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Facultative cheater mutants reveal the genetic complexity of cooperation in social amoebae (2008)

L. A. Santorelli ; C. R. Thompson ; E. Villegas ; [et al.]

Nature Publishing Group (NPG)

In: Nature. 451(7182): 1107-10. doi: 10.1038/nature06558.

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Publication Date: 2008-02-15

Description: Cooperation is central to many major transitions in evolution, including the emergence of eukaryotic cells, multicellularity and eusociality. Cooperation can be destroyed by the spread of cheater mutants that do not cooperate but gain the benefits of cooperation from others. However, cooperation can be preserved if cheaters are facultative, cheating others but cooperating among themselves. Several cheater mutants have been studied before, but no study has attempted a genome-scale investigation of the genetic opportunities for cheating. Here we describe such a screen in a social amoeba and show that cheating is multifaceted by revealing cheater mutations in well over 100 genes of diverse types. Many of these mutants cheat facultatively, producing more than their fair share of spores in chimaeras, but cooperating normally when clonal. These findings indicate that phenotypically stable cooperative systems may nevertheless harbour genetic conflicts. The opportunities for evolutionary moves and countermoves in such conflicts may select for the involvement of multiple pathways and numerous genes.〈br /〉〈span class="detail_caption"〉Notes: 〈/span〉Santorelli, Lorenzo A -- Thompson, Christopher R L -- Villegas, Elizabeth -- Svetz, Jessica -- Dinh, Christopher -- Parikh, Anup -- Sucgang, Richard -- Kuspa, Adam -- Strassmann, Joan E -- Queller, David C -- Shaulsky, Gad -- G0400103/Medical Research Council/United Kingdom -- Wellcome Trust/United Kingdom -- England -- Nature. 2008 Feb 28;451(7182):1107-10. doi: 10.1038/nature06558. Epub 2008 Feb 13.〈br /〉〈span class="detail_caption"〉Author address: 〈/span〉Department of Ecology and Evolutionary Biology, Rice University, Houston, Texas 77005, USA.〈br /〉〈span class="detail_caption"〉Record origin:〈/span〉 〈a href="http://www.ncbi.nlm.nih.gov/pubmed/18272966" target="_blank"〉PubMed〈/a〉

Keywords: Amoeba/genetics/physiology ; Animals ; Cell Aggregation ; Chimera/genetics/physiology ; *Cooperative Behavior ; Dictyostelium/cytology/*genetics/*physiology ; Genes, Protozoan/genetics ; Genome/genetics ; Genomics ; Mutation/*genetics ; Myxococcus xanthus/genetics/physiology ; Phenotype ; *Social Behavior ; Spores, Protozoan/genetics/physiology

Print ISSN: 0028-0836

Electronic ISSN: 1476-4687

Topics: Biology , Chemistry and Pharmacology , Medicine , Natural Sciences in General , Physics

Published by Nature Publishing Group (NPG)

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Cheater-resistance is not futile (2009)

A. Khare ; L. A. Santorelli ; J. E. Strassmann ; [et al.]

Nature Publishing Group (NPG)

In: Nature. 461(7266): 980-2. doi: 10.1038/nature08472.

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Publication Date: 2009-10-02

Description: Cooperative social systems are susceptible to cheating by individuals that reap the benefits of cooperation without incurring the costs. There are various theoretical mechanisms for the repression of cheating and many have been tested experimentally. One possibility that has not been tested rigorously is the evolution of mutations that confer resistance to cheating. Here we show that the presence of a cheater in a population of randomly mutated social amoebae can select for cheater-resistance. Furthermore, we show that this cheater-resistance can be a noble strategy because the resister strain does not necessarily exploit other strains. Thus, the evolution of resisters may be instrumental in preserving cooperative behaviour in the face of cheating.〈br /〉〈span class="detail_caption"〉Notes: 〈/span〉Khare, Anupama -- Santorelli, Lorenzo A -- Strassmann, Joan E -- Queller, David C -- Kuspa, Adam -- Shaulsky, Gad -- England -- Nature. 2009 Oct 15;461(7266):980-2. doi: 10.1038/nature08472. Epub 2009 Sep 30.〈br /〉〈span class="detail_caption"〉Author address: 〈/span〉Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030, USA.〈br /〉〈span class="detail_caption"〉Record origin:〈/span〉 〈a href="http://www.ncbi.nlm.nih.gov/pubmed/19794414" target="_blank"〉PubMed〈/a〉

Keywords: Animals ; Cooperative Behavior ; Dictyostelium/genetics/*physiology ; Evolution, Molecular ; Genes, Protozoan/genetics ; *Models, Biological ; Mutation/genetics ; Protozoan Proteins/genetics/metabolism ; *Social Behavior ; Spores, Protozoan/physiology

Print ISSN: 0028-0836

Electronic ISSN: 1476-4687

Topics: Biology , Chemistry and Pharmacology , Medicine , Natural Sciences in General , Physics

Published by Nature Publishing Group (NPG)

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Periodic signaling controlled by an oscillatory circuit that includes protein kinases ERK2 and PKA (2004)

M. Maeda ; S. Lu ; G. Shaulsky ; [et al.]

American Association for the Advancement of Science (AAAS)

In: Science. 304(5672): 875-8. doi: 10.1126/science.1094647.

