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Originally published as Genetics Published Articles Ahead of Print on April 19, 2006.

Genetics, Vol. 173, 515-526, June 2006, Copyright © 2006
doi:10.1534/genetics.106.055863

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Adaptive Divergence in Experimental Populations of Pseudomonas fluorescens. II. Role of the GGDEF Regulator WspR in Evolution and Development of the Wrinkly Spreader Phenotype

Patrick Goymer*, Sophie G. Kahn*, Jacob G. Malone{dagger}, Stefanie M. Gehrig*, Andrew J. Spiers* and Paul B. Rainey*,{ddagger},1

* Department of Plant Sciences, University of Oxford, South Parks Road, Oxford OX1 3RB, United Kingdom, {dagger} Division of Molecular Microbiology, Biozentrum, University of Basel, 4056 Basel, Switzerland and {ddagger} School of Biological Sciences, University of Auckland, Auckland, New Zealand

1 Corresponding author: School of Biological Sciences, University of Auckland, Private Bag 92019, Auckland, New Zealand.
E-mail: p.rainey{at}auckland.ac.nz

Wrinkly spreader (WS) genotypes evolve repeatedly in model Pseudomonas populations undergoing adaptive radiation. Previous work identified genes contributing to the evolutionary success of WS. Here we scrutinize the GGDEF response regulator protein WspR and show that it is both necessary and sufficient for WS. Activation of WspR occurs by phosphorylation and different levels of activation generate phenotypic differences among WS genotypes. Five alleles of wspR, each encoding a protein with a single amino acid substitution, were generated by mutagenesis. Two alleles are constitutively active and cause the ancestral genotype to develop a WS phenotype; the phenotypic effects are allele specific and independent of phosphorylation. Three alleles contain changes in the GGDEF domain and when overexpressed in WS cause reversion to the ancestral phenotype. Ability to mimic this effect by overexpression of a liberated N-terminal domain shows that in WS, regulatory components upstream of WspR are overactive. To connect changes at the nucleotide level with fitness, the effects of variant alleles were examined in both structured and unstructured environments: alleles had adaptive and deleterious effects with trade-offs evident across environments. Despite the proclivity of mutations within wspR to generate WS, sequence analysis of wspR from 53 independently obtained WS showed no evidence of sequence change in this gene.




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