Cuticle Protein LmACP19 Is Required for the Stability of Epidermal Cells in Wing Development and Morphogenesis of Locusta migratoria.

Xiaoming Zhao,Xin Gou,Ti Shao,Jianzhen Zhang,Weimin Liu,Jing Zhang,Yazhi Su

doi:10.3390/ijms23063106

Abstract

Insect wing consists of a double layer of epidermal cells that produce and secrete the dorsal and ventral cuticular components. It is important for the stability of epidermal cells during wing development and morphogenesis, but its specific gene expression and physiological function during this process remain unclear. In our previous work, a wing cuticle protein gene LmACP19 was identified in Locusta migratoria based on transcriptomic data. Here, we report on its roles in wing development and morphogenesis. LmACP19 encodes a chitin-binding protein belonging to RR-2 subfamily of CPR family, which is highly homologous to CP19-like proteins in other insect species. RT-qPCR analysis revealed that LmACP19 is highly expressed in wing pads of fifth-instar nymphs, and its encoded protein is located in two layers of epidermal cells but not in the cuticle. Suppression of LmACP19 by RNA interference led to abnormal wing pad and wing morphogenesis with curved, unclosed, and wrinkled phenotypes during nymph-to-nymph and nymph-to-adult transition, respectively. Furthermore, deficiency of LmACP19 affected arrangement of epidermal cells, resulting in apoptosis. Our results indicate that LmACP19 is indispensable for wing development and normal morphological structure by maintaining the stability of epidermal cells during L. migratoria molting.

Highlights

The exoskeleton of insects is formed by layered cuticles that mainly consist of chitin and associated proteins, which are produced by epidermal cells
Based on our previous comparative transcriptomics [17,19], two wing cuticle protein genes (LmACP7 and LmACP19) were identified, which were highly expressed in preecdysis (Figure 1A–A0 )
We further explore the function of LmACP19 during the development of locust wing

Summary

Introduction

Accepted: 11 March 2022Insects are the largest class of the phylum Arthropoda, which are characterized by their exoskeleton structure, segmented body, and paired and jointed appendages. The exoskeleton of insects is formed by layered cuticles that mainly consist of chitin and associated proteins, which are produced by epidermal cells. Insect cuticle is composed of three functionally distinct horizontal layers, including the outermost waterproof envelope, the middle protein-enriched epicuticle, and the innermost chitinous procuticle that contacts the apical plasma membrane of epidermal cells [1]. The exocuticle is formed before insect ecdysis, whereas the endocuticle begins to deposit after ecdysis and ends just before the molting [2]. Because the nongrowth of cuticle restricts the growth and development of insects, the cuticle must be periodically replaced and remodeled during molting. The epidermal cells play a crucial role in the molting process, which produce and release a variety of enzymes that degrade the endocuticle of old cuticle, and synthesize a new cuticle [3]

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