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

Author:

Narita Takaaki B12,Kawabe Yoshinori1,Kin Koryu1,Gibbs Richard A3,Kuspa Adam345,Muzny Donna M3,Richards Stephen36,Strassmann Joan E7,Sucgang Richard34,Worley Kim C3,Schaap Pauline1

Affiliation:

1. School of Life Sciences, University of Dundee, United Kingdom

2. Department of Life Science, Faculty of Advanced Engineering, Chiba Institute of Technology, Chiba, Japan

3. Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, Texas

4. Verna and Marrs McLean Department of Biochemistry and Molecular Biology, Baylor College of Medicine, Houston, Texas

5. The Welch Foundation, Houston, TX

6. Genome Sequencing Center, University of California Davis, Davis, CA

7. Department of Biology, Washington University

Abstract

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.

Funder

National Science Foundation

National Institutes of Health

Japanese Society for the Promotion of Science

European Molecular Biology Organisation

Wellcome Trust

European Research Council

Publisher

Oxford University Press (OUP)

Subject

Genetics,Ecology, Evolution, Behavior and Systematics

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