Temporal analysis of microRNAs associated with wing development in the English grain aphid, Sitobion avenae (F.) (Homoptera: Aphidiae)

Authors: LI, XIANGRUI - Chinese Academy Of Agricultural Sciences; ZHANG, FANGMEI - Chinese Academy Of Agricultural Sciences; Coates, Brad; WEI, CHANGPING - Chinese Academy Of Agricultural Sciences; ZHANG, YUNHUI - Chinese Academy Of Agricultural Sciences; ZHOU, XUGUO - University Of Kentucky

Submitted to: Insect Biochemistry and Molecular Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/7/2021
Publication Date: 4/22/2021
Citation: Li, X., Zhang, F., Coates, B.S., Wei, C., Zhang, Y., Zhou, X. 2021. Temporal analysis of microRNAs associated with wing development in the English grain aphid, Sitobion avenae (F.) (Homoptera: Aphidiae). Insect Biochemistry and Molecular Biology. 142. Article 103579. https://doi.org/10.1016/j.ibmb.2021.103579.
DOI: https://doi.org/10.1016/j.ibmb.2021.103579

Interpretive Summary: Aphids are insects that feed on crop plants. Their feeding style helps spread disease within corn, soybean and wheat, impacting crop health. Aphids have a unique biology where genetically identical clones developed from a single female can either develop wings or remain wingless depending upon their environmental conditions. For instance, winged individuals develop when aphids become crowded on host plants or when a host plant is of poor nutritional quality. This induced wing development allows aphids to quickly adapt to changing environments within a year by moving (flying) to and infesting different plants. The change in proportion winged aphids is altered by direct response to the environment instead of being strictly controlled by inherited genetic factors. In order to understand this complex change, a USDA researcher worked within a collaborative team of domestic university and international researchers to document that the variation in expression of a class of active gene messages, known as microRNAs (miRNAs), are important regulators of the shift from wingless to winged aphids. The absence of wings was shown to result from changes in miRNA-based inhibition of genes that function in basic wing development. These results are important in understanding mechanisms that control movement (migration) of these insect crop pests within the agricultural landscape, and may lead to novel strategies for the control of crop damage. This research will be of interest to university, government, and industry stakeholders, as well as regulatory agencies interested in understanding the factors affecting arthropod pest species movement within the agroecosystem.

Technical Abstract: Molecular mechanisms underlying the wing evolution and development have been a point of scientific inquiry for decades. Phloem-feeding aphids are one of the most devastating global insect pests, where dispersal of winged morphs lead to annual movements, migrations, and long-term range expansions. Aphids show a polyphenic wing dimorphism trait, and offer a model to study the role of environment in determining morphological plasticity of a single genotype. Despite progress towards understanding the molecular genetic contributions to wing formation, the precise influence of environmental cues on wing polyphenism remain unresolved. To examine the roles of miRNAs in wing development of the English grain aphid, Sitobion avenae (F.), small RNA sequencing identified 113 conserved and 730 S. avenae-specific miRNAs across six different S. avenae developmental stages. Gene Ontology and KEGG pathway analyses revealed that six differentially expressed candidate wing development signaling pathway miRNAs. Validation of stage-specific expression was confirmed by qPCR for candidate miRNAs, showing five miRNAs are highly expressed in N1 and N2 stages, except miR-14. Direct feeding of agomirs (mimics) and antagomirs (antisense inhibitors), of three corresponding candidate miRNAs induced mortality and development of higher proportions of wingless morphs. Wing malformation of S. avenae are observed in miR-2 and miR-306 agomirs and miR-2 and miR-14 antagomirs, suggesting that candidate miRNAs may have roles in wing development dimorphic among S. avenae. Our study provides insight into the molecular mechanisms regulating aphid wing development and differentiation, and provide theoretical basis for prediction of dispersal and integrated management of phloem-feeding aphids.