Loss of the Polyketide Synthase StlB Results in Stalk Cell Over production in Polysphondylium violaceum

Takaaki B. Narita, Yoshinori Kawabe, Koryu Kin, Richard A. Gibbs, Adam Kuspa, Donna Muzny, Stephen Richards, Joan E. Strassmann, Richard Sucgang, Kim C. Worley, Pauline Schaap (Lead / Corresponding author)

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Abstract

Major phenotypic innovations in social amoeba evolution occurred at the transition between the Polysphondylia and group 4 Dictyostelia, which comprise the model organism Dictyostelium discoideum, such as the formation of a new structure, the basal disk. Basal disk differentiation and robust stalk formation require the morphogen DIF-1, synthesized by the polyketide synthase StlB, the des-methyl-DIF-1 methyltransferase DmtA, and the chlorinase ChlA, which are conserved throughout Dictyostelia. To understand how the basal disk and other innovations evolved in group 4, we sequenced and annotated the Polysphondylium violaceum (Pvio) genome, performed cell type-specific transcriptomics to identify cell-type marker genes, and developed transformation and gene knock-out procedures for Pvio. We used the novel methods to delete the Pvio stlB gene. The Pvio stlB− mutants formed misshapen curly sorogens with thick and irregular stalks. As fruiting body formation continued, the upper stalks became more regular, but structures contained 40% less spores. The stlB− sorogens overexpressed a stalk gene and underexpressed a (pre)spore gene. Normal fruiting body formation and sporulation were restored in Pvio stlB− by including DIF-1 in the supporting agar. These data indicate that, although conserved, stlB and its product(s) acquired both a novel role in the group 4 Dictyostelia and a role opposite to that in its sister group.
Original languageEnglish
Pages (from-to)674-683
Number of pages10
JournalGenome Biology and Evolution
Volume12
Issue number5
Early online date9 May 2020
DOIs
Publication statusPublished - May 2020

Keywords

  • Polysphondylium violaceum genome
  • cell type-specific transcriptome
  • evolution of novel cell types
  • genetic transformation
  • DIF-1
  • polyketide synthase

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    Narita, T. B., Kawabe, Y., Kin, K., Gibbs, R. A., Kuspa, A., Muzny, D., Richards, S., Strassmann, J. E., Sucgang, R., Worley, K. C., & Schaap, P. (2020). Loss of the Polyketide Synthase StlB Results in Stalk Cell Over production in Polysphondylium violaceum. Genome Biology and Evolution, 12(5), 674-683. https://doi.org/10.1093/gbe/evaa079