Identification and functional analysis of the doublesex gene in the sexual development of a hemimetabolous insect, the brown planthopper

Ji-Chong Zhuo; Qing-Ling Hu; Hou-Hong Zhang; Meng-Qiu Zhang; Song Bok Jo; Chuan-Xi Zhang

doi:10.1016/j.ibmb.2018.09.007

Identification and functional analysis of the doublesex gene in the sexual development of a hemimetabolous insect, the brown planthopper

Insect Biochem Mol Biol. 2018 Nov:102:31-42. doi: 10.1016/j.ibmb.2018.09.007. Epub 2018 Sep 17.

Authors

Ji-Chong Zhuo¹, Qing-Ling Hu¹, Hou-Hong Zhang¹, Meng-Qiu Zhang¹, Song Bok Jo², Chuan-Xi Zhang³

Affiliations

¹ State Key Laboratory of Rice Biology and Ministry of Agriculture Key Laboratory of Agricultural Entomology, Institute of Insect Science, Zhejiang University, Hangzhou 310058, China.
² State Key Laboratory of Rice Biology and Ministry of Agriculture Key Laboratory of Agricultural Entomology, Institute of Insect Science, Zhejiang University, Hangzhou 310058, China; Kim Jong Suk University of Education, Democratic People's Republic of Korea.
³ State Key Laboratory of Rice Biology and Ministry of Agriculture Key Laboratory of Agricultural Entomology, Institute of Insect Science, Zhejiang University, Hangzhou 310058, China. Electronic address: chxzhang@zju.edu.cn.

PMID: 30237076
DOI: 10.1016/j.ibmb.2018.09.007

Abstract

In the sex determination cascade, the genes dsx (doublesex) in insects, mab-3 (male abnormal 3) in nematodes, and Dmrt1 (dsx/mab-3 related transcription factor-1) in vertebrates act as the base molecular switches and play important roles. Moreover, these genes share the same conserved feature domain-DNA-binding oligomerization domain (OD1), and female-specific dsx also has a conserved oligomerization domain 2 (OD2). Although sex determination and the functions of dsx in several holometabolous insects have been well documented, sex determination and the function of dsx in hemimetabolous insects remain a mystery. In this study, four dsx homologs were unexpectedly found in the Nilaparvata lugens (brown planthopper, BPH, order Hemiptera), which also showed a different evolutionary status. We found that only one of the four homologs, Nldsx, which has three alternative splicing variants (female-specific Nldsx^F, male-specific Nldsx^M, non-sex-specific Nldsx^C), was required in the sexual development of N. lugens. Compared with that of holometabolous species, the dsx of N. lugens contains a less conserved OD1, while the OD2 domain of BPH was not identifiable because the common region is poorly conserved, and the female-specific region is short. RNAi-mediated knockdown of Nldsx in female BPH resulted in a larger body size with a normal abdomen and reproductive system, while no changes in fertility were noted. However, adult males with RNA interference knockdown of Nldsx^M in nymphs became pseudofemales, were infertile, had abnormal copulatory organs, and had impassable deferent ducts with hyperplastic walls; additionally, the pseudofemales could not produce the normal courtship signals. Our results suggest that dsx plays a critical role in male BPH somatic development and mating behavior. This is the first study to show that dsx is essential for sexual development in a hemipteran species.

Keywords: Doublesex; Hemimetabolous insect; Nilaparvata lugens; RNAi; Sex determination.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
DNA-Binding Proteins* / genetics
DNA-Binding Proteins* / metabolism
Female
Hemiptera* / genetics
Hemiptera* / growth & development
Insect Proteins* / genetics
Insect Proteins* / metabolism
Male
Sex Characteristics*
Sexual Development / physiology*

Substances

DNA-Binding Proteins
Insect Proteins