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Cheating by Exploitation of Developmental Prestalk Patterning in


The cooperative developmental system of the social amoeba Dictyostelium discoideum is susceptible to exploitation by cheaters—strains that make more than their fair share of spores in chimerae. Laboratory screens in Dictyostelium have shown that the genetic potential for facultative cheating is high, and field surveys have shown that cheaters are abundant in nature, but the cheating mechanisms are largely unknown. Here we describe cheater C (chtC), a strong facultative cheater mutant that cheats by affecting prestalk differentiation. The chtC gene is developmentally regulated and its mRNA becomes stalk-enriched at the end of development. chtC mutants are defective in maintaining the prestalk cell fate as some of their prestalk cells transdifferentiate into prespore cells, but that defect does not affect gross developmental morphology or sporulation efficiency. In chimerae between wild-type and chtC mutant cells, the wild-type cells preferentially give rise to prestalk cells, and the chtC mutants increase their representation in the spore mass. Mixing chtC mutants with other cell-type proportioning mutants revealed that the cheating is directly related to the prestalk-differentiation propensity of the victim. These findings illustrate that a cheater can victimize cooperative strains by exploiting an established developmental pathway.


Vyšlo v časopise: Cheating by Exploitation of Developmental Prestalk Patterning in. PLoS Genet 6(2): e32767. doi:10.1371/journal.pgen.1000854
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1000854

Souhrn

The cooperative developmental system of the social amoeba Dictyostelium discoideum is susceptible to exploitation by cheaters—strains that make more than their fair share of spores in chimerae. Laboratory screens in Dictyostelium have shown that the genetic potential for facultative cheating is high, and field surveys have shown that cheaters are abundant in nature, but the cheating mechanisms are largely unknown. Here we describe cheater C (chtC), a strong facultative cheater mutant that cheats by affecting prestalk differentiation. The chtC gene is developmentally regulated and its mRNA becomes stalk-enriched at the end of development. chtC mutants are defective in maintaining the prestalk cell fate as some of their prestalk cells transdifferentiate into prespore cells, but that defect does not affect gross developmental morphology or sporulation efficiency. In chimerae between wild-type and chtC mutant cells, the wild-type cells preferentially give rise to prestalk cells, and the chtC mutants increase their representation in the spore mass. Mixing chtC mutants with other cell-type proportioning mutants revealed that the cheating is directly related to the prestalk-differentiation propensity of the victim. These findings illustrate that a cheater can victimize cooperative strains by exploiting an established developmental pathway.


Zdroje

1. Maynard SmithJ

SzathmáryE

1997 The major transitions in evolution: Oxford University Press, USA.

2. AbbotP

WithgottJH

MoranNA

2001 Genetic conflict and conditional altruism in social aphid colonies. Proceedings of the National Academy of Sciences 98 12068

3. HughesWOH

BoomsmaJJ

2008 Genetic royal cheats in leaf-cutting ant societies. Proceedings of the National Academy of Sciences 105 5150

4. WenseleersT

RatnieksFLW

de F RibeiroM

de A AlvesD

Imperatriz-FonsecaVL

2005 Working-class royalty: bees beat the caste system. Biology Letters 1 125

5. KessinRH

2001 Dictyostelium: evolution, cell biology, and the development of multicellularity: Cambridge University Press.

6. GilbertOM

FosterKR

MehdiabadiNJ

StrassmannJE

QuellerDC

2007 High relatedness maintains multicellular cooperation in a social amoeba by controlling cheater mutants. Proceedings of the National Academy of Sciences 104 8913

7. StrassmannJE

ZhuY

QuellerDC

2000 Altruism and social cheating in the social amoeba Dictyostelium discoideum. Nature 408 965 967

8. EnnisHL

DaoDN

PukatzkiSU

KessinRH

2000 Dictyostelium amoebae lacking an F-box protein form spores rather than stalk in chimeras with wild type. Proceedings of the National Academy of Sciences 97 3292

9. SantorelliLA

ThompsonCRL

VillegasE

SvetzJ

DinhC

2008 Facultative cheater mutants reveal the genetic complexity of cooperation in social amoebae. Nature 451 1107

10. KhareA

SantorelliLA

StrassmannJE

QuellerDC

KuspaA

2009 Cheater-resistance is not futile. Nature 461 980 982

11. SilloA

BloomfieldG

BalestA

BalboA

PergolizziB

2008 Genome-wide transcriptional changes induced by phagocytosis or growth on bacteria in Dictyostelium. BMC Genomics 9 291

12. EichingerL

2006 Dictyostelium discoideum protocols: Humana Press.

13. HuangE

BlaggSL

KellerT

KatohM

ShaulskyG

2006 bZIP transcription factor interactions regulate DIF responses in Dictyostelium. Development 133 449 458

