Genetics. Published Articles Ahead of Print: April 19, 2006, Copyright © 2006
doi:10.1534/genetics.106.055863


A more recent version of this article appeared on June 1, 2006.

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Adaptive divergence in experimental populations of Pseudomonas fluorescens. II. The role of the GGDEF regulator WspR in evolution and development of the wrinkly spreader phenotype

Patrick Goymer 1, Sophie Kahn , Jacob Malone 2, Stefanie Gehrig 3, Andrew Spiers 4 and Paul Rainey 5*

1 Nature Genetics
2 Biocentrum Basel
3 Oxford University Press
4 University of Oxford
5 University of Auckland

* To whom correspondence should be addressed. E-mail: p.rainey{at}auckland.ac.nz.

Submitted on January 14, 2006
Revised on February 15, 2006
Accepted on 20 March 2006


Abstract

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 over-expressed in WS cause reversion to the ancestral phenotype. Ability to mimic this effect by over-expression of a liberated N-terminal domain shows that in WS, regulatory components upstream of WspR are over-active. 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 more than 50 independently obtained WS showed no evidence of sequence change in this gene.

Key Words: GGDEF, di-guanylate cyclase, response regulator,, signal transduction




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