Evolved differences incisandtransregulation between the maternal and zygotic mRNA complements in theDrosophilaembryo

Abstract

During embryogenesis in animals, initial developmental processes are driven entirely by maternally provided gene products that are deposited into the oocyte. The zygotic genome is transcriptionally activated later, when developmental control is handed off from maternal gene products to the zygote during the maternal to zygotic transition. The maternal to zygotic transition is highly regulated and conserved across all animals, and while some details change across model systems where it has been studied, most are too evolutionarily diverged to make comparisons as to how this process evolves. There are differences in maternal gene products and their zygotic complements across Drosophila species, so here we used hybrid crosses between sister species of Drosophila (D. simulans, D. sechellia, and D. mauritiana) and transcriptomics to determine how gene regulation changes in early embryogenesis across species. We find that regulation of maternal transcript deposition and zygotic transcription evolve through different mechanisms. Changes in transcript levels occur predominantly through differences in trans regulation for maternal genes, while changes in zygotic transcription occur through a combination of regulatory changes in cis, trans, and both cis and trans. We find that patterns of transcript level inheritance in hybrids relative to parental species differs between maternal and zygotic transcripts; maternal transcript levels are more likely to be conserved but both stages have a large proportion of transcripts showing dominance of one parental species. Differences in the underlying regulatory landscape in the mother and the zygote are likely the primary determinants for how maternal and zygotic transcripts evolve.

Maternal patterns of inheritance alter transcript expression in eggs

“…Variation in mRNA provisioning can certainly occur within a species, particularly due to maternal condition or genotype, but this variation is usually small and pertains to a few genes. In Drosophila melanogaster the difference in oocyte gene expression between extreme environmental maternal conditions (starved mothers fed 5% of control mothers’ diet) is only ∼1.8% (58,59) . For mice, the difference in mRNA expression (of at least 4-fold) between pubertal (3 week old) and climacteric (58 weeks old) oocytes is 2% (60) .…”

“…An advantage of our cross design is that we can determine the mode of regulation for differentially expressed genes. Typically regulatory analyses of cis and trans acting factors are conducted in hybrids (35)(36)(37)(38)81,59) , however, we were able to carry out these analyses in intraspecific comparisons with the caveat that there are far fewer distinguishing polymorphisms between the alleles of the two parents. We focus on the genes that are differentially expressed between the two morphs.…”

Evolution of maternal and early zygotic transcript regulation across Drosophila

“…Ludwig, Patel, and Kreitman 1998), despite the observation that changes in regulatory DNA can be responsible for changes in transcript level. Additionally, in a previous study in closely related species, changes in both cis-and trans-regulatory factors were identified as important to the evolution of differences in transcript level for zygotic genes at the stage also examined here (Cartwright and Lott 2020). While that study was not designed to look at either specific binding sites or changes in specific regulators, it seems likely that changes in both may be important to evolving transcript level differences for zygotic genes.…”

“…However, it seems most likely that evolved changes in transcript abundance at the maternal stage may be due to changes in abundance of the chromatin-modifying regulatory proteins. Previous work indicates that many changes in maternal gene expression between closely related species are due to trans-regulatory changes (such as those in regulatory proteins), and that closely related species also have differences in the abundance of transcripts for the important chromatin regulators of maternal transcription (Cartwright and Lott 2020).…”

Evolution of the regulation of developmental gene expression in blind Mexican cavefish

“…Looking at changes in gene regulation is critical to understand how species evolve and adapt to their environment. The contribution of cis -versus trans -regulation to the process is increasingly studied in animals and plants [4, 5, 20-22, 38, 39]. To our knowledge, this work is the first to examine transcriptome-wide the regulatory changes occurring during early developmental evolution in a teleost.…”