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Allopatric Plant Pathogen Population Divergence following Disease Emergence.

ABSTRACT: Within the landscape of globally distributed pathogens, populations differentiate via both adaptive and nonadaptive forces. Individual populations are likely to show unique trends of genetic diversity, host-pathogen interaction, and ecological adaptation. In plant pathogens, allopatric divergence may occur particularly rapidly within simplified agricultural monoculture landscapes. As such, the study of plant pathogen populations in monocultures can highlight the distinct evolutionary mechanisms that lead to local genetic differentiation. Xylella fastidiosa is a plant pathogen known to infect and damage multiple monocultures worldwide. One subspecies, Xylella fastidiosa subsp. fastidiosa, was first introduced to the United States ∼150 years ago, where it was found to infect and cause disease in grapevines (Pierce's disease of grapevines, or PD). Here, we studied PD-causing subsp. fastidiosa populations, with an emphasis on those found in the United States. Our study shows that following their establishment in the United States, PD-causing strains likely split into populations on the East and West Coasts. This diversification has occurred via both changes in gene content (gene gain/loss events) and variations in nucleotide sequence (mutation and recombination). In addition, we reinforce the notion that PD-causing populations within the United States acted as the source for subsequent subsp. fastidiosa outbreaks in Europe and Asia.IMPORTANCE Compared to natural environments, the reduced diversity of monoculture agricultural landscapes can lead bacterial plant pathogens to quickly adapt to local biological and ecological conditions. Because of this, accidental introductions of microbial pathogens into naive regions represents a significant economic and environmental threat. Xylella fastidiosa is a plant pathogen with an expanding host and geographic range due to multiple intra- and intercontinental introductions. X. fastidiosa subsp. fastidiosa infects and causes disease in grapevines (Pierce's disease of grapevines [PD]). This study focused on PD-causing X. fastidiosa populations, particularly those found in the United States but also invasions into Taiwan and Spain. The analysis shows that PD-causing X. fastidiosa has diversified via multiple cooccurring evolutionary forces acting at an intra- and interpopulation level. This analysis enables a better understanding of the mechanisms leading to the local adaptation of X. fastidiosa and how a plant pathogen diverges allopatrically after multiple and sequential introduction events.

SUBMITTER: Castillo AI

PROVIDER: S-EPMC8091610 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundElucidating the effects of geography and selection on genetic variation is critical for understanding the relative importance of adaptation in driving differentiation and identifying the environmental factors underlying its occurrence. Adaptive genetic variation is common in tree species, especially widely distributed long-lived species. Pseudotaxus chienii can occupy diverse habitats with environmental heterogeneity and thus provides an ideal material for investigating the process of population adaptive evolution. Here, we characterize genetic and expression variation patterns and investigate adaptive genetic variation in P. chienii populations.ResultsWe generated population transcriptome data and identified 13,545 single nucleotide polymorphisms (SNPs) in 5037 unigenes across 108 individuals from 10 populations. We observed lower nucleotide diversity (π = 0.000701) among the 10 populations than observed in other gymnosperms. Significant negative correlations between expression diversity and nucleotide diversity in eight populations suggest that when the species adapts to the surrounding environment, gene expression and nucleotide diversity have a reciprocal relationship. Genetic structure analyses indicated that each distribution region contains a distinct genetic group, with high genetic differentiation among them due to geographical isolation and local adaptation. We used FST outlier, redundancy analysis, and latent factor mixed model methods to detect molecular signatures of local adaptation. We identified 244 associations between 164 outlier SNPs and 17 environmental variables. The mean temperature of the coldest quarter, soil Fe and Cu contents, precipitation of the driest month, and altitude were identified as the most important determinants of adaptive genetic variation. Most candidate unigenes with outