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PHF7 exhibits male-specific expression in early germ cells, germline stem cells and spermatogonia in insects, and its expression promotes spermatogenesis in germ cells when they are present in a male soma. However, the influence of male-specific PHF7 on female reproductive biology via mating remains unclear. Thus, we investigated the potential impacts of male PHF7, existed in seminal fluid of Nilaparvata lugens (NlPHF7), on fecundity and population growth via mating. Our results revealed that suppressing male NlPHF7 expression by RNAi led to decreases in body weight, soluble accessory gland protein content, arginine content, and reproductive organ development in males, resulting in significant reduction of oviposition periods and fecundity in females, and significant decrease in body weight, fat body and ovarian protein content, yeast-like symbionts abundance, ovarian development and vitellogenin gene expression in their female mating partners. Similarly, suppression of NlPHF7 expression in males mated with the control female reduced population growth and egg hatching rate, but did not influence gender ratio. We infer that NlPHF7 play a role important in stimulating female fecundity via mating. This study provides valuable information by identifying a potentially effective target gene for managing BPH population through RNAi.

The brown planthopper (BPH) is a devastating pest of rice throughout Asia. In this paper we document the BPH biogeographic range expansion in China over the 20-year period, 1992 to 2012. We posed the hypothesis that the range expansion is due to a syndrome of adaptations to the continuous presence of agricultural chemicals (insecticides and a fungicide) over the last 40 years. With respect to biogeography, BPH ranges have expanded by 13% from 1992 to 1997 and by another 3% from 1997 to 2012. In our view, such expansions may follow primarily from the enhancing effects of JGM, among other agricultural chemicals, and from global warming. JGM treatments led to increased thermotolerance, recorded as decreased mortality under heat stress at 40 ± 1 °C (down from 80% to 55%) and increased fecundity (by 49%) at 34 °C. At the molecular level, JGM treatments led to increased abundances of mRNA encoding Acetyl Co-A carboxylase (Acc) (up 25%) and Hsp70 (up 32%) in experimental BPH. RNAi silencing of Hsp70 and Acc eliminated the JGM effects on fecundity and silencing Hsp70 reduced JGM-induced thermotolerance. Integrated with global climate change scenarios, such syndromes in pest insect species have potential for regional- and global-scale agricultural disasters.

In our previous study with the brown planthopper (BPH), Nilaparvata lugens, triazophos (tzp) 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 is expressed in testes, we posed the hypothesis that NlSPATA5 occurs in BPH seminal fluid and it operates in fecundity via mating. We tested the hypothesis by investigating the influence of suppressing NlSPATA5 expression in BPH males on fecundity. Reduced expression of NlSPATA5 led to decreased male accessory gland protein content and reproductive system development compared to controls. These changes in males led to prolonged pre-oviposition periods and decreased fecundity in females. For both genders, we recorded no difference in the body weight, oviposition periods, and longevity compared to controls. NlSPATA5 suppression in males also led to decreased fat body and ovarian protein content, yeast-like symbionts abundance and ovarian development as well as vitellogenin gene expression in their mating partners. We infer that increased NlSPATA5 expression may be one molecular mechanism of tzp-driven reproduction and population increases in BPH.

The antibiotic jinggangmycin (JGM) is an agrochemical product widely used in China for controlling rice sheath blight, Rhizoctonia solani. Unexpectedly, it stimulates reproduction in the brown planthopper (BPH), Nilaparvata lugens (Stål). However, the underlying molecular mechanisms of the stimulation are unclear. The present investigation demonstrates that adipose triglyceride lipase (Atgl) is one of the enzymes involved in the JGM-stimulated reproduction in BPH. Silence of Atgl in JGM-treated (JGM + dsAtgl) females eliminated JGM-stimulated fecundity of BPH females. In addition, Atgl knockdown significantly reduced the protein and glycerin contents in the ovaries and fat bodies of JGM + dsAtgl females required for reproduction. We conclude that Atgl is one of the key enzymes responsible for JGM-stimulated reproduction in BPH.

A major challenge in ecology lies in understanding the coexistence of intraguild species, well documented at the organismal level, but not at the molecular level. This study focused on the effects of the antibiotic, jinggangmycin (JGM), a fungicide widely used in Asian rice agroecosystems, on reproduction of insects within the planthopper guild, including the brown planthopper (BPH) Nilaparvata lugens and the white-backed planthopper (WBPH) Sogatella furcifera, both serious resurgence rice pests. JGM exposure significantly increased BPH fecundity and population growth, but suppressed both parameters in laboratory and field WBPH populations. We used digital gene expression and transcriptomic analyses to identify a panel of differentially expressed genes, including a set of up-regulated genes in JGM-treated BPH, which were down-regulated in JGM-treated WBPH. RNAi silencing of Acetyl Co-A carboxylase (ACC), highly expressed in JGM-treated BPH, reduced ACC expression (by > 60%) and eliminated JGM-induced fecundity increases in BPH. These findings support our hypothesis that differences in ACC expression separates intraguild species at the molecular level.

The brown planthopper (BPH), Nilaparvata lugens, sugar transporter gene 6 (Nlst6) is a facilitative glucose/fructose transporter (often called a passive carrier) expressed in midgut that mediates sugar transport from the midgut lumen to hemolymph. The influence of down regulating expression of sugar transporter genes on insect growth, development, and fecundity is unknown. Nonetheless, it is reasonable to suspect that transporter-mediated uptake of dietary sugar is essential to the biology of phloem-feeding insects. Based on this reasoning, we posed the hypothesis that silencing, or reducing expression, of a BPH sugar transporter gene would be deleterious to the insects. To test our hypothesis, we examined the effects of Nlst6 knockdown on BPH biology. Reducing expression of Nlst6 led to profound effects on BPHs. It significantly prolonged the pre-oviposition period, shortened the oviposition period, decreased the number of eggs deposited and reduced body weight, compared to controls. Nlst6 knockdown also significantly decreased fat body and ovarian (particularly vitellogenin) protein content as well as vitellogenin gene expression. Experimental BPHs accumulated less fat body glucose compared to controls. We infer that Nlst6 acts in BPH growth and fecundity, and has potential as a novel target gene for control of phloem-feeding pest insects.