Suppressing male spermatogenesis-associated protein 5-like gene expression reduces vitellogenin gene expression and fecundity in Nilaparvata lugens Stål

Authors: GE, LIN-QUAN - Yangzhou University; XIA, TING - Yangzhou University; HUANG, BO - Yangzhou University; SONG, QI-SHENG - University Of Missouri; ZHANG, HONG-WEI - University Of Missouri; Stanley, David; YANG, GUO-QING - Yangzhou University; WU, JIN-CAI - Yangzhou University

Submitted to: Scientific Reports
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/31/2016
Publication Date: 6/16/2016
Citation: Ge, L., Xia, T., Huang, B., Song, Q., Zhang, H., Stanley, D.W., Yang, G., Wu, J. 2016. Suppressing male spermatogenesis-associated protein 5-like gene expression reduces vitellogenin gene expression and fecundity in Nilaparvata lugens Stål. Scientific Reports. 6: 28111.

Interpretive Summary: Long-term agricultural sustainability is severely threatened by widespread use of classical insecticides. Threats include increasing resistance to insecticides and sharply decreasing environmental quality. These issues drive research into alternatives to classical insecticides. One potential alternative is based on applying molecular tools to inhibit expression of genes that are crucial to insect pest biology. In this paper, we examined the impact of inhibiting a specific gene responsible for production of proteins necessary for successful reproduction in a pest insect species. We found that inhibiting this gene in males of the pest led to reduced fecundity in their mating partners. These findings demonstrate that this gene may be a novel target for developing insect pest control technologies. This research will influence scientists working to develop novel pest control technologies and, ultimately, will benefit farmers who produce food crops and the people who consume them.

Technical Abstract: In our previous study with the brown planthopper (BPH), Nilaparvata lugens, triazophos (tzp, organophosphate) treatments led to substantial up-regulation of a male spermatogenesis-associated protein 5-like gene (NlSPATA5) compared to untreated controls. Mating with tzp-treated males significantly increased fecundity (as numbers of eggs laid), relative to females mated with untreated males. Because SPATA5 acts in mammalian sperm development and functions, and is expressed in testes, we posed the question of whether NlSPATA5 occurs in BPH seminal fluid and operates by influencing fecundity of mating partners. We tested the idea by investigating the influence of suppressing NlSPATA5 expression in BPH males on fecundity of females after mating with the experimental males. Reduced expression of NlSPATA5 led to decreased male accessory gland soluble protein content and to failures of reproductive system development in both genders, compared to controls. These changes in males led to prolonged pre-oviposition periods and decreased fecundity in their mating partners. For both genders, we recorded no differences in the body weight, oviposition periods, or longevity compared to controls. NlSPATA5 knockdown in males also led to decreases in several parameters in their mating partners. These include fat body and ovarian soluble protein content, abundances of yeast-like symbionts, ovarian development and vitellogenin gene expression. These findings positively answer our question and drive on-going research into the question of whether tzp increases BPH fecundity and population sizes by increasing NlSPATA5 expression.