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Cyclic di-GMP Activates Adenylate Cyclase A and Protein Kinase A to Induce Stalk Formation in Dictyostelium

  • Zhi-hui Chen
  • Christina Schilde
  • Pauline SchaapEmail author
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Abstract

Cyclic di-GMP, an important prokaryote second messenger is used by the eukaryote Dictyostelium discoideum as a secreted signal to trigger stalk formation in fruiting bodies. Cyclic di-GMP is synthesized by a prokaryote-type diguanylate cyclase DgcA, but its mode of action was unknown. Transcriptional profiling yielded several target genes for cyclic di-GMP, which were tested for cyclic di-GMP induced expression in mutants with similar phenotypes as dgca-. A mutant with reduced PKA activity showed defective cyclic di-GMP induced stalk gene expression. Cyclic di-GMP increased cAMP levels in wild-type cells, but not in a mutant that lacked adenylate cyclase A (ACA) activity in slugs. This mutant also did not show cyclic di-GMP induced stalk gene expression. The stalk-less dgca- mutant regained its stalk by expression of a light-activated adenylate cyclase from the ACA promoter and exposure to light, indicating that cAMP is the intermediate for cyclic di-GMP in normal development. ACA is expressed at the tip of emerging fruiting bodies, where it produces the cAMP pulses that organize morphogenetic movement. The tip is also the site where stalk differentiation initiates. Our finding that cyclic di-GMP acts on tip-expressed ACA explains why the Dictyostelium stalk is always formed at the morphogenetic organizer.

Keywords

Dictyostelium discoideum Cyclic di-GMP Fruiting bodies Stalk formation Protein kinase A Adenylate cyclase A Organizer 

Notes

Acknowledgment

Research reported in this study was funded by Leverhulme Trust grants RPG-2012-746 and RPG-2016-220, Wellcome Trust grant 100293/Z/12/Z and European Research Council grant 742288.

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Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  • Zhi-hui Chen
    • 1
  • Christina Schilde
    • 1
  • Pauline Schaap
    • 1
    Email author
  1. 1.School of Life SciencesUniversity of DundeeDundeeUK

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