Genetical control of 2D pattern and depth of the primordial furrow that prefigures 3D shape of the rhinoceros beetle horn

Haruhiko Adachi,Teruyuki Niimi,Keisuke Matsuda,Shigeru Kondo,Hiroki Gotoh

doi:10.1038/s41598-020-75709-y

Haruhiko Adachi, Teruyuki Niimi + Show 3 more

Open Access

https://doi.org/10.1038/s41598-020-75709-y

Copy DOI

Abstract

The head horn of the Asian rhinoceros beetle develops as an extensively folded primordium before unfurling into its final 3D shape at the pupal molt. The information of the final 3D structure of the beetle horn is prefigured in the folding pattern of the developing primordium. However, the developmental mechanism underlying epithelial folding of the primordium is unknown. In this study, we addressed this gap in our understanding of the developmental patterning of the 3D horn shape of beetles by focusing on the formation of furrows at the surface of the primordium that become the bifurcated 3D shape of the horn. By gene knockdown analysis via RNAi, we found that knockdown of the gene Notch disturbed overall horn primordial furrow depth without affecting the 2D furrow pattern. In contrast, knockdown of CyclinE altered 2D horn primordial furrow pattern without affecting furrow depth. Our results show how the depth and 2D pattern of primordial surface furrows are regulated at least partially independently during beetle horn development, and how both can alter the final 3D shape of the horn.

Highlights

The head horn of the Asian rhinoceros beetle develops as an extensively folded primordium before unfurling into its final 3D shape at the pupal molt
The primordium is unfurled to form its final 3D shape using fluid pressure from hemolymph, much like blowing up a balloon. This transformation from a folded primordium to a fully extended horn does not require any living cell a ctivities[6]. This indicates that the information for the final 3D structure of the beetle horn is patterned within the primordium by this time
We investigated how the macro structure and micro furrows of the horn primordia contributed to variation in the size of the tip region and whether these parameters fluctuated simultaneously or independently

Summary

Introduction

The head horn of the Asian rhinoceros beetle develops as an extensively folded primordium before unfurling into its final 3D shape at the pupal molt. During the final larval molt of holometabolous insects this feat is especially complicated, since the newly forming cuticle may have a shape that differs markedly from the prior one, including entirely new structures not present in larvae such as wings, genitalia, and secondary sexual structures like h orns[4,5]. Packing these new structures within the confined space of a smaller, larval cuticle is accomplished through precise patterns of cuticular furrows, or folds. We screened genes that produced RNAi-induced abnormal head horn phenotypes to find genes which affect the primordial parameter(s) accounting for final horn shape

Objectives

Methods

Results

Conclusion