The Maternal-to-Zygotic Transition Targets Actin to Promote Robustness during Morphogenesis

Abstract

Robustness is a property built into biological systems to ensure stereotypical outcomes despite fluctuating inputs from gene dosage, biochemical noise, and the environment. During development, robustness safeguards embryos against structural and functional defects. Yet, our understanding of how robustness is achieved in embryos is limited. While much attention has been paid to the role of gene and signaling networks in promoting robust cell fate determination, little has been done to rigorously assay how mechanical processes like morphogenesis are designed to buffer against variable conditions. Here we show that the cell shape changes that drive morphogenesis can be made robust by mechanisms targeting the actin cytoskeleton. We identified two novel members of the Vinculin/α-Catenin Superfamily that work together to promote robustness during Drosophila cellularization, the dramatic tissue-building event that generates the primary epithelium of the embryo. We find that zygotically-expressed Serendipity-α (Sry-α) and maternally-loaded Spitting Image (Spt) share a redundant, actin-regulating activity during cellularization. Spt alone is sufficient for cellularization at an optimal temperature, but both Spt plus Sry-α are required at high temperature and when actin assembly is compromised by genetic perturbation. Our results offer a clear example of how the maternal and zygotic genomes interact to promote the robustness of early developmental events. Specifically, the Spt and Sry-α collaboration is informative when it comes to genes that show both a maternal and zygotic requirement during a given morphogenetic process. For the cellularization of Drosophilids, Sry-α and its expression profile may represent a genetic adaptive trait with the sole purpose of making this extreme event more reliable. Since all morphogenesis depends on cytoskeletal remodeling, both in embryos and adults, we suggest that robustness-promoting mechanisms aimed at actin could be effective at all life stages.

Building early-larval sexing systems for genetic control of the Australian sheep blow fly Lucilia cuprina using two constitutive promoters

“…Similarly, in D. melanogaster spt RNA is maternally provided 19 . DH3 and DH4 (carry a Lsspt-tTA transgene) females died mostly at the embryo stage under non-permissive conditions.…”

­Back-to-back mechanisms drive actomyosin ring closure during Drosophila embryo cleavage

“…For manipulation of maternal dosage of Cofilin and Pnut, 1/2cofilin and 1/2pnut embryos were collected from y 1 w*; P{FRT(w hs )}G13 P{A92}tsr 1 /CyO, P{sevRas1.V12}FK1 (FBst0009107) and cn 1 P{PZ}pnut 02502 /CyO; ry 506 (FBst0011194) mothers, respectively. This loss-of-function strategy was previously established for F-actin regulators that are maternally provided for cellularization (Zheng et al, 2013). For anillin maternal effect mutants, anillin HP /CyO males and anillin RS /CyO females were crossed to generate anillin HP/RS transheterozygous females, which were crossed with anillin HP /CyO males (Field et al, 2005).…”

Evolving Robust Gene Regulatory Networks

“…Therefore, the in-depth understanding of biological robustness has become the prerequisite to complete understanding of biological systems. Naturally, robustness has become the topic of choice to researchers working in a wide range of biological disciplines: from evolutionary biologists [ 1 – 3 ] to computational biologists [ 4 – 6 ], from geneticists [ 7 – 9 ] to immunologists [ 10 , 11 ], from ecologists [ 12 , 13 ] to cancer researchers [ 14 , 15 ]. Numerous studies, undertaken to uncover the features and mechanism of robustness in different biological processes, now enable us to envisage the outline of the bigger picture but many pieces of the puzzle are yet to be discovered to comprehend it.…”