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

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 R 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 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

doi:10.1371/journal.pbio.1002005

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

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 R Alonso, Zivkos Apostolou, Peshtewani Aqrawi, Wallace Arthur, Jennifer C J Barna, Kerstin P Blankenburg, Daniela Brites, Salvador Capella-Gutiérrez, Marcus Coyle, Peter K DeardenLouis 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 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

Cell and Neurobiology

148 Citations (Scopus)

962 Downloads (Pure)

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	https://doi.org/10.1371/journal.pbio.1002005
Publication status	Published - 2014

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The First Myriapod Genome Sequence Reveals Conservative Arthropod Gene Content and Genome Organisation in the Centipede Strigamia maritimaFinal published version, 1.98 MB

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Chipman, A. D., Ferrier, D. E. K., Brena, C., Qu, J., Hughes, D. S. T., Schröder, R., Torres-Oliva, M., Znassi, N., Jiang, H., Almeida, F. C., Alonso, C. R., Apostolou, Z., Aqrawi, P., Arthur, W., Barna, J. C. J., Blankenburg, K. P., Brites, D., Capella-Gutiérrez, S., Coyle, M., ... Richards, S. (2014). The first myriapod genome sequence reveals conservative arthropod gene content and genome organisation in the centipede Strigamia maritima. P L o S Biology, 12(11), e1002005. https://doi.org/10.1371/journal.pbio.1002005

Chipman, AD, Ferrier, DEK, Brena, C, Qu, J, Hughes, DST, Schröder, R, Torres-Oliva, M, Znassi, N, Jiang, H, Almeida, FC, Alonso, CR, Apostolou, Z, Aqrawi, P, Arthur, W, Barna, JCJ, Blankenburg, KP, Brites, D, Capella-Gutiérrez, S, Coyle, M, Dearden, PK, Du Pasquier, L, Duncan, EJ, Ebert, D, Eibner, C, Erikson, G, Evans, PD, Extavour, CG, Francisco, L, Gabaldón, T, Gillis, WJ, Goodwin-Horn, EA, Green, JE, Griffiths-Jones, S, Grimmelikhuijzen, C, Gubbala, S, Guigó, R, Han, Y, Hauser, F, Havlak, P, Hayden, L, Helbing, S, Holder, M, Hui, JHL, Hunn, JP, Hunnekuhl, VS, Jackson, L, Javaid, M, Jhangiani, SN, Jiggins, FM, Jones, TE, Kaiser, TS, Kalra, D, Kenny, NJ, Korchina, V, Kovar, CL, Kraus, FB, Lapraz, F, Lee, SL, Lv, J, Mandapat, C, Manning, G, Mariotti, M, Mata, R, Mathew, T, Neumann, T, Newsham, I, Ngo, DN, Ninova, M, Okwuonu, G, Ongeri, F, Palmer, WJ, Patil, S, Patraquim, P, Pham, C, Pu, L-L, Putman, NH, Rabouille, C, Ramos, OM, Rhodes, AC, Robertson, HE, Robertson, HM, Ronshaugen, M, Rozas, J, Saada, N, Sánchez-Gracia, A, Scherer, SE, Schurko, AM, Siggens, KW, Simmons, D, Stief, A, Stolle, E, Telford, MJ, Tessmar-Raible, K, Thornton, R, van der Zee, M, von Haeseler, A, Williams, JM, Willis, JH, Wu, Y, Zou, X, Lawson, D, Muzny, DM, Worley, KC, Gibbs, RA, Akam, M & Richards, S 2014, 'The first myriapod genome sequence reveals conservative arthropod gene content and genome organisation in the centipede Strigamia maritima', P L o S Biology, vol. 12, no. 11, pp. e1002005. https://doi.org/10.1371/journal.pbio.1002005

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

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.",

author = "Chipman, {Ariel D.} and Ferrier, {David E.K.} and Carlo Brena and Jiaxin Qu and Hughes, {Daniel S.T.} and Reinhard Schr{\"o}der and Montserrat Torres-Oliva and Nadia Znassi and Huaiyang Jiang and Almeida, {Francisca C} and Alonso, {Claudio R} and Zivkos Apostolou and Peshtewani Aqrawi and Wallace Arthur and Barna, {Jennifer C J} and Blankenburg, {Kerstin P} and Daniela Brites and Salvador Capella-Guti{\'e}rrez and Marcus Coyle and Dearden, {Peter K} and {Du Pasquier}, Louis and Duncan, {Elizabeth J} and Dieter Ebert and Cornelius Eibner and Galina Erikson and Evans, {Peter D} and Extavour, {Cassandra G} and Liezl Francisco and Toni Gabald{\'o}n and Gillis, {William J} and Goodwin-Horn, {Elizabeth A} and Green, {Jack E} and Sam Griffiths-Jones and Cornelis Grimmelikhuijzen and Sai Gubbala and Roderic Guig{\'o} and Yi Han and Frank Hauser and Paul Havlak and Luke Hayden and Sophie Helbing and Michael Holder and Hui, {Jerome H L} and Hunn, {Julia P} and Hunnekuhl, {Vera S} and LaRonda Jackson and Mehwish Javaid and Jhangiani, {Shalini N} and Jiggins, {Francis M} and Jones, {Tamsin E} and Kaiser, {Tobias S} and Divya Kalra and Kenny, {Nathan J} and Viktoriya Korchina and Kovar, {Christie L} and Kraus, {F Bernhard} and Fran{\c c}ois Lapraz and Lee, {Sandra L} and Jie Lv and Christigale Mandapat and Gerard Manning and Marco Mariotti and Robert Mata and Tittu Mathew and Tobias Neumann and Irene Newsham and Ngo, {Dinh N} and Maria Ninova and Geoffrey Okwuonu and Fiona Ongeri and Palmer, {William J} and Shobha Patil and Pedro Patraquim and Christopher Pham and Ling-Ling Pu and Putman, {Nicholas H} and Catherine Rabouille and Ramos, {Olivia Mendivil} and Rhodes, {Adelaide C} and Robertson, {Helen E} and Robertson, {Hugh M} and Matthew Ronshaugen and Julio Rozas and Nehad Saada and Alejandro S{\'a}nchez-Gracia and Scherer, {Steven E} and Schurko, {Andrew M} and Siggens, {Kenneth W} and DeNard Simmons and Anna Stief and Eckart Stolle and Telford, {Maximilian J} and Kristin Tessmar-Raible and Rebecca Thornton and {van der Zee}, Maurijn and {von Haeseler}, Arndt and Williams, {James M} and Willis, {Judith H} and Yuanqing Wu and Xiaoyan Zou and Daniel Lawson and Muzny, {Donna M} and Worley, {Kim C} and Gibbs, {Richard A} and Michael Akam and Stephen Richards",

year = "2014",

doi = "10.1371/journal.pbio.1002005",

language = "English",

volume = "12",

pages = "e1002005",

journal = "P L o S Biology",

issn = "1544-9173",

publisher = "Public Library of Science",

number = "11",

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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

SN - 1544-9173

VL - 12

SP - e1002005

JO - P L o S Biology

JF - P L o S Biology

IS - 11

ER -

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

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