Natural variation in the maternal and zygotic mRNA complements of the early embryo in Drosophila melanogaster

Maternal gene products supplied to the egg during oogenesis drive the earliest events of development in all metazoans. After the initial stages of embryogenesis, maternal transcripts are degraded as zygotic transcription is activated, this is known as the maternal to zygotic transition (MZT). Altering the abundances of maternally deposited factors in the laboratory can have a dramatic effect on development, adult phenotypes and ultimately fitness. Zygotic transcription activation is a tightly regulated process, where the zygotic genome takes over control of development from the maternal genome, and is required for the viability of the organism. Recently, it has been shown that the expression of maternal and zygotic transcripts have evolved in the Drosophila genus over the course of 50 million years of evolution. However, the extent of natural variation of maternal and zygotic transcripts within a species has yet to be determined. We asked how the maternal and zygotic pools of mRNA vary within and between populations of D. melanogaster. In order to maximize sampling of genetic diversity, African lines of D. melanogaster originating from Zambia as well as DGRP lines originating from North America were chosen for transcriptomic analysis. Single embryo RNA-seq was performed at a stage before and a stage after zygotic genome activation in order to determine which transcripts are maternally deposited and which are zygotically expressed within and between these populations. Differential gene expression analysis has been used to quantify quantitative changes in RNA levels within populations as well as fixed expression differences between populations at both stages. Generally, we find that maternal transcripts are more highly conserved, and zygotic transcripts evolve at a higher rate. We find that there is more within population variation in transcript abundance than between populations and that expression variation is highest post- MZT between African lines. Determining the natural variation of gene expression surrounding the MZT in natural populations of D. melanogaster gives insight into the extent of how a tightly regulated process may vary within a species, the extent of developmental constraint at both stages and on both the maternal and zygotic genomes, and reveals expression changes allowing this species to adapt as it spread across the world.

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Pluripotency factors select gene expression repertoire at Zygotic Genome Activation

10.1101/2020.02.16.949362 ◽

2020 ◽

Cited By ~ 1

Author(s):

Meijiang Gao ◽

Marina Veil ◽

Marcus Rosenblatt ◽

Anna Gebhard ◽

Helge Hass ◽

...

Keyword(s):

Gene Expression ◽

Transcription Factors ◽

Early Gene ◽

Zebrafish Embryos ◽

Fate Specification ◽

Pluripotency Factors ◽

Zygotic Transcription ◽

Simultaneous Loss ◽

Genome Activation ◽

Zygotic Genome

AbstractAwakening of zygotic transcription in animal embryos relies on maternal pioneer transcription factors. The interplay of global and specific functions of these proteins remains poorly understood. Here, we analyzed nucleosome positioning, H3K27 acetylation, transcription, and gastrulation rates in zebrafish embryos lacking pluripotency factors Pou5f3 and Sox19b. We show that the bulk transcriptional onset does not require Sox19b and Pou5f3, but is sensitive to their balance. Pou5f3 docks H3K27ac on the enhancers of genes involved in gastrulation and ventral fate specification. Sox19b facilitates Pou5f3 access to one-third of these enhancers. The genes regulating mesendodermal and dorsal fates are primed for activation independently on Pou5f3 and Sox19b. Strikingly, the loss of either factor results in activation of silent enhancers; simultaneous loss of both leads to premature expression of differentiation genes. Our results uncover how independent activities of maternal Pou5f3 and Sox19b add up or antagonize to determine the early gene expression repertoire.

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Negative control of Xenopus GATA-2 by activin and noggin with eventual expression in precursors of the ventral blood islands

Development ◽

10.1242/dev.120.9.2519 ◽

1994 ◽

Vol 120 (9) ◽

pp. 2519-2529 ◽

Cited By ~ 17

Author(s):

M.E. Walmsley ◽

M.J. Guille ◽

D. Bertwistle ◽

J.C. Smith ◽

J.A. Pizzey ◽

...

