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

Xiangrui Li; Fangmei Zhang; Brad Coates; Changping Wei; Xun Zhu; Yunhui Zhang; Xuguo Zhou

doi:10.1016/j.ibmb.2021.103579

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

Xiangrui Li, Fangmei Zhang, Brad Coates, Changping Wei, Xun Zhu, Yunhui Zhang, Xuguo Zhou

Entomology

Research output: Contribution to journal › Article › peer-review

5 Scopus citations

Abstract

Molecular mechanisms underlying 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 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 recent progresses in the genetic understanding of wing polyphenism, the influence of environmental cues remains unclear. To investigate the involvement of miRNAs in wing development, we sequenced small RNA libraries of the English grain aphid, Sitobion avenae (F.) across six different developmental stages. As a result, we identified 113 conserved and 193 S. avenae-specific miRNAs. Gene Ontology and KEGG pathway analyses of putative target mRNAs for the six differentially expressed miRNAs are enriched for wing development processes. Dietary uptake of miR-263a, miR-316, and miR-184a agomirs and antagomirs led to significantly higher mortality (>70%) and a lower proportion of winged morphs (<5%). On the other hand, wing malformation was observed in miR-2 and miR-306 agomirs and miR-2 and miR-14 antagomirs, respectively, suggesting their involvement in S. avenae wing morphogenesis. These combined results not only shed light on the regulatory role of miRNAs in wing dimorphism, but also provide potential novel targets for the long-term sustainable management of S. avenae, a devastating global grain pest.

Original language	English
Article number	103579
Journal	Insect Biochemistry and Molecular Biology
Volume	142
DOIs	https://doi.org/10.1016/j.ibmb.2021.103579
State	Published - Mar 2022

Bibliographical note

Funding Information:
This research was supported by the National Natural Science Foundation of China (Award number: 31772163), National Key Research and DevelopmentFoundation, Ministry of Science and Technology of China (Award number: 2016YFD0300705), China Agriculture Research System of MOF and MARA (Award number: CARS-3). The information reported in this paper is part of a project of the Kentucky Agricultural Experiment Station and is published with the approval of the Director. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Contributions by BSC was supported by the United States Department of Agriculture (USDA) Agricultural Research Service (ARS) (CRIS Project 5030-22000-019-00D) and the Iowa Agriculture and Home Economics Experiment Station, Ames, IA (Project 3543). Any mention of products or services is for research purposes only, and does not constitute an endorsement for use by USDA. USDA is an equal opportunity employer and provider. Authors would like to thank anonymous reviewers for their constructive criticisms and comments to improve this manuscript.

Funding Information:
This research was supported by the National Natural Science Foundation of China (Award number: 31772163), National Key Research and Development Foundation, Ministry of Science and Technology of China (Award number: 2016YFD0300705), China Agriculture Research System of MOF and MARA (Award number: CARS-3). The information reported in this paper is part of a project of the Kentucky Agricultural Experiment Station and is published with the approval of the Director. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Contributions by BSC was supported by the United States Department of Agriculture ( USDA ) Agricultural Research Service ( ARS ) (CRIS Project 5030-22000-019-00D) and the Iowa Agriculture and Home Economics Experiment Station, Ames, IA (Project 3543). Any mention of products or services is for research purposes only, and does not constitute an endorsement for use by USDA. USDA is an equal opportunity employer and provider. Authors would like to thank anonymous reviewers for their constructive criticisms and comments to improve this manuscript.

Publisher Copyright:
© 2021

Keywords

Developmental stages
Functional analysis
Sitobion avenae
Wing
miRNA

ASJC Scopus subject areas

Biochemistry
Molecular Biology
Insect Science

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Li, X., Zhang, F., Coates, B., Wei, C., Zhu, X., Zhang, Y., & Zhou, X. (2022). Temporal analysis of microRNAs associated with wing development in the English grain aphid, Sitobion avenae (F.) (Homoptera: Aphidiae): Functional dissection of miRNAs associated with wing development in Sitobion avenae. Insect Biochemistry and Molecular Biology, 142, [103579]. https://doi.org/10.1016/j.ibmb.2021.103579

