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

BACKGROUND: 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). 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. 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. RESULTS: 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. CONCLUSIONS: 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.

A negative-feedback loop maintains optimal chemokine concentrations for directional cell migration.

Chemoattractant gradients frequently guide migrating cells. To achieve the most directional signal, such gradients should be maintained with concentrations around the dissociation constant (Kd)1-6 of the chemoreceptor. Whether this actually occurs in animals is unknown. Here we investigate whether a moving tissue, the zebrafish posterior lateral line primordium, buffers its attractant in this concentration range to achieve robust migration. We find that the Cxcl12 (also known as Sdf1) attractant gradient ranges from 0 to 12 nM, values similar to the 3.4 nM Kd of its receptor Cxcr4. When we increase the Kd of Cxcl12 for Cxcr4, primordium migration is less directional. Furthermore, a negative-feedback loop between Cxcl12 and its clearance receptor Ackr3 (also known as Cxcr7) regulates the Cxcl12 concentrations. Breaking this negative feedback by blocking the phosphorylation of the cytoplasmic tail of Ackr3 also results in less directional primordium migration. Thus, directed migration of the primordium is dependent on a close match between the Cxcl12 concentration and the Kd of Cxcl12 for Cxcr4, which is maintained by buffering of the chemokine levels. Quantitative modelling confirms the plausibility of this mechanism. We anticipate that buffering of attractant concentration is a general mechanism for ensuring robust cell migration.

Effect of Larval Nutrition on Maternal mRNA Contribution to the Drosophila Egg.

Embryonic development begins under the control of maternal gene products, mRNAs and proteins that the mother deposits into the egg; the zygotic genome is activated some time later. Maternal control of early development is conserved across metazoans. Gene products contributed by mothers are critical to many early developmental processes, and set up trajectories for the rest of development. Maternal deposition of these factors is an often-overlooked aspect of parental investment. If the mother experiences challenging environmental conditions, such as poor nutrition, previous studies in Drosophila melanogaster have demonstrated a plastic response wherein these mothers may produce larger eggs to buffer the offspring against the same difficult environment. This additional investment can produce offspring that are more fit in the challenging environment. With this study, we ask whether D. melanogaster mothers who experience poor nutrition during their own development change their gene product contribution to the egg. We perform mRNA-Seq on eggs at a stage where all mRNAs are maternally derived, from mothers with different degrees of nutritional limitation. We find that nutritional limitation produces similar transcript changes at all degrees of limitation tested. Genes that have lower transcript abundance in nutritionally limited mothers are those involved in translation, which is likely one of the most energetically costly processes occurring in the early embryo. We find an increase in transcripts for transport and localization of macromolecules, and for the electron transport chain. The eggs produced by nutrition-limited mothers show a plastic response in mRNA deposition, which may better prepare the future embryo for development in a nutrition-limited environment.