Keyword(s):

Negative Control ◽

Early Embryo ◽

Signalling Pathways ◽

Vertebrate Development ◽

Dorsoventral Patterning ◽

Dorsal Region ◽

Blood Island ◽

Zygotic Transcription ◽

Maternal Transcripts ◽

Marginal Zones

To increase our understanding of haematopoiesis during early vertebrate development, we have studied the expression pattern of the transcription factor GATA-2 in Xenopus embryos, and asked how this is regulated. We show that the blood island precursors of the ventral mesoderm express GATA-2 RNA at neural tube stages, some 5 hours before globin RNA is detected in their derivatives. Prior to this however, GATA-2 is expressed much more widely within the embryo. Maternal transcripts are uniformly distributed, and zygotic transcription is activated during gastrulation throughout ventral and lateral regions of the embryo, with expression highest in the sensorial ectoderm and only weak in the ventral mesoderm. The domain of GATA-2 expression in neurulae outlines the region of the neural plate and suggests a possible wider role in dorsoventral patterning. To identify the signals involved in regulating this pattern of expression, we performed experiments with embryo explants. GATA-2 is activated autonomously in isolated animal caps and this activation is suppressed by the mesoderm-inducing factor activin, but not by FGF. Thus, the down-regulation of GATA-2 observed in the region of the Spemann organiser may be a response to an activin-like signal emanating from the dorsal-vegetal region or Nieuwkoop centre. GATA-2 activation in animal caps and ventral marginal zones was suppressed by co-culturing with dorsal marginal zones, suggesting that a signal from the Spemann organiser is involved in suppression of GATA-2 in the dorsal region of the embryo. Expression of a candidate for this signal, noggin, had the same effect. Taken together, the observations presented here suggest that GATA-2 activation occurs by default in the absence of signals, that the restriction of its expression within the early embryo is controlled by negative signals emanating from the Nieuwkoop centre and the organiser, and that noggin and activin-like molecules play a role in these signalling pathways.

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Pathway dynamics can delineate the sources of transcriptional noise in gene expression

10.1101/2020.09.30.319814 ◽

2020 ◽

Author(s):

Lucy Ham ◽

Marcel Jackson ◽

Michael P.H. Stumpf

Keyword(s):

Gene Expression ◽

Formal Analysis ◽

Single Gene ◽

Population Data ◽

Transcript Abundance ◽

Population Variation ◽

Stochastic Simulations ◽

Transcriptional Level ◽

Extrinsic Noise ◽

Dual Reporter

Single-cell expression profiling is destructive, giving rise to only static snapshots of cellular states. This loss of temporal information presents significant challenges in inferring dynamics from population data. Here we provide a formal analysis of the extent to which dynamic variability from within individual systems (“intrinsic noise”) is distinguishable from variability across the population (“extrinsic noise”). Our results mathematically formalise observations that it is impossible to identify these sources of variability from the transcript abundance distribution alone. Notably, we find that systems subject to population variation invariably inflate the apparent degree of burstiness of the underlying process. Such identifiability problems can be remedied by the dual-reporter method, which separates the total gene expression noise into intrinsic and extrinsic contributions. This noise decomposition, however, requires strictly independent and identical gene reporters integrated into the same cell, which can be difficult to implement experimentally in many systems. Here we demonstrate mathematically that, in some cases, the same noise decomposition can be achieved at the transcriptional level with non-identical and not-necessarily independent reporters. We use our result to show that generic reporters lying in the same biochemical pathways (e.g. mRNA and protein) can replace dual reporters, enabling the noise decomposition to be obtained from only a single gene. Stochastic simulations are used to support our theory, and show that our “pathway-reporter” method compares favourably to the dual-reporter method.

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Comprehensive cross production system assessment of the impact of in vitro microenvironment on the expression of messengers and long non-coding RNAs in the bovine blastocyst

Reproduction ◽

10.1530/rep-10-0477 ◽

2011 ◽

Vol 142 (1) ◽

pp. 99-112 ◽

Cited By ~ 18

Author(s):

Isabelle Côté ◽

Christian Vigneault ◽

Isabelle Laflamme ◽

Joanie Laquerre ◽

Éric Fournier ◽

...

