Review Evolution, genomics and epidemiology of Pseudomonas syringae Challenges in Bacterial Molecular Plant Pathology DAVID A. BALTRUS 1, †, HONOUR C. MCCANN 2 AND DAVID S. GUTTMAN 3,4, † , * 1 School of Plant Sciences, University of Arizona, Tucson, AZ 85721, USA 2 New Zealand Institute for Advanced Study, Massey University, Auckland 0632, New Zealand 3 Department of Cell and Systems Biology, University of Toronto, Toronto, ON M5S 3B2, Canada 4 Centre for the Analysis of Genome Evolution and Function, University of Toronto, Toronto, ON M5S 3B2, Canada SUMMARY A remarkable shift in our understanding of plant-pathogenic bacte- ria is underway. Until recently, nearly all research on phytopatho- genic bacteria was focused on a small number of model strains, which provided a deep, but narrow, perspective on plant–microbe interactions. Advances in genome sequencing technologies have changed this by enabling the incorporation of much greater diver- sity into comparative and functional research. We are now moving beyond a typological understanding of a select collection of strains to a more generalized appreciation of the breadth and scope of plant–microbe interactions. The study of natural populations and evolution has particularly benefited from the expansion of genomic data. We are beginning to have a much deeper understanding of the natural genetic diversity, niche breadth, ecological constraints and defining characteristics of phytopathogenic species. Given this expanding genomic and ecological knowledge, we believe the time is ripe to evaluate what we know about the evolutionary dynamics of plant pathogens. Keywords: evolution, mutation, natural selection, Pseudomonas syringae, population structure, recombination, species definition. INTRODUCTION Pseudomonas syringae is one of the pre-eminent models for the exploration of plant–microbe interactions in both natural and labo- ratory systems. The species has played a central role in seminal studies and publications, including the development of the guard hypothesis (Dangl and Jones, 2001) and the zig–zag model (Jones and Dangl, 2006) of plant immunity. There is also a growing body of literature exploring its tremendous natural diversity (Baltrus et al., 2011; Berge et al., 2014; O’Brien et al., 2011b; Thakur et al., 2016). This foundation of molecular, genomic and ecological knowl- edge, coupled with near environmental ubiquity, have turned P. syringae into a powerful emerging model system for the study of microbial evolution in nature (Hirano and Upper, 2000; Morris et al., 2013; O’Brien et al., 2011b). Consequently, this review focuses exclusively on fundamental questions as they apply to P. syringae. Our goal is to discuss how the principles of population genet- ics guide our understanding of the evolutionary processes that have shaped the natural diversity and host interactions of P. syrin- gae. We specifically examine questions related to the cohesion of the P. syringae species complex, whether it should even be con- sidered as a species, and why this is important. We then address the nature of bacterial populations, and how fundamental evolu- tionary forces impact P. syringae natural diversity, as well as the community of microbes with which it interacts. IS P. SYRINGAE A SPECIES? Much time and effort have been spent on debating whether bacte- rial lineages can be circumscribed into natural species, and how these bounds can and should be defined. Although these argu- ments may seem fairly esoteric, they have both practical conse- quences for pathologists working on field isolates and fundamental implications for how we understand and interpret the ecological and evolutionary pressures that give rise to natural genetic diver- sity. With an increased appreciation of the extensive degree of genetic exchange among bacterial lineages, it is possible that no single, clear-cut answer will ever emerge. However, we believe that it is worthwhile to examine the classification of P. syringae from both philosophical and biological standpoints with the hope that a broad analysis can provide structure for future discussions. Species concepts and species delimitation There has been considerable debate over the composition of the species P. syringae and whether the P. syringae complex is a cohe- sive unit or should be split into distinct species (Bull et al ., 2010; Janse et al., 1996). The road describing the taxonomy and *Correspondence: Email: david.guttman@utoronto.ca †These authors contributed equally to this work. 152 V C 2016 BSPP AND JOHN WILEY & SONS LTD MOLECULAR PLANT PATHOLOGY (2017) 18 (1), 152–168 DOI: 10.1111/mpp.12506