TY - JOUR

T1 - The first myriapod genome sequence reveals conservative arthropod gene content and genome organisation in the centipede Strigamia maritima

AU - Chipman, Ariel D.

AU - Ferrier, David E.K.

AU - Brena, Carlo

AU - Qu, Jiaxin

AU - Hughes, Daniel S.T.

AU - Schröder, Reinhard

AU - Torres-Oliva, Montserrat

AU - Znassi, Nadia

AU - Jiang, Huaiyang

AU - Almeida, Francisca C

AU - Alonso, Claudio R

AU - Apostolou, Zivkos

AU - Aqrawi, Peshtewani

AU - Arthur, Wallace

AU - Barna, Jennifer C J

AU - Blankenburg, Kerstin P

AU - Brites, Daniela

AU - Capella-Gutiérrez, Salvador

AU - Coyle, Marcus

AU - Dearden, Peter K

AU - Du Pasquier, Louis

AU - Duncan, Elizabeth J

AU - Ebert, Dieter

AU - Eibner, Cornelius

AU - Erikson, Galina

AU - Evans, Peter D

AU - Extavour, Cassandra G

AU - Francisco, Liezl

AU - Gabaldón, Toni

AU - Gillis, William J

AU - Goodwin-Horn, Elizabeth A

AU - Green, Jack E

AU - Griffiths-Jones, Sam

AU - Grimmelikhuijzen, Cornelis

AU - Gubbala, Sai

AU - Guigó, Roderic

AU - Han, Yi

AU - Hauser, Frank

AU - Havlak, Paul

AU - Hayden, Luke

AU - Helbing, Sophie

AU - Holder, Michael

AU - Hui, Jerome H L

AU - Hunn, Julia P

AU - Hunnekuhl, Vera S

AU - Jackson, LaRonda

AU - Javaid, Mehwish

AU - Jhangiani, Shalini N

AU - Jiggins, Francis M

AU - Jones, Tamsin E

AU - Kaiser, Tobias S

AU - Kalra, Divya

AU - Kenny, Nathan J

AU - Korchina, Viktoriya

AU - Kovar, Christie L

AU - Kraus, F Bernhard

AU - Lapraz, François

AU - Lee, Sandra L

AU - Lv, Jie

AU - Mandapat, Christigale

AU - Manning, Gerard

AU - Mariotti, Marco

AU - Mata, Robert

AU - Mathew, Tittu

AU - Neumann, Tobias

AU - Newsham, Irene

AU - Ngo, Dinh N

AU - Ninova, Maria

AU - Okwuonu, Geoffrey

AU - Ongeri, Fiona

AU - Palmer, William J

AU - Patil, Shobha

AU - Patraquim, Pedro

AU - Pham, Christopher

AU - Pu, Ling-Ling

AU - Putman, Nicholas H

AU - Rabouille, Catherine

AU - Ramos, Olivia Mendivil

AU - Rhodes, Adelaide C

AU - Robertson, Helen E

AU - Robertson, Hugh M

AU - Ronshaugen, Matthew

AU - Rozas, Julio

AU - Saada, Nehad

AU - Sánchez-Gracia, Alejandro

AU - Scherer, Steven E

AU - Schurko, Andrew M

AU - Siggens, Kenneth W

AU - Simmons, DeNard

AU - Stief, Anna

AU - Stolle, Eckart

AU - Telford, Maximilian J

AU - Tessmar-Raible, Kristin

AU - Thornton, Rebecca

AU - van der Zee, Maurijn

AU - von Haeseler, Arndt

AU - Williams, James M

AU - Willis, Judith H

AU - Wu, Yuanqing

AU - Zou, Xiaoyan

AU - Lawson, Daniel

AU - Muzny, Donna M

AU - Worley, Kim C

AU - Gibbs, Richard A

AU - Akam, Michael

AU - Richards, Stephen

PY - 2014

Y1 - 2014

N2 - 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.

AB - 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.

U2 - 10.1371/journal.pbio.1002005

DO - 10.1371/journal.pbio.1002005

M3 - Journal article

C2 - 25423365

VL - 12

SP - e1002005

JO - PLoS Biology

JF - PLoS Biology

SN - 1544-9173

IS - 11

ER -