A chordate species lackingNodalutilizes calcium oscillation andBmpfor left–right patterning

Abstract

Larvaceans are chordates with a tadpole-like morphology. In contrast to most chordates of which early embryonic morphology is bilaterally symmetric and the left–right (L–R) axis is specified by the Nodal pathway later on, invariant L–R asymmetry emerges in four-cell embryos of larvaceans. The asymmetric cell arrangements exist through development of the tailbud. The tail thus twists 90° in a counterclockwise direction relative to the trunk, and the tail nerve cord localizes on the left side. Here, we demonstrate that larvacean embryos have nonconventional L–R asymmetries: 1) L- and R-cells of the two-cell embryo had remarkably asymmetric cell fates; 2) Ca2+ oscillation occurred through embryogenesis; 3) Nodal, an evolutionarily conserved left-determining gene, was absent in the genome; and 4) bone morphogenetic protein gene (Bmp) homolog Bmp.a showed right-sided expression in the tailbud and larvae. We also showed that Ca2+ oscillation is required for Bmp.a expression, and that BMP signaling suppresses ectopic expression of neural genes. These results indicate that there is a chordate species lacking Nodal that utilizes Ca2+ oscillation and Bmp.a for embryonic L–R patterning. The right-side Bmp.a expression may have arisen via cooption of conventional BMP signaling in order to restrict neural gene expression on the left side.

Massive Gene Loss and Function Shuffling in Appendicularians Stretch the Boundaries of Chordate Wnt Family Evolution

“…From early hatchling to mid hatchling stages, Odi_Wnt10 also labeled a single cell posterior to the end of the notochord (Figures 2P,Q green asterisk). This position of this conspicuous cell could correspond with an α-tubulin positive cell described during the characterization of the nervous system in O. diocia (Søviknes et al, 2007), although the ontogenic nature of this cell needs further investigation (Onuma et al, 2020).…”

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

“…Second, percentages of sequence similarity and gap sequences of exons, introns and intergenic regions were estimated for three genes, Brachury, Bmp.a, and Pax6. These genes have been identified as plausible orthologous genes in both Japanese and Norwegian O. dioica (Omotezako et al, 2013;Danks et al, 2013;Onuma et al, 2020). Their gene IDs are summarized in Table 1.…”

“…We thus adopted the OSKA2016 as the best genome assembly for Japanese O. dioica. It is reasonable that less than 90% of BUSCO was recovered, because O. dioica is shown to have the smallest and most highly rearranged genome amongst non-parasitic metazoans (Seo et al, 2001;Denoeud et al, 2010), and often lacks evolutionarily conserved genes, such as those for retinoic acid signal (Martí-Solans et al, 2016), Nodal signal (Onuma et al, 2020), and the non-homologous DNA end-joining pathway (Deng et al, 2018).…”

“…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.…”

Statistical Validation Verifies That Enantiomorphic States of Chiral Cells Are Determinant Dictating the Left- or Right-Handed Direction of the Hindgut Rotation in Drosophila

“…Cell chirality contributes to LR-asymmetric development in several organs in Drosophila, suggesting that it plays general roles in the LR-asymmetric development of this species [20,[30][31][32]. Cell chirality has been observed not only in snails, nematodes, and Drosophila, but also in Chordata, such as Larvaceans and chickens, and cell chirality is thought to be involved in these species' LR-asymmetric development as well [33,34]. In addition to cell chirality observed in vivo during development, cultured cells from diverse species, from Dictyostelium to humans, demonstrate intrinsic chirality in their structure and movement [35][36][37][38][39].…”