Short Neuropeptide F and Its Receptor Regulate Feeding Behavior in Pea Aphid (Acyrthosiphon pisum)

Abstract

Insect short neuropeptide F (sNPF), an ortholog of prolactin-releasing peptide of invertebrates, regulates diverse biological processes, including feeding, olfaction, locomotion, and sleep homeostasis in insects. However, its function is still unclear in an important model insect and agricultural pest, the pea aphid (Acyrthosiphon pisum). Here, we investigated short neuropeptide F (ApsNPF) and its receptor (ApsNPFR) in A. pisum. The sNPF gene contains three exons and two long introns. In addition, the genome contains a single sNPF receptor with seven transmembrane domains. Stage- and tissue-specific transcript profiling by qRT-PCR revealed that ApsNPF and ApsNPFR were mainly expressed in the central nervous system. The receptor was also detected in antennae, midgut, and integument. The highest expression levels were found in first instar nymphs compared to other developmental stages. Besides, the starvation-induced pattern indicated that the sNPF network depends on the nutritional state of the insect. An electrical penetration graph showed that probing time and phloem duration of A. pisum on broad bean plants decreased in response to dssNPF and dssNPFR in RNAi assays. sNPF silencing reduced the number of nymphs per female but not aphid survival. We believe that our results advance in-depth knowledge of the sNPF/sNPFR signaling cascade and its place in regulating feeding behavior in insects. In turn, it may contribute to the potential design of new strategies to control aphids, with a focus on the sNPF system.

Effect of short neuropeptide F signaling on larval feeding in Mythimna separata

“…4A, B) based on RT-qPCR, which provided evidence that the sNPF signaling pathway is potentially related to the modulation of versatile physiological roles of M. separata. Both sNPF and sNPFR1 had significantly highest expression levels in the 1st instar larvae, which was consistent with sNPF and sNPFR in A. pisum (Peng et al, 2021) and R. padi (Amir et al, 2022). Tissue distribution of M. separata revealed that sNPF and sNPFR1 were highly expressed in the CNS, whereas sNPFR2 had higher transcript levels in the midgut and Malpighian tubules of larvae.…”

“…Its cognate receptor sNPFR belongs to the rhodopsin superfamily of G protein-coupled receptors (GPCRs), which share a 7 α-helical transmembrane structure (Mertens et al, 2002). To date, sNPF and its receptor have been reported in many insects, such as Diptera (Nässel et al, 2008;Li et al, 2022), Orthoptera (Dillen et al, 2013(Dillen et al, , 2014, and Coleoptera (Marciniak et al, 2020;Liu et al, 2021a), Hemiptera (Peng et al, 2021;Amir et al, 2022), Hymenoptera (Lu & Pietrantonio, 2011;Bestea et al, 2022b), and Lepidoptera (Nagata et al, 2012;Ma et al, 2017;Cheng et al, 2021). These data suggest that sNPF family neuropeptide signals widely exist in insect species.…”

“…It is a post-transcriptional gene silencing mechanism mediated by small RNA molecules, including double-stranded RNA (dsRNA) (Cooper et al, 2019;Liu et al, 2020). RNAi-mediated gene silencing in Dendroctonus armandi (Liu et al, 2021a) and Acyrthosiphon pisum (Amir et al, 2022) revealed that short neuropeptide F (sNPF) and its receptors are involved in feeding modulation. Then, studies highlighted tremendous potential of RNAi-based insect pest control in M. separata.…”

Nicotine‐mediated dopamine regulates short neuropeptide F to inhibit brown planthopper feeding behavior in tobacco‐rice rotation cropping

“…Given that these insects are evolutionarily distant, it is likely that the shift in sNPF activity from feeding promotion to inhibition might have occurred repeatedly during the evolutionary process. In addition, a previous report demonstrated the role of sNPF in regulating insect feeding, such as in the hemiptera where it regulates the feeding behavior of pea aphid 21,22 . Therefore, it is reasonable to speculate that sNPF is potentially involved in nicotinic regulation of BPH feeding.…”

“…In addition, a previous report demonstrated the role of sNPF in regulating insect feeding, such as in the hemiptera where it regulates the feeding behavior of pea aphid. 21,22 Therefore, it is reasonable to speculate that sNPF is potentially involved in nicotinic regulation of BPH feeding.…”