Early zebrafish development: it's in the maternal genes

Abstract

The earliest stages of embryonic development in all animals examined rely on maternal gene products that are generated during oogenesis and supplied to the egg. The period of maternal control of embryonic development varies among animals according to the onset of zygotic transcription and the persistence of maternal gene products. This maternal regulation has been little studied in vertebrates, owing to the difficulty in manipulating maternal gene function and lack of basic molecular information. However, recent maternal-effect screens in the zebrafish have generated more than 40 unique mutants that are providing new molecular entry points to the maternal control of early vertebrate development. Here we discuss recent studies of 12 zebrafish mutant genes that illuminate the maternal molecular controls on embryonic development, including advances in the regulation of animal-vegetal polarity, egg activation, cleavage development, body plan formation, tissue morphogenesis, microRNA function and germ cell development.

Figure 1. Maternal-effect mutant genes in zebrafish disrupt development at distinct Stages

Mutants discussed here are indicated in red. acytokinesis[11], atomos[9], aura[9], barrette[9], bo peep[9], bedazzled[10], blistered[10], claustro[9], 2004 #2}, cobblestone[9], emulsion [8], golden gate[9], indivisible[8], irreducible[8], jumpstart[8], kwai[9], misson impossible[9], nebel[9], over easy[8], poky[10], pollywog[10], pug[10], slow[10], ruehrei[8], souffle[8], screeching halt[10], sunny side up[8], under repair[9], waldo[9], weeble[9].

Figure 2. mRNA localization during oocyte development

During stage I of oogenesis buc, nanos, vasa, and dazl transcripts localize to the Balibani body (Bb, pink), while cyclinB begins to be localized to the animal pole. By stage II of oogenesis the Bb has disassembled, leaving buc, vasa, and dazl mRNAs at the vegetal cortex, whereas nanos becomes unlocalized, and pou2 becomes localized to the animal pole. Note vasa has a broad vegetal cortical domain at stage II. By stage III bruno-like and mago nashi become vegetally localized (late pathway); now buc, and Vg1 are localized to the animal pole and vasa is localized radially at the cortex. Animal (An) pole is to top and vegetal (Ve) to bottom.

Figure 3. The role of BMP and early and late Wnt signaling in dorsoventral patterning

A) Maternal Pou2 induces early zygotic bmp ligand expression. bmp expression is initially present throughout the blastoderm (grey). An early maternal Wnt signal from the yolk cell promotes future dorsal organizer (DO) formation. B) By the late blastula stage (50% epiboly), a BMP activity gradient (highest ventrally (black)) is established that promotes ventral fates. At this stage Wnt 8 signaling opposes dorsal fate specification ventrally. Ventral is positioned to the left and dorsal to the right.

Figure 4. miRNA regulation of germ line development

In the soma miR-430 inhibits expression of germ line specific genes (GLSGs). In the germ line Dnd blocks miR-430 - mediated repression of GLSGs. Note that an unidentified factor X is required in the soma to silence GLSGs that are not regulated by miR-430. Soma shown in gray; germ line in purple.