Effect of the brain and suboesophageal ganglion on pupal development in Helicoverpa armigera through regulation of FXPRLamide neuropeptides
Introduction
Insect neuropeptides are involved in various physiological and developmental events such as growth, molting, metamorphosis, reproduction, diapause, metabolism, etc. [1]. The peptides of the FXPRLamide family share a common C-terminal pentapeptide sequence, FXPRLamide (X=G, S, T, or V). This pentapeptide sequence is thought to be the active core required for their activity [2]. The peptides of this family include diapause hormone (DH), pheromone biosynthesis activating neuropeptide (PBAN), melanization and reddish coloration hormone (MRCH), myotropin, and pyrokinin. They regulate various aspects of physiological functions, such as induction of embryonic diapause in Bombyx mori [3], sex pheromone biosynthesis in Helicoverpa zea [4], coloration in phase polymorphism in Pseudaletia separata [5] and Spodoptera littoralis [6], and stimulation of muscle contraction in the hindguts and oviducts in Locusta migratoria [7].
Generally, insect growth and development are regulated by ecdysteroids, juvenile hormone (JH), and their regulators: prothoracicotropic hormone (PTTH) [8], prothoracicostatic peptide (PTSP) [9], allatotropin (AT) [10], and allatostatin (AST) [11]. In H. armigera, a pupal diapause species, the immediate cause of pupal diapause is the failure of the brain to secrete PTTH and the failure of the prothoracic glands to secrete ecdysteroids [12], [13], [14], [15]. Recently, Zhang et al. proved that DH and FXPRLamide family peptides secreted from the suboesophageal ganglion (SG) of H. armigera could break pupal diapause and promote development by stimulating the prothoracic glands to synthesize and release ecdysteroids (data not shown). Therefore, the FXPRLamide family neuropeptides may have a regulatory role in insect development with the brain and SG as the central in dictating the developmental fate of H. armigera.
To understand the molecular events in FXPRLamide neuropeptide regulating insect development, we report the effects of brain and SG on the synthesis and release of FXPRLamide neuropeptides, and the relationship between the changes of FXPRLamide titer in hemolymph and pupal development. The results show that the SG is a major site for synthesis and release of FXPRLamide neuropeptides, and the thoracic ganglia (TGs) can act as the main site for FXPRLamide neuropeptides in the absence of SG. The brain can determine pupal development through regulation of the expression of DH-PBAN gene, and FXPRLamide neuropeptides might accelerate pupal development in H. armigera.
Section snippets
Animals
H. armigera were kindly provided by Prof. Jin-Liang Shen, Nanjing Agricultural University, Nanjing, and maintained for 4 years at our laboratory. Larvae were reared on an artificial diet at 25 °C, with a L14:D10 photoperiod (nondiapause type) and all the pupae developed without entering diapause. When larvae were reared at 22 °C, with a L10:D14 photoperiod (diapause type), more than 90% of the individuals entered diapause. The developmental stages were synchronized at each molt by collecting
Role of the SG in pupal development
Our previous studies have demonstrated that FXPRLamide neuropeptides (DH, PBAN, β-SGNP, and γ-SGNP) secreted from the SG can break pupal diapause and promote development in H. armigera [25]. This finding suggested that the SG might have an important role in the regulation of pupal development. To elucidate the function of FXPRLamide neuropeptides, we investigated the developmental status of nondiapause pupae by SG ablation. As shown in Fig. 1, the SG-removed pupae could not enter diapause-like
Discussion
DH is produced by neurosecretory cells of the SG in B. mori, and transplanting the SG of diapause type into nondiapause pupa can induce embryonic diapause in B. mori [2]. In contrast, Zdarek et al. [28] demonstrated that peptides of the FXPRLamide family could accelerate pupariation in the fleshfly, Sarcophaga bullata. Recently, we have demonstrated that the FXPRLamide peptides, DH, PBAN, and SGNPs produced by the DH-PBAN gene, could break pupal diapause and promote development by stimulating
Acknowledgments
We thank Prof. J.L. Shen for providing the insect strain and the rearing method. This work was supported by a Grant-In-Aids for the Natural Scientific Foundation (30070115) from the National Natural Science Foundation of China, the Major State Basic Research Development Program of the P.R. China (G20000162) from the Ministry of Science and Technology, and a Grant-In-Aid for Young Scientists from the Chinese Academy of Science.
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2018, Insect Biochemistry and Molecular BiologyCitation Excerpt :The results showed that the p-AKT levels were elevated, accompanied with reduced POU and PTEN levels (Fig. 6A), implying that ROS can decrease POU/PTEN levels to elevate p-AKT levels. Previous studies have shown that POU can respond to ecdysone signaling and plays a key role in pupal development (Lin and Xu, 2016; Zhang and Xu, 2009); furthermore, both ecdysone titers in the blood and POU expression in the brains of diapause-destined pupae are significantly lower than the levels found in nondiapause pupae (Lin and Xu, 2016; Sun et al., 2003). To clarify whether POU/PTEN respond to ecdysone signaling, ecdysone was injected into diapausing pupae to break the diapause and restart pupal-adult development.
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2013, Current Topics in Developmental BiologyCitation Excerpt :Although PTTH and DA signaling appear import, the full regulatory mechanism underlying pupal diapause is likely to be more complex, since DH is also required to reactivate postdiapause growth in synergism with PTTH. Such DH functions are well documented for the pupal diapause of noctuids belonging to the Heliothis/Helicoverpa complex (Sun, Zhang, Zhang, & Xu, 2003; Sun et al., 2005; Zhang, Sun, Zhang, Shen, & Xu, 2004; Zhang, Sun, Zhang, Xu, et al., 2004). In these moths, DH injections into “nonchilled” diapausing pupae induce them to break dormancy (Xu & Denlinger, 2003; Zhang, Nachman, Kaczmarek, Zabrocki, & Denlinger, 2011; Zhang, Sun, Zhang, Shen, et al., 2004; Zhang, Sun, Zhang, Xu, et al., 2004; Zhang, Zdarek, Nachman, & Denlinger, 2008) in a temperature-dependent way: it is unable to break diapause at 20 °C, but does so in dormant pupae shifted to 25 °C (Zhang, Sun, Zhang, Shen, et al., 2004; Zhang, Sun, Zhang, Xu, et al., 2004).