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

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posted on 2023-06-08, 23:59 authored by Chris Tyler-Smith, Ariel D Chipman, David E K Ferrier, Carlo Brena, Jiaxin Qu, Daniel S T Hughes, Reinhard Schröder, Montserrat Torres-Oliva, Nadia Znassi, Huaiyang Jiang, Francisca C Almeida, Claudio AlonsoClaudio Alonso, Zivkos Apostolou, Peshtewani Aqrawi, Wallace Arthur, Jennifer C J Barna, Kerstin P Blankenburg, Daniela Brites, Salvador Capella-Gutiérrez, Marcus Coyle, Peter K Dearden, Louis Du Pasquier, Elizabeth J Duncan, Dieter Ebert, Cornelius Eibner, Galina Erikson, Peter D Evans, Cassandra G Extavour, Liezl Francisco, Toni Gabaldón, William J Gillis, Elizabeth A Goodwin-Horn, Jack E Green, Sam Griffiths-Jones, Cornelis J P Grimmelikhuijzen, Sai Gubbala, Roderic Guigó, Yi Han, Frank Hauser, Paul Havlak, Luke Hayden, Sophie Helbing, Michael Holder, Jerome H L Hui, Julia P Hunn, Vera S Hunnekuhl, LaRonda Jackson, Mehwish Javaid, Shalini N Jhangiani, Francis M Jiggins, Tamsin E Jones, Tobias S Kaiser, Divya Kalra, Nathan J Kenny, Viktoriya Korchina, Christie L Kovar, F. Bernhard Kraus, François Lapraz, Sandra L Lee, Jie Lv, Christigale Mandapat, Gerard Manning, Marco Mariotti, Robert Mata, Tittu Mathew, Tobias Neumann, Irene Newsham, Dinh N Ngo, Maria Ninova, Geoffrey Okwuonu, Fiona Ongeri, William J Palmer, Shobha Patil, Pedro Patraquim, Christopher Pham, Ling-Ling Pu, Nicholas H Putman, Catherine Rabouille, Olivia Mendivil Ramos, Adelaide C Rhodes, Helen E Robertson, Hugh M Robertson, Matthew Ronshaugen, Julio Rozas, Nehad Saada, Alejandro Sánchez-Gracia, Steven E Scherer, Andrew M Schurko, Kenneth W Siggens, DeNard Simmons, Anna Stief, Eckart Stolle, Maximilian J Telford, Kristin Tessmar-Raible, Rebecca Thornton, Maurijn van der Zee, Arndt von Haeseler, James M Williams, Judith H Willis, Yuanqing Wu, Xiaoyan Zou, Daniel Lawson, Donna M Muzny, Kim C Worley, Richard A Gibbs, Michael Akam, Stephen Richards
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.

Funding

The molecular regulation of Hox genes during animal development; G0952; WELLCOME TRUST; 098410/Z/12/Z

History

Publication status

  • Published

File Version

  • Published version

Journal

PLoS Biology

ISSN

1545-7885

Publisher

Public Library of Science

Issue

11

Volume

12

Page range

1-24

Article number

e1002005

Department affiliated with

  • Neuroscience Publications

Full text available

  • Yes

Peer reviewed?

  • Yes

Legacy Posted Date

2016-01-15

First Open Access (FOA) Date

2016-01-15

First Compliant Deposit (FCD) Date

2016-01-15

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