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.
Original language | English |
---|---|
Journal | P L o S Biology |
Volume | 12 |
Issue number | 11 |
Pages (from-to) | e1002005 |
Number of pages | 24 |
ISSN | 1544-9173 |
DOIs | |
Publication status | Published - 2014 |
Access to Document
Cite this
- APA
- Standard
- Harvard
- Vancouver
- Author
- BIBTEX
- RIS
The first myriapod genome sequence reveals conservative arthropod gene content and genome organisation in the centipede Strigamia maritima. / Chipman, Ariel D.; Ferrier, David E.K.; Brena, Carlo; Qu, Jiaxin; Hughes, Daniel S.T.; Schröder, Reinhard; Torres-Oliva, Montserrat; Znassi, Nadia; Jiang, Huaiyang; Almeida, Francisca C; Alonso, Claudio R; Apostolou, Zivkos; Aqrawi, Peshtewani; Arthur, Wallace; Barna, Jennifer C J; Blankenburg, Kerstin P; Brites, Daniela; Capella-Gutiérrez, Salvador; Coyle, Marcus; Dearden, Peter K; Du Pasquier, Louis; Duncan, Elizabeth J; Ebert, Dieter; Eibner, Cornelius; Erikson, Galina; Evans, Peter D; Extavour, Cassandra G; Francisco, Liezl; Gabaldón, Toni; Gillis, William J; Goodwin-Horn, Elizabeth A; Green, Jack E; Griffiths-Jones, Sam; Grimmelikhuijzen, Cornelis; Gubbala, Sai; Guigó, Roderic; Han, Yi; Hauser, Frank; Havlak, Paul; Hayden, Luke; Helbing, Sophie; Holder, Michael; Hui, Jerome H L; Hunn, Julia P; Hunnekuhl, Vera S; Jackson, LaRonda; Javaid, Mehwish; Jhangiani, Shalini N; Jiggins, Francis M; Jones, Tamsin E; Kaiser, Tobias S; Kalra, Divya; Kenny, Nathan J; Korchina, Viktoriya; Kovar, Christie L; Kraus, F Bernhard; Lapraz, François; Lee, Sandra L; Lv, Jie; Mandapat, Christigale; Manning, Gerard; Mariotti, Marco; Mata, Robert; Mathew, Tittu; Neumann, Tobias; Newsham, Irene; Ngo, Dinh N; Ninova, Maria; Okwuonu, Geoffrey; Ongeri, Fiona; Palmer, William J; Patil, Shobha; Patraquim, Pedro; Pham, Christopher; Pu, Ling-Ling; Putman, Nicholas H; Rabouille, Catherine; Ramos, Olivia Mendivil; Rhodes, Adelaide C; Robertson, Helen E; Robertson, Hugh M; Ronshaugen, Matthew; Rozas, Julio; Saada, Nehad; Sánchez-Gracia, Alejandro; Scherer, Steven E; Schurko, Andrew M; Siggens, Kenneth W; Simmons, DeNard; Stief, Anna; Stolle, Eckart; Telford, Maximilian J; Tessmar-Raible, Kristin; Thornton, Rebecca; van der Zee, Maurijn; von Haeseler, Arndt; Williams, James M; Willis, Judith H; Wu, Yuanqing; Zou, Xiaoyan; Lawson, Daniel; Muzny, Donna M; Worley, Kim C; Gibbs, Richard A; Akam, Michael; Richards, Stephen.
In: P L o S Biology, Vol. 12, No. 11, 2014, p. e1002005.Research output: Contribution to journal › Journal article › Research › peer-review
}
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 -