Abstract
BackgroundGenotype and environment can interact during development to produce novel adaptive traits that support life in extreme conditions. The development of the annual killifish Austrofundulus limnaeus is unique among vertebrates because the embryos have distinct cell movements that separate epiboly from axis formation during early development, can enter into a state of metabolic dormancy known as diapause and can survive extreme environmental conditions. The ability to enter into diapause can be maternally programmed, with young females producing embryos that do not enter into diapause. Alternately, embryos can be programmed to “escape” from diapause and develop directly by both maternal factors and embryonic incubation conditions. Thus, maternally packaged gene products are hypothesized to regulate developmental trajectory and perhaps the other unique developmental characters in this species.ResultsUsing high-throughput RNA sequencing, we generated transcriptomic profiles of mRNAs, long non-coding RNAs and small non-coding RNAs (sncRNAs) in 1–2 cell stage embryos of A. limnaeus. Transcriptomic analyses suggest maternal programming of embryos through alternatively spliced mRNAs and antisense sncRNAs. Comparison of these results to those of comparable studies on zebrafish and other fishes reveals a surprisingly high abundance of transcripts involved in the cellular response to stress and a relatively lower expression of genes required for rapid transition through the cell cycle.ConclusionsMaternal programming of developmental trajectory is unlikely accomplished by differential expression of diapause-specific genes. Rather, evidence suggests a role for trajectory-specific splice variants of genes expressed in both phenotypes. In addition, based on comparative studies with zebrafish, the A. limnaeus 1–2 cell stage transcriptome is unique in ways that are consistent with their unique life history. These results not only impact our understanding of the genetic mechanisms that regulate entrance into diapause, but also provide insight into the epigenetic regulation of gene expression during development.
Highlights
Genotype and environment can interact during development to produce novel adaptive traits that support life in extreme conditions
This paper describes for the first time the maternally derived transcriptome of early embryos of A. limnaeus, explores the possibility of maternal control of entrance into diapause through differential packaging of RNA and uses a comparative approach to identify aspects of the transcriptome that may explain some of the unique attributes of development in this species compared to more typical teleosts
Gene ontology (GO) analysis revealed enrichment for highly expressed genes (500 most abundant transcripts; >180 FPKM) in categories that include RNA-binding proteins, cytoskeletal proteins as well as redox reaction enzymes and pathways enriched for ATP synthesis and G-protein-coupled signaling (Additional file 3)
Summary
Genotype and environment can interact during development to produce novel adaptive traits that support life in extreme conditions. The development of the annual killifish Austrofundulus limnaeus is unique among vertebrates because the embryos have distinct cell movements that separate epiboly from axis formation during early development, can enter into a state of metabolic dormancy known as diapause and can survive extreme environmental conditions. Embryos of A. limnaeus can tolerate and survive extreme environmental stresses, such as long-term anoxia and dehydration [6]. Despite these unique characters, the development of A. limnaeus is quintessentially vertebrate and appears to utilize the Romney and Podrabsky EvoDevo (2017)8:6 same conserved genetic networks that govern development of the typical vertebrate body plan [4]. The mix of unique and apparently conserved developmental characteristics of this species makes it an excellent model for examining the evolutionary and mechanistic adaptations of novelty in vertebrate development
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