Noise transmission during the dynamic pattern formation in fly embryos

Abstract

Background: Developmental patterning is highly reproducible and accurate at the single-cell level during fly embryogenesis despite the gene expression noise and external perturbations such as the variation of the embryo length, temperature and genes. To reveal the underlying mechanism, it is very important to characterize the noise transmission during the dynamic pattern formation. Two hypotheses have been proposed. The "channel" scenario requires a highly reproducible input and an accurate interpretation by downstream genes. In contrast, the "filter" scenario proposes a noisy input and a noise filter via the cross-regulation of the downstream network. It has been under great debates which scenario the fly embryogenesis follows. Results: The first 3-h developmental patterning of fly embryos is orchestrated by a hierarchical segmentation gene network, which rewires upon the maternal to zygotic transition. Starting from the highly reproducible maternal gradients, the positional information is refined to the single-cell precision through the highly dynamical evolved zygotic gene expression profiles. Thus the fly embryo development might strictly fit into neither the originally proposed "filter" nor "channel" scenario. The controversy that which scenario the fly embryogenesis follows could be further clarified by combining quantitative measurements and modeling. Conclusions: Fly embryos have become one of the perfect model systems for quantitative systems biology studies. The underlying mechanism discovered from fly embryogenesis will deepen our understanding of the noise control of the gene network, facilitate searching for more efficient and safer methods for cell programming and reprogramming, and have the great potential for tissue engineering and regenerative medicine.Keywords: pattern formation; gene regulatory network; noise; embryogenesis; Drosophila Author summary: It is intriguing how the development of organisms is highly reproducible and accurate despite the external and internal noise. The key to solve this mystery is to explore the noise transmission during development and discover the underlying mechanism. The developmental system could generate precise inputs and outputs in each step, or gradually generate a final precise output by filtering a noisy input according to the "channel" or "filter" scenario, respectively. The quantitative studies on the early development of the fruit fly's embryos show that the developmental process is highly dynamic and its noise transmission may employ a hybridized strategy.

Single-Cell Transcriptomes Reveal Characteristics of MicroRNAs in Gene Expression Noise Reduction

“…Such variability can increase overall fitness in evolution by expanding the range of phenotypes [4] , [5] . However, noise can result in nonreproducible coordinating cellular functions during tissue morphogenesis and homeostasis [6] , [7] . Maintaining precise and robust gene expression in fluctuating environments is necessary for cells to function physiologically.…”

The dynamic transmission of positional information in stau- mutants during Drosophila embryogenesis

“…During the development of multicellular systems, the expression of patterning genes dynamically evolves and stochastically fluctuates ( Dubuis et al, 2013 ; Gregor et al, 2007a ; Gregor et al, 2007b ; Jaeger et al, 2004 ; Kanodia et al, 2009 ; Liu et al, 2013 ; Yang et al, 2018 ).The high degree of accuracy ( Dubuis et al, 2013 ; Gregor et al, 2007a ) and robustness ( Houchmandzadeh et al, 2002 ; Inomata et al, 2013 ; Liu et al, 2013 ; Lucchetta et al, 2005 ) that developmental patterning achieves is intriguing. Two hypotheses have been proposed to explain these traits: one is the threshold-dependent positional information model, that is the French flag model, which assumes that the positional information is faithfully transferred from precise upstream patterning ( He et al, 2008 ; Wolpert, 2011 ; Gregor et al, 2007a ); the other is the self-organized filtering model, which assumes that noisy upstream patterning needs to be refined to form downstream patterning with sufficient positional information ( Dubuis et al, 2013 ; Houchmandzadeh et al, 2002 ; Jaeger et al, 2004 ; Kanodia et al, 2009 ; Manu et al, 2009 ).…”

Quantifying Temperature Compensation of Bicoid Gradients with a Fast T-Tunable Microfluidic Device

“…As the temperature increases from 18 °C to 29 °C, the development time of embryos in the first 13 nuclear cycles shortens from 210 min to 110 min (4,6), and the embryo laid by the flies raised in different temperatures for weeks also adapts to shorter length by 8% (12). One would expect that the developmental patterns in early fly embryos be much more strongly affected by temperature.…”