A horizontally acquired expansin gene increases virulence of the emerging plant pathogen Erwinia tracheiphila

Abstract

AbstractAll land plants depend on proteins called ‘expansins’ that non-enzymatically loosen structural cellulose, enabling cell wall extension during normal growth. Surprisingly, expansin genes are also present – but functionally uncharacterized – in taxonomically diverse bacteria and fungi that do not produce cellulosic cell walls. Here, we find that Erwinia tracheiphila (Enterobacteriaceae), the causative agent of bacterial wilt of cucurbits, has horizontally acquired an operon with a microbial expansin (exlx) gene and a glycoside hydrolase family 5 (gh5) gene. E. tracheiphila is an unusually virulent plant pathogen that induces systemic wilt symptoms followed by plant death, and has only recently emerged into cultivated cucurbit populations in temperate Eastern North America. Plant inoculation experiments with deletion mutants show that EXLX-GH5 is a secreted virulence factor that confers efficient xylem movement and colonization ability to E. tracheiphila. Bacterial colonization of xylem blocks sap flow, inducing wilt symptoms and causing plant death. Together, these results suggest that the horizontal acquisition of the exlx-gh5 locus was likely a key step driving the recent emergence of E. tracheiphila. The increase in E. tracheiphila virulence conferred by microbial expansins, the presence of this gene in many other bacterial and fungal wilt-inducing plant pathogen species, and the amenability of microbial expansins to horizontal gene transfer suggest this gene may be an under-appreciated virulence factor in taxonomically diverse agricultural pathogens.ImportanceErwinia tracheiphila is a bacterial plant pathogen that causes a fatal wilt infection in cucurbit crop plants. Here, we report that E. tracheiphila has horizontally acquired a microbial expansin gene (exlx) adjacent to a glycoside hydrolase family 5 (gh5) gene. Expansins are predominantly associated with plants due to their essential role in loosening structural cell wall cellulose during normal growth. We find that the EXLX and GH5 proteins in E. tracheiphila function as a single complex to facilitate xylem colonization, possibly by manipulating the size of xylem structures that normally exclude the passage of bacteria. This suggests that horizontal acquisition of the exlx-gh5 locus was likely a key step in the recent emergence of E. tracheiphila as an unusually virulent plant pathogen. The presence of microbial expansin genes in diverse species of bacterial and fungal wilt-inducing pathogens suggests it may be an under-appreciated virulence factor for other microbes.