ABSTRACT
Patterning of the vertebrate anteroposterior (AP) axis proceeds temporally from anterior to posterior. How dorsoventral (DV) axial patterning relates to AP temporal patterning is unknown. We examined the temporal activity of BMP signaling in patterning ventrolateral cell fates along the AP axis, using transgenes that rapidly turn "off" or "on" BMP signaling. We show that BMP signaling patterns rostral DV cell fates at the onset of gastrulation, whereas progressively more caudal DV cell fates are patterned at progressively later intervals during gastrulation. Increased BMP signal duration is not required to pattern more caudal DV cell fates; rather, distinct temporal intervals of signaling are required. This progressive action is regulated downstream of, or in parallel to, BMP signal transduction at the level of Smad1/5 phosphorylation. We propose that a temporal cue regulates a cell's competence to respond to BMP signaling, allowing the acquisition of a cell's DV and AP identity simultaneously.
Subject(s)
Body Patterning/physiology , Bone Morphogenetic Proteins/physiology , Vertebrates/embryology , Animals , Body Patterning/genetics , Bone Morphogenetic Proteins/genetics , Brain/embryology , Chick Embryo/physiology , Chickens , Embryo, Nonmammalian/physiology , Embryonic Development , In Situ Hybridization , Models, Biological , Phenotype , Signal TransductionABSTRACT
Maternal factors control development prior to the activation of the embryonic genome. In vertebrates, little is known about the molecular mechanisms by which maternal factors regulate embryonic development. To understand the processes controlled by maternal factors and identify key genes involved, we embarked on a maternal-effect mutant screen in the zebrafish. We identified 68 maternal-effect mutants. Here we describe 15 mutations in genes controlling processes prior to the midblastula transition, including egg development, blastodisc formation, embryonic polarity, initiation of cell cleavage, and cell division. These mutants exhibit phenotypes not previously observed in zygotic mutant screens. This collection of maternal-effect mutants provides the basis for a molecular genetic analysis of the maternal control of embryogenesis in vertebrates.
Subject(s)
Blastula/metabolism , Embryo, Nonmammalian/embryology , Gene Expression Regulation, Developmental/genetics , Mutation/genetics , Zebrafish/embryology , Zebrafish/genetics , Animals , Blastula/cytology , Cell Division/genetics , Cell Polarity/genetics , Chromosome Mapping , Embryo, Nonmammalian/cytology , Female , Infertility, Male/genetics , Male , Oocytes/cytology , Oocytes/metabolism , Sex Differentiation/genetics , Sex FactorsABSTRACT
Many maternal factors in the oocyte persist in the embryo. They are required to initiate zygotic transcription but also function beyond this stage, where they interact with zygotic gene products during embryonic development. In a four-generation screen in the zebrafish, we identified 47 maternal-effect and five paternal-effect mutants that manifest their phenotypes at the time of, or after, zygotic genome activation. We propagated a subset of 13 mutations that cause developmental arrest at the midblastula transition, defects in cell viability, embryonic morphogenesis, and establishment of the embryonic body plan. This diverse group of mutants, many not previously observed in vertebrates, demonstrates a substantial maternal contribution to the "zygotic" period of embryogenesis and a surprising degree of paternal control. These mutants provide powerful tools to dissect the maternal and paternal control of vertebrate embryogenesis.
