The miR-9b microRNA mediates dimorphism and development of wing in aphids

Abstract

Wing dimorphism is a phenomenon of phenotypic plasticity in aphid dispersal. However, the signal transduction for perceiving environmental cues (e.g., crowding) and the regulation mechanism remain elusive. Here, we found that aci-miR-9b was the only down-regulated microRNA (miRNA) in both crowding-induced wing dimorphism and during wing development in the brown citrus aphid Aphis citricidus. We determined a targeted regulatory relationship between aci-miR-9b and an ABC transporter (AcABCG4). Inhibition of aci-miR-9b increased the proportion of winged offspring under normal conditions. Overexpression of aci-miR-9b resulted in decline of the proportion of winged offspring under crowding conditions. In addition, overexpression of aci-miR-9b also resulted in malformed wings during wing development. This role of aci-miR-9b mediating wing dimorphism and development was also confirmed in the pea aphid Acyrthosiphon pisum. The downstream action of aci-miR-9b-AcABCG4 was based on the interaction with the insulin and insulin-like signaling pathway. A model for aphid wing dimorphism and development was demonstrated as the following: maternal aphids experience crowding, which results in the decrease of aci-miR-9b. This is followed by the increase of ABCG4, which then activates the insulin and insulin-like signaling pathway, thereby causing a high proportion of winged offspring. Later, the same cascade, “miR-9b-ABCG4-insulin signaling,” is again involved in wing development. Taken together, our results reveal that a signal transduction cascade mediates both wing dimorphism and development in aphids via miRNA. These findings would be useful in developing potential strategies for blocking the aphid dispersal and reducing viral transmission.

Transcriptomic Profiling of Various Developmental Stages of Aphis Aurantii to Provide a Genetic Resource for Gene Expression and SSR Analysis

“…Wing dimorphism is a phenomenon of phenotypic plasticity associated with aphid dispersal. Aphids have been demonstrated to have high phenotypic plasticity and can transform from wingless to winged forms under conditions of over-crowding, lack of nutrition, and interactions with other organisms (Shang et al, 2020b ). Diverse processes take place during wing dimorphism and development (Zhang et al, 2019 ).…”

“…Diverse processes take place during wing dimorphism and development (Zhang et al, 2019 ). Many studies focused on the regulatory mechanism of wing dimorphism and development (Xu et al, 2015 ; Song et al, 2018 ; Shang et al, 2020b ). Finally, 390 of these DEGs also showed differences in the last ecdysis process from 4th instar nymph to wingless adult, and 1,887 genes only showed differences between winged and wingless adults.…”

“…Aphids are wide-spread pests that feed on a wide range of fruits and vegetables, most of them are vectors of plant viruses (Huang and Qiao, 2014 ; Hulle et al, 2020 ). Except the tea aphid, there have been previous functional studies on genes associated with the development (Ding et al, 2017 ; Ye et al, 2019 ), reproduction (Shang et al, 2018 ; Ullah et al, 2019b ), wing development (Shang et al, 2020b ), response to the stress (Gao et al, 2018 ; Jing et al, 2018 ), and pest control (Mohammed et al, 2018 ; Ullah et al, 2019a ) of other aphids pests (e.g., Ap. citricidus, Ap.…”

“…In addition, gene expression has been studied by RNA-Seq in multiple tissues to identify tissue-specific genes involved in female fertility in B. dorsalis [e.g., vitellogenin and vitelline membrane protein in female (Wei et al, 2018 , 2019 )]. In aphids, RNA-Seq was used to analyze the gene expression between dispersing and non-dispersing morphs (Shang et al, 2016 , 2020b ). Thus, RNA-Seq technology allows us to determine the gene expression to underlie certain biological functions of critical genes and identify potential targets of new environmentally friendly insecticides for pest control.…”

Identification and Analysis of MicroRNAs Associated with Wing Polyphenism in the Brown Planthopper, Nilaparvata lugens

“…Numerous studies have shown that miRNAs play roles in a complex regulatory system for biological processes [ 21 , 22 , 23 , 24 , 25 , 26 ]. In insects, miRNAs are involved in the regulation of growth, metamorphosis and reproduction [ 27 , 28 , 29 , 30 , 31 , 32 ]. For instance, multiple miRNAs jointly regulate the metamorphosis development via the biosynthesis of 20E in Chilo suppressalis [ 27 ].…”