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

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 pe...

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Main Authors: Muhammad Bilal Amir, Yan Shi, Hehe Cao, Muhammad Yasir Ali, Muhammad Afaq Ahmed, Guy Smagghe, Tong-Xian Liu
Format: Article
Language:English
Published: MDPI AG 2022-03-01
Series:Insects
Subjects:
Online Access:https://www.mdpi.com/2075-4450/13/3/282
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author Muhammad Bilal Amir
Yan Shi
Hehe Cao
Muhammad Yasir Ali
Muhammad Afaq Ahmed
Guy Smagghe
Tong-Xian Liu
author_facet Muhammad Bilal Amir
Yan Shi
Hehe Cao
Muhammad Yasir Ali
Muhammad Afaq Ahmed
Guy Smagghe
Tong-Xian Liu
author_sort Muhammad Bilal Amir
collection DOAJ
description 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 (<i>Acyrthosiphon pisum</i>). Here, we investigated short neuropeptide F (<i>ApsNPF</i>) and its receptor (<i>ApsNPFR</i>) in <i>A. pisum</i>. 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 <i>ApsNPF</i> and <i>ApsNPFR</i> 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 <i>A. pisum</i> 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.
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spelling doaj.art-a65588f186474b36928b6cbade5a97a12023-11-24T01:43:56ZengMDPI AGInsects2075-44502022-03-0113328210.3390/insects13030282Short Neuropeptide F and Its Receptor Regulate Feeding Behavior in Pea Aphid (<i>Acyrthosiphon pisum</i>)Muhammad Bilal Amir0Yan Shi1Hehe Cao2Muhammad Yasir Ali3Muhammad Afaq Ahmed4Guy Smagghe5Tong-Xian Liu6Key Laboratory of Insect Ecology and Molecular Biology, College of Plant Health and Medicine, Qingdao Agricultural University, Qingdao 266109, ChinaKey Laboratory of Insect Ecology and Molecular Biology, College of Plant Health and Medicine, Qingdao Agricultural University, Qingdao 266109, ChinaKey Laboratory of Insect Ecology and Molecular Biology, College of Plant Health and Medicine, Qingdao Agricultural University, Qingdao 266109, ChinaKey Laboratory of Insect Ecology and Molecular Biology, College of Plant Health and Medicine, Qingdao Agricultural University, Qingdao 266109, ChinaKey Laboratory of Insect Ecology and Molecular Biology, College of Plant Health and Medicine, Qingdao Agricultural University, Qingdao 266109, ChinaLaboratory of Agrozoology, Department of Plants and Crops, Faculty of Bioscience Engineering, Ghent University, 9000 Ghent, BelgiumKey Laboratory of Insect Ecology and Molecular Biology, College of Plant Health and Medicine, Qingdao Agricultural University, Qingdao 266109, ChinaInsect 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 (<i>Acyrthosiphon pisum</i>). Here, we investigated short neuropeptide F (<i>ApsNPF</i>) and its receptor (<i>ApsNPFR</i>) in <i>A. pisum</i>. 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 <i>ApsNPF</i> and <i>ApsNPFR</i> 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 <i>A. pisum</i> 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.https://www.mdpi.com/2075-4450/13/3/282<i>Acyrthosiphon pisum</i>short neuropeptide FG protein-coupled receptortranscriptional expressionRNA interferencefeeding regulation
spellingShingle Muhammad Bilal Amir
Yan Shi
Hehe Cao
Muhammad Yasir Ali
Muhammad Afaq Ahmed
Guy Smagghe
Tong-Xian Liu
Short Neuropeptide F and Its Receptor Regulate Feeding Behavior in Pea Aphid (<i>Acyrthosiphon pisum</i>)
Insects
<i>Acyrthosiphon pisum</i>
short neuropeptide F
G protein-coupled receptor
transcriptional expression
RNA interference
feeding regulation
title Short Neuropeptide F and Its Receptor Regulate Feeding Behavior in Pea Aphid (<i>Acyrthosiphon pisum</i>)
title_full Short Neuropeptide F and Its Receptor Regulate Feeding Behavior in Pea Aphid (<i>Acyrthosiphon pisum</i>)
title_fullStr Short Neuropeptide F and Its Receptor Regulate Feeding Behavior in Pea Aphid (<i>Acyrthosiphon pisum</i>)
title_full_unstemmed Short Neuropeptide F and Its Receptor Regulate Feeding Behavior in Pea Aphid (<i>Acyrthosiphon pisum</i>)
title_short Short Neuropeptide F and Its Receptor Regulate Feeding Behavior in Pea Aphid (<i>Acyrthosiphon pisum</i>)
title_sort short neuropeptide f and its receptor regulate feeding behavior in pea aphid i acyrthosiphon pisum i
topic <i>Acyrthosiphon pisum</i>
short neuropeptide F
G protein-coupled receptor
transcriptional expression
RNA interference
feeding regulation
url https://www.mdpi.com/2075-4450/13/3/282
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