Keyword(s):

Gene Expression ◽

Transcript Abundance ◽

Early Embryo ◽

Substantial Improvement ◽

Intergenic Regions ◽

Negative Impacts ◽

Additional Level ◽

The Impact

In vitroproduction (IVP) of cattle embryos over the past two decades has revealed several negative impacts that have been attributed to the artificial microenvironment. Studies on embryos producedin vitroclearly point to aberrant gene expression levels. So far, the causal association between phenotype and measured gene expression has not led to substantial improvement of IVP systems. The aim of this study was to generate a unique dataset composed of microarray-derived relative transcript abundance values for blastocysts produced in tenin vitrosystems differing primarily in culture medium formulation. Between-group comparisons determine the level of overall similarity among systems relative toin vivoreference embryos. The use of the dataset to contrast allin vitrotreatments with thein vivoblastocysts pointed to a single common gene network. The ‘boutique’ array contained a panel of novel uncharacterized transcripts that were variably expressed depending on the medium in which the blastocysts were produced. These novel transcripts were differentially expressed in blastocysts even as carryover from conditions encountered 7 days earlier during oocyte maturation. All of the selected novel candidates thus expressed were from intergenic regions. The function of this long non-coding RNA remains unknown but clearly points to an additional level of complexity in early embryo development.

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Faculty Opinions recommendation of Natural variation in cardiac metabolism and gene expression in Fundulus heteroclitus.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.1023148.266659 ◽

2005 ◽

Author(s):

Michael O'Donovan

Keyword(s):

Gene Expression ◽

Natural Variation ◽

Fundulus Heteroclitus ◽

Cardiac Metabolism

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Comparisons among rainbow trout, Oncorhynchus mykiss, populations of maternal transcript profile associated with egg viability

BMC Genomics ◽

10.1186/s12864-021-07773-1 ◽

2021 ◽

Vol 22 (1) ◽

Author(s):

Gregory M. Weber ◽

Jill Birkett ◽

Kyle Martin ◽

Doug Dixon ◽

Guangtu Gao ◽

...

Keyword(s):

Rainbow Trout ◽

Egg Quality ◽

Transcript Abundance ◽

Differentially Expressed ◽

Rainbow Trout Oncorhynchus Mykiss ◽

Analysis Group ◽

Maternal Transcripts ◽

Single Batch ◽

Insight Into

Abstract Background Transcription is arrested in the late stage oocyte and therefore the maternal transcriptome stored in the oocyte provides nearly all the mRNA required for oocyte maturation, fertilization, and early cleavage of the embryo. The transcriptome of the unfertilized egg, therefore, has potential to provide markers for predictors of egg quality and diagnosing problems with embryo production encountered by fish hatcheries. Although levels of specific transcripts have been shown to associate with measures of egg quality, these differentially expressed genes (DEGs) have not been consistent among studies. The present study compares differences in select transcripts among unfertilized rainbow trout eggs of different quality based on eyeing rate, among 2 year classes of the same line (A1, A2) and a population from a different hatchery (B). The study compared 65 transcripts previously reported to be differentially expressed with egg quality in rainbow trout. Results There were 32 transcripts identified as DEGs among the three groups by regression analysis. Group A1 had the most DEGs, 26; A2 had 15, 14 of which were shared with A1; and B had 12, 7 of which overlapped with A1 or A2. Six transcripts were found in all three groups, dcaf11, impa2, mrpl39_like, senp7, tfip11 and uchl1. Conclusions Our results confirmed maternal transcripts found to be differentially expressed between low- and high-quality eggs in one population of rainbow trout can often be found to overlap with DEGs in other populations. The transcripts differentially expressed with egg quality remain consistent among year classes of the same line. Greater similarity in dysregulated transcripts within year classes of the same line than among lines suggests patterns of transcriptome dysregulation may provide insight into causes of decreased viability within a hatchery population. Although many DEGs were identified, for each of the genes there is considerable variability in transcript abundance among eggs of similar quality and low correlations between transcript abundance and eyeing rate, making it highly improbable to predict the quality of a single batch of eggs based on transcript abundance of just a few genes.

