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PMID: 15470238 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Transcriptional transitions during Dictyostelium spore germination.

Eukaryotic cell ·Vol. 3 ·No. 5 ·2004-10-00 ·Pages 1101-10

Xu Q, Ibarra M, Mahadeo D, Shaw C, Huang E, Kuspa A, Cotter D, Shaulsky G

Abstract

Many protozoa form spores in response to adversity; therefore, spore germination is a key process in their life cycle. Dictyostelium discoideum sporulates in response to starvation following a developmental program. Germination is characterized by two visible changes, spore swelling and the emergence of amoeba from the spore capsule. Several studies have indicated that an additional process termed spore activation is also required, but the physiological changes that characterize the three phases are largely uncharacterized. We used microarrays to monitor global transcriptional transitions as a surrogate measure of the physiological changes that occur during germination. Using two independent methods to induce germination, we identified changes in mRNA levels that characterized the germination process rather than changes that resulted from the induction method. We found that germination is characterized by three transitions. The first transition occurs during activation, while the spores appear dormant, the largest transition occurs when swelling begins, and the third transition occurs when emergence begins. These findings indicate that activation and swelling are not passive occurrences, such as dilution of inhibitors or spore rehydration, but are active processes that are accompanied by dramatic events in mRNA degradation and de novo transcription. These findings confirm and extend earlier reports that genes such as celA are regulated during spore germination. We also found by mutation analysis that the unconventional myosin gene myoI, which is induced during early germination, plays roles in the maintenance of dormancy and in spore swelling. This finding suggests that some of the observed transcriptional changes are required for spore germination.

