Comparative genomic analysis of six Glossina genomes, vectors of African trypanosomes.


Journal

Genome biology
ISSN: 1474-760X
Titre abrégé: Genome Biol
Pays: England
ID NLM: 100960660

Informations de publication

Date de publication:
02 09 2019
Historique:
received: 31 01 2019
accepted: 22 07 2019
entrez: 4 9 2019
pubmed: 4 9 2019
medline: 29 1 2020
Statut: epublish

Résumé

Tsetse flies (Glossina sp.) are the vectors of human and animal trypanosomiasis throughout sub-Saharan Africa. Tsetse flies are distinguished from other Diptera by unique adaptations, including lactation and the birthing of live young (obligate viviparity), a vertebrate blood-specific diet by both sexes, and obligate bacterial symbiosis. This work describes the comparative analysis of six Glossina genomes representing three sub-genera: Morsitans (G. morsitans morsitans, G. pallidipes, G. austeni), Palpalis (G. palpalis, G. fuscipes), and Fusca (G. brevipalpis) which represent different habitats, host preferences, and vectorial capacity. Genomic analyses validate established evolutionary relationships and sub-genera. Syntenic analysis of Glossina relative to Drosophila melanogaster shows reduced structural conservation across the sex-linked X chromosome. Sex-linked scaffolds show increased rates of female-specific gene expression and lower evolutionary rates relative to autosome associated genes. Tsetse-specific genes are enriched in protease, odorant-binding, and helicase activities. Lactation-associated genes are conserved across all Glossina species while male seminal proteins are rapidly evolving. Olfactory and gustatory genes are reduced across the genus relative to other insects. Vision-associated Rhodopsin genes show conservation of motion detection/tracking functions and variance in the Rhodopsin detecting colors in the blue wavelength ranges. Expanded genomic discoveries reveal the genetics underlying Glossina biology and provide a rich body of knowledge for basic science and disease control. They also provide insight into the evolutionary biology underlying novel adaptations and are relevant to applied aspects of vector control such as trap design and discovery of novel pest and disease control strategies.

Sections du résumé

BACKGROUND
Tsetse flies (Glossina sp.) are the vectors of human and animal trypanosomiasis throughout sub-Saharan Africa. Tsetse flies are distinguished from other Diptera by unique adaptations, including lactation and the birthing of live young (obligate viviparity), a vertebrate blood-specific diet by both sexes, and obligate bacterial symbiosis. This work describes the comparative analysis of six Glossina genomes representing three sub-genera: Morsitans (G. morsitans morsitans, G. pallidipes, G. austeni), Palpalis (G. palpalis, G. fuscipes), and Fusca (G. brevipalpis) which represent different habitats, host preferences, and vectorial capacity.
RESULTS
Genomic analyses validate established evolutionary relationships and sub-genera. Syntenic analysis of Glossina relative to Drosophila melanogaster shows reduced structural conservation across the sex-linked X chromosome. Sex-linked scaffolds show increased rates of female-specific gene expression and lower evolutionary rates relative to autosome associated genes. Tsetse-specific genes are enriched in protease, odorant-binding, and helicase activities. Lactation-associated genes are conserved across all Glossina species while male seminal proteins are rapidly evolving. Olfactory and gustatory genes are reduced across the genus relative to other insects. Vision-associated Rhodopsin genes show conservation of motion detection/tracking functions and variance in the Rhodopsin detecting colors in the blue wavelength ranges.
CONCLUSIONS
Expanded genomic discoveries reveal the genetics underlying Glossina biology and provide a rich body of knowledge for basic science and disease control. They also provide insight into the evolutionary biology underlying novel adaptations and are relevant to applied aspects of vector control such as trap design and discovery of novel pest and disease control strategies.

Identifiants

pubmed: 31477173
doi: 10.1186/s13059-019-1768-2
pii: 10.1186/s13059-019-1768-2
pmc: PMC6721284
doi:

Substances chimiques

DNA Transposable Elements 0
Insect Proteins 0

Types de publication

Comparative Study Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

187

Subventions

Organisme : FIC NIH HHS
ID : D43 TW007391
Pays : United States
Organisme : NIH HHS
ID : R01AI051584
Pays : United States
Organisme : NIAID NIH HHS
ID : R01 AI051584
Pays : United States
Organisme : NIAID NIH HHS
ID : R01 AI068932
Pays : United States
Organisme : NIH HHS
ID : R03TW008413
Pays : United States
Organisme : NHGRI NIH HHS
ID : U54HG003079
Pays : United States
Organisme : NIAID NIH HHS
ID : U01 AI115648
Pays : United States
Organisme : NIH HHS
ID : R03TW009444
Pays : United States
Organisme : NIH HHS
ID : U01AI115648
Pays : United States
Organisme : National Institute of Allergy and Infectious Diseases
ID : R21AI109263
Pays : International

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Auteurs

Geoffrey M Attardo (GM)

Department of Entomology and Nematology, University of California, Davis, Davis, CA, USA. gmattardo@ucdavis.edu.

Adly M M Abd-Alla (AMM)

Insect Pest Control Laboratory, Joint FAO/IAEA Division of Nuclear Techniques in Food & Agriculture, Vienna, Vienna, Austria.

Alvaro Acosta-Serrano (A)

Department of Vector Biology, Liverpool School of Tropical Medicine, Merseyside, Liverpool, UK.

James E Allen (JE)

VectorBase, European Molecular Biology Laboratory, European Bioinformatics Institute (EMBL-EBI), Cambridge, Cambridgeshire, UK.

Rosemary Bateta (R)

Department of Biochemistry, Biotechnology Research Institute - Kenya Agricultural and Livestock Research Organization, Kikuyu, Kenya.

Joshua B Benoit (JB)

Department of Biological Sciences, University of Cincinnati, Cincinnati, OH, USA.

Kostas Bourtzis (K)

Insect Pest Control Laboratory, Joint FAO/IAEA Division of Nuclear Techniques in Food & Agriculture, Vienna, Vienna, Austria.

Jelle Caers (J)

Department of Biology - Functional Genomics and Proteomics Group, KU Leuven, Leuven, Belgium.

Guy Caljon (G)

Laboratory of Microbiology, Parasitology and Hygiene, University of Antwerp, Antwerp, Belgium.

Mikkel B Christensen (MB)

VectorBase, European Molecular Biology Laboratory, European Bioinformatics Institute (EMBL-EBI), Cambridge, Cambridgeshire, UK.

David W Farrow (DW)

Department of Biological Sciences, University of Cincinnati, Cincinnati, OH, USA.

Markus Friedrich (M)

Department of Biological Sciences, Wayne State University, Detroit, MI, USA.

Aurélie Hua-Van (A)

Laboratoire Evolution, Genomes, Comportement, Ecologie, CNRS, IRD, Univ. Paris-Sud, Université Paris-Saclay, Gif-sur-Yvette, France.

Emily C Jennings (EC)

Department of Biological Sciences, University of Cincinnati, Cincinnati, OH, USA.

Denis M Larkin (DM)

Department of Comparative Biomedical Sciences, Royal Veterinary College, London, UK.

Daniel Lawson (D)

Department of Life Sciences, Imperial College London, London, UK.

Michael J Lehane (MJ)

Department of Vector Biology, Liverpool School of Tropical Medicine, Merseyside, Liverpool, UK.

Vasileios P Lenis (VP)

Schools of Medicine and Dentistry, University of Plymouth, Plymouth, UK.

Ernesto Lowy-Gallego (E)

VectorBase, European Molecular Biology Laboratory, European Bioinformatics Institute (EMBL-EBI), Cambridge, Cambridgeshire, UK.

Rosaline W Macharia (RW)

Molecular Biology and Bioinformatics Unit, International Center for Insect Physiology and Ecology, Nairobi, Kenya.
Centre for Biotechnology and Bioinformatics, University of Nairobi, Nairobi, Kenya.

Anna R Malacrida (AR)

Department of Biology and Biotechnology, University of Pavia, Pavia, Italy.

Heather G Marco (HG)

Department of Biological Sciences, University of Cape Town, Rondebosch, South Africa.

Daniel Masiga (D)

Molecular Biology and Bioinformatics Unit, International Center for Insect Physiology and Ecology, Nairobi, Kenya.

Gareth L Maslen (GL)

VectorBase, European Molecular Biology Laboratory, European Bioinformatics Institute (EMBL-EBI), Cambridge, Cambridgeshire, UK.

Irina Matetovici (I)

Biomedical Sciences, Institute of Tropical Medicine, Antwerp, Belgium.

Richard P Meisel (RP)

Department of Biology and Biochemistry, University of Houston, Houston, TX, USA.

