State Key Laboratory of Rice Biology and Ministry of Agriculture Key Laboratory of Agricultural Entomology, Institute of Insect Science, Zhejiang University, Hangzhou 310058, China.
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.
Insect Biochem Mol Biol. 2018 Nov;102:31-42. doi: 10.1016/j.ibmb.2018.09.007. Epub 2018 Sep 17.
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, male-specific Nldsx, non-sex-specific Nldsx), 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 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.
在性别决定级联中，昆虫中的 dsx（双倍性别）、线虫中的 mab-3（雄性异常 3）和脊椎动物中的 Dmrt1（dsx/mab-3 相关转录因子-1）作为基本分子开关发挥重要作用。此外，这些基因具有相同的保守特征结构域-DNA 结合寡聚化结构域（OD1），雌性特异性 dsx 还具有保守的寡聚化结构域 2（OD2）。尽管有报道称几种完全变态昆虫的性别决定和 dsx 的功能，但半变态昆虫的性别决定和 dsx 的功能仍然是个谜。在这项研究中，在褐飞虱（Nilaparvata lugens，半翅目）中意外发现了四个 dsx 同源物，它们也表现出不同的进化状态。我们发现，四个同源物中只有一个，即 Nldsx，它有三种选择性剪接变体（雌性特异性 Nldsx、雄性特异性 Nldsx、非性别特异性 Nldsx），是褐飞虱性发育所必需的。与完全变态物种相比，褐飞虱的 dsx 含有较少保守的 OD1，而 BPH 的 OD2 结构域由于共同区域保守性差，雌性特异性区域较短而无法识别。在雌性 BPH 中用 RNAi 敲低 Nldsx 导致体型增大，腹部和生殖系统正常，但生育力没有变化。然而，在若虫期用 RNAi 敲低 Nldsx 的成年雄性变成了拟雌性，不育，交配器官异常，输精管无法通过，壁增生；此外，拟雌性无法产生正常的求爱信号。我们的结果表明，dsx 在雄性褐飞虱的体发育和交配行为中起着关键作用。这是首次研究表明 dsx 对半翅目物种的性发育至关重要。
