Transcriptomic analysis of maternally provisioned cues for phenotypic plasticity in the annual killifish, Austrofundulus limnaeus

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.Electronic supplementary materialThe online version of this article (doi:10.1186/s13227-017-0069-7) contains supplementary material, which is available to authorized users.

Cell cycle dynamics during diapause entry and exit in an annual killifish revealed by FUCCI technology

“…It is known that diapause II is characterized by reduced protein synthesis, cell cycle arrest and remodelling of mitochondrial physiology and it is controlled by insulin-like growth factor 1 signalling [29][30][31][32][33][34][35].Recently, RNAseq studies have shown that , gene-expression patterns during diapause resemble those observed during aging [36] and vitamin D signalling controls to the choice between direct development and diapause II [37]. While early embryonic development following fertilisation have been in part studied [7][8][9], the characterization of the physiological and molecular events occurring during diapause I has been started to be investigated only recently [35,38,39]. Here, to investigate entry and exit form diapause I and II, we created a stable transgenic line in N. furzeri that expresses fluorescent reporters for cell cycle phases [40].…”

Embryonic development of the annual killifish Austrofundulus limnaeus: An emerging model for ecological and evolutionary developmental biology research and instruction

“…In addition to their extremophile biology, these fish are relatively easy to maintain in captivity, highly fecund, and share many of the characteristics of traditional model organisms. Recent work on this species has resulted in the availability of an annotated draft genome (Wagner et al, ), and a wealth of transcriptomic data to detail the expression of genes across development and in response to environmental stresses (Romney et al, ), and to identify those transcripts that are maternally packaged (Romney and Podrabsky, ).…”

ArHsp40 and ArHsp40-2 contribute to stress tolerance and longevity in Artemia franciscana, but only ArHsp40 influences diapause entry

“…Diapause is divided into phases termed initiation, maintenance and termination, which may be further subdivided (Koštál, 2006;Yocum et al, 2009;Koštál et al, 2017). Diapause initiation can entail diet change, differential gene expression and protein synthesis, structural changes for tissue defence, and lipid accumulation (Hayward et al, 2005;Hahn and Denlinger, 2007;MacRae, 2010;Clark et al, 2012;Tarrant et al, 2014Tarrant et al, , 2016Romney and Podrabsky, 2017;Arezo et al, 2017). Initiation leads to maintenance where, most notably, stress tolerance and metabolic depression are maximized.…”