Host–microbe interactions: the response of fungal and oomycete pathogens to the host environment

Abstract

The interactions of fungi and oomycetes with plant and animal hosts involve specific adaptations that allow the pathogens to adhere to and penetrate tissue, to remodel metabolic capabilities to utilize host nutrients, and to deal with stresses generated by host defense mechanisms. These fascinating adjustments require major reprogramming events as the pathogens move from the environment (with its own challenges) to host tissue. This year’s collection of six reviews on the interactions between fungi or oomycetes and their hosts reflect several emerging themes in our developing view of pathogen response to the host environment. These themes include the demonstrated utility of genomic resources for the discovery and characterization of pathogen traits with key roles in adaptation to the host environment. The benefits of the long-awaited appearance of these genomic resources for fungal and oomycete pathogens are clearly apparent from the seamless inclusion of genomic approaches in each of the reviews. In particular, transcriptome analyses show great promise for defining the broad features of pathogen gene expression during infection. A second theme expands on the longstanding appreciation of the importance of secreted proteins for fungal pathogens of both animals and plants. Striking observations in recent years elevate secretion to a new level of sophistication with the identification of proteins from plant pathogens that are translocated into host cells. This work raises the possibility that these pathogens not only modify the extracellular host environment, but also manipulate the intracellular compartment in ways that may contribute to virulence or suppress host defense. These observations may ultimately reach the level of detail available for the effector proteins that are delivered into host cells by bacterial pathogens of plants and animals. Additional themes concern the importance of metabolic remodeling in the host environment for nutrient acquisition and utilization, and the interconnections between metabolism, morphogenesis, and the response to stress. Mechanistic details are appearing from genetic and genomic approaches, and provide notice for what promises to be an explosion in the application of similar approaches in a wide range of fungal and oomycete species. As described in the first review, Candida albicans has emerged as perhaps the best characterized fungal pathogen of humans in terms of the analysis of gene expression during infection. Earlier detailed studies characterized specific factors that play roles during infection including secreted hydrolases and adhesins that are expressed in a niche-specific fashion in the host. In addition, much effort has gone into characterizing the relevance of the yeast-hyphal transition and associated changes in gene expression as a component of the infection process. Brown, Odds and Gow present an overview of approaches to evaluate the expression of C. albicans genes during infection and describe the body of evidence that leads to the question of whether environmental adaptation is the main key to pathogenicity. The expression of specific sets of virulence factors during infection has been studied in detail including the analysis of