Irene Meki (I)

Insect Pest Control Laboratory, Joint FAO/IAEA Division of Nuclear Techniques in Food & Agriculture, Vienna, Vienna, Austria.

Veronika Michalkova (V)

Department of Biological Sciences, Florida International University, Miami, Florida, USA.
Institute of Zoology, Slovak Academy of Sciences, Bratislava, Slovakia.

Wolfgang J Miller (WJ)

Department of Cell and Developmental Biology, Medical University of Vienna, Vienna, Austria.

Patrick Minx (P)

McDonnell Genome Institute, Washington University School of Medicine, St. Louis, MO, USA.

Paul O Mireji (PO)

Department of Biochemistry, Biotechnology Research Institute - Kenya Agricultural and Livestock Research Organization, Kikuyu, Kenya.
Centre for Geographic Medicine Research Coast, Kenya Medical Research Institute, Kilifi, Kenya.

Lino Ometto (L)

Department of Sustainable Ecosystems and Bioresources, Research and Innovation Centre, Fondazione Edmund Mach, San Michele all'Adige, TN, Italy.
Department of Biology and Biotechnology, University of Pavia, Pavia, Italy.

Andrew G Parker (AG)

Insect Pest Control Laboratory, Joint FAO/IAEA Division of Nuclear Techniques in Food & Agriculture, Vienna, Vienna, Austria.

Rita Rio (R)

Department of Biology, West Virginia University, Morgantown, WV, USA.

Clair Rose (C)

Department of Vector Biology, Liverpool School of Tropical Medicine, Merseyside, Liverpool, UK.

Andrew J Rosendale (AJ)

Department of Biology, Mount St. Joseph University, Cincinnati, OH, USA.
Department of Biological Sciences, University of Cincinnati, Cincinnati, OH, USA.

Omar Rota-Stabelli (O)

Department of Sustainable Ecosystems and Bioresources, Research and Innovation Centre, Fondazione Edmund Mach, San Michele all'Adige, TN, Italy.

Grazia Savini (G)

Department of Biology and Biotechnology, University of Pavia, Pavia, Italy.

Liliane Schoofs (L)

Department of Biology - Functional Genomics and Proteomics Group, KU Leuven, Leuven, Belgium.

Francesca Scolari (F)

Department of Biology and Biotechnology, University of Pavia, Pavia, Italy.

Martin T Swain (MT)

Institute of Biological, Environmental and Rural Sciences, Aberystwyth University, Aberystwyth, Ceredigion, UK.

Peter Takáč (P)

Department of Animal Systematics, Ústav zoológie SAV; Scientica, Ltd, Bratislava, Slovakia.

Chad Tomlinson (C)

McDonnell Genome Institute, Washington University School of Medicine, St. Louis, MO, USA.

George Tsiamis (G)

Department of Environmental and Natural Resources Management, University of Patras, Agrinio, Etoloakarnania, Greece.

Jan Van Den Abbeele (J)

Biomedical Sciences, Institute of Tropical Medicine, Antwerp, Belgium.

Aurelien Vigneron (A)

Department of Epidemiology of Microbial Diseases, Yale School of Public Health, New Haven, CT, USA.

Jingwen Wang (J)

School of Life Sciences, Fudan University, Shanghai, China.

Wesley C Warren (WC)

McDonnell Genome Institute, Washington University School of Medicine, St. Louis, MO, USA.
Bond Life Sciences Center, University of Missouri, Columbia, MO, USA.

Robert M Waterhouse (RM)

Department of Ecology & Evolution, Swiss Institute of Bioinformatics, University of Lausanne, Lausanne, Switzerland.

Matthew T Weirauch (MT)

Center for Autoimmune Genomics and Etiology and Divisions of Biomedical Informatics and Developmental Biology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, USA.

Brian L Weiss (BL)

Department of Epidemiology of Microbial Diseases, Yale School of Public Health, New Haven, CT, USA.

Richard K Wilson (RK)

McDonnell Genome Institute, Washington University School of Medicine, St. Louis, MO, USA.

Xin Zhao (X)

CAS Center for Influenza Research and Early-warning (CASCIRE), Chinese Academy of Sciences, Beijing, China.

Serap Aksoy (S)

Department of Epidemiology of Microbial Diseases, Yale School of Public Health, New Haven, CT, USA. serap.aksoy@yale.edu.

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