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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Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
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