title: Proteome Analysis of the Hemolymph, Mushroom Body, and Antenna Provides Novel Insight into Honeybee Resistance against Varroa Infestation.
abstract: Varroa destructor has been identified as a major culprit responsible for the losses of millions of honeybee colonies. Varroa sensitive hygiene (VSH) is a suite of behaviors from adult bees to suppress mite reproduction by uncapping and/or removing mite infested pupae from a sealed brood. Despite the efforts to elucidate the molecular underpinnings of VSH, they remain largely unknown. We investigated the proteome of mushroom bodies (MBs) and antennae of adult bees with and without VSH from a stock selected for VSH based on their response to artificially Varroa-infected brood cells by near-infrared camera observation. The pupal hemolymph proteome was also compared between the VSH-line and the line that was not selected for VSH. The identified 8609 proteins in the hemolymph, MBs, and antennae represent the most depth coverage of the honeybee proteome (>55%) to date. In the hemolymph, the VSH-line adapts a unique strategy to boost the social immunity and drive pupal organogenesis by enhancing energy metabolism and protein biosynthesis. In MBs, the up-regulated proteins implicated in neuronal sensitivity suggest their roles to promote the execution of VSH by activation of synaptic vesicles and calcium channel activities. In antennae, the highly expressed proteins associated with sensitivity of olfactory senses and signal transmissions signify their roles by inputting a strong signal to the MBs for initiating VSH. These observations illustrate that the enhanced social immunities and olfactory and neuronal sensitivity play key roles in the combat against Varroa infestation. The identified candidate markers may be useful for accelerating marker-associated selection for VSH to aid in resistance to a parasite responsible for decline in honeybee health.
authors.affiliation: Institute of Apicultural Research/Key Laboratory of Pollinating Insect Biology, Ministry of Agriculture, Chinese Academy of Agricultural Science , Beijing 100093, China.
authors.forename: Han
authors.initials: H
authors.lastname: Hu
authors.affiliation: Institute for Bee ResearchHohen Neuendorf , F.-Engels-Strasse 32, 16540 Hohen Neuendorf, Germany.
authors.forename: Kaspar
authors.initials: K
authors.lastname: Bienefeld
authors.affiliation: Institute for Bee ResearchHohen Neuendorf , F.-Engels-Strasse 32, 16540 Hohen Neuendorf, Germany.
authors.forename: Jakob
authors.initials: J
authors.lastname: Wegener
authors.affiliation: Institute for Bee ResearchHohen Neuendorf , F.-Engels-Strasse 32, 16540 Hohen Neuendorf, Germany.
authors.forename: Fred
authors.initials: F
authors.lastname: Zautke
authors.affiliation: Institute of Apicultural Research/Key Laboratory of Pollinating Insect Biology, Ministry of Agriculture, Chinese Academy of Agricultural Science , Beijing 100093, China.
authors.forename: Yue
authors.initials: Y
authors.lastname: Hao
authors.affiliation: Institute of Apicultural Research/Key Laboratory of Pollinating Insect Biology, Ministry of Agriculture, Chinese Academy of Agricultural Science , Beijing 100093, China.
authors.forename: Mao
authors.initials: M
authors.lastname: Feng
authors.affiliation: Institute of Apicultural Research/Key Laboratory of Pollinating Insect Biology, Ministry of Agriculture, Chinese Academy of Agricultural Science , Beijing 100093, China.
authors.forename: Bin
authors.initials: B
authors.lastname: Han
authors.affiliation: Institute of Apicultural Research/Key Laboratory of Pollinating Insect Biology, Ministry of Agriculture, Chinese Academy of Agricultural Science , Beijing 100093, China.
authors.forename: Yu
authors.initials: Y
authors.lastname: Fang
authors.affiliation: Institute of Apicultural Research/Key Laboratory of Pollinating Insect Biology, Ministry of Agriculture, Chinese Academy of Agricultural Science , Beijing 100093, China.
authors.forename: Abebe Jenberie
authors.initials: AJ
authors.lastname: Wubie
authors.affiliation: Institute of Apicultural Research/Key Laboratory of Pollinating Insect Biology, Ministry of Agriculture, Chinese Academy of Agricultural Science , Beijing 100093, China.
authors.forename: Jianke
authors.initials: J
authors.lastname: Li
mesh_terms: D000818:Animals; D057506:Arthropod Antennae / Q000166:cytology; D001516:Bees / Q000276:immunology* / Q000469:parasitology; D004734:Energy Metabolism; D006458:Hemolymph / Q000737:chemistry; D006790:Host-Parasite Interactions / Q000276:immunology*; D008924:Mite Infestations / Q000276:immunology; D024521:Mushroom Bodies / Q000737:chemistry; D018034:Olfactory Receptor Neurons; D014176:Protein Biosynthesis; D020543:Proteome / Q000032:analysis*; D040901:Proteomics; D011679:Pupa / Q000469:parasitology; D015398:Signal Transduction; D015854:Up-Regulation; D057077:Varroidae / Q000472:pathogenicity*
chemical_list: D020543:Proteome
keywords: Apis mellifera; Varroa destructor; Varroa sensitive hygiene; antennae; hemolymph; mushroom body