The Gonium pectorale genome demonstrates co-option of cell cycle regulation during the evolution of multicellularity

Persistent Link:
http://hdl.handle.net/10150/614763
Title:
The Gonium pectorale genome demonstrates co-option of cell cycle regulation during the evolution of multicellularity
Author:
Hanschen, Erik R.; Marriage, Tara N.; Ferris, Patrick J.; Hamaji, Takashi ( 0000-0002-2801-2148 ) ; Toyoda, Atsushi; Fujiyama, Asao; Neme, Rafik ( 0000-0001-8462-5291 ) ; Noguchi, Hideki; Minakuchi, Yohei; Suzuki, Masahiro; Kawai-Toyooka, Hiroko; Smith, David R. ( 0000-0001-9560-5210 ) ; Sparks, Halle; Anderson, Jaden; Bakarić, Robert; Luria, Victor; Karger, Amir ( 0000-0002-4561-3850 ) ; Kirschner, Marc W.; Durand, Pierre M.; Michod, Richard E.; Nozaki, Hisayoshi; Olson, Bradley J. S. C.
Affiliation:
Univ Arizona, Dept Ecol & Evolutionary Biol
Issue Date:
2016-04-22
Publisher:
NATURE PUBLISHING GROUP
Citation:
The Gonium pectorale genome demonstrates co-option of cell cycle regulation during the evolution of multicellularity 2016, 7:11370 Nature Communications
Journal:
Nature Communications
Rights:
This work is licensed under a Creative Commons Attribution 4.0 International License.
Collection Information:
This item from the UA Faculty Publications collection is made available by the University of Arizona with support from the University of Arizona Libraries. If you have questions, please contact us at repository@u.library.arizona.edu.
Abstract:
The transition to multicellularity has occurred numerous times in all domains of life, yet its initial steps are poorly understood. The volvocine green algae are a tractable system for understanding the genetic basis of multicellularity including the initial formation of cooperative cell groups. Here we report the genome sequence of the undifferentiated colonial alga, Gonium pectorale, where group formation evolved by co-option of the retinoblastoma cell cycle regulatory pathway. Significantly, expression of the Gonium retinoblastoma cell cycle regulator in unicellular Chlamydomonas causes it to become colonial. The presence of these changes in undifferentiated Gonium indicates extensive group-level adaptation during the initial step in the evolution of multicellularity. These results emphasize an early and formative step in the evolution of multicellularity, the evolution of cell cycle regulation, one that may shed light on the evolutionary history of other multicellular innovations and evolutionary transitions.
ISSN:
2041-1723
DOI:
10.1038/ncomms11370
Keywords:
RETINOBLASTOMA TUMOR-SUPPRESSOR; TRANSCRIPTION FACTOR DATABASE; PROTEIN FAMILIES DATABASE; PHYLOGENETIC ANALYSIS; EXTRACELLULAR-MATRIX; VOLVOCINE ALGAE; DIFFERENTIATION; COMPLEXITY; GENE; INDIVIDUALITY
Version:
Final published version
Sponsors:
We acknowledge the support of the National Aeronautics and Space Administration (grant number NNX13AH41G to R.E.M., P.J.F. and P.M.D.), the National Institute of Health (grant number GM084905 to the University of Arizona, P20GM103638 to B.J.S.C.O., P20GM103418 to B.J.S.C.O. and T.N.M., GM103785-02 to M.W.K.), the National Science Foundation (grant number MCB-1412395 to B.J.S.C.O. and R.E.M., grant number DGE-0654435 to the University of Arizona and PHY11-25915 to U.C.S.B., K.I.T.P.), the KSU Johnson Cancer Center (Innovative Research Award to B.J.S.C.O.), MEXT/JSPS KAKENHI Scientific Research on Innovative Areas 'Genome Science' (grant number 221S0002 to A.T.), MEXT/JSPS KAKENHI Scientific Research (A) (grant number 24247042 to H.N.), JSPS Fellows (19-7661 and 23-5499 to T.H.) and the JSPS Postdoctoral Fellowship for Research Abroad (26-495 to T.H.). Part of this work was undertaken during the U.C.S.B. K.I.T.P. 'Cooperation and the Evolution of Multi-cellularity' program. Part of the computing for this project was performed on the Beocat Research Cluster at KSU, which is funded in part by NSF grants CNS-1006860, EPS-1006860 and EPS-0919443. We thank M. Barker and M. Sanderson for technical assistance; A. M. Nedelcu for comments; three anonymous reviewers for comments and all the technical staff of the Comparative Genomics lab at the National Institute of Genetics for their assistance. Publication of this article was funded in part by the Kansas State University Open Access Publishing Fund.
Additional Links:
http://www.nature.com/doifinder/10.1038/ncomms11370

