Bilaterally Asymmetric Helical Myofibrils in Ascidian Tadpole Larvae.

Koichi Matsuo,Akihisa Takeuchi,Kohji Hotta,Koh Hashimoto,Yanlin Wu,Ryota Tamura,Mayu Okada,Atsuo Nishino,Atsushi Momose,Hidekazu Takano

doi:10.3389/fcell.2021.800455

Abstract

The locomotor system is highly bilateral at the macroscopic level. Homochirality of biological molecules is fully compatible with the bilateral body. However, whether and how single-handed cells contribute to the bilateral locomotor system is obscure. Here, exploiting the small number of cells in the swimming tadpole larva of the ascidian Ciona, we analyzed morphology of the tail at cellular and subcellular scales. Quantitative phase-contrast X-ray tomographic microscopy revealed a high-density midline structure ventral to the notochord in the tail. Muscle cell nuclei on each side of the notochord were roughly bilaterally aligned. However, fluorescence microscopy detected left-right asymmetry of myofibril inclination relative to the longitudinal axis of the tail. Zernike phase-contrast X-ray tomographic microscopy revealed the presence of left-handed helices of myofibrils in muscle cells on both sides. Therefore, the locomotor system of ascidian larvae harbors symmetry-breaking left-handed helical cells, while maintaining bilaterally symmetrical cell alignment. These results suggest that bilateral animals can override cellular homochirality to generate the bilateral locomotor systems at the supracellular scale.

Highlights

Morphological bilateral symmetry is crucial for movement and locomotion
In the absence of osmium, we reproducibly observed high density of the otolith, as well as of the ventral structure in midsagittal sections (Figure 1E) and vertical cross-sections (Figure 1F), while high density of the anterior notochord, which was consistently observed in osmium-fixed larvae, was not apparent in unstained larvae
The locomotor system of the Ciona tail is characterized by bilateral muscles seen on both left and right sides inducing bilaterally symmetric and asymmetric flexion (Nishino et al, 2011; Rudolf et al, 2019)

Summary

Introduction

Morphological bilateral symmetry is crucial for movement and locomotion. The morphology of vertebrate musculoskeletal and nervous systems exhibits highly bilateral symmetry, and lateralization of movement develops to allow coordinated unilateral or alternate movement in mammals including humans (Welniarz et al, 2015). The swimming tadpole larva of ascidians is composed of a trunk ( referred to as the “head”) and tail. A century ago, analyzing locomotion of the swimming tadpole larva of the ascidians Amaroucium and Botryllus, Grave reported clockwise rotational swimming of the larva around its long axis in circular or curved paths and recognized lateral asymmetry of the body and the oblique orientation of the muscle fibrillae (Grave, 1920). Ciona larvae display swimming paths characterized as spiral, curved and random (Sakurai et al, 2004) or

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Conclusion