Abstract
BackgroundParasitoid wasps are well-known natural enemies of major agricultural pests and arthropod borne diseases. The parasitoid wasp Macrocentrus cingulum (Hymenoptera: Braconidae) has been widely used to control the notorious insect pests Ostrinia furnacalis (Asian Corn Borer) and O. nubilalis (European corn borer). One striking phenomenon exhibited by M. cingulum is polyembryony, the formation of multiple genetically identical offspring from a single zygote. Moreover, M. cingulum employs a passive parasitic strategy by preventing the host’s immune system from recognizing the embryo as a foreign body. Thus, the embryos evade the host’s immune system and are not encapsulated by host hemocytes. Unfortunately, the mechanism of both polyembryony and immune evasion remains largely unknown.ResultsWe report the genome of the parasitoid wasp M. cingulum. Comparative genomics analysis of M. cingulum and other 11 insects were conducted, finding some gene families with apparent expansion or contraction which might be linked to the parasitic behaviors or polyembryony of M. cingulum. Moreover, we present the evidence that the microRNA miR-14b regulates the polyembryonic development of M. cingulum by targeting the c-Myc Promoter-binding Protein 1 (MBP-1), histone-lysine N-methyltransferase 2E (KMT2E) and segmentation protein Runt. In addition, Hemomucin, an O-glycosylated transmembrane protein, protects the endoparasitoid wasp larvae from being encapsulated by host hemocytes. Motif and domain analysis showed that only the hemomucin in two endoparasitoids, M. cingulum and Venturia canescens, possessing the ability of passive immune evasion has intact mucin domain and similar O-glycosylation patterns, indicating that the hemomucin is a key factor modulating the immune evasion.ConclusionsThe microRNA miR-14b participates in the regulation of polyembryonic development, and the O-glycosylation of the mucin domain in the hemomucin confers the passive immune evasion in this wasp. These key findings provide new insights into the polyembryony and immune evasion.
Highlights
Parasitoid wasps are well-known natural enemies of major agricultural pests and arthropod borne diseases
The microRNA miR-14b participates in the regulation of polyembryonic development, and the O-glycosylation of the mucin domain in the hemomucin confers the passive immune evasion in this wasp
Assembly and annotation We sequenced the genome of M. cingulum from ~ 1000 male wasps of an inbred strain which was maintained by sibling mating for five generations
Summary
Parasitoid wasps are well-known natural enemies of major agricultural pests and arthropod borne diseases. Parasitoid wasps are a group of hymenopteran insects that parasitize the eggs, larvae or pupae of other arthropods [1] These wasps differ from other parasitic organisms because they kill their host, and the adult wasps are free-living. Polyembryony appears in only some parasitic species within four families of Hymenoptera and one species of Strepsiptera in insects, and is believed to have evolved independently at least four times among parasitoid wasps [6] This includes the endoparasitic wasp Macrocentrus cingulum, for which some details of polyembryonic development have been described [6, 7]. Proliferation of embryos are mainly related to the egg cleavage and the formation of morula These meticulous physical observations of polyembryonic development have not yet been complemented with molecular analyses. There remains tremendous opportunities for investigating the molecular mechanisms underlying the developmental complexity of polyembryony
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