An Overview of Embryogenesis: External Morphology and Transcriptome Profiling in the Hemipteran Insect Nilaparvata lugens

Xiao-Bin Fan,Wen-Qing Zhang,Wan-Xue Li,Dan Li,Rui Pang,Abhishek Ojha

doi:10.3389/fphys.2020.00106

Abstract

During embryogenesis of insects, the morphological and transcriptional changes are important signatures to obtain a better understanding of insect patterning and evolution. The brown planthopper Nilaparvata lugens is a serious insect pest of rice plants, but its embryogenesis has not uncovered. Here, we described embryonic development process of the pest and found it belongs to an intermediate-germ mode. The RNA-seq data from different times (6, 30, 96, and 150 h, after egg laying) of embryogenesis were then analyzed, and a total of 10,895 genes were determined as differentially expressed genes (DEGs) based on pairwise comparisons. Afterward, 1,898 genes, differentially expressed in at least two comparisons of adjacent embryonic stages were divided into 10 clusters using K means cluster analysis (KMCA). Eight-gene modules were established using a weighted gene co-expression network analysis (WGCNA). Gene expression patterns in the different embryonic stages were identified by combining the functional enrichments of the stage-specific clusters and modules, which displayed the expression level and reprogramming of multiple developmental genes during embryogenesis. The “hub” genes at each embryonic stage with possible crucial roles were identified. Notably, we found a “center” set of genes that were related to overall membrane functions and might play important roles in the embryogenesis process. After parental RNAi of the MSTRG.3372, the hub gene, the embryo was observed as abnormal. Furthermore, some homologous genes in classic embryonic development processes and signaling pathways were also involved in embryogenesis of this insect. An improved comprehensive finding of embryogenesis within the N. lugens reveals better information on genetic and genomic studies of embryonic development and might be a potential target for RNAi-based control of this insect pest.

Highlights

During embryonic development, the beginning of the life cycle, embryogenesis is established with different development stages such as zygote formation, morula formation, blastoderm formation, germ band formation, elongation, segmentation, appendage formation, and dorsal closure (Davis and Patel, 2002)
Gene regulatory networks (GRNs) associated with transcription factors (TFs) in each embryonic stage were conducted following the two steps: first, we focused on each module that was highly specific in some embryonic stage with gene ontology enrichment analysis (Supplementary Table S4), which emphasized key biological processes in different embryonic stages and was consistent with the previous analysis using K-means clustering (Figure 4B and Supplementary Table S2), different algorithms were used
We noticed the rate of change in the length/width decreased in the mid-embryogenesis (Figure 2D), existing in the intermediate germ insect, G. bimaculatus (Donoughe and Extavour, 2016) and we speculated it maybe due to katatrepsis, that occurred in this phase

Summary

Introduction

The beginning of the life cycle, embryogenesis is established with different development stages such as zygote formation, morula formation, blastoderm formation, germ band formation, elongation, segmentation, appendage formation, and dorsal closure (Davis and Patel, 2002). Many different embryogenesis characteristics exist among these three modes, including several major aspects: (1) oogenesis types (Lynch and Roth, 2011); (2) the size of the germ anlage relative to the length of entire egg (Davis and Patel, 2002); (3) metamorphosis; (4) blastokinesis; and (5) the order of segment specification. The vast majority of insects, such as Lepidopterans (e.g., Bombyx mori, Manduca sexta), Coleoptera (e.g., Tribolium castaneum) and Orthopterans (e.g., Gryllus bimaculatus), are short or intermediate germ insects, which represents an ancestral type of insect embryogenesis (Davis and Patel, 2002; Liu and Kaufman, 2005; Mito et al, 2011)

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Discussion

Conclusion