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

被引:117
作者
Hanschen, Erik R. [1 ]
Marriage, Tara N. [2 ]
Ferris, Patrick J. [1 ]
Hamaji, Takashi [3 ]
Toyoda, Atsushi [4 ,5 ]
Fujiyama, Asao [4 ,5 ]
Neme, Rafik [6 ]
Noguchi, Hideki [4 ]
Minakuchi, Yohei [5 ]
Suzuki, Masahiro [7 ]
Kawai-Toyooka, Hiroko [7 ]
Smith, David R. [8 ]
Sparks, Halle [2 ]
Anderson, Jaden [2 ]
Bakaric, Robert [9 ]
Luria, Victor [10 ,11 ]
Karger, Amir [12 ]
Kirschner, Marc W. [10 ]
Durand, Pierre M. [1 ,13 ,14 ,15 ]
Michod, Richard E. [1 ,11 ]
Nozaki, Hisayoshi [7 ]
Olson, Bradley J. S. C. [2 ,11 ]
机构
[1] Univ Arizona, Dept Ecol & Evolutionary Biol, Tucson, AZ 85712 USA
[2] Kansas State Univ, Div Biol, Ackert Hall, Manhattan, KS 66506 USA
[3] Donald Danforth Plant Sci Ctr, St Louis, MO 63132 USA
[4] Natl Inst Genet, Ctr Adv Genom, Mishima, Shizuoka 4118540, Japan
[5] Natl Inst Genet, Ctr Informat Biol, Mishima, Shizuoka 4118540, Japan
[6] Max Planck Inst Evolutionary Biol, Dept Evolutionary Genet, D-24306 Plon, Germany
[7] Univ Tokyo, Grad Sch Sci, Dept Biol Sci, Bunkyo Ku, Tokyo 113003, Japan
[8] Univ Western Ontario, Dept Biol, London, ON N6A 5B7, Canada
[9] Rudjer Boskovic Inst, Div Mol Biol, POB 1016, Zagreb 10000, Croatia
[10] Harvard Univ, Sch Med, Dept Syst Biol, Boston, MA 02115 USA
[11] Univ Calif Santa Barbara, Kavli Inst Theoret Phys, Santa Barbara, CA 93106 USA
[12] Harvard Univ, Sch Med, Res Comp Div, Boston, MA 02115 USA
[13] Univ Witwatersrand, Fac Hlth Sci, Dept Mol Med & Haematol, ZA-2000 Johannesburg, South Africa
[14] Univ Witwatersrand, Evolutionary Studies Inst, ZA-2000 Johannesburg, South Africa
[15] Univ Western Cape, Dept Biodivers & Conservat Biol, ZA-7535 Cape Town, South Africa
基金
美国国家科学基金会; 美国国家航空航天局;
关键词
RETINOBLASTOMA TUMOR-SUPPRESSOR; TRANSCRIPTION FACTOR DATABASE; PROTEIN FAMILIES DATABASE; PHYLOGENETIC ANALYSIS; EXTRACELLULAR-MATRIX; VOLVOCINE ALGAE; DIFFERENTIATION; COMPLEXITY; GENE; INDIVIDUALITY;
D O I
10.1038/ncomms11370
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
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.
引用
收藏
页数:10
相关论文
共 69 条
[1]  
[Anonymous], TEMPO MODE EVOLUTION
[2]   Involvement of the D-type cyclins in germ cell proliferation and differentiation in the mouse [J].
Beumer, TL ;
Roepers-Gajadien, HL ;
Gademan, IS ;
Kal, HB ;
de Rooij, DG .
BIOLOGY OF REPRODUCTION, 2000, 63 (06) :1893-1898
[3]   The genome of the polar eukaryotic microalga Coccomyxa subellipsoidea reveals traits of cold adaptation [J].
Blanc, Guillaume ;
Agarkova, Irina ;
Grimwood, Jane ;
Kuo, Alan ;
Brueggeman, Andrew ;
Dunigan, David D. ;
Gurnon, James ;
Ladunga, Istvan ;
Lindquist, Erika ;
Lucas, Susan ;
Pangilinan, Jasmyn ;
Proeschold, Thomas ;
Salamov, Asaf ;
Schmutz, Jeremy ;
Weeks, Donald ;
Yamada, Takashi ;
Lomsadze, Alexandre ;
Borodovsky, Mark ;
Claverie, Jean-Michel ;
Grigoriev, Igor V. ;
Van Etten, James L. .
GENOME BIOLOGY, 2012, 13 (05)
[4]   The Chlorella variabilis NC64A Genome Reveals Adaptation to Photosymbiosis, Coevolution with Viruses, and Cryptic Sex [J].
Blanc, Guillaume ;
Duncan, Garry ;
Agarkova, Irina ;
Borodovsky, Mark ;
Gurnon, James ;
Kuo, Alan ;
Lindquist, Erika ;
Lucas, Susan ;
Pangilinan, Jasmyn ;
Polle, Juergen ;
Salamov, Asaf ;
Terry, Astrid ;
Yamada, Takashi ;
Dunigan, David D. ;
Grigoriev, Igor V. ;
Claverie, Jean-Michel ;
Van Etten, James L. .
PLANT CELL, 2010, 22 (09) :2943-2955
[5]  
Bonner John Tyler, 1998, Integrative Biology, V1, P27
[6]   Count: evolutionary analysis of phylogenetic profiles with parsimony and likelihood [J].
Csuroes, Miklos .
BIOINFORMATICS, 2010, 26 (15) :1910-1912
[7]   Genome analysis of the smallest free-living eukaryote Ostreococcus tauri unveils many unique features [J].
Derelle, Evelyne ;
Ferraz, Conchita ;
Rombauts, Stephane ;
Rouze, Pierre ;
Worden, Alexandra Z. ;
Robbens, Steven ;
Partensky, Frederic ;
Degroeve, Sven ;
Echeynie, Sophie ;
Cooke, Richard ;
Saeys, Yvan ;
Wuyts, Jan ;
Jabbari, Kamel ;
Bowler, Chris ;
Panaud, Olivier ;
Piegu, Benoit ;
Ball, Steven G. ;
Ral, Jean-Philippe ;
Bouget, Francois-Yves ;
Piganeau, Gwenael ;
De Baets, Bernard ;
Picard, Andre ;
Delseny, Michel ;
Demaille, Jacques ;
Van de Peer, Yves ;
Moreau, Herve .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2006, 103 (31) :11647-11652
[8]   Altered cell cycle distribution, hyperplasia, and inhibited differentiation in arabidopsis caused by the D-type cyclin CYCD3 [J].
Dewitte, W ;
Riou-Khamlichi, C ;
Scofield, S ;
Healy, JMS ;
Jacqmard, A ;
Kilby, NJ ;
Murray, JAH .
PLANT CELL, 2003, 15 (01) :79-92
[9]   A phylostratigraphy approach to uncover the genomic history of major adaptations in metazoan lineages [J].
Domazet-Loso, Tomislav ;
Brajkovic, Josip ;
Tautz, Diethard .
TRENDS IN GENETICS, 2007, 23 (11) :533-539
[10]   The VARL gene family and the evolutionary origins of the master cell-type regulatory gene, regA, in Volvox carteri [J].
Duncan, Leonard ;
Nishii, Ichiro ;
Harryman, Alexandra ;
Buckley, Stephanie ;
Howard, Alicia ;
Friedman, Nicholas R. ;
Miller, Stephen M. .
JOURNAL OF MOLECULAR EVOLUTION, 2007, 65 (01) :1-11