Orchestration of the distinct morphogenetic movements in different tissues drives tail regression during ascidian metamorphosis.

Metamorphosis is the dramatic conversion of an animal body from larva to adult. In ascidians, tadpole-shaped, swimming larvae become sessile juveniles by losing their tail during metamorphosis. This study investigated the cellular and molecular mechanisms underlying this metamorphic event called tail regression, in the model ascidian Ciona. The ascidian tail consists of internal organs such as muscle, notochord, nerve cord, and the outer epidermal layer surrounding them. We found that the epidermis and internal organs show different regression strategies. Epidermal cells are shortened along the anterior-posterior axis and gather at the posterior region. The epidermal mass is then invaginated into the trunk by apical constriction. The internal tissues, by contrast, enter into the trunk by forming coils. During coiling, notches are introduced into the muscle cells, which likely reduces their rigidness to promote coiling. Actin filament is the major component necessary for the regression events in both the epidermis and internal tissues. The shortening and invagination of the epidermis depend on the phosphorylation of the myosin regulatory light chain (mrlc) regulated by rho-kinase (ROCK). The coiling of internal tissues does not require ROCK-dependent phosphorylation of mrlc, and they can complete coiling without epidermis, although epidermis can facilitate the coiling of internal tissues. We conclude that tail regression in ascidians consists of active morphogenetic movements in which each tissue's independent mechanism is orchestrated with the others to complete this event within the available time window.

GABA-Induced GnRH Release Triggers Chordate Metamorphosis.

Metamorphosis, a widespread life history strategy in metazoans, allows dispersal and use of different ecological niches through a dramatic body change from a larval stage [1, 2]. Despite its conservation and importance, the molecular mechanisms underlying its initiation and progression have been characterized in only a few animal models. In this study, through pharmacological and gene functional analyses, we identified neurotransmitters responsible for metamorphosis of the ascidian Ciona. Ciona metamorphosis converts swimming tadpole larvae into vase-like, sessile adults. Here, we show that the neurotransmitter GABA is a key regulator of metamorphosis. We found that gonadotropin-releasing hormone (GnRH) is a downstream neuropeptide of GABA. Although GABA is generally thought of as an inhibitory neurotransmitter, we found that it positively regulates secretion of GnRH through the metabotropic GABA receptor during Ciona metamorphosis. GnRH is necessary for reproductive maturation in vertebrates, and GABA is an important excitatory regulator of GnRH in the hypothalamus during puberty [3, 4]. Our findings reveal another role of the GABA-GnRH axis in the regulation of post-embryonic development in chordates.

Time course for tail regression during metamorphosis of the ascidian Ciona intestinalis.

In most ascidians, the tadpole-like swimming larvae dramatically change their body-plans during metamorphosis and develop into sessile adults. The mechanisms of ascidian metamorphosis have been researched and debated for many years. Until now information on the detailed time course of the initiation and completion of each metamorphic event has not been described. One dramatic and important event in ascidian metamorphosis is tail regression, in which ascidian larvae lose their tails to adjust themselves to sessile life. In the present study, we measured the time associated with tail regression in the ascidian Ciona intestinalis. Larvae are thought to acquire competency for each metamorphic event in certain developmental periods. We show that the timing with which the competence for tail regression is acquired is determined by the time since hatching, and this timing is not affected by the timing of post-hatching events such as adhesion. Because larvae need to adhere to substrates with their papillae to induce tail regression, we measured the duration for which larvae need to remain adhered in order to initiate tail regression and the time needed for the tail to regress. Larvae acquire the ability to adhere to substrates before they acquire tail regression competence. We found that when larvae adhered before they acquired tail regression competence, they were able to remember the experience of adhesion until they acquired the ability to undergo tail regression. The time course of the events associated with tail regression provides a valuable reference, upon which the cellular and molecular mechanisms of ascidian metamorphosis can be elucidated.