Dataset Information

The essential role of Dnmt1 in gametogenesis in the large milkweed bug Oncopeltus fasciatus.

ABSTRACT: Given the importance of DNA methylation in protection of the genome against transposable elements and transcriptional regulation in other taxonomic groups, the diversity in both levels and patterns of DNA methylation in the insects raises questions about its function and evolution. We show that the maintenance DNA methyltransferase, DNMT1, affects meiosis and is essential to fertility in milkweed bugs, Oncopeltus fasciatus, while DNA methylation is not required in somatic cells. Our results support the hypothesis that Dnmt1 is required for the transition of germ cells to gametes in O. fasciatus and that this function is conserved in male and female gametogenesis. They further suggest that DNMT1 has a function independent of DNA methylation in germ cells. Our results raise thequestion as to how a gene that is so critical to fitness across multiple insect species is able to diverge widely across the insect tree of life.

SUBMITTER: Washington JT

PROVIDER: S-EPMC8064748 | biostudies-literature | 2021 Apr

REPOSITORIES: biostudies-literature

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The essential role of Dnmt1 in gametogenesis in the large milkweed bug Oncopeltus fasciatus.

Washington Joshua T JT Cavender Katelyn R KR Amukamara Ashley U AU McKinney Elizabeth C EC Schmitz Robert J RJ Moore Patricia J PJ

eLife 20210412

Given the importance of DNA methylation in protection of the genome against transposable elements and transcriptional regulation in other taxonomic groups, the diversity in both levels and patterns of DNA methylation in the insects raises questions about its function and evolution. We show that the maintenance DNA methyltransferase, DNMT1, affects meiosis and is essential to fertility in milkweed bugs, Oncopeltus fasciatus, while DNA methylation is not required in somatic cells. Our resul ...[more]

PMID: 33843583

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Project description:BackgroundMost evolutionary developmental biology ("evo-devo") studies of emerging model organisms focus on small numbers of candidate genes cloned individually using degenerate PCR. However, newly available sequencing technologies such as 454 pyrosequencing have recently begun to allow for massive gene discovery in animals without sequenced genomes. Within insects, although large volumes of sequence data are available for holometabolous insects, developmental studies of basally branching hemimetabolous insects typically suffer from low rates of gene discovery.ResultsWe used 454 pyrosequencing to sequence over 500 million bases of cDNA from the ovaries and embryos of the milkweed bug Oncopeltus fasciatus, which lacks a sequenced genome. This indirectly developing insect occupies an important phylogenetic position, branching basal to Diptera (including fruit flies) and Hymenoptera (including honeybees), and is an experimentally tractable model for short-germ development. 2,087,410 reads from both normalized and non-normalized cDNA assembled into 21,097 sequences (isotigs) and 112,531 singletons. The assembled sequences fell into 16,617 unique gene models, and included predictions of splicing isoforms, which we examined experimentally. Discovery of new genes plateaued after assembly of ~1.5 million reads, suggesting that we have sequenced nearly all transcripts present in the cDNA sampled. Many transcripts have been assembled at close to full length, and there is a net gain of sequence data for over half of the pre-existing O. fasciatus accessions for developmental genes in GenBank. We identified 10,775 unique genes, including members of all major conserved metazoan signaling pathways and genes involved in several major categories of early developmental processes. We also specifically address the effects of cDNA normalization on gene discovery in de novo transcriptome analyses.ConclusionsOur sequencing, assembly and annotation framework provide a simple and effective way to achieve high-throughput gene discovery for organisms lacking a sequenced genome. These data will have applications to the study of the evolution of arthropod genes and genetic pathways, and to the wider evolution, development and genomics communities working with emerging model organisms.[The sequence data from this study have been submitted to GenBank under study accession number SRP002610 (http://www.ncbi.nlm.nih.gov/sra?term=SRP002610). Custom scripts generated are available at http://www.extavourlab.com/protocols/index.html. Seven Additional files are available.].

Project description:Regional populations of geographically widespread species may respond to different environmental factors across the species' range, generating divergent effects of climate change on life-history phenology. Using thousands of citizen science observations extracted from iNaturalist and associated with corresponding temperature, precipitation, elevation, and daylength information, we examined the drivers of adult mating and of nymphal phenology, development, and group size for populations of the large milkweed bug, Oncopeltus fasciatus, in different ecoregions. Research-grade iNaturalist images were correctly identified 98.3% of the time and yielded more than 3000 observations of nymphal groups and 1000 observations of mating adults spanning 18 years. Mating phenology showed distinct regional patterns, ranging from year-round mating in California to temporally restricted mating in the Great Lakes Northeastern Coast ecoregion. Relative temperature increases of 1°C for a given daylength expanded the mating season by more than a week in western ecoregions. While increases in relative temperature delayed mating phenology in all ecoregions, greater winter precipitation advanced mating in the California ecoregion. In the eastern ecoregions, nymphal phenology was delayed by increases in summer rainfall but was advanced by relative temperature increases, whereas in western regions, relative temperature increases delayed nymphal phenology. Furthermore, accumulated growing degree days (AGDD) was a poor predictor of developmental progression, as we found a positive but weak correlation between AGDD and age structure only for the Appalachian Southeast North America and the Great Lakes Northern Coast ecoregions. These complex phenological responses of O. fasciatus are just one example of how populations may be differentially susceptible to a diversity of climatic effects; using data across a species' whole distribution is critical for exposing regional variations, especially for species with large, continental-scale ranges. This study demonstrates the potential of photodocumented biodiversity data to aid in the monitoring of life history, host plant-insect interactions, and climate responsiveness.

Dataset Information

The essential role of Dnmt1 in gametogenesis in the large milkweed bug Oncopeltus fasciatus.

Publications

The essential role of Dnmt1 in <i>gametogenesis</i> in the large milkweed bug <i>Oncopeltus fasciatus</i>.

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