Full metadata record

DC FieldValue Language
dc.contributor.authorHanschen, Erik R.en
dc.contributor.authorMarriage, Tara N.en
dc.contributor.authorFerris, Patrick J.en
dc.contributor.authorHamaji, Takashien
dc.contributor.authorToyoda, Atsushien
dc.contributor.authorFujiyama, Asaoen
dc.contributor.authorNeme, Rafiken
dc.contributor.authorNoguchi, Hidekien
dc.contributor.authorMinakuchi, Yoheien
dc.contributor.authorSuzuki, Masahiroen
dc.contributor.authorKawai-Toyooka, Hirokoen
dc.contributor.authorSmith, David R.en
dc.contributor.authorSparks, Halleen
dc.contributor.authorAnderson, Jadenen
dc.contributor.authorBakarić, Roberten
dc.contributor.authorLuria, Victoren
dc.contributor.authorKarger, Amiren
dc.contributor.authorKirschner, Marc W.en
dc.contributor.authorDurand, Pierre M.en
dc.contributor.authorMichod, Richard E.en
dc.contributor.authorNozaki, Hisayoshien
dc.contributor.authorOlson, Bradley J. S. C.en
dc.date.accessioned2016-06-24T23:34:19Z-
dc.date.available2016-06-24T23:34:19Z-
dc.date.issued2016-04-22-
dc.identifier.citationThe Gonium pectorale genome demonstrates co-option of cell cycle regulation during the evolution of multicellularity 2016, 7:11370 Nature Communicationsen
dc.identifier.issn2041-1723-
dc.identifier.doi10.1038/ncomms11370-
dc.identifier.urihttp://hdl.handle.net/10150/614763-
dc.description.abstractThe transition to multicellularity has occurred numerous times in all domains of life, yet its initial steps are poorly understood. The volvocine green algae are a tractable system for understanding the genetic basis of multicellularity including the initial formation of cooperative cell groups. Here we report the genome sequence of the undifferentiated colonial alga, Gonium pectorale, where group formation evolved by co-option of the retinoblastoma cell cycle regulatory pathway. Significantly, expression of the Gonium retinoblastoma cell cycle regulator in unicellular Chlamydomonas causes it to become colonial. The presence of these changes in undifferentiated Gonium indicates extensive group-level adaptation during the initial step in the evolution of multicellularity. These results emphasize an early and formative step in the evolution of multicellularity, the evolution of cell cycle regulation, one that may shed light on the evolutionary history of other multicellular innovations and evolutionary transitions.en
dc.description.sponsorshipWe acknowledge the support of the National Aeronautics and Space Administration (grant number NNX13AH41G to R.E.M., P.J.F. and P.M.D.), the National Institute of Health (grant number GM084905 to the University of Arizona, P20GM103638 to B.J.S.C.O., P20GM103418 to B.J.S.C.O. and T.N.M., GM103785-02 to M.W.K.), the National Science Foundation (grant number MCB-1412395 to B.J.S.C.O. and R.E.M., grant number DGE-0654435 to the University of Arizona and PHY11-25915 to U.C.S.B., K.I.T.P.), the KSU Johnson Cancer Center (Innovative Research Award to B.J.S.C.O.), MEXT/JSPS KAKENHI Scientific Research on Innovative Areas 'Genome Science' (grant number 221S0002 to A.T.), MEXT/JSPS KAKENHI Scientific Research (A) (grant number 24247042 to H.N.), JSPS Fellows (19-7661 and 23-5499 to T.H.) and the JSPS Postdoctoral Fellowship for Research Abroad (26-495 to T.H.). Part of this work was undertaken during the U.C.S.B. K.I.T.P. 'Cooperation and the Evolution of Multi-cellularity' program. Part of the computing for this project was performed on the Beocat Research Cluster at KSU, which is funded in part by NSF grants CNS-1006860, EPS-1006860 and EPS-0919443. We thank M. Barker and M. Sanderson for technical assistance; A. M. Nedelcu for comments; three anonymous reviewers for comments and all the technical staff of the Comparative Genomics lab at the National Institute of Genetics for their assistance. Publication of this article was funded in part by the Kansas State University Open Access Publishing Fund.en
dc.language.isoenen
dc.publisherNATURE PUBLISHING GROUPen
dc.relation.urlhttp://www.nature.com/doifinder/10.1038/ncomms11370en
dc.rightsThis work is licensed under a Creative Commons Attribution 4.0 International License.en
dc.subjectRETINOBLASTOMA TUMOR-SUPPRESSORen
dc.subjectTRANSCRIPTION FACTOR DATABASEen
dc.subjectPROTEIN FAMILIES DATABASEen
dc.subjectPHYLOGENETIC ANALYSISen
dc.subjectEXTRACELLULAR-MATRIXen
dc.subjectVOLVOCINE ALGAEen
dc.subjectDIFFERENTIATIONen
dc.subjectCOMPLEXITYen
dc.subjectGENEen
dc.subjectINDIVIDUALITYen
dc.titleThe Gonium pectorale genome demonstrates co-option of cell cycle regulation during the evolution of multicellularityen
dc.typeArticleen
dc.contributor.departmentUniv Arizona, Dept Ecol & Evolutionary Biolen
dc.identifier.journalNature Communicationsen
dc.description.collectioninformationThis item from the UA Faculty Publications collection is made available by the University of Arizona with support from the University of Arizona Libraries. If you have questions, please contact us at repository@u.library.arizona.edu.en
dc.eprint.versionFinal published versionen
All Items in UA Campus Repository are protected by copyright, with all rights reserved, unless otherwise indicated.