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Genomes of animals as different as sponges and humans show conservation of global architecture. Here we show that multiple genomic features including transposon diversity, developmental gene repertoire, physical gene order, and intron-exon organization are shattered in the tunicate Oikopleura, belonging to the sister group of vertebrates and retaining chordate morphology. Ancestral architecture of animal genomes can be deeply modified and may therefore be largely nonadaptive. This rapidly evolving animal lineage thus offers unique perspectives on the level of genome plasticity. It also illuminates issues as fundamental as the mechanisms of intron gain.

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Maternal information stored in particular regions of the egg cytoplasm has an important function in the determination of developmental fate during early animal development. Ascidians show mosaic development; such autonomous development has been taken as evidence that prelocalized ooplasmic factors specify tissue precursor cells during embryogenesis. Interest has been concentrated on the mechanisms underlying the formation of muscle cells in the tail, as yellow-coloured myoplasm in eggs is preferentially segregated into muscle-lineage blastomeres. Here we show that maternal messenger RNA of the macho-1 gene is a determinant of muscle fate in the ascidian Halocynthia roretzi. The macho-1 mRNA encodes a zinc-finger protein, and the mRNA is localized to the myoplasm of eggs. Depletion of the mRNA specifically resulted in the loss of primary muscle cells in the tail, as shown by the expression of muscle-specific molecular markers. The myoplasm of macho-1-deficient eggs lost its ability to promote muscle formation. Injection of synthesized macho-1 mRNA caused ectopic muscle formation in non-muscle-lineage cells. Our results indicate that macho-1 maybe both required and sufficient for specification of muscle fate, and that the mRNA is a genuine, localized muscle determinant.

Setting up future body axes is the first important event before and at the beginning of embryogenesis. The ascidian embryo is a classic model that has been used to gain insight into developmental processes for over a century. This review summarizes advances made in this decade in our understanding of the developmental processes involved in the specification of the embryonic axes and cell fates during early ascidian embryogenesis. Maternal factors, including mRNAs, are translocated to specific regions of the egg by cytoplasmic and cortical reorganization, so-called ooplasmic segregation, and specify the animal-vegetal axis and the one perpendicular to it, which is defined as the anteroposterior axis in ascidians. Some postplasmic/PEM RNAs that are anchored to cortical endoplasmic reticulum are brought to the future posterior pole of fertilized eggs, and play crucial roles in posterior development. Following specification of the animal-vegetal axis, nuclear localization of ␤-catenin takes place in the vegetal blastomeres; this occurrence is important for the acquisition of the vegetal character of the blastomeres in later development. Positioning of these maternal factors lead to subsequent cell interactions and zygotic gene expression responsible for axis establishment and for cell fate specification. We describe how endoderm blastomeres in the vegetal pole region emanate inductive signals mainly attributable to fibroblast growth factor. Marginal blastomeres next to endoderm blastomeres respond differently in ways that are determined by intrinsic competence factors. Expression patterns of developmentally important genes, including key transcription factors of each tissue type, are also summarized.