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Recombination of ecologically and evolutionarily significant loci maintains genetic cohesion in the Pseudomonas syringae species complex.

ABSTRACT: BACKGROUND:Pseudomonas syringae is a highly diverse bacterial species complex capable of causing a wide range of serious diseases on numerous agronomically important crops. We examine the evolutionary relationships of 391 agricultural and environmental strains using whole-genome sequencing and evolutionary genomic analyses. RESULTS:We describe the phylogenetic distribution of all 77,728 orthologous gene families in the pan-genome, reconstruct the core genome phylogeny using the 2410 core genes, hierarchically cluster the accessory genome, identify the diversity and distribution of type III secretion systems and their effectors, predict ecologically and evolutionary relevant loci, and establish the molecular evolutionary processes operating on gene families. Phylogenetic and recombination analyses reveals that the species complex is subdivided into primary and secondary phylogroups, with the former primarily comprised of agricultural isolates, including all of the well-studied P. syringae strains. In contrast, the secondary phylogroups include numerous environmental isolates. These phylogroups also have levels of genetic diversity typically found among distinct species. An analysis of rates of recombination within and between phylogroups revealed a higher rate of recombination within primary phylogroups than between primary and secondary phylogroups. We also find that "ecologically significant" virulence-associated loci and "evolutionarily significant" loci under positive selection are over-represented among loci that undergo inter-phylogroup genetic exchange. CONCLUSIONS:While inter-phylogroup recombination occurs relatively rarely, it is an important force maintaining the genetic cohesion of the species complex, particularly among primary phylogroup strains. This level of genetic cohesion, and the shared plant-associated niche, argues for considering the primary phylogroups as a single biological species.

SUBMITTER: Dillon MM

PROVIDER: S-EPMC6317194 | biostudies-literature | 2019 Jan

REPOSITORIES: biostudies-literature

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Recombination of ecologically and evolutionarily significant loci maintains genetic cohesion in the Pseudomonas syringae species complex.

Dillon Marcus M MM Thakur Shalabh S Almeida Renan N D RND Wang Pauline W PW Weir Bevan S BS Guttman David S DS

Genome biology 20190103 1

<h4>Background</h4>Pseudomonas syringae is a highly diverse bacterial species complex capable of causing a wide range of serious diseases on numerous agronomically important crops. We examine the evolutionary relationships of 391 agricultural and environmental strains using whole-genome sequencing and evolutionary genomic analyses.<h4>Results</h4>We describe the phylogenetic distribution of all 77,728 orthologous gene families in the pan-genome, reconstruct the core genome phylogeny using the 24 ...[more]

PMID: 30606234

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Project description:Pseudomonas viridiflava is a gram-negative pseudomonad that is phylogenetically placed within the Pseudomonas syringae species complex. P. viridiflava has a wide host range and causes a variety of symptoms in different plant parts, including stems, leaves, and blossoms. Outside of its role as a pathogen, P. viridiflava also exists as an endophyte, epiphyte, and saprophyte. Increased reports of P. viridiflava causing disease on new hosts in recent years coincide with increased research on its genetic variability, virulence, phylogenetics, and phenotypes. There is high variation in its core genome, virulence factors, and phenotypic characteristics. The main virulence factors of this pathogen include the enzyme pectate lyase and virulence genes encoded within one or two pathogenicity islands. The delineation of P. viridiflava in the P. syringae complex has been investigated using several molecular approaches. P. viridiflava comprises its own species, within the complex. While seemingly an outsider to the complex as a whole due to differences in the core genome and virulence genes, low average nucleotide identity to other of P. syringae complex members, and some phenotypic traits, it remains as part of the complex. Defining phylogenetic, phenotypic, and genomic characteristics of P. viridiflava in comparison to other P. syringae members is important to understanding this pathogen and for the development of disease resistance and management practices.TaxonomyKingdom Bacteria; Phylum Proteobacteria; Class Gammaproteobacteria; Family Pseudomonadaceae; Genus Pseudomonas; Species Pseudomonas syringae species complex, Genomospecies 6, Phylogroup 7 and 8.Microbiological propertiesGram-negative, fluorescent, aerobic, motile, rod-shaped, oxidase negative, arginine dihydrolase negative, levan production negative (or positive), potato rot positive (or negative), tobacco hypersensitivity positive.GenomeThere are two complete genomes, five chromosome-level genomes, and 1,540 genomes composed of multiple scaffolds of P. viridiflava available in the National Center for Biotechnology Information Genome database. The median total length of these assemblies is 5,975,050 bp, the median number of protein coding genes is 5,208, and the median G + C content is 59.3%.Disease symptomsP. viridiflava causes a variety of disease symptoms, including spots, streaks, necrosis, rots, and more in above- and below-ground plant parts on at least 50 hosts.EpidemiologyThere have been several significant disease outbreaks on field and horticultural crops caused by P. viridiflava since the turn of the century. P. viridiflava has been reported as a pathogen, epiphyte, endophyte, and saprophyte. This species has been isolated from a variety of environmental sources, including asymptomatic wild plants, snow, epilithic biofilms, and icepacks.

Project description:The Pseudomonas syringae complex comprises different genetic groups that include strains from both agricultural and environmental habitats. This complex group has been used for decades as a "hodgepodge," including many taxonomically related species. More than 60 pathovars of P. syringae have been described based on distinct host ranges and disease symptoms they cause. These pathovars cause disease relying on an array of virulence mechanisms. However, P. syringae pv. syringae (Pss) is the most polyphagous bacterium in the P. syringae complex, based on its wide host range, that primarily affects woody and herbaceous host plants. In early 1990s, bacterial apical necrosis (BAN) of mango trees, a critical disease elicited by Pss in Southern Spain was described for the first time. Pss exhibits important epiphytic traits and virulence factors, which may promote its survival and pathogenicity in mango trees and in other plant hosts. Over more than two decades, Pss strains isolated from mango trees have been comprehensively investigated to elucidate the mechanisms that governs their epiphytic and pathogenic lifestyles. In particular, the vast majority of Pss strains isolated from mango trees produce an antimetabolite toxin, called mangotoxin, whose leading role in virulence has been clearly demonstrated. Moreover, phenotypic, genetic and phylogenetic approaches support that Pss strains producers of BAN symptoms on mango trees all belong to a single phylotype within phylogroup 2, are adapted to the mango host, and produce mangotoxin. Remarkably, a genome sequencing project of the Pss model strain UMAF0158 revealed the presence of other factors that may play major roles in its different lifestyles, such as the presence of two different type III secretion systems, two type VI secretion systems and an operon for cellulose biosynthesis. The role of cellulose in increasing mango leaf colonization and biofilm formation, and impairing virulence of Pss, suggests that cellulose may play a pivotal role with regards to the balance of its different lifestyles. In addition, 62-kb plasmids belonging to the pPT23A-family of plasmids (PFPs) have been strongly associated with Pss strains that inhabit mango trees. Further, complete sequence and comparative genomic analyses revealed major roles of PFPs in detoxification of copper compounds and ultraviolet radiation resistance, both improving the epiphytic lifestyle of Pss on mango surfaces. Hence, in this review we summarize the research that has been conducted on Pss by our research group to elucidate the molecular mechanisms that underpin the epiphytic and pathogenic lifestyle on mango trees. Finally, future directions in this particular plant-pathogen story are discussed.

Dataset Information

Recombination of ecologically and evolutionarily significant loci maintains genetic cohesion in the Pseudomonas syringae species complex.

Publications

Recombination of ecologically and evolutionarily significant loci maintains genetic cohesion in the Pseudomonas syringae species complex.

Similar Datasets

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