Nodal signaling regulates specification of ascidian peripheral neurons through control of the BMP signal

Abstract

The neural crest and neurogenic placodes are thought to be a vertebrate innovation that gives rise to much of the peripheral nervous system (PNS). Despite their importance for understanding chordate evolution and vertebrate origins, little is known about the evolutionary origin of these structures. Here, we investigated the mechanisms underlying the development of ascidian trunk epidermal sensory neurons (ESNs), which are thought to function as mechanosensory neurons in the rostral-dorsal trunk epidermis. We found that trunk ESNs are derived from the anterior and lateral neural plate border, as is the case in the vertebrate PNS. Pharmacological experiments indicated that intermediate levels of bone morphogenetic protein (BMP) signal induce formation of ESNs from anterior ectodermal cells. Gene knockdown experiments demonstrated that HrBMPa (60A-subclass BMP) and HrBMPb (dpp-subclass BMP) act to induce trunk ESNs at the tailbud stage and that anterior trunk ESN specification requires Chordin-mediated antagonism of the BMP signal, but posterior trunk ESN specification does not. We also found that Nodal functions as a neural plate border inducer in ascidians. Nodal signaling regulates expression of HrBMPs and HrChordin in the lateral neural plate, and consequently specifies trunk ESNs. Collectively, these findings show that BMP signaling that is regulated spatiotemporally by Nodal signaling is required for trunk ESN specification, which clearly differs from the BMP gradient model proposed for vertebrate neural induction.

Nodal–Activin pathway is a conserved neural induction signal in chordates

“…Indeed, although BMP signal inhibition is necessary for neural induction in all vertebrates 3, BMP plays no role in this process in tunicates 12 and BMP inhibition appears insufficient to trigger neural induction in chick and amphioxus although it may be required to maintain the anterior neural territory in both species 9. The situation is different in the urochordate Ciona , where FGF is the main neural inducer13, whereas Nodal is required for posterior neural tube formation and for the specification of trunk epidermal sensory neurons 28–30. Concerning vertebrates, Nodal activity was shown to be required to prevent precocious neural differentiation in the mouse pluripotent epiblast 31.…”

Neurogenesis in sea urchin embryos and the diversity of deuterostome neurogenic mechanisms

“…However, a role for FGF in initiating neurogenesis in other metazoans suggests that this is a conserved function (Rentzsch et al, 2008;Sinigaglia et al, 2013). In ascidians, FGF is essential for the specification of peripheral neurons that are arrayed laterally along the tail, a process that is initiated during cleavage (Ohtsuka et al, 2014). In vertebrates, FGF has an essential role in the specification of sensory placodes (Ariza-Cosano et al, 2015;Kengaku and Okamoto, 1993).…”

Formation of adult organs through metamorphosis in ascidians

“…15,16 More recently, a lipophilic orange-red fluorescent dye, DiI, has also been used for this purpose in Halocynthia and Ciona. 18,19 This dye can be absorbed into the plasma membrane upon attaching its drop onto the membrane, and thus it is not necessary to inject the dye into cells for labeling.…”