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. 1986 Dec;6(12):4353–4361. doi: 10.1128/mcb.6.12.4353

Multiple regulatory genes control expression of a gene family during development of Dictyostelium discoideum.

S Alexander, A M Cibulsky, S D Cuneo
PMCID: PMC367217  PMID: 3796605

Abstract

Mutant strains of Dictyostelium discoideum carrying dis mutations fail to transcribe specifically the family of developmentally regulated discoidin lectin genes during morphogenesis. The phenotypes of these mutants strongly suggested that the mutations reside in regulatory genes. Using these mutant strains, we showed that multiple regulatory genes are required for the expression of the lectin structural genes and that these regulatory genes (the dis+ alleles) act in trans to regulate this gene family. These regulatory genes fall into two complementation groups (disA and disB) and map to linkage groups II and III, respectively. A further regulatory locus was defined by the identification of an unlinked supressor gene, drsA (discoidin restoring), which is epistatic to disB, but not disA, and results in the restoration of lectin expression in cells carrying the disB mutation. Mutant cells carrying the drsA allele express the discoidin lectin gene family during growth and development, in contrast to wild-type cells which express it only during development. Therefore, the suppressor activity of the drsA allele appears to function by making the expression of the discoidin lectins constitutive and no longer strictly developmentally regulated. The data indicate that normal expression of the discoidin lectins is dependent on the sequential action of the disB+, drsA+, and disA+ gene products. Thus, we described an interacting network of regulatory genes which in turn controls the developmental expression of a family of genes during the morphogenesis of D. discoideum.

