Pleiotropic Functions of FoxN1: Regulating Different Target Genes during Embryogenesis and Nymph Molting in the Brown Planthopper

Int J Mol Sci. 2020 Jun 13;21(12):4222. doi: 10.3390/ijms21124222.

Abstract

FoxN1 gene belongs to the forkhead box gene family that comprises a diverse group of "winged helix" transcription factors that have been implicated in a variety of biochemical and cellular processes. In the brown planthopper (BPH), FoxN1 is highly expressed in the ovaries and newly laid eggs, where it acted as an indispensable gene through its molecular targets to regulate early embryonic development. Moreover, the results of the RNAi experiments indicated that Nilaparvata lugens FoxN1 (NlFoxN1) exhibited pleiotropism: they not only affected the embryogenesis, but also played an important role in molting. RNA-seq and RNAi were further used to reveal potential target genes of NlFoxN1 in different stages. In the eggs, ten downregulated genes were defined as potential target genes of NlFoxN1 because of the similar expression patterns and functions with NlFoxN1. Knockdown of NlFoxN1 or any of these genes prevented the development of the eggs, resulting in a zero hatchability. In the nymphs, NlFoxN1 regulated the expression of a keratin gene, type I cytoskeletal keratin 9 (NlKrt9), to participate in the formation of an intermediate filament framework. Depletion of NlFoxN1 or NlKrt9 in nymphs, BPHs failed to shed their old cuticle during nymph-to-nymph or nymph-to-adult molting and the mortality was almost 100%. Altogether, the pleiotropic roles of NlFoxN1 during embryogenesis and nymph molting were supported by the ability to coordinate the temporal and spatial gene expression of their target genes.

Keywords: FoxN1; brown planthopper; embryogenesis; keratin gene; pleiotropism.

MeSH terms

  • Animals
  • Embryonic Development
  • Female
  • Forkhead Transcription Factors / genetics*
  • Forkhead Transcription Factors / metabolism*
  • Gene Expression Profiling / veterinary*
  • Gene Expression Regulation, Developmental
  • Hemiptera / metabolism
  • Hemiptera / physiology*
  • Keratin-9 / genetics*
  • Molting
  • Nymph / physiology
  • Ovary / metabolism
  • RNA Interference
  • Sequence Analysis, RNA / veterinary

Substances

  • Forkhead Transcription Factors
  • Keratin-9
  • Whn protein