometabolous

insect species. We propose that the ancestral role of osk was

to connect an upstream network ancestrally involved in mRNA localization and

translational control to a downstream regulatory network ancestrally involved in

executing the germ cell program.


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