Duplication and neofunctionalization of a horizontally-transferred xyloglucanase as a facet of the red queen co-evolutionary dynamic.

Oomycetes are heterotrophic protists that share phenotypic similarities with fungi, including the ability to cause plant diseases, but branch in a separate and distant region of the eukaryotic tree of life. It has been suggested that multiple horizontal gene transfers (HGTs) from fungi-to-oomycetes contributed to the evolution of plant-pathogenic traits. These HGTs are predicted to include secreted proteins that degrade plant cell walls. This is a key trait in the pathology of many oomycetes, as the plant cell wall represents a primary barrier to pathogen invasion and a rich source of carbohydrates. Many of the HGT gene families identified have undergone multiple rounds of duplication. Using a combination of phylogenomic analysis and functional assays, we investigate the diversification of a horizontally-transferred xyloglucanase gene family in the model oomycete species Significance Statement: The oomycetes are a diverse group of eukaryotic microbes that include some of the most devastating pathogens of plants. Oomycetes perceive, invade, and colonize plants in similar ways to fungi, in part because they acquired the genes to attack and feed on plants from fungi. These genes are predicted to be useful to oomycete plant pathogens because they have undergone multiple rounds of gene duplication. One key enzyme for attacking plant cell wall structures is called xyloglucanase. Xyloglucanase in the oomycetes has undergone multiple rounds of gene duplication, leading to variants including an enzyme with a C-terminal extension that increases activity. Some xyloglucanase variants trigger unique patterns of reactive oxygen species (ROS)