title: Ultrabithorax is essential for bacteriocyte development.
abstract: Symbiosis often entails the emergence of novel adaptive traits in organisms. Microbial symbionts are indispensable for diverse insects via provisioning of essential nutrients, wherein novel host cells and organs for harboring the microbes, called bacteriocytes and bacteriomes, have evolved repeatedly. Molecular and developmental mechanisms underpinning the emergence of novel symbiotic cells and organs comprise an unsolved question in evolutionary developmental biology. Here, we report that a conserved homeotic gene, Ultrabithorax, plays a pivotal role in the bacteriocyte differentiation in a hemipteran insect Nysius plebeius. During embryonic development, six pairs of aggregated presumptive bacteriocytes appear on both sides of six abdominal segments, incorporate the symbiotic bacteria at the stage of germband retraction, and fuse into a pair of lateral bacteriomes at the stage of germband flip, where bacteriocyte-associated Ultrabithorax expression coincides with the symbiont infection process. Suppression of Ultrabithorax expression by maternal RNA interference results in disappearance of the bacteriocytes and the symbiont localization therein, suggesting that Ultrabithorax is involved in differentiation of the host cells for symbiosis. Suppression of other homeotic genes abdominal-A and Antennapedia disturbs integrity and positioning of the bacteriomes, affecting the configuration of the host organs for symbiosis. Our findings unveil the molecular and developmental mechanisms underlying the bacteriocyte differentiation, which may have evolved either via cooption of the transcription factors for inducing the novel symbiotic cells, or via revival of the developmental pathway for the bacteriocytes that had existed in the ancestral hemipterans.
authors.affiliation: Bioproduction Research Institute, National Institute of Advanced Industrial Science and Technology, Tsukuba 305-8566, Japan; Graduate School of Environmental Science, Hokkaido University, Sapporo 060-0810, Japan; Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba 305-8572, Japan;
authors.forename: Yu
authors.initials: Y
authors.lastname: Matsuura
authors.affiliation: Bioproduction Research Institute, National Institute of Advanced Industrial Science and Technology, Hokkaido Center, Sapporo 062-8517, Japan.
authors.forename: Yoshitomo
authors.initials: Y
authors.lastname: Kikuchi
authors.affiliation: Graduate School of Environmental Science, Hokkaido University, Sapporo 060-0810, Japan;
authors.forename: Toru
authors.initials: T
authors.lastname: Miura
authors.affiliation: Bioproduction Research Institute, National Institute of Advanced Industrial Science and Technology, Tsukuba 305-8566, Japan; Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba 305-8572, Japan; t-fukatsu@aist.go.jp.
authors.forename: Takema
authors.initials: T
authors.lastname: Fukatsu
mesh_terms: D000818:Animals; D001419:Bacteria; D001483:Base Sequence; D003001:Cloning, Molecular; D029721:Drosophila Proteins / Q000502:physiology*; D019143:Evolution, Molecular; D005260:Female; D020869:Gene Expression Profiling; D018507:Gene Expression Regulation, Developmental; D006430:Hemiptera / Q000382:microbiology / Q000502:physiology*; D018398:Homeodomain Proteins / Q000378:metabolism / Q000502:physiology*; D017403:In Situ Hybridization; D019476:Insect Proteins / Q000502:physiology*; D007814:Larva / Q000382:microbiology / Q000502:physiology; D008297:Male; D008855:Microscopy, Electron, Scanning; D008969:Molecular Sequence Data; D010641:Phenotype; D034622:RNA Interference; D013559:Symbiosis; D014157:Transcription Factors / Q000378:metabolism / Q000502:physiology*
chemical_list: D029721:Drosophila Proteins; D018398:Homeodomain Proteins; D019476:Insect Proteins; D014157:Transcription Factors; C066177:Ubx protein, Drosophila
keywords: bacteriocyte; evolution; homeotic gene; symbiosis; transcription factor