MeSH Terms
Animals Cellulase/genetics Dictyostelium/genetics,growth & development,physiology Gene Expression Regulation, Developmental Genes, Protozoan Mutation Myosin Type I/genetics Protozoan Proteins/genetics RNA, Messenger/genetics,metabolism RNA, Protozoan/genetics,metabolism Spores, Protozoan/genetics,physiology Transcription, Genetic
Chemicals
Protozoan Proteins RNA, Messenger RNA, Protozoan CelA endoglucanase Cellulase Myosin Type I
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Xu Qikai
Graduate Program in Structural and Computational Biology and Molecular Biophysics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.
Ibarra Miroslava
Mahadeo Dana
Shaw Chad
Huang Eryong
Kuspa Adam
Cotter David
Shaulsky Gad
References (42)
42 references, click to expand
  1. Distinct types of diffuse large B-cell lymphoma identified by gene expression profiling.
    Nature. 2000 Feb 3;403(6769):503-11 PMID: 10676951
  2. A MAP kinase necessary for receptor-mediated activation of adenylyl cyclase in Dictyostelium.
    J Cell Biol. 1995 Feb;128(3):405-13 PMID: 7844154
  3. The role of unconventional myosins in Dictyostelium endocytosis.
    J Eukaryot Microbiol. 2000 May-Jun;47(3):191-6 PMID: 10847335
  4. Functional discovery via a compendium of expression profiles.
    Cell. 2000 Jul 7;102(1):109-26 PMID: 10929718
  5. Environmental regulation of pathways controlling sporulation, dormancy and germination utilizes bacterial-like signaling complexes in Dictyostelium discoideum.
    Protist. 2000 Aug;151(2):111-26 PMID: 10965951
  6. The molecular mechanisms of conidial germination.
    FEMS Microbiol Lett. 2001 May 30;199(2):153-60 PMID: 11377860
  7. Requirements for the adenylyl cyclases in the development of Dictyostelium.
    Development. 2001 Sep;128(18):3649-54 PMID: 11566867
  8. Comparison of morphogenetic networks of filamentous fungi and yeast.
    Fungal Genet Biol. 2001 Nov;34(2):63-82 PMID: 11686673
  9. The formation of actin rods composed of actin tubules in Dictyostelium discoideum spores.
    J Struct Biol. 2001 Oct;136(1):7-19 PMID: 11858703
  10. A transcriptional profile of multicellular development in Dictyostelium discoideum.
    Development. 2002 Apr;129(7):1543-52 PMID: 11923193
  11. Large-scale prediction of Saccharomyces cerevisiae gene function using overlapping transcriptional clusters.
    Nat Genet. 2002 Jul;31(3):255-65 PMID: 12089522
  12. Functional profiling of the Saccharomyces cerevisiae genome.
    Nature. 2002 Jul 25;418(6896):387-91 PMID: 12140549
  13. Parallel phenotypic analysis of sporulation and postgermination growth in Saccharomyces cerevisiae.
    Proc Natl Acad Sci U S A. 2002 Nov 26;99(24):15530-5 PMID: 12432101
  14. TagA, a putative serine protease/ABC transporter of Dictyostelium that is required for cell fate determination at the onset of development.
    Development. 2003 Jul;130(13):2953-65 PMID: 12756178
  15. A novel developmental mechanism in Dictyostelium revealed in a screen for communication mutants.
    Dev Biol. 2003 Jul 15;259(2):193-208 PMID: 12871696
  16. Genome-wide expression analyses of gene regulation during early development of Dictyostelium discoideum.
    Eukaryot Cell. 2003 Aug;2(4):664-70 PMID: 12912885
  17. A cell-adhesion pathway regulates intercellular communication during Dictyostelium development.
    Dev Biol. 2003 Dec 15;264(2):506-21 PMID: 14651934
  18. An orderly retreat: Dedifferentiation is a regulated process.
    Proc Natl Acad Sci U S A. 2004 May 4;101(18):7005-10 PMID: 15103019
  19. Spore germination in Dictyostelium discoideum. II. Effects of dimethyl sulfoxide on post-activation lag as evidence for the multistate model of activation.
    Arch Microbiol. 1976 May 3;108(1):93-8 PMID: 945047
  20. Autoactivation of spore germination in mutant and wild type strains of Dictyostelium discoideum.
    Microbios. 1978;23(93-94):153-66 PMID: 756953
  21. Nogalamycin inhibits ribonucleic acid synthesis in growing and developing cells of the slime mold Dictyostelium discoideum.
    Antimicrob Agents Chemother. 1981 Apr;19(4):657-65 PMID: 7247388
  22. Adenylyl cyclase G, an osmosensor controlling germination of Dictyostelium spores.
    J Biol Chem. 1996 Sep 27;271(39):23623-5 PMID: 8798577
  23. Developmental signal transduction pathways uncovered by genetic suppressors.
    Proc Natl Acad Sci U S A. 1996 Dec 24;93(26):15260-5 PMID: 8986798
  24. Endogenous autoinhibitors regulate changes in actin tyrosine phosphorylation during Dictyostelium spore germination.
    Cell Signal. 1997 Jan;9(1):79-83 PMID: 9067634
  25. Unconventional myosins in cell movement, membrane traffic, and signal transduction.
    Science. 1998 Jan 23;279(5350):527-33 PMID: 9438839
  26. A cAMP-phosphodiesterase controls PKA-dependent differentiation.
    Development. 1998 Feb;125(4):691-9 PMID: 9435289
  27. The hybrid histidine kinase dhkB regulates spore germination in Dictyostelium discoideum.
    Dev Biol. 1998 Apr 15;196(2):171-83 PMID: 9576830
  28. High levels of actin tyrosine phosphorylation: correlation with the dormant state of Dictyostelium spores.
    J Cell Sci. 1998 Oct;111 ( Pt 19):2923-32 PMID: 9730984
  29. Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis.
    Science. 1999 Aug 6;285(5429):901-6 PMID: 10436161
  30. Ammonium phosphate in sori of Dictyostelium discoideum promotes spore dormancy through stimulation of the osmosensor ACG.
    Microbiology. 1999 Aug;145 ( Pt 8):1891-901 PMID: 10463155
  31. A new class of rapidly developing mutants in Dictyostelium discoideum: implications for cyclic AMP metabolism and cell differentiation.
    Dev Biol. 1983 Jan;95(1):200-10 PMID: 6298035
  32. The stage specific inhibition of Dictyostelium discoideum spore germination by the mutagen 4-nitroquinoline 1-oxide.
    Chem Biol Interact. 1984 Jan;48(1):1-14 PMID: 6420082
  33. Developmental regulation of Dictyostelium discoideum actin gene fusions carried on low-copy and high-copy transformation vectors.
    Mol Cell Biol. 1986 Nov;6(11):3973-83 PMID: 3025622
  34. Cultivation and synchronous morphogenesis of Dictyostelium under controlled experimental conditions.
    Methods Cell Biol. 1987;28:9-29 PMID: 3298997
  35. Characterization of genes that are developmentally regulated during Dictyostelium discoideum spore germination.
    Dev Genet. 1988;9(4-5):303-13 PMID: 3243024
  36. A shared internal threonine-glutamic acid-threonine-proline repeat defines a family of Dictyostelium discoideum spore germination specific proteins.
    Biochemistry. 1990 Aug 7;29(31):7264-9 PMID: 1976383
  37. Structure, expression, and regulation of members of the developmentally controlled V and H gene classes from Dictyostelium.
    Dev Genet. 1991;12(1-2):88-97 PMID: 2049884
  38. Disruption of the sporulation-specific gene spiA in Dictyostelium discoideum leads to spore instability.
    Genes Dev. 1992 Jun;6(6):1058-70 PMID: 1592257
  39. Tagging developmental genes in Dictyostelium by restriction enzyme-mediated integration of plasmid DNA.
    Proc Natl Acad Sci U S A. 1992 Sep 15;89(18):8803-7 PMID: 1326764
  40. Patterning of development in Dictyostelium discoideum: factors regulating growth, differentiation, spore dormancy, and germination.
    Biochem Cell Biol. 1992 Oct-Nov;70(10-11):892-919 PMID: 1338416
  41. Discovery of myosin genes by physical mapping in Dictyostelium.
    Proc Natl Acad Sci U S A. 1994 Sep 27;91(20):9446-50 PMID: 7937787
  42. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium.
    Nat Genet. 2000 May;25(1):25-9 PMID: 10802651
Article Info
Journal
Eukaryotic cell
Abbr.
Eukaryot Cell
ISSN
1535-9778
Published
2004-10-00
Pages
1101-10
Language
English
Region
United States
NLM ID
101130731
PMCID
PMC522591
Subset
IM
Grants
NICHD NIH HHS · P01 HD039691 · United States
NICHD NIH HHS · P01 HD39691 · United States
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