Comparative Transcriptomics of Steinernema and Caenorhabditis Single Embryos Reveals Orthologous Gene Expression Convergence during Late Embryogenesis

Abstract

Cells express distinct sets of genes in a precise spatio-temporal manner during embryonic development. There is a wealth of information on the deterministic embryonic development of Caenorhabditis elegans, but much less is known about embryonic development in nematodes from other taxa, especially at the molecular level. We are interested in insect pathogenic nematodes from the genus Steinernema as models of parasitism and symbiosis as well as a satellite model for evolution in comparison to C. elegans. To explore gene expression differences across taxa, we sequenced the transcriptomes of single embryos of two Steinernema species and two Caenorhabditis species at 11 stages during embryonic development and found several interesting features. Our findings show that zygotic transcription initiates at different developmental stages in each species, with the Steinernema species initiating transcription earlier than Caenorhabditis. We found that ortholog expression conservation during development is higher at the later embryonic stages than at the earlier ones. The surprisingly higher conservation of orthologous gene expression in later embryonic stages strongly suggests a funnel-shaped model of embryonic developmental gene expression divergence in nematodes. This work provides novel insight into embryonic development across distantly related nematode species and demonstrates that the mechanisms controlling early development are more diverse than previously thought at the transcriptional level.

The gene regulatory program of Acrobeloides nanus reveals conservation of phylum-specific expression

“…However, genes that originated in the early metazoan lineage and with the ecdysozoan superphylum are expressed during the middevelopmental transition. We further tested this result by examining the expression of genes of different ages in the recently published developmental transcriptome of the parasitic clade IV species Steinernema carpocapsae (43). Again, we found the same pattern ( Fig.…”

“…study examining the developmental transcriptomes of the parasitic clade IV species S. carpocapsae (43). Our phylostratigraphical analysis shows that genes that emerged during the origin of the superphylum Ecdysozoa and the Nematoda are more conserved in their developmental expression.…”

Conserved Patterns in Developmental Processes and Phases, Rather than Genes, Unite the Highly Divergent Bilateria

“…A conserved profile of developmental gene expression was observed in several studies across animal phyla, including in non-bilaterians, when developmental time course data were analyzed [ 12 ]. These studies suggest the existence of a phylotypic stage late in development, but see [ 12 , 48 , 62 ]. We observed low expression of young genes that originated after the emergence of Bilateria and of set genes in early development.…”

Evolution and Developmental System Drift in the Endoderm Gene Regulatory Network of Caenorhabditis and Other Nematodes

“…Comparisons of early embryonic transcripts across many Drosophila species and the mosquito Aedes aegypti has revealed that maternal transcript pools that, like those of C. elegans skn-1, are present only transiently during early embryogenesis, and that their expression levels are highly variable across these species, spanning ∼60 million years of evolution (Atallah and Lott, 2018). Similarly, considerable variation in the expression of maternal factor genes is found between different nematode species (Levin et al, 2012;Macchietto et al, 2017;Schiffer et al, 2018). This hourglass pattern of variation is attributable to the lack of negative selection of maternal-effect genes (Barker et al, 2005;Cruickshank and Wade, 2008;Cutter et al, 2019), as well as to increased developmental constraints during mid-embryogenesis (Raff, 1996;Zalts and Yanai, 2017).…”