Conserved and unique putative effectors expressed in the salivary glands of three related gall midge species

Authors: AL-JBORY, ZAINAB - Kansas State University; EL-BOUHSSINI, MUSTAPHA - Kansas State University; Chen, Ming-Shun

Submitted to: Journal of Insect Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/7/2018
Publication Date: 1/11/2019
Citation: Al-Jbory, Z., El-Bouhssini, M., Chen, M. 2019. Conserved and unique putative effectors expressed in the salivary glands of three related gall midge species. Journal of Insect Science. 18(5):15; 1-9. https://doi.org/10.1093/jisesa/iey135.
DOI: https://doi.org/10.1093/jisesa/iey135

Interpretive Summary: Hessian fly, barley midge, and oat midge are insect pests of small grains. The three species look very similar and are very hard to distinguish by human eye. The three species also have the same feeding mechanism, namely, injecting saliva to control host plants, resulting in identical plant symptoms. Yet, Hessian fly mainly attacks wheat, barley midge only attacks barley, while oat midge only attacks oat. We hypothesize that each of the midges injects two sets of salivary proteins into host plants, one common set for plant manipulation (resulting in identical symptom) and one set unique to each species to neutralize specific defense response from different host plant. This study has analyzed putative genes encoding salivary proteins from the three midges. By comparison, we have identified genes encoding salivary proteins common to the three midges, and genes encoding salivary proteins that are unique to each species. The results provide a basis for future studies to determine how all three species to manipulate host plants, and how each species to overcome defenses from the respective host plants. A better understanding of the feeding mechanism may result in better methods for controlling these destructive insect pests.

Technical Abstract: Species in the stem gall midge genus Mayetiola (Diptera: Cecidomyiidae) cause serious damage to small grain crops. Among Mayetiola species are Hessian fly (M. destructor), barley midge (M. hordei), and oat midge (M. avenae). Larvae of these species inject saliva into host tissues to manipulate plants. To identify putative effectors, transcriptomic analyses were conducted on transcripts encoding Secreted Salivary Gland Proteins (SSGPs) from first instar larvae of the barley and oat midges, since SSGPs are the most likely source for effector proteins delivered into host tissues. From barley midge, 178 SSGP-encoding unigenes were identified, which were sorted into 51 groups. From oat midge, 194 were obtained and sorted into 50 groups. Predicted proteins within a group had a highly conserved secretion signal peptide and shared at least 30% amino acid identity. Among the identified unigenes from both barley and oat midges, ~68% are conserved either among the three species or between two of them. Conserved SSGPs included members belonging to SSGP-1, SSGP-4, SSGP-11, and SSGP-71 families. Unconventional conservation patterns exist among family members within a species and among different gall midges, indicating that these genes are under high selection pressure, a characteristic of effector genes. SSGPs that are unique to each species were also identified. Those conserved SSGPs may be responsible for host manipulation since the three gall midges produce identical phenotypic symptoms to host plants, whereas the SSGPs unique to each species may be responsible for different host specificity.