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Title: Massive shift in gene expression during transitions between developmental stages of the Gall Midge, Mayetiola destructor

Author
item Chen, Ming-Shun
item LIU, SANZHEN - Kansas State University
item WANG, HAIYAN - Kansas State University
item CHENG, XIAOYAN - Kansas State University
item EL BOUHSSINI, MUSTAPHA - International Center For Agricultural Research In The Dry Areas (ICARDA)
item WHITWORTH, ROBERT - Kansas State University

Submitted to: PLOS ONE
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/2/2016
Publication Date: 5/25/2016
Publication URL: https://handle.nal.usda.gov/10113/5491329
Citation: Chen, M., Liu, S., Wang, H., Cheng, X., El Bouhssini, M., Whitworth, R.J. 2016. Massive shift in gene expression during transitions between developmental stages of the Gall Midge, Mayetiola destructor. PLoS One. 11(5): e0155616. doi:10.1371/journal.pone.0155616.

Interpretive Summary: Hessian fly is a destructive pest of wheat and a model organism to study gall midges. Hessian fly has six developmental stages including eggs, three instars of larvae, pupae and adults. The molecular mechanisms controlling the transition between different stages are not known and could provide useful information to develop new means to control this destructive pest. This research used the recently developed technology called RNA-Seq to systematically analyze genes that are differentially expressed between two successive stages of Hessian fly. We found that there was a massive shift in gene expression when the insect transitioned from one stage to the next, and each stage expressed a unique combination of genes. The large data sets of differentially expressed genes identified in this study should be very useful to provide targets for further research that could eventually lead to new means to control this insect pest. The information reported in this study should also be very useful for comparative researches for other insect species as well as for non-insect organisms.

Technical Abstract: The gall midge Mayetiola destructor is a destructive pest of wheat worldwide and a model organism for studying plant – insect interactions. The insect has six different developmental stages including eggs, three instars of larvae, pupae, and adults. Molecular mechanisms controlling the transition between different developmental stages remain unknown. Here we systematically analyzed (via RNA-sequencing) genes that were expressed differentially between two successive developmental stages, including larvae at 1, 3, 5, and 7 days, pupae, and adults. A total of 17,344 genes were expressed during one or more of these identified stages of the insect. Among the expressed genes, 38-68% were differently expressed between two successive stages, with roughly equal percentages of up- and down-regulated genes. Analysis of the functions of the differentially expressed genes revealed that each developmental stage had some unique types of expressed genes that are characteristic of the physiology at that stage. For example, effector genes for host manipulation and genes associated with cell division were broadly up-regulated when 1-day old larvae advanced to 3-day old larvae, reflecting the state of actively attacking host plants and cell division-based larval growth during this period. This is the first genome-wide analysis of genes differentially expressed in different developmental stages in a gall midge species and also represents the most comprehensive analysis so far among all other insect species. The large dataset of up- and down-regulated genes in each stage of the insect shall be very useful for future research to elucidate molecular mechanisms regulating insect development and other biological processes.