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Natural variation in social conditions affects male mate choosiness in the amphipod Gammarus roeselii

Current Zoology ◽

10.1093/cz/zoab016 ◽

2021 ◽

Author(s):

Konrad Lipkowski ◽

Sophie Steigerwald ◽

Lisa M Schulte ◽

Carolin Sommer-Trembo ◽

Jonas Jourdan

Keyword(s):

Population Density ◽

Sex Ratio ◽

Natural Variation ◽

Natural Populations ◽

Social Background ◽

Social Conditions ◽

Background Information ◽

Male Mating ◽

Natural Environments ◽

Male Mate

Abstract The extent of male mate choosiness is driven by a trade-off between various environmental factors associated with the costs of mate acquisition, quality assessment and opportunity costs. Our knowledge about natural variation in male mate choosiness across different populations of the same species, however, remains limited. In this study, we compared male mate choosiness across 10 natural populations of the freshwater amphipod Gammarus roeselii (Gervais 1835), a species with overall high male mating investments, and evaluated the relative influence of population density and sex ratio (both affecting mate availability) on male mate choosiness. We investigated amplexus establishment after separating mating pairs and presenting focal males with a novel, size-matched female from the same population. Our analysis revealed considerable effects of sex ratio and (to a lesser extent) population density on time until amplexus establishment (choosiness). Male amphipods are able to perceive variable social conditions (e.g., sex ratio) and modify their mating strategy accordingly: We found choosiness to be reduced in increasingly male-biased populations, whereas selectivity increases when sex ratio becomes female biased. With this, our study expands our limited knowledge on natural variations in male mate choosiness and illustrates the importance of sex ratio (i.e., level of competition) for male mating decisions in natural environments. Accounting for variation in sex ratios, therefore, allows envisioning a distinctive variation of choosiness in natural populations and highlights the importance of considering social background information in future behavioral studies.

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Natural variation in yolk fatty acids, but not androgens, predicts offspring fitness in a wild bird

Frontiers in Zoology ◽

10.1186/s12983-021-00422-z ◽

2021 ◽

Vol 18 (1) ◽

Author(s):

Lucia Mentesana ◽

Martin N. Andersson ◽

Stefania Casagrande ◽

Wolfgang Goymann ◽

Caroline Isaksson ◽

...

Keyword(s):

Fatty Acids ◽

Polyunsaturated Fatty Acids ◽

Maternal Effects ◽

Natural Variation ◽

De Novo ◽

Natural Populations ◽

Egg Laying ◽

Interactive Effects ◽

Free Living ◽

Offspring Fitness

Abstract Background In egg-laying animals, mothers can influence the developmental environment and thus the phenotype of their offspring by secreting various substances into the egg yolk. In birds, recent studies have demonstrated that different yolk substances can interactively affect offspring phenotype, but the implications of such effects for offspring fitness and phenotype in natural populations have remained unclear. We measured natural variation in the content of 31 yolk components known to shape offspring phenotypes including steroid hormones, antioxidants and fatty acids in eggs of free-living great tits (Parus major) during two breeding seasons. We tested for relationships between yolk component groupings and offspring fitness and phenotypes. Results Variation in hatchling and fledgling numbers was primarily explained by yolk fatty acids (including saturated, mono- and polyunsaturated fatty acids) - but not by androgen hormones and carotenoids, components previously considered to be major determinants of offspring phenotype. Fatty acids were also better predictors of variation in nestling oxidative status and size than androgens and carotenoids. Conclusions Our results suggest that fatty acids are important yolk substances that contribute to shaping offspring fitness and phenotype in free-living populations. Since polyunsaturated fatty acids cannot be produced de novo by the mother, but have to be obtained from the diet, these findings highlight potential mechanisms (e.g., weather, habitat quality, foraging ability) through which environmental variation may shape maternal effects and consequences for offspring. Our study represents an important first step towards unraveling interactive effects of multiple yolk substances on offspring fitness and phenotypes in free-living populations. It provides the basis for future experiments that will establish the pathways by which yolk components, singly and/or interactively, mediate maternal effects in natural populations.

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