The Gonium pectorale genome demonstrates co-option of cell cycle regulation during the evolution of multicellularity.
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.
Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, Arizona 85712, USA.
Erik R
ER
Hanschen
Division of Biology, Kansas State University, Manhattan, Kansas 66506, USA.
Tara N
TN
Marriage
Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, Arizona 85712, USA.
Patrick J
PJ
Ferris
Donald Danforth Plant Science Center, St Louis, Missouri 63132, USA.
Takashi
http://orcid.org/0000-0002-2801-2148
T
Hamaji
Center for Advanced Genomics, National Institute of Genetics, Mishima, Shizuoka 411-8540, Japan.|Center for Information Biology, National Institute of Genetics, Mishima, Shizuoka 411-8540, Japan.
Atsushi
A
Toyoda
Center for Advanced Genomics, National Institute of Genetics, Mishima, Shizuoka 411-8540, Japan.|Center for Information Biology, National Institute of Genetics, Mishima, Shizuoka 411-8540, Japan.
Asao
A
Fujiyama
Department of Evolutionary Genetics, Max Planck Institute for Evolutionary Biology, 24306 Plön, Germany.
Rafik
http://orcid.org/0000-0001-8462-5291
R
Neme
Center for Advanced Genomics, National Institute of Genetics, Mishima, Shizuoka 411-8540, Japan.
Hideki
H
Noguchi
Center for Information Biology, National Institute of Genetics, Mishima, Shizuoka 411-8540, Japan.
Yohei
Y
Minakuchi
Department of Biological Sciences, Graduate School of Science, University of Tokyo, Bunkyo-ku, Tokyo 113-003, Japan.
Masahiro
M
Suzuki
Department of Biological Sciences, Graduate School of Science, University of Tokyo, Bunkyo-ku, Tokyo 113-003, Japan.
Hiroko
H
Kawai-Toyooka
Department of Biology, Western University, London, Ontario, Canada N6A 5B7.
David R
http://orcid.org/0000-0001-9560-5210
DR
Smith
Division of Biology, Kansas State University, Manhattan, Kansas 66506, USA.
Halle
H
Sparks
Division of Biology, Kansas State University, Manhattan, Kansas 66506, USA.
Jaden
J
Anderson
Division of Molecular Biology, Ruđer Bošković Institute, Zagreb 10000, Croatia.
Robert
R
Bakarić
Department of Systems Biology, Harvard Medical School, Boston, Massachusetts 02115, USA.|Kavli Institute for Theoretical Physics, University of California Santa Barbara, Santa Barbara, California 93106, USA.
Victor
V
Luria
Research Computing Division, Harvard Medical School, Boston, Massachusetts 02115, USA.
Amir
http://orcid.org/0000-0002-4561-3850
A
Karger
Department of Systems Biology, Harvard Medical School, Boston, Massachusetts 02115, USA.
Marc W
MW
Kirschner
Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, Arizona 85712, USA.|Department of Molecular Medicine and Haematology, Faculty of Health Sciences and Evolutionary Studies Institute, University of the Witwatersrand, Johannesburg 2000, South Africa.|Department of Biodiversity and Conservation Biology, University of the Western Cape, Cape Town 7535, South Africa.
Pierre M
PM
Durand
Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, Arizona 85712, USA.|Kavli Institute for Theoretical Physics, University of California Santa Barbara, Santa Barbara, California 93106, USA.
Richard E
RE
Michod
Department of Biological Sciences, Graduate School of Science, University of Tokyo, Bunkyo-ku, Tokyo 113-003, Japan.
Hisayoshi
H
Nozaki
Division of Biology, Kansas State University, Manhattan, Kansas 66506, USA.|Kavli Institute for Theoretical Physics, University of California Santa Barbara, Santa Barbara, California 93106, USA.
Bradley J S C
BJ
Olson
D005075:Biological Evolution; D059447:Cell Cycle Checkpoints / Q000235:genetics*; D002696:Chlamydomonas / Q000166:cytology / Q000235:genetics*; D000460:Chlorophyta / Q000145:classification / Q000166:cytology / Q000235:genetics*; D018506:Gene Expression Regulation, Plant; D059646:Genome Size; D018745:Genome, Plant; D010802:Phylogeny; D059828:Plant Cells / Q000378:metabolism; D010957:Plasmids / Q000737:chemistry / Q000378:metabolism; D016160:Retinoblastoma Protein / Q000235:genetics / Q000378:metabolism; D014170:Transformation, Genetic
D016160:Retinoblastoma Protein