The Plant Pathogen Pseudomonas syringae pv. tomato Is Genetically Monomorphic and under Strong Selection to Evade Tomato Immunity

• DOI: 10.1371/journal.ppat.1002130
• Publication Date: 2011-08-25T20:55:02Z
• Authors: Rongman Cai; James Lewis; Shuangchun Yan; Haijie Liu; Christopher R. Cl...; Francesco Campanile; Nalvo F. Almeida; David J. Studholme; Magdalen Lindeberg; David Schneider; Massimo Zaccardelli; Joao C. Setubal; Nadia P. Morales-...; Adriana Bernal; Gitta Coaker; Christy Baker; Carol L. Bender; Scotland Leman; Boris A. Vinatzer
• Keywords: Genetic Markers; 0301 basic medicine; 572; QH301-705.5; Virulence Factors; Pseudomonas syringae; Polymorphism, Single Nucleotide; 03 medical and health sciences; Solanum lycopersicum; Gene Expression Regulation, Plant; Plant Immunity; Lycopersicon esculentum; Polymorphism; Biology (General); Alleles; DNA Primers; Plant Diseases; 580; Plant; Single Nucleotide; DNA; Sequence Analysis, DNA; RC581-607; 3. Good health; Europe; Plant Leaves; Phylogeography; Gene Expression Regulation; Genetic Loci; Host-Pathogen Interactions; Mutation; North America; Immunologic diseases. Allergy; Sequence Analysis; Research Article; Flagellin

Recently, genome sequencing of many isolates of genetically monomorphic bacterial human pathogens has given new insights into pathogen microevolution and phylogeography. Here, we report a genome-based micro-evolutionary study of a bacterial plant pathogen, Pseudomonas syringae pv. tomato. Only 267 mutations were identified between five sequenced isolates in 3,543,009 nt of analyzed genome sequence, which suggests a recent evolutionary origin of this pathogen. Further analysis with genome-derived markers of 89 world-wide isolates showed that several genotypes exist in North America and in Europe indicating frequent pathogen movement between these world regions. Genome-derived markers and molecular analyses of key pathogen loci important for virulence and motility both suggest ongoing adaptation to the tomato host. A mutational hotspot was found in the type III-secreted effector gene hopM1. These mutations abolish the cell death triggering activity of the full-length protein indicating strong selection for loss of function of this effector, which was previously considered a virulence factor. Two non-synonymous mutations in the flagellin-encoding gene fliC allowed identifying a new microbe associated molecular pattern (MAMP) in a region distinct from the known MAMP flg22. Interestingly, the ancestral allele of this MAMP induces a stronger tomato immune response than the derived alleles. The ancestral allele has largely disappeared from today's Pto populations suggesting that flagellin-triggered immunity limits pathogen fitness even in highly virulent pathogens. An additional non-synonymous mutation was identified in flg22 in South American isolates. Therefore, MAMPs are more variable than expected differing even between otherwise almost identical isolates of the same pathogen strain.