Control of Cell Type Proportioning in Dictyostelium Discoideum by Differentiation-inducing Factor As Determined by in Situ Hybridization

Overview

Journal Eukaryot Cell

Publisher American Society for Microbiology

Specialty Molecular Biology

Date 2004 Oct 8

PMID 15470253

Citations 15

Authors

Toshinari Maruo

Haruyo Sakamoto

Negin Iranfar

Danny Fuller

Takahiro Morio

Hideko Urushihara

Yoshimasa Tanaka

Mineko Maeda

William F Loomis

Affiliations

Soon will be listed here.

Abstract

We have determined the proportions of the prespore and prestalk regions in Dictyostelium discoideum slugs by in situ hybridization with a large number of prespore- and prestalk-specific genes. Microarrays were used to discover genes expressed in a cell type-specific manner. Fifty-four prespore-specific genes were verified by in situ hybridization, including 18 that had been previously shown to be cell type specific. The 36 new genes more than doubles the number of available prespore markers. At the slug stage, the prespore genes hybridized to cells uniformly in the posterior 80% of wild-type slugs but hybridized to the posterior 90% of slugs lacking the secreted alkylphenone differentiation-inducing factor 1 (DIF-1). There was a compensatory twofold decrease in prestalk cells in DIF-less slugs. Removal of prespore cells resulted in cell type conversion in both wild-type and DIF-less anterior fragments. Thus, DIF-1 appears to act in concert with other processes to establish cell type proportions.

Citing Articles

Transition state dynamics during a stochastic fate choice.

Antolovic V, Lenn T, Miermont A, Chubb J Development. 2019; 146(12).

PMID: 30890571 PMC: 6602359. DOI: 10.1242/dev.173740.

Implications of expansin-like 3 gene in Dictyostelium morphogenesis.

Kawata T, Nakamura Y, Saga Y, Iwade Y, Ishikawa M, Sakurai A Springerplus. 2015; 4:190.

PMID: 25932374 PMC: 4408306. DOI: 10.1186/s40064-015-0964-0.

Evolutionary reconstruction of pattern formation in 98 Dictyostelium species reveals that cell-type specialization by lateral inhibition is a derived trait.

Schilde C, Skiba A, Schaap P Evodevo. 2015; 5:34.

PMID: 25904998 PMC: 4406040. DOI: 10.1186/2041-9139-5-34.

Mef2A, a homologue of animal Mef2 transcription factors, regulates cell differentiation in Dictyostelium discoideum.

Galardi-Castilla M, Fernandez-Aguado I, Suarez T, Sastre L BMC Dev Biol. 2013; 13:12.

PMID: 23577638 PMC: 3640940. DOI: 10.1186/1471-213X-13-12.

Systematic analysis of γ-aminobutyric acid (GABA) metabolism and function in the social amoeba Dictyostelium discoideum.

Wu Y, Janetopoulos C J Biol Chem. 2013; 288(21):15280-90.

PMID: 23548898 PMC: 3663548. DOI: 10.1074/jbc.M112.427047.

References

Thompson C, Kay R . The role of DIF-1 signaling in Dictyostelium development. Mol Cell. 2001; 6(6):1509-14. DOI: 10.1016/s1097-2765(00)00147-7. View

Morio T, Urushihara H, Saito T, Ugawa Y, Mizuno H, Yoshida M . The Dictyostelium developmental cDNA project: generation and analysis of expressed sequence tags from the first-finger stage of development. DNA Res. 1999; 5(6):335-40. DOI: 10.1093/dnares/5.6.335. View

Kay R, Thompson C . Cross-induction of cell types in Dictyostelium: evidence that DIF-1 is made by prespore cells. Development. 2001; 128(24):4959-66. DOI: 10.1242/dev.128.24.4959. View

Maeda M, Sakamoto H, Iranfar N, Fuller D, Maruo T, Ogihara S . Changing patterns of gene expression in dictyostelium prestalk cell subtypes recognized by in situ hybridization with genes from microarray analyses. Eukaryot Cell. 2003; 2(3):627-37. PMC: 161460. DOI: 10.1128/EC.2.3.627-637.2003. View

