Long-distance cell migration during larval development in the appendicularian, Oikopleura dioica

Abstract

The appendicularian, Oikopleura dioica, is a planktonic chordate. Its simple and transparent body, invariant cell lineages and short life cycle of 5 days make it a promising model organism for studies of chordate development. Here we describe the cell migration that occurs during development of the O. dioica larva. Using time-lapse imaging facilitated by florescent labeling of cells, three cell populations exhibiting long-distance migration were identified and characterized. These included (i) a multinucleated oral gland precursor that migrates anteriorly within the trunk region and eventually separates into the left and right sides, (ii) endodermal strand cells that are collectively retracted from the tail into the trunk in a tractor movement, and (iii) two subchordal cell precursors that individually migrate out from the trunk to the tip of the tail. The migration of subchordal cell precursors starts when all of the endodermal strand cells enter the trunk, and follows the same path but in a direction opposite to that of the latter. Labeling of these cells with a photoconvertible fluorescent protein, Kaede, demonstrated that the endodermal strand cells and subchordal cell precursors have distinct origins and eventual fates. Surgical removal of the trunk from the tail demonstrated that the endodermal strand cells do not require the trunk for migration, and that the subchordal cell precursors would be attracted by the distal part of the tail. This well-defined, invariant and traceable long-distance cell migration provides a unique experimental system for exploring the mechanisms of versatile cell migration in this simple organism with a chordate body plan.

3D reconstruction of structures of hatched larva and young juvenile of the larvacean Oikopleura dioica using SBF-SEM

“…The amount of DNA in single nuclei in adults increases by 1248-fold after endoduplication 31 . The formation of the oral gland during larval development is a peculiar process 39 . An oral gland precursor cell has four nuclei and migrates from the posterior region to the anterior region of the trunk.…”

“…In addition, cell lineages during embryogenesis has been known to be invariant 6 – 8 , as well as spatial arrangement of epidermis cells in the oikoplastic epidermis 2 . During larval development, cell numbers and behaviors are stereotyped for cells that show long distance migration 39 and cells that are involved in formation of the oral region 3 . Therefore, even the data from a single animal would be valuable for future studies.…”

Regulation and evolution of muscle development in tunicates

“…While this inversion is crucial for the sessile ascidian to function as an adult, there is seemingly no reason for such an epidermal rotation in the pelagic appendicularians. Similarly, the intestine in O. dioica develops from a straight endodermal “strand” that extends down the length of the developing tail but later forms a U-shaped tube back toward the head [173, 304]. This is highly evocative of intestinal development in ascidians, in which endodermal strand cells must migrate into the head as the larval tail is reabsorbed, and form a U-shaped tube that is uniquely adapted to the sessile ascidian body plan [168, 230].…”

A genome database for a Japanese population of the larvacean Oikopleura dioica

“…Here, we determined the genome sequence of Japanese O. dioica. Using the same population, we have developed tools for molecular, cellular, and genetic techniques, including gene knockdown methods (Omotezako et al, 2013(Omotezako et al, , 2015(Omotezako et al, , 2017, fluorescent live imaging of larvae (Kishi et al, 2014(Kishi et al, , 2017, and maternal and zygotic transcriptomes of the eggs and larvae (Wang et al, 2015).…”

“…These have been used to gain insights into cell migration (Kishi et al, 2014), patterning of epidermal cells (Kishi et al, 2017), left-right patterning (Onuma et al, 2020) and meiotic arrest of the unfertilized egg (Matsuo et al, 2020). Moreover, transcriptome-wide comparison has implied a high level of sequence variation between the Japanese and Norwegian O. dioica (Wang et al, 2015): only 91.0% and 94.8% of exon sequences were conserved at nucleotide and amino acid levels on average, respectively.…”