The histone deacetylase NlHDAC1 regulates both female and male fertility in the brown planthopper, Nilaparvata lugens.

Jin-Li Zhang,Sheng-Jie Fu,Xiao-Bo Yuan,Wen-Hua Xue,Hai-Jun Xu,Nan Xu,Chuan-Xi Zhang,Hao-Hao Chen,Sun-Jie Chen

doi:10.1098/rsob.180158

Abstract

Histone acetylation is a specific type of chromatin modification that serves as a key regulatory mechanism for many cellular processes in mammals. However, little is known about its biological function in invertebrates. Here, we identified 12 members of histone deacetylases (NlHDACs) in the brown planthopper (BPH), Nilaparvata lugens. RNAi-mediated silencing assay showed that NlHdac1, NlHdac3 and NlHdac4 played critical roles in female fertility via regulating ovary maturation or ovipositor development. Silencing of NlHdac1 substantially increased acetylation level of histones H3 and H4 in ovaries, indicating NlHDAC1 is the main histone deacetylase in ovaries of BPH. RNA sequencing (RNA-seq) analysis showed that knockdown of NlHdac1 impaired ovary development via multiple signalling pathways including the TOR pathway. Acoustic recording showed that males with NlHdac1 knockdown failed to make courtship songs, and thus were unacceptable to wild-type females, resulting in unfertilized eggs. Competition mating assay showed that wild-type females overwhelmingly preferred to mate with control males over NlHdac1-knockdown males. These findings improve our understanding of reproductive strategies controlled by HDACs in insects and provide a potential target for pest control.

Highlights

Histone acetylation is a specific type of chromatin modification that serves as a key regulatory mechanism for many cellular processes including DNA replication and regulation of gene expression [1,2,3,4,5,6]
We showed that males with NlHdac1 knockdown failed to make courtship songs and accomplish copulation, suggesting that NlHdac1 plays an essential role in courtship and mating success of brown planthopper (BPH) males
A phylogenetic analysis based on 70 histone deacetylases (HDACs) orthologues from 19 species suggested that six NlHDACs in BPH were classified into three classes: NlHDAC1 and NlHDAC3 in class I, NlHDAC4 and NlHDAC6 in class II, and NlHDAC11 and NlHDAC11_l in class IV

Summary

Introduction

Histone acetylation is a specific type of chromatin modification that serves as a key regulatory mechanism for many cellular processes including DNA replication and regulation of gene expression [1,2,3,4,5,6]. The steady state of histone acetylation is determined by the antagonistic activities of histone acetyltransferases (HATs) and histone deacetylases (HDACs) [7]. The HATs acetylate the lysine residues on N-terminal tails of core histones, a process that generally correlates with gene activity [5]. HDACs catalyse the removal of acetyl groups from lysine side chains on core histones and a range of other proteins [8], which is frequently associated with transcriptional repression. These deacetylases are divided into two families, the classical HDAC family (zinc-dependent HDACs) and the sirtuin (sir2-like protein) family of NADþ-dependent deacetylases [11 –15]. Class III is represented by the sirtuin family which contains seven members (SIRTs 1– 7), homologous to the yeast Saccharomyces cerevisiae Sir protein [16,17]

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