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PLoS Biol. 2014 Nov 25;12(11):e1002005. doi: 10.1371/journal.pbio.1002005. eCollection 2014 Nov.

The first myriapod genome sequence reveals conservative arthropod gene content and genome organisation in the centipede Strigamia maritima.

Author information

1
The Department of Ecology, Evolution and Behavior, The Alexander Silberman Institute of Life Sciences, The Hebrew University of Jerusalem, Givat Ram, Jerusalem, Israel.
2
The Scottish Oceans Institute, Gatty Marine Laboratory, University of St Andrews, St Andrews, Fife, United Kingdom.
3
Department of Zoology, University of Cambridge, Cambridge, United Kingdom.
4
Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, Texas, United States of America.
5
EMBL - European Bioinformatics Institute, Hinxton, Cambridgeshire, United Kingdom.
6
Institut für Biowissenschaften, Universität Rostock, Abt. Genetik, Rostock, Germany.
7
Departament de Genètica and Institut de Recerca de la Biodiversitat (IRBio), Universitat de Barcelona, Barcelona, Spain; Consejo Nacional de Investigaciones Científicas y Tecnológicas (CONICET), Universidad Nacional de Tucumán, Facultad de Ciencias Naturales e Instituto Miguel Lillo, San Miguel de Tucumán, Argentina.
8
School of Life Sciences, University of Sussex, Brighton, United Kingdom.
9
Department of Zoology, University of Cambridge, Cambridge, United Kingdom; Institute of Molecular Biology & Biotechnology, Foundation for Research & Technology - Hellas, Heraklion, Crete, Greece.
10
Department of Zoology, National University of Ireland, Galway, Ireland.
11
Department of Biochemistry, University of Cambridge, Cambridge, United Kingdom.
12
Evolutionsbiologie, Zoologisches Institut, Universität Basel, Basel, Switzerland; Swiss Tropical and Public Health Institute, Basel, Switzerland.
13
Centre for Genomic Regulation, Barcelona, Barcelona, Spain.
14
Gravida and Genetics Otago, Biochemistry Department, University of Otago, Dunedin, New Zealand.
15
Evolutionsbiologie, Zoologisches Institut, Universität Basel, Basel, Switzerland.
16
Razavi Newman Center for Bioinformatics, Salk Institute, La Jolla, California, United States of America; Scripps Translational Science Institute, La Jolla, California, United States of America.
17
The Babraham Institute, Cambridge, United Kingdom.
18
Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts, United States of America.
19
Centre for Genomic Regulation, Barcelona, Barcelona, Spain; Universitat Pompeu Fabra (UPF), Barcelona, Spain; Institució Catalana de Recerca i Estudis Avançats (ICREA), Barcelona, Spain.
20
Department of Biochemistry and Cell Biology, Center for Developmental Genetics, Stony Brook University, Stony Brook, New York, United States of America.
21
Department of Biology, Hendrix College, Conway, Arkansas, United States of America.
22
Faculty of Life Sciences, University of Manchester, Manchester, United Kingdom.
23
Center for Functional and Comparative Insect Genomics, University of Copenhagen, Copenhagen, Denmark.
24
Universitat Pompeu Fabra (UPF), Barcelona, Spain; Center for Genomic Regulation, Barcelona, Spain.
25
Department of Ecology and Evolutionary Biology, Rice University, Houston, Texas, United States of America.
26
Institut für Biologie, Martin-Luther-Universität Halle-Wittenberg, Halle, Germany.
27
School of Life Sciences, The Chinese University of Hong Kong, Shatin, NT, Hong Kong SAR, China.
28
Department of Biochemistry and Cell Biology, Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands.
29
Department of Genetics, University of Cambridge, Cambridge, United Kingdom.
30
Max F. Perutz Laboratories, University of Vienna, Vienna, Austria.
31
Institut für Biologie, Martin-Luther-Universität Halle-Wittenberg, Halle, Germany; Department of Laboratory Medicine, University Hospital Halle (Saale), Halle (Saale), Germany.
32
Department of Genetics, Evolution and Environment, University College London, London, United Kingdom.
33
Razavi Newman Center for Bioinformatics, Salk Institute, La Jolla, California, United States of America.
34
Max F. Perutz Laboratories, University of Vienna, Vienna, Austria; Center for Integrative Bioinformatics Vienna, Max F. Perutz Laboratories, University of Vienna, Medical University of Vienna, Vienna, Austria.
35
Hubrecht Institute for Developmental Biology and Stem Cell Research, Utrecht, The Netherlands.
36
Harte Research Institute, Texas A&M University Corpus Christi, Corpus Christi, Texas, United States of America.
37
Department of Entomology, University of Illinois at Urbana-Champaign, Urbana, Illinois, United States of America.
38
Departament de Genètica and Institut de Recerca de la Biodiversitat (IRBio), Universitat de Barcelona, Barcelona, Spain.
39
Department of Zoology, University of Cambridge, Cambridge, United Kingdom; Institute for Biochemistry and Biology, University Potsdam, Potsdam-Golm, Germany.
40
Max F. Perutz Laboratories, University of Vienna, Vienna, Austria; Research Platform "Marine Rhythms of Life", Vienna, Austria.
41
Institute of Biology, Leiden University, Leiden, The Netherlands.
42
Center for Integrative Bioinformatics Vienna, Max F. Perutz Laboratories, University of Vienna, Medical University of Vienna, Vienna, Austria; Bioinformatics and Computational Biology, Faculty of Computer Science, University of Vienna, Vienna, Austria.
43
Department of Cellular Biology, University of Georgia, Athens, Georgia, United States of America.

Abstract

Myriapods (e.g., centipedes and millipedes) display a simple homonomous body plan relative to other arthropods. All members of the class are terrestrial, but they attained terrestriality independently of insects. Myriapoda is the only arthropod class not represented by a sequenced genome. We present an analysis of the genome of the centipede Strigamia maritima. It retains a compact genome that has undergone less gene loss and shuffling than previously sequenced arthropods, and many orthologues of genes conserved from the bilaterian ancestor that have been lost in insects. Our analysis locates many genes in conserved macro-synteny contexts, and many small-scale examples of gene clustering. We describe several examples where S. maritima shows different solutions from insects to similar problems. The insect olfactory receptor gene family is absent from S. maritima, and olfaction in air is likely effected by expansion of other receptor gene families. For some genes S. maritima has evolved paralogues to generate coding sequence diversity, where insects use alternate splicing. This is most striking for the Dscam gene, which in Drosophila generates more than 100,000 alternate splice forms, but in S. maritima is encoded by over 100 paralogues. We see an intriguing linkage between the absence of any known photosensory proteins in a blind organism and the additional absence of canonical circadian clock genes. The phylogenetic position of myriapods allows us to identify where in arthropod phylogeny several particular molecular mechanisms and traits emerged. For example, we conclude that juvenile hormone signalling evolved with the emergence of the exoskeleton in the arthropods and that RR-1 containing cuticle proteins evolved in the lineage leading to Mandibulata. We also identify when various gene expansions and losses occurred. The genome of S. maritima offers us a unique glimpse into the ancestral arthropod genome, while also displaying many adaptations to its specific life history.

PMID:
25423365
PMCID:
PMC4244043
DOI:
10.1371/journal.pbio.1002005
[Indexed for MEDLINE]
Free PMC Article

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