Intercalation of a new tier of transcription regulation into an ancient circuit

被引:58
作者
Booth, Lauren N. [1 ,2 ]
Tuch, Brian B. [1 ,2 ]
Johnson, Alexander D. [1 ,2 ]
机构
[1] Univ Calif San Francisco, Dept Microbiol & Immunol, San Francisco, CA 94158 USA
[2] Univ Calif San Francisco, Dept Biochem & Biophys, San Francisco, CA 94158 USA
基金
美国国家卫生研究院;
关键词
HETEROTRIMERIC G-PROTEIN; YEAST CANDIDA-ALBICANS; CELL-CYCLE ARREST; SACCHAROMYCES-CEREVISIAE; KLUYVEROMYCES-LACTIS; GENE-EXPRESSION; EVOLUTION; PHEROMONE; IDENTIFICATION; MEIOSIS;
D O I
10.1038/nature09560
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
Changes in gene regulatory networks are a major source of evolutionary novelty(1-3). Here we describe a specific type of network rewiring event, one that intercalates a new level of transcriptional control into an ancient circuit. We deduce that, over evolutionary time, the direct ancestral connections between a regulator and its target genes were broken and replaced by indirect connections, preserving the overall logic of the ancestral circuit but producing a new behaviour. The example was uncovered through a series of experiments in three ascomycete yeasts: the bakers' yeast Saccharomyces cerevisiae, the dairy yeast Kluyveromyces lactis and the human pathogen Candida albicans. All three species have three cell types: two mating-competent cell forms (a and alpha) and the product of their mating (a/alpha), which is mating-incompetent. In the ancestral mating circuit, two homeodomain proteins, Mata1 and Mat alpha 2, form a heterodimer that directly represses four genes that are expressed only in a and alpha cells and are required for mating(4-6). In a relatively recent ancestor of K. lactis, a reorganization occurred. The Mata1-Mat alpha 2 heterodimer represses the same four genes (known as the core haploid-specific genes) but now does so indirectly through an intermediate regulatory protein, Rme1. The overall logic of the ancestral circuit is preserved (haploid-specific genes ON in a and alpha cells and OFF in a/alpha cells), but a new phenotype was produced by the rewiring: unlike S. cerevisiae and C. albicans, K. lactis integrates nutritional signals, by means of Rme1, into the decision of whether or not to mate.
引用
收藏
页码:959 / U358
页数:7
相关论文
共 45 条
[1]  
Bailey T L, 1994, Proc Int Conf Intell Syst Mol Biol, V2, P28
[2]   Ume6 Is Required for the MATa/MATα Cellular Identity and Transcriptional Silencing in Kluyveromyces lactis [J].
Barsoum, E. ;
Sjostrand, J. O. O. ;
Astrom, S. U. .
GENETICS, 2010, 184 (04) :999-U176
[3]   α3, a transposable element that promotes host sexual reproduction [J].
Barsoum, Emad ;
Martinez, Paula ;
Astrom, Stefan U. .
GENES & DEVELOPMENT, 2010, 24 (01) :33-44
[4]   Identification and characterization of a Candida albicans mating pheromone [J].
Bennett, RJ ;
Uhl, MA ;
Miller, MG ;
Johnson, AD .
MOLECULAR AND CELLULAR BIOLOGY, 2003, 23 (22) :8189-8201
[5]   The role of Far1p in linking the heterotrimeric G protein to polarity establishment proteins during yeast mating [J].
Butty, AC ;
Pryciak, PM ;
Huang, LS ;
Herskowitz, I ;
Peter, M .
SCIENCE, 1998, 282 (5393) :1511-1516
[6]   Evo-devo and an expanding evolutionary synthesis: A genetic theory of morphological evolution [J].
Carroll, Sean B. .
CELL, 2008, 134 (01) :25-36
[7]   IDENTIFICATION OF A GENE NECESSARY FOR CELL-CYCLE ARREST BY A NEGATIVE GROWTH-FACTOR OF YEAST - FAR1 IS AN INHIBITOR OF A G1 CYCLIN, CLN2 [J].
CHANG, F ;
HERSKOWITZ, I .
CELL, 1990, 63 (05) :999-1011
[8]   The pheromone response pathway of Kluyveromyces lactis [J].
Coria, R ;
Kawasaki, L ;
Torres-Quiroz, F ;
Ongay-Larios, L ;
Sánchez-Paredes, E ;
Velázquez-Zavala, N ;
Navarro-Olmos, R ;
Rodríguez-González, M ;
Aguilar-Corachán, R ;
Coello, G .
FEMS YEAST RESEARCH, 2006, 6 (03) :336-344
[9]   The role of Candida albicans FAR1 in regulation of pheromone-mediated mating, gene expression and cell cycle arrest [J].
Cote, Pierre ;
Whiteway, Malcolm .
MOLECULAR MICROBIOLOGY, 2008, 68 (02) :392-404
[10]   REPRESSION BY THE YEAST MEIOTIC INHIBITOR RME1 [J].
COVITZ, PA ;
MITCHELL, AP .
GENES & DEVELOPMENT, 1993, 7 (08) :1598-1608