Natural size variation among embryos leads to the corresponding scaling in gene expression

Leibovich, Avi; Edri, Tamir; Klein, Steven L.; Moody, Sally A.; Fainsod, Abraham

doi:10.1016/j.ydbio.2020.03.014

Cited by 14 publications

(8 citation statements)

References 72 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Migration of the PCM is a very dynamic process dependent on the progression of gastrulation. To minimize the effect of slight size differences between the embryos ( Leibovich et al, 2020 ), the migration distance was normalized to the embryo diameter and presented as a relative migration from the value in control embryos ( Figure 2D ). The results showed that citral treatment inhibited PCM migration by 57.1% and DEAB inhibited it by 71.7%.…”

Section: Resultsmentioning

confidence: 99%

“…To ensure that our visual staging seleted embryos within a limited range of blastopore sizes, for each embryo we measured its diameter and the diameter of the blastopore and calculated the ratio between them ( Figure 2E ). The use of this ratio has been shown to normalize staging of embryos of different sizes during gastrulation stages ( Leibovich et al, 2020 ). This comparison of the relative blastopore sizes supported the conclusion that the treated and control embryos were at statistically similar developmental stages, and that the reduction of PCM migration was a direct result of reduced RA signaling rather than overall developmental delay.…”

Section: Resultsmentioning

confidence: 99%

See 1 more Smart Citation

Retinoic Acid is Required for Normal Morphogenetic Movements During Gastrulation

Gur

Edri

Moody

et al. 2022

Front. Cell Dev. Biol.

Self Cite

View full text Add to dashboard Cite

Retinoic acid (RA) is a central regulatory signal that controls numerous developmental processes in vertebrate embryos. Although activation of Hox expression is considered one of the earliest functions of RA signaling in the embryo, there is evidence that embryos are poised to initiate RA signaling just before gastrulation begins, and manipulations of the RA pathway have been reported to show gastrulation defects. However, which aspects of gastrulation are affected have not been explored in detail. We previously showed that partial inhibition of RA biosynthesis causes a delay in the rostral migration of some of the earliest involuting cells, the leading edge mesendoderm (LEM) and the prechordal mesoderm (PCM). Here we identify several detrimental gastrulation defects resulting from inhibiting RA biosynthesis by three different treatments. RA reduction causes a delay in the progression through gastrulation as well as the rostral migration of the goosecoid-positive PCM cells. RA inhibition also hampered the elongation of explanted dorsal marginal zones, the compaction of the blastocoel, and the length of Brachet’s cleft, all of which indicate an effect on LEM/PCM migration. The cellular mechanisms underlying this deficit were shown to include a reduced deposition of fibronectin along Brachet’s cleft, the substrate for their migration, as well as impaired separation of the blastocoel roof and involuting mesoderm, which is important for the formation of Brachet’s cleft and successful LEM/PCM migration. We further show reduced non-canonical Wnt signaling activity and altered expression of genes in the Ephrin and PDGF signaling pathways, both of which are required for the rostral migration of the LEM/PCM, following RA reduction. Together, these experiments demonstrate that RA signaling performs a very early function critical for the progression of gastrulation morphogenetic movements.

show abstract

Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Retinoic Acid is Required for Normal Morphogenetic Movements During Gastrulation

Gur

Edri

Moody

et al. 2022

Front. Cell Dev. Biol.

Self Cite

View full text Add to dashboard Cite

show abstract

“…For example, across cichlid species egg size is linked with differences in maternal RNA deposition, especially in growth related genes (20) . In frogs, maternal RNA localization differs in species with different egg sizes (21,22) and RNA content changes with naturally occurring egg size differences within species (23) . When egg size is linked to life-history mode, it is unclear whether transcript abundance will change with egg size so that larger eggs receive a different amount of mRNA (quantitative change), or if completely different mRNAs are provided in conjunction with metabolic demands or new cellular functions (qualitative change).…”

Section: Introductionmentioning

confidence: 99%

Maternal patterns of inheritance alter transcript expression in eggs

Zakas

Harry

2022

Preprint

View full text Add to dashboard Cite

Modifications to early development can lead to evolutionary diversification. The early stages of development are under maternal control, as mothers produce eggs loaded with nutrients, proteins and mRNAs that direct early embryogenesis. Maternally provided mRNAs are the only expressed genes in initial stages of development and are known to be tightly regulated. Differences in maternal mRNA provisioning could lead to phenotypic changes in embryogenesis and ultimately evolutionary changes in development. However, the extent to which variation in maternal mRNA provisioning impacts ontogeny or life-history is unknown. Here, we use a species with dimorphic development— where females make eggs and larvae of different sizes and life-history modes—to investigate the extent of variation in maternal mRNA provisioning to the egg. We examine the effect of gene expression differences on subsequent generations of egg provisioning and determine the regulatory architecture underlying mRNA provisioning differences. We find that there is significant variation in gene expression across eggs of different development modes, and that both parent-of-origin and allele-specific effects contribute to mRNA expression differences. We also find that offspring of intraspecific crosses differentially provision their eggs based on their parents' cross direction. This effect of allelic expression based on parent-of-origin has not been previously demonstrated in reproductive traits like oogenesis.

show abstract

“…Studies in humans have shown the involvement of genetic variability in absorption and metabolism components in determining the status and bioavailability of vitamin A for RA biosynthesis (Borel and Desmarchelier, 2017). We have recently shown that gene expression levels can vary extensively between Xenopus laevis clutches (Leibovich et al, 2020). Also, a recent comparative study of the genetic variability between two Xenopus laevis strains revealed extensive genetic polymorphisms (Savova et al, 2017).…”

Section: Discussionmentioning

confidence: 99%

Retinoic acid fluctuation activates an uneven, direction-dependent network-wide robustness response in early embryogenesis

Parihar

Bendelac-Kapon

Gur

et al. 2020

Preprint

Self Cite

View full text Add to dashboard Cite

Retinoic acid (RA) is a central developmental signal whose perturbation results in teratogenic outcomes. We performed transient physiological RA signaling disturbances during embryogenesis followed by kinetic RNAseq and high-throughput qPCR analysis of the recovery. Unbiased comparative pattern analysis identified the RA network as a key differentially regulated module aimed at achieving RA signaling robustness. We analyzed this module using a principal curve-based approach determining clutch-wise variability, and organized the results into a robustness efficiency matrix comparing the shifts in RA feedback regulation and hox gene expression. We found that feedback autoregulation was sensitive to the direction of the RA perturbation: RA knock-down exhibited an upper response limit, whereas RA addition did not activate a feedback response below a threshold. These results suggest an asymmetric capacity for robust feedback control of RA signal during early development based on genetic polymorphisms, likely a significant contributor to the manifestation of developmental defects.

show abstract

Natural size variation among embryos leads to the corresponding scaling in gene expression

Cited by 14 publications

References 72 publications

Retinoic Acid is Required for Normal Morphogenetic Movements During Gastrulation

Retinoic Acid is Required for Normal Morphogenetic Movements During Gastrulation

Maternal patterns of inheritance alter transcript expression in eggs

Retinoic acid fluctuation activates an uneven, direction-dependent network-wide robustness response in early embryogenesis

Contact Info

Product

Resources

About