Iranfar N, Fuller D, Loomis W . Genome-wide expression analyses of gene regulation during early development of Dictyostelium discoideum. Eukaryot Cell. 2003; 2(4):664-70. PMC: 178357. DOI: 10.1128/EC.2.4.664-670.2003. View

Thompson C, Fu Q, Buhay C, Kay R, Shaulsky G . A bZIP/bRLZ transcription factor required for DIF signaling in Dictyostelium. Development. 2004; 131(3):513-23. DOI: 10.1242/dev.00939. View

Urushihara H, Morio T, Saito T, Kohara Y, Koriki E, Ochiai H . Analyses of cDNAs from growth and slug stages of Dictyostelium discoideum. Nucleic Acids Res. 2004; 32(5):1647-53. PMC: 390320. DOI: 10.1093/nar/gkh262. View

Kay R, Jermyn K . A possible morphogen controlling differentiation in Dictyostelium. Nature. 1983; 303(5914):242-4. DOI: 10.1038/303242a0. View

Brookman J, Jermyn K, Kay R . Nature and distribution of the morphogen DIF in the Dictyostelium slug. Development. 1987; 100(1):119-24. DOI: 10.1242/dev.100.1.119. View

10.

Early A, G Williams J . A Dictyostelium prespore-specific gene is transcriptionally repressed by DIF in vitro. Development. 1988; 103(3):519-24. DOI: 10.1242/dev.103.3.519. View

11.

Jermyn K, Duffy K, G Williams J . A new anatomy of the prestalk zone in Dictyostelium. Nature. 1989; 340(6229):144-6. DOI: 10.1038/340144a0. View

12.

G Williams J, Duffy K, Lane D, McRobbie S, Harwood A, Traynor D . Origins of the prestalk-prespore pattern in Dictyostelium development. Cell. 1989; 59(6):1157-63. DOI: 10.1016/0092-8674(89)90771-x. View

13.

Haberstroh L, Firtel R . A spatial gradient of expression of a cAMP-regulated prespore cell-type-specific gene in Dictyostelium. Genes Dev. 1990; 4(4):596-612. DOI: 10.1101/gad.4.4.596. View

14.

Kay R . Cell differentiation and patterning in Dictyostelium. Curr Opin Cell Biol. 1992; 4(6):934-8. DOI: 10.1016/0955-0674(92)90121-r. View

15.

Fosnaugh K, Loomis W . Enhancer regions responsible for temporal and cell-type-specific expression of a spore coat gene in Dictyostelium. Dev Biol. 1993; 157(1):38-48. DOI: 10.1006/dbio.1993.1110. View

16.

Shaulsky G, Loomis W . Mitochondrial DNA replication but no nuclear DNA replication during development of Dictyostelium. Proc Natl Acad Sci U S A. 1995; 92(12):5660-3. PMC: 41756. DOI: 10.1073/pnas.92.12.5660. View

17.

Richardson D, Loomis W, Kimmel A . Progression of an inductive signal activates sporulation in Dictyostelium discoideum. Development. 1994; 120(10):2891-900. DOI: 10.1242/dev.120.10.2891. View

18.

Early A, Abe T, Williams J . Evidence for positional differentiation of prestalk cells and for a morphogenetic gradient in Dictyostelium. Cell. 1995; 83(1):91-9. DOI: 10.1016/0092-8674(95)90237-6. View

19.

Shaulsky G, Loomis W . Initial cell type divergence in Dictyostelium is independent of DIF-1. Dev Biol. 1996; 174(2):214-20. DOI: 10.1006/dbio.1996.0067. View

20.

Loomis W . Genetic networks that regulate development in Dictyostelium cells. Microbiol Rev. 1996; 60(1):135-50. PMC: 239421. DOI: 10.1128/mr.60.1.135-150.1996. View