14. ShaulskyG

KuspaA

LoomisWF

1995 A multidrug resistance transporter/serine protease gene is required for prestalk specialization in Dictyostelium. Genes & Development 9 1111 1122

15. ShaulskyG

LoomisWF

1996 Initial Cell Type Divergence in Dictyostelium is Independent of DIF-1. Developmental Biology 174 214 220

16. JermynKA

DuffyKTI

WilliamsJG

1989 A new anatomy of the prestalk zone in Dictyostelium. Nature 340 144 146

17. RaperKB

1940 Pseudoplasmodium formation and organization in Dictyostelium discoideum. J Elisha Mitchell Sci Soc 56 241 282

18. ShaulskyG

LoomisWF

1993 Cell type regulation in response to expression of ricin A in Dictyostelium. Developmental Biology 160 85 98

19. FosnaughKL

LoomisWF

1993 Enhancer regions responsible for temporal and cell-type-specific expression of a spore coat gene in Dictyostelium. Developmental biology 157 38

20. CabralM

AnjardC

LoomisWF

KuspaA

2006 Genetic Evidence that the Acyl Coenzyme A Binding Protein AcbA and the Serine Protease/ABC Transporter TagA Function Together in Dictyostelium discoideum Cell Differentiation? Eukaryotic Cell 5 2024 2032

21. GoodJR

CabralM

SharmaS

YangJ

Van DriesscheN

2003 TagA, a putative serine protease/ABC transporter of Dictyostelium that is required for cell fate determination at the onset of development. Development 130 2953 2965

22. ChangWT

NewellPC

GrossJD

1996 Identification of the cell fate gene stalky in Dictyostelium. Cell 87 471 482

23. JaiswalJK

MujumdarN

MacWilliamsHK

NanjundiahV

2006 Trishanku, a novel regulator of cell-type stability and morphogenesis in Dictyostelium discoideum. Differentiation 74 596 607

24. MohantyS

FirtelRA

1999 Control of spatial patterning and cell-type proportioning in Dictyostelium. Seminars in Cell & Developmental Biology 597 608

25. WestSA

DiggleSP

BucklingA

GardnerA

GriffinAS

2007 The social lives of microbes. Annual Review of Ecology, Evolution and Systematics 38 53 77

26. FaixJ

KreppelL

ShaulskyG

SchleicherM

KimmelAR

2004 A rapid and efficient method to generate multiple gene disruptions in Dictyostelium discoideum using a single selectable marker and the Cre-loxP system. Nucleic Acids Research 32 e143

27. JermynKA

WilliamsJG

1991 An analysis of culmination in Dictyostelium using prestalk and stalk-specific cell autonomous markers. Development 111 779 787

28. SussmanM

1987 Cultivation and synchronous morphogenesis of Dictyostelium under controlled experimental conditions. Methods Cell Biol 28 9 29

29. OstrowskiEA

KatohM

ShaulskyG

QuellerDC

StrassmannJE

2008 Kin Discrimination Increases with Genetic Distance in a Social Amoeba. PLoS Biol 6 e287 doi:10.1371/journal.pbio.0060287

30. InsallR

1994 CRAC, a cytosolic protein containing a pleckstrin homology domain, is required for receptor and G protein-mediated activation of adenylyl cyclase in Dictyostelium. The Journal of Cell Biology 126 1537 1545

31. KatohM

CurkT

XuQ

ZupanB

KuspaA

2006 Developmentally Regulated DNA Methylation in Dictyostelium discoideum. Eukaryotic Cell 5 18 25

32. VollrathD

DavisRW

ConnellyC

HieterP

1988 Physical Mapping of Large DNA by Chromosome Fragmentation. Proceedings of the National Academy of Sciences 85 6027 6031

33. KiblerK

NguyenTL

SvetzJ

DriesscheNV

IbarraM

2003 A novel developmental mechanism in Dictyostelium revealed in a screen for communication mutants. Developmental Biology 259 193 208

34. FeinbergAP

VogelsteinB

1983 A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Analytical Biochemistry 132 6 13

35. BenabentosR

HiroseS

SucgangR

CurkT

KatohM

2009 Polymorphic Members of the lag Gene Family Mediate Kin Discrimination in Dictyostelium. Current Biology 19 567 572

36. EscalanteR

LoomisWF

1995 Whole-Mount in Situ Hybridization of Cell-Type-Specific mRNAs in Dictyostelium. Developmental Biology 171 262 266

37. KnechtDA

CohenSM

LoomisWF

LodishHF

1986 Developmental regulation of Dictyostelium discoideum actin gene fusions carried on low-copy and high-copy transformation vectors. Molecular and Cellular Biology 6 3973 3983

38. FosterKR

ShaulskyG

StrassmannJE

QuellerDC

ThompsonCRL

2004 Pleiotropy as a mechanism to stabilize cooperation. Nature 431 693 696

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