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Publication Date: 2004-05-08

Description: Self-regulating systems often use robust oscillatory circuits. One such system controls the chemotactic signaling mechanism of Dictyostelium, where pulses of adenosine 3',5'-monophosphate (cAMP) are generated with a periodicity of 7 minutes. We have observed spontaneous oscillations in activation of the mitogen-activated protein (MAP) kinase ERK2 that occur in phase with peaks of cAMP, and we show that ERK2 modulates cAMP levels through the phosphodiesterase RegA. Computer modeling and simulations of the underlying circuit faithfully account for the ability of the cells to spontaneously generate periodic pulses during specific stages of development. Similar oscillatory processes may occur in cells of many different species.〈br /〉〈span class="detail_caption"〉Notes: 〈/span〉Maeda, Mineko -- Lu, Sijie -- Shaulsky, Gad -- Miyazaki, Yuji -- Kuwayama, Hidekazu -- Tanaka, Yoshimasa -- Kuspa, Adam -- Loomis, William F -- GM52359/GM/NIGMS NIH HHS/ -- GM62350/GM/NIGMS NIH HHS/ -- R01 GM052359/GM/NIGMS NIH HHS/ -- New York, N.Y. -- Science. 2004 May 7;304(5672):875-8.〈br /〉〈span class="detail_caption"〉Author address: 〈/span〉Department of Biology, Graduate School of Science, Osaka University, Machikaneyama-cho 1-16, Toyonaka, Osaka 560-0043, Japan.〈br /〉〈span class="detail_caption"〉Record origin:〈/span〉 〈a href="http://www.ncbi.nlm.nih.gov/pubmed/15131307" target="_blank"〉PubMed〈/a〉

Keywords: 3',5'-Cyclic-AMP Phosphodiesterases ; Adenylyl Cyclases/metabolism ; Animals ; Computer Simulation ; Cyclic AMP/*metabolism ; Cyclic AMP-Dependent Protein Kinases/genetics/*metabolism ; Dictyostelium/enzymology/genetics/growth & development/*metabolism ; Enzyme Activation ; Mitogen-Activated Protein Kinase 1/genetics/*metabolism ; Models, Biological ; Mutagenesis, Site-Directed ; Mutation ; Phosphorylation ; Protozoan Proteins/genetics/metabolism ; Receptors, Cyclic AMP/metabolism ; *Signal Transduction

Print ISSN: 0036-8075

Electronic ISSN: 1095-9203

Topics: Biology , Chemistry and Pharmacology , Computer Science , Medicine , Natural Sciences in General , Physics

Published by American Association for the Advancement of Science (AAAS)

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Nucleocytoplasmic shuttling of a GATA transcription factor functions as a development timer (2014)

H. Cai ; M. Katoh-Kurasawa ; T. Muramoto ; [et al.]

American Association for the Advancement of Science (AAAS)

In: Science. 343(6177): 1249531. doi: 10.1126/science.1249531.

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Publication Date: 2014-03-22

Description: Biological oscillations are observed at many levels of cellular organization. In the social amoeba Dictyostelium discoideum, starvation-triggered multicellular development is organized by periodic cyclic adenosine 3',5'-monophosphate (cAMP) waves, which provide both chemoattractant gradients and developmental signals. We report that GtaC, a GATA transcription factor, exhibits rapid nucleocytoplasmic shuttling in response to cAMP waves. This behavior requires coordinated action of a nuclear localization signal and reversible G protein (heterotrimeric guanine nucleotide-binding protein)-coupled receptor-mediated phosphorylation. Although both are required for developmental gene expression, receptor occupancy promotes nuclear exit of GtaC, which leads to a transient burst of transcription at each cAMP cycle. We demonstrate that this biological circuit filters out high-frequency signals and counts those admitted, thereby enabling cells to modulate gene expression according to the dynamic pattern of the external stimuli.〈br /〉〈br /〉〈a href="https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4061987/" target="_blank"〉〈img src="https://static.pubmed.gov/portal/portal3rc.fcgi/4089621/img/3977009" border="0"〉〈/a〉 〈a href="https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4061987/" target="_blank"〉This paper as free author manuscript - peer-reviewed and accepted for publication〈/a〉〈br /〉〈br /〉〈span class="detail_caption"〉Notes: 〈/span〉Cai, Huaqing -- Katoh-Kurasawa, Mariko -- Muramoto, Tetsuya -- Santhanam, Balaji -- Long, Yu -- Li, Lei -- Ueda, Masahiro -- Iglesias, Pablo A -- Shaulsky, Gad -- Devreotes, Peter N -- GM 28007/GM/NIGMS NIH HHS/ -- GM 34933/GM/NIGMS NIH HHS/ -- HD 039691/HD/NICHD NIH HHS/ -- P01 HD039691/HD/NICHD NIH HHS/ -- R01 GM028007/GM/NIGMS NIH HHS/ -- R01 GM034933/GM/NIGMS NIH HHS/ -- R37 GM028007/GM/NIGMS NIH HHS/ -- New York, N.Y. -- Science. 2014 Mar 21;343(6177):1249531. doi: 10.1126/science.1249531.〈br /〉〈span class="detail_caption"〉Author address: 〈/span〉Department of Cell Biology, School of Medicine, Johns Hopkins University, Baltimore, MD 21205, USA.〈br /〉〈span class="detail_caption"〉Record origin:〈/span〉 〈a href="http://www.ncbi.nlm.nih.gov/pubmed/24653039" target="_blank"〉PubMed〈/a〉