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Selected References

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  1. Alexander S., Cibulsky A. M., Mitchell L., Soll D. R. The regulation of 'early' enzymes during the development and dedifferentiation of Dictyostelium discoideum. Differentiation. 1985;30(1):1–6. doi: 10.1111/j.1432-0436.1985.tb00505.x. [DOI] [PubMed] [Google Scholar]
  2. Alexander S., Shinnick T. M., Lerner R. A. Mutants of Dictyostelium discoideum blocked in expression of all members of the developmentally regulated discoidin multigene family. Cell. 1983 Sep;34(2):467–475. doi: 10.1016/0092-8674(83)90380-x. [DOI] [PubMed] [Google Scholar]
  3. Alton T. H., Lodish H. F. Developmental changes in messenger RNAs and protein synthesis in Dictyostelium discoideum. Dev Biol. 1977 Oct 1;60(1):180–206. doi: 10.1016/0012-1606(77)90118-x. [DOI] [PubMed] [Google Scholar]
  4. Berger E. A., Clark J. M. Specific cell-cell contact serves as the developmental signal to deactivate discoidin I gene expression in Dictyostelium discoideum. Proc Natl Acad Sci U S A. 1983 Aug;80(16):4983–4987. doi: 10.1073/pnas.80.16.4983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Blumberg D. D., Lodish H. F. Changes in the messenger RNA population during differentiation of dictyostelium discoideum. Dev Biol. 1980 Aug;78(2):285–300. doi: 10.1016/0012-1606(80)90337-1. [DOI] [PubMed] [Google Scholar]
  6. Botstein D., Maurer R. Genetic approaches to the analysis of microbial development. Annu Rev Genet. 1982;16:61–83. doi: 10.1146/annurev.ge.16.120182.000425. [DOI] [PubMed] [Google Scholar]
  7. Crowley T. E., Nellen W., Gomer R. H., Firtel R. A. Phenocopy of discoidin I-minus mutants by antisense transformation in Dictyostelium. Cell. 1985 Dec;43(3 Pt 2):633–641. doi: 10.1016/0092-8674(85)90235-1. [DOI] [PubMed] [Google Scholar]
  8. Demerec M., Adelberg E. A., Clark A. J., Hartman P. E. A proposal for a uniform nomenclature in bacterial genetics. Genetics. 1966 Jul;54(1):61–76. doi: 10.1093/genetics/54.1.61. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Devine J. M., Tsang A. S., Williams J. G. Differential expression of the members of the discoidin I multigene family during growth and development of Dictyostelium discoideum. Cell. 1982 Apr;28(4):793–800. doi: 10.1016/0092-8674(82)90058-7. [DOI] [PubMed] [Google Scholar]
  10. Dimond R. L., Brenner M., Loomis W. F., Jr Mutations affecting N-acetylglucosaminidase in Dictyostelium discoideum. Proc Natl Acad Sci U S A. 1973 Dec;70(12):3356–3360. doi: 10.1073/pnas.70.12.3356. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Free S. J., Schimke R. T. The structural gene for alpha-mannosidase-1 in Dictyostellium discoideum. Genetics. 1976 Oct;84(2):159–174. doi: 10.1093/genetics/84.2.159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Katz E. R., Sussman M. Parasexual recombination in Dictyostelium discoideum: selection of stable diploid heterozygotes and stable haploid segregants (clones-temperature sensitive-ploidy-fruiting bodies-spore-slime mold). Proc Natl Acad Sci U S A. 1972 Feb;69(2):495–498. doi: 10.1073/pnas.69.2.495. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  14. Loomis W. F. Genetic analysis of the gene for N-acetylglucosaminidase in Dictyostelium discoideum. Genetics. 1978 Feb;88(2):277–284. doi: 10.1093/genetics/88.2.277. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Ma G. C., Firtel R. A. Regulation of the synthesis of two carbohydrate-binding proteins in Dictyostelium discoideum. J Biol Chem. 1978 Jun 10;253(11):3924–3932. [PubMed] [Google Scholar]
  16. Morrissey J. H. Deficiency in homogentisic acid oxidase activity associated with the brown phenotype of Dictyostelium discoideum. J Gen Microbiol. 1983 Apr;129(4):1127–1132. doi: 10.1099/00221287-129-4-1127. [DOI] [PubMed] [Google Scholar]
  17. Morrissey J. H., Wheeler S., Loomis W. F. New Loci in DICTYOSTELIUM DISCOIDEUM Determining Pigment Formation and Growth on BACILLUS SUBTILIS. Genetics. 1980 Sep;96(1):115–123. doi: 10.1093/genetics/96.1.115. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Newell P. C. Genetics of the cellular slime molds. Annu Rev Genet. 1978;12:69–93. doi: 10.1146/annurev.ge.12.120178.000441. [DOI] [PubMed] [Google Scholar]
  19. Ratner D. I., Newell P. C. Linkage analysis in Dictyostelium discoideum using multiply marked tester strains: establishment of linkage group VII and the reassessment of earlier linkage data. J Gen Microbiol. 1978 Dec;109(2):225–236. doi: 10.1099/00221287-109-2-225. [DOI] [PubMed] [Google Scholar]
  20. Rosen S. D., Kafka J. A., Simpson D. L., Barondes S. H. Developmentally regulated, carbohydrate-binding protein in Dictyostelium discoideum. Proc Natl Acad Sci U S A. 1973 Sep;70(9):2554–2557. doi: 10.1073/pnas.70.9.2554. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Rowekamp W., Poole S., Firtel R. A. Analysis of the multigene family coding the developmentally regulated carbohydrate-binding protein discoidin-I in D. discoideum. Cell. 1980 Jun;20(2):495–505. doi: 10.1016/0092-8674(80)90636-4. [DOI] [PubMed] [Google Scholar]
  22. Soll D. R. Timers in developing systems. Science. 1979 Mar 2;203(4383):841–849. doi: 10.1126/science.419408. [DOI] [PubMed] [Google Scholar]
  23. Springer W. R., Cooper D. N., Barondes S. H. Discoidin I is implicated in cell-substratum attachment and ordered cell migration of Dictyostelium discoideum and resembles fibronectin. Cell. 1984 Dec;39(3 Pt 2):557–564. doi: 10.1016/0092-8674(84)90462-8. [DOI] [PubMed] [Google Scholar]
  24. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350–4354. doi: 10.1073/pnas.76.9.4350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Tsang A. S., Devine J. M., Williams J. G. The multiple subunits of discoidin I are encoded by different genes. Dev Biol. 1981 May;84(1):212–217. doi: 10.1016/0012-1606(81)90385-7. [DOI] [PubMed] [Google Scholar]
  26. Welker D. L., Williams K. L. Translocations in Dictyostelium discoideum. Genetics. 1985 Feb;109(2):341–364. doi: 10.1093/genetics/109.2.341. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Williams J. G., Tsang A. S., Mahbubani H. A change in the rate of transcription of a eukaryotic gene in response to cyclic AMP. Proc Natl Acad Sci U S A. 1980 Dec;77(12):7171–7175. doi: 10.1073/pnas.77.12.7171. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Williams K. L., Kessin R. H., Newell P. C. Parasexual genetics in Dictyostelium discoideum: mitotic analysis of acriflavin resistance and growth in axenic medium. J Gen Microbiol. 1974 Sep;84(1):59–69. doi: 10.1099/00221287-84-1-59. [DOI] [PubMed] [Google Scholar]

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