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title = "Temporal analysis of microRNAs associated with wing development in the English grain aphid, Sitobion avenae (F.) (Homoptera: Aphidiae): Functional dissection of miRNAs associated with wing development in Sitobion avenae",

abstract = "Molecular mechanisms underlying 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 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 recent progresses in the genetic understanding of wing polyphenism, the influence of environmental cues remains unclear. To investigate the involvement of miRNAs in wing development, we sequenced small RNA libraries of the English grain aphid, Sitobion avenae (F.) across six different developmental stages. As a result, we identified 113 conserved and 193 S. avenae-specific miRNAs. Gene Ontology and KEGG pathway analyses of putative target mRNAs for the six differentially expressed miRNAs are enriched for wing development processes. Dietary uptake of miR-263a, miR-316, and miR-184a agomirs and antagomirs led to significantly higher mortality (>70%) and a lower proportion of winged morphs (<5%). On the other hand, wing malformation was observed in miR-2 and miR-306 agomirs and miR-2 and miR-14 antagomirs, respectively, suggesting their involvement in S. avenae wing morphogenesis. These combined results not only shed light on the regulatory role of miRNAs in wing dimorphism, but also provide potential novel targets for the long-term sustainable management of S. avenae, a devastating global grain pest.",

keywords = "Developmental stages, Functional analysis, Sitobion avenae, Wing, miRNA",

author = "Xiangrui Li and Fangmei Zhang and Brad Coates and Changping Wei and Xun Zhu and Yunhui Zhang and Xuguo Zhou",

note = "Funding Information: This research was supported by the National Natural Science Foundation of China (Award number: 31772163), National Key Research and DevelopmentFoundation, Ministry of Science and Technology of China (Award number: 2016YFD0300705), China Agriculture Research System of MOF and MARA (Award number: CARS-3). The information reported in this paper is part of a project of the Kentucky Agricultural Experiment Station and is published with the approval of the Director. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Contributions by BSC was supported by the United States Department of Agriculture (USDA) Agricultural Research Service (ARS) (CRIS Project 5030-22000-019-00D) and the Iowa Agriculture and Home Economics Experiment Station, Ames, IA (Project 3543). Any mention of products or services is for research purposes only, and does not constitute an endorsement for use by USDA. USDA is an equal opportunity employer and provider. Authors would like to thank anonymous reviewers for their constructive criticisms and comments to improve this manuscript. Funding Information: This research was supported by the National Natural Science Foundation of China (Award number: 31772163), National Key Research and Development Foundation, Ministry of Science and Technology of China (Award number: 2016YFD0300705), China Agriculture Research System of MOF and MARA (Award number: CARS-3). The information reported in this paper is part of a project of the Kentucky Agricultural Experiment Station and is published with the approval of the Director. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Contributions by BSC was supported by the United States Department of Agriculture ( USDA ) Agricultural Research Service ( ARS ) (CRIS Project 5030-22000-019-00D) and the Iowa Agriculture and Home Economics Experiment Station, Ames, IA (Project 3543). Any mention of products or services is for research purposes only, and does not constitute an endorsement for use by USDA. USDA is an equal opportunity employer and provider. Authors would like to thank anonymous reviewers for their constructive criticisms and comments to improve this manuscript. Publisher Copyright: {\textcopyright} 2021",

year = "2022",

month = mar,

doi = "10.1016/j.ibmb.2021.103579",

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volume = "142",

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Li, X, Zhang, F, Coates, B, Wei, C, Zhu, X, Zhang, Y & Zhou, X 2022, 'Temporal analysis of microRNAs associated with wing development in the English grain aphid, Sitobion avenae (F.) (Homoptera: Aphidiae): Functional dissection of miRNAs associated with wing development in Sitobion avenae', Insect Biochemistry and Molecular Biology, vol. 142, 103579. https://doi.org/10.1016/j.ibmb.2021.103579

Temporal analysis of microRNAs associated with wing development in the English grain aphid, Sitobion avenae (F.) (Homoptera: Aphidiae) : Functional dissection of miRNAs associated with wing development in Sitobion avenae. / Li, Xiangrui; Zhang, Fangmei; Coates, Brad et al.

In: Insect Biochemistry and Molecular Biology, Vol. 142, 103579, 03.2022.

Research output: Contribution to journal › Article › peer-review

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AU - Zhou, Xuguo

N1 - Funding Information: This research was supported by the National Natural Science Foundation of China (Award number: 31772163), National Key Research and DevelopmentFoundation, Ministry of Science and Technology of China (Award number: 2016YFD0300705), China Agriculture Research System of MOF and MARA (Award number: CARS-3). The information reported in this paper is part of a project of the Kentucky Agricultural Experiment Station and is published with the approval of the Director. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Contributions by BSC was supported by the United States Department of Agriculture (USDA) Agricultural Research Service (ARS) (CRIS Project 5030-22000-019-00D) and the Iowa Agriculture and Home Economics Experiment Station, Ames, IA (Project 3543). Any mention of products or services is for research purposes only, and does not constitute an endorsement for use by USDA. USDA is an equal opportunity employer and provider. Authors would like to thank anonymous reviewers for their constructive criticisms and comments to improve this manuscript. Funding Information: This research was supported by the National Natural Science Foundation of China (Award number: 31772163), National Key Research and Development Foundation, Ministry of Science and Technology of China (Award number: 2016YFD0300705), China Agriculture Research System of MOF and MARA (Award number: CARS-3). The information reported in this paper is part of a project of the Kentucky Agricultural Experiment Station and is published with the approval of the Director. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Contributions by BSC was supported by the United States Department of Agriculture ( USDA ) Agricultural Research Service ( ARS ) (CRIS Project 5030-22000-019-00D) and the Iowa Agriculture and Home Economics Experiment Station, Ames, IA (Project 3543). Any mention of products or services is for research purposes only, and does not constitute an endorsement for use by USDA. USDA is an equal opportunity employer and provider. Authors would like to thank anonymous reviewers for their constructive criticisms and comments to improve this manuscript. Publisher Copyright: © 2021

PY - 2022/3

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N2 - Molecular mechanisms underlying 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 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 recent progresses in the genetic understanding of wing polyphenism, the influence of environmental cues remains unclear. To investigate the involvement of miRNAs in wing development, we sequenced small RNA libraries of the English grain aphid, Sitobion avenae (F.) across six different developmental stages. As a result, we identified 113 conserved and 193 S. avenae-specific miRNAs. Gene Ontology and KEGG pathway analyses of putative target mRNAs for the six differentially expressed miRNAs are enriched for wing development processes. Dietary uptake of miR-263a, miR-316, and miR-184a agomirs and antagomirs led to significantly higher mortality (>70%) and a lower proportion of winged morphs (<5%). On the other hand, wing malformation was observed in miR-2 and miR-306 agomirs and miR-2 and miR-14 antagomirs, respectively, suggesting their involvement in S. avenae wing morphogenesis. These combined results not only shed light on the regulatory role of miRNAs in wing dimorphism, but also provide potential novel targets for the long-term sustainable management of S. avenae, a devastating global grain pest.

AB - Molecular mechanisms underlying 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 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 recent progresses in the genetic understanding of wing polyphenism, the influence of environmental cues remains unclear. To investigate the involvement of miRNAs in wing development, we sequenced small RNA libraries of the English grain aphid, Sitobion avenae (F.) across six different developmental stages. As a result, we identified 113 conserved and 193 S. avenae-specific miRNAs. Gene Ontology and KEGG pathway analyses of putative target mRNAs for the six differentially expressed miRNAs are enriched for wing development processes. Dietary uptake of miR-263a, miR-316, and miR-184a agomirs and antagomirs led to significantly higher mortality (>70%) and a lower proportion of winged morphs (<5%). On the other hand, wing malformation was observed in miR-2 and miR-306 agomirs and miR-2 and miR-14 antagomirs, respectively, suggesting their involvement in S. avenae wing morphogenesis. These combined results not only shed light on the regulatory role of miRNAs in wing dimorphism, but also provide potential novel targets for the long-term sustainable management of S. avenae, a devastating global grain pest.

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Li X, Zhang F, Coates B, Wei C, Zhu X, Zhang Y et al. Temporal analysis of microRNAs associated with wing development in the English grain aphid, Sitobion avenae (F.) (Homoptera: Aphidiae): Functional dissection of miRNAs associated with wing development in Sitobion avenae. Insect Biochemistry and Molecular Biology. 2022 Mar;142:103579. doi: 10.1016/j.ibmb.2021.103579

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

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

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