Keywords: Active Transport, Cell Nucleus ; Cell Nucleus/*metabolism ; Cyclic AMP/metabolism/pharmacology ; Cytoplasm/*metabolism ; Dictyostelium/growth & development/*metabolism ; GATA Transcription Factors/chemistry/genetics/*metabolism ; Gene Expression Regulation ; Heterotrimeric GTP-Binding Proteins/metabolism ; Nuclear Localization Signals ; Phosphorylation ; Protozoan Proteins/chemistry/genetics/*metabolism ; Receptors, G-Protein-Coupled/metabolism

Print ISSN: 0036-8075

Electronic ISSN: 1095-9203

Topics: Biology , Chemistry and Pharmacology , Computer Science , Medicine , Natural Sciences in General , Physics

Published by American Association for the Advancement of Science (AAAS)

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Self-recognition in social amoebae is mediated by allelic pairs of tiger genes (2011)

S. Hirose ; R. Benabentos ; H. I. Ho ; [et al.]

American Association for the Advancement of Science (AAAS)

In: Science. 333(6041): 467-70. doi: 10.1126/science.1203903.

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Publication Date: 2011-06-28

Description: Free-living cells of the social amoebae Dictyostelium discoideum can aggregate and develop into multicellular fruiting bodies in which many die altruistically as they become stalk cells that support the surviving spores. Dictyostelium cells exhibit kin discrimination--a potential defense against cheaters, which sporulate without contributing to the stalk. Kin discrimination depends on strain relatedness, and the polymorphic genes tgrB1 and tgrC1 are potential components of that mechanism. Here, we demonstrate a direct role for these genes in kin discrimination. We show that a matching pair of tgrB1 and tgrC1 alleles is necessary and sufficient for attractive self-recognition, which is mediated by differential cell-cell adhesion. We propose that TgrB1 and TgrC1 proteins mediate this adhesion through direct binding. This system is a genetically tractable ancient model of eukaryotic self-recognition.〈br /〉〈br /〉〈a href="https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3142563/" target="_blank"〉〈img src="https://static.pubmed.gov/portal/portal3rc.fcgi/4089621/img/3977009" border="0"〉〈/a〉 〈a href="https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3142563/" target="_blank"〉This paper as free author manuscript - peer-reviewed and accepted for publication〈/a〉〈br /〉〈br /〉〈span class="detail_caption"〉Notes: 〈/span〉Hirose, Shigenori -- Benabentos, Rocio -- Ho, Hsing-I -- Kuspa, Adam -- Shaulsky, Gad -- F31 GM086131/GM/NIGMS NIH HHS/ -- R01 GM084992/GM/NIGMS NIH HHS/ -- R01 GM084992-03/GM/NIGMS NIH HHS/ -- New York, N.Y. -- Science. 2011 Jul 22;333(6041):467-70. doi: 10.1126/science.1203903. Epub 2011 Jun 23.〈br /〉〈span class="detail_caption"〉Author address: 〈/span〉Verna and Marrs McLean Department of Biochemistry and Molecular Biology, Baylor College of Medicine, Houston, TX 77030, USA.〈br /〉〈span class="detail_caption"〉Record origin:〈/span〉 〈a href="http://www.ncbi.nlm.nih.gov/pubmed/21700835" target="_blank"〉PubMed〈/a〉

Keywords: Alleles ; Amino Acid Sequence ; *Cell Adhesion ; Cell Aggregation ; Dictyostelium/*genetics/*physiology ; Gene Deletion ; *Genes, Protozoan ; Molecular Sequence Data ; Protein Binding ; Protozoan Proteins/*metabolism ; Spores, Protozoan/physiology

Print ISSN: 0036-8075

Electronic ISSN: 1095-9203

Topics: Biology , Chemistry and Pharmacology , Computer Science , Medicine , Natural Sciences in General , Physics

Published by American Association for the Advancement of Science (AAAS)

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