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. 2021 Sep 17:12:736906.
doi: 10.3389/fendo.2021.736906. eCollection 2021.

Transcriptome Analysis of Ostrinia furnacalis Female Pheromone Gland: Esters Biosynthesis and Requirement for Mating Success

Shuangyan Yao  1 , Shuai Zhou  1 , Xiang Li  1 , Xiaoguang Liu  1 , Wenli Zhao  1 , Jizhen Wei  1 , Mengfang Du  1 , Shiheng An  1
Affiliations

Transcriptome Analysis of Ostrinia furnacalis Female Pheromone Gland: Esters Biosynthesis and Requirement for Mating Success

Shuangyan Yao et al. Front Endocrinol (Lausanne). .

Abstract

Female moths use sex pheromones to attract males, and corresponding regulatory mechanism underlying sex pheromone biosynthesis is species-dependent. However, the detailed mechanism involved in sex pheromone biosynthesis in Ostrinia furnacalis has not yet been fully addressed. In the present study, transcriptome sequencing of O. furnacalis pheromone glands screened a serials of candidate genes involved in sex pheromone biosynthesis. Our analysis showed that sex pheromone release in O. furnacalis females arrives its peak at the 2nd scotophase, consistent with its mating behavior. Pheromone biosynthesis-activating neuropeptide (PBAN) was confirmed to regulate sex pheromone biosynthesis, and Ca2+ is the secondary messenger of PBAN signaling in O. furnacalis. The functional analysis of candidate genes demonstrated that the decreased mRNA levels or activities of calcineurin (CaN) and acetyl-CoA carboxylase (ACC) led to significant decrease in sex pheromone production and female capability to attract males, as demonstrated by RNAi-mediated knockdown and pharmacological inhibitor assay. Most importantly, the activities of CaN and ACC depend on the activation of PBAN/PBANR/Ca2+. Furthermore, fatty-acyl reductase 14 was involved in PBAN-mediated sex pheromone biosynthesis. Altogether, our results demonstrated that PBAN regulates sex pheromone biosynthesis through PBANR/Ca2+/CaN/ACC pathway to promote sex pheromone biosynthesis in O. furnacalis and provided a reference for non-model organism to study neuropeptide signal transduction.

Keywords: Ostrinia furnacalis; PBAN; secondary messenger; sex pheromone; signal transduction.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

Figure 1
Figure 1
PBAN signal mediates sex pheromone production in O. furnacalis. (A, B) The titer of sex pheromone in PGs after PBAN incubation. Data represent the mean ± SE (n = 3). A multiple comparison test with P < 0.05 was conducted to test the significant differences in different development time points (based on Tukey’s test, DPS7.05). (C) RNAi efficiency of PBANR. (D) The effect of dsPBANR knockdown on sex pheromone production. Data represent the mean ± SE (n = 3). Statistically significant difference was denoted with * (P < 0.05) and *** (P < 0.001) as determined by Student’s t-test. Small letters a-d indicate significant difference.
Figure 2
Figure 2
Second messengers of PBAN signal in O. furnacalis. (A) cAMP level in PGs after PBAN challenge in O. furnacalis. (B) The concentration of Ca2+ in PGs after PBAN incubation in O. furnacalis. Data represent the mean ± SE (n = 3). A multiple comparison test with P < 0.05 was conducted to test the significant differences in different development time points (based on Tukey’s test, DPS7.05). (C) Effect of the calcium channel inhibitor LaCl3 on sex pheromone production in O. furnacalis PGs. Data represent the mean ± SE (n = 3). Statistically significant difference was denoted with *** (P < 0.001) as determined by Student’s t-test. Small letters a-f indicate significant difference.
Figure 3
Figure 3
PBAN regulated CaN and ACC activity in O. furnacalis PGs. (A, B) The activity of CaN and ACC after PBAN incubation in O. furnacalis PGs. Data represent the mean ± SE (n = 3). A multiple comparison test with P < 0.05 was conducted to test the significant differences in different development time points (based on Tukey’s test, DPS7.05). NS, not significant. Small letters a-c indicate significant difference.
Figure 4
Figure 4
CaN positively regulates sex pheromone biosynthesis in O. furnacalis PGs. (A) The effects of dsRNA injection on the expression of CaN transcript. (B) Effect of dsCaN knockdown on sex pheromone production in O. furnacalis PGs. (C) Effect of the CaN inhibitor FK506 on sex pheromone production in O. furnacalis PGs. (D) Effect of dsCaN knockdown on female capability to attract males. Data represent the mean ± SE (n = 3). Statistically significant differences were denoted with * (P < 0.05), ** (P < 0.01), and *** (P < 0.001) as determined by Student’s t-test. NS, not significant.
Figure 5
Figure 5
ACC positively regulates sex pheromone biosynthesis in O. furnacalis PGs. (A) The effects of dsRNA injection on the expression of ACC transcript. (B) Effect of dsACC knockdown on sex pheromone production in O. furnacalis PGs. (C) Effect of the ACC inhibitor TOFA on sex pheromone production in O. furnacalis PGs. (D) Effect of dsACC knockdown on female capability to attract males. Data represent the mean ± SE (n = 3). Statistically significant differences were denoted with ** (P < 0.01) and *** (P < 0.001) as determined by Student’s t-test. NS, not significant.
Figure 6
Figure 6
CaN positively regulates ACC enzyme activity in O. furnacalis PGs. (A) Effect of dsCaN knockdown on ACC enzyme activity in O. furnacalis PGs. (B) Effect of the CaN inhibitor FK506 on ACC enzyme activity in O. furnacalis PGs. Data represent the mean ± SE (n = 3). Statistically significant differences were denoted with ** (P < 0.01) as determined by Student’s t-test.
Figure 7
Figure 7
The model of PBAN signal transduction pathway in O. furnacalis PGs. The binding of PBAN with its receptor PBANR activates the second messenger (Ca2+). Ca2+ influx in turn activates CaN and ACC and ultimately regulates the production of sex pheromones under the catalysis of FAR14. PBAN, pheromone biosynthesis-activating neuropeptide; PBANR, PBANR receptor; CaCn, calcium channel; CaM, calmodulin; CaN, Calcineurin; ACC, Acetyl CoA carboxylase; FAS, fatty acid synthase; Des-14, delta 14 desaturase; FAR14, fatty acyl reductases 14; ACT, acyl transferase.
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