The evolution of insect germline specification strategies

Quan, Honghu; Lynch, Jeremy A.

doi:10.1016/j.cois.2016.02.013

Cited by 15 publications

(8 citation statements)

References 64 publications

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“…We find that the oskar locus has been lost independently in some insect orders, including near-total absence from the order Hemiptera, and clarify that the absence of oskar from the Bombyx mori and Tribolium castaneum genomes (discussed in Quan and Lynch 2016) does not reflect a general absence of oskar from Lepidoptera or Coleoptera. By comparing Oskar sequences in a phylogenetic context, we reveal that distinct biophysical properties of Oskar are associated with Hemimetabola and Holometabola.…”

Section: Introductionsupporting

confidence: 54%

“…To date, sequences of approximately 100 oskar orthologs have been reported (Lynch, et al 2011; Jeske, et al 2015; Quan and Lynch 2016; Blondel, et al 2020). However, the vast majority of these are from the Holometabola, and it is thus unclear whether analysis of these sequences alone would have sufficient power to allow extrapolation of conservation and divergence of putative biochemical properties across insects broadly speaking.…”

Section: Introductionmentioning

confidence: 99%

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Evolution of a cytoplasmic determinant: evidence for the biochemical basis of functional evolution of a novel germ line regulator

Blondel

Besse

Extavour

2021

Preprint

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Germ line specification is essential in sexually reproducing organisms. Despite their critical role, the evolutionary history of the genes that specify animal germ cells is heterogeneous and dynamic. In many insects, the gene oskar is required for the specification of the germ line. However, the germ line role of oskar is thought to be a derived role resulting from co-option from an ancestral somatic role. To address how evolutionary changes in protein sequence could have led to changes in the function of Oskar protein that enabled it to regulate germ line specification, we searched for oskar orthologs in 1565 publicly available insect genomic and transcriptomic datasets. The earliest-diverging lineage in which we identified an oskar ortholog was the order Zygentoma (silverfish and firebrats), suggesting that oskar originated before the origin of winged insects. We noted some order-specific trends in oskar sequence evolution, including whole gene duplications, clade-specific losses, and rapid divergence. An alignment of all known 379 Oskar sequences revealed new highly conserved residues as candidates that promote dimerization of the LOTUS domain. Moreover, we identified regions of the OSK domain with conserved predicted RNA binding potential. Furthermore, we show that despite a low overall amino acid conservation, the LOTUS domain shows higher conservation of predicted secondary structure than the OSK domain. Finally, we suggest new key amino acids in the LOTUS domain that may be involved in the previously reported Oskar-Vasa physical interaction that is required for its germ line role.

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Section: Introductionsupporting

confidence: 54%

Section: Introductionmentioning

confidence: 99%

Evolution of a cytoplasmic determinant: evidence for the biochemical basis of functional evolution of a novel germ line regulator

Blondel

Besse

Extavour

2021

Preprint

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“…The Drosophila oskar gene encodes a germ granule protein that is synthesized at the posterior pole of the oocyte. Oskar initiates germplasm assembly and germ cell determination; this gene appears to have been lost in the Hemiptera ( Ephrussi and Lehmann, 1992 ; Lynch et al, 2011 ; Quan and Lynch, 2016 ; Blondel et al, 2021 ). For this reason, it is expected that there should be fundamental differences in the transcriptomes of embryos during oogenesis and early embryogenesis.…”

Section: Introductionmentioning

confidence: 99%

Gene Editing and Genetic Control of Hemipteran Pests: Progress, Challenges and Perspectives

Pacheco

Walling

Atkinson

2022

Front. Bioeng. Biotechnol.

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The origin of the order Hemiptera can be traced to the late Permian Period more than 230 MYA, well before the origin of flowering plants 100 MY later in during the Cretaceous period. Hemipteran species consume their liquid diets using a sucking proboscis; for phytophagous hemipterans their mouthparts (stylets) are elegant structures that enable voracious feeding from plant xylem or phloem. This adaptation has resulted in some hemipteran species becoming globally significant pests of agriculture resulting in significant annual crop losses. Due to the reliance on chemical insecticides for the control of insect pests in agricultural settings, many hemipteran pests have evolved resistance to insecticides resulting in an urgent need to develop new, species-specific and environmentally friendly methods of pest control. The rapid advances in CRISPR/Cas9 technologies in model insects such as Drosophila melanogaster, Tribolium castaneum, Bombyx mori, and Aedes aegypti has spurred a new round of innovative genetic control strategies in the Diptera and Lepidoptera and an increased interest in assessing genetic control technologies for the Hemiptera. Genetic control approaches in the Hemiptera have, to date, been largely overlooked due to the problems of introducing genetic material into the germline of these insects. The high frequency of CRISPR-mediated mutagenesis in model insect species suggest that, if the delivery problem for Hemiptera could be solved, then gene editing in the Hemiptera might be quickly achieved. Significant advances in CRISPR/Cas9 editing have been realized in nine species of Hemiptera over the past 4 years. Here we review progress in the Hemiptera and discuss the challenges and opportunities for extending contemporary genetic control strategies into species in this agriculturally important insect orderr.

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“…Structural and biochemical studies revealed that Osk binds RNA and more recently, that it increases the helicase activity of its interaction partner Vasa [ 12 – 15 ]. Despite its potent activity as a germ plasm organizer, Osk homologs were not discovered outside of insect genomes [reviewed in 16 ].…”

Section: Introductionmentioning

confidence: 99%

Functional equivalence of germ plasm organizers

et al. 2018

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The proteins Oskar (Osk) in Drosophila and Bucky ball (Buc) in zebrafish act as germ plasm organizers. Both proteins recapitulate germ plasm activities but seem to be unique to their animal groups. Here, we discover that Osk and Buc show similar activities during germ cell specification. Drosophila Osk induces additional PGCs in zebrafish. Surprisingly, Osk and Buc do not show homologous protein motifs that would explain their related function. Nonetheless, we detect that both proteins contain stretches of intrinsically disordered regions (IDRs), which seem to be involved in protein aggregation. IDRs are known to rapidly change their sequence during evolution, which might obscure biochemical interaction motifs. Indeed, we show that Buc binds to the known Oskar interactors Vasa protein and nanos mRNA indicating conserved biochemical activities. These data provide a molecular framework for two proteins with unrelated sequence but with equivalent function to assemble a conserved core-complex nucleating germ plasm.

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The evolution of insect germline specification strategies

Cited by 15 publications

References 64 publications

Evolution of a cytoplasmic determinant: evidence for the biochemical basis of functional evolution of a novel germ line regulator

Evolution of a cytoplasmic determinant: evidence for the biochemical basis of functional evolution of a novel germ line regulator

Gene Editing and Genetic Control of Hemipteran Pests: Progress, Challenges and Perspectives

Functional equivalence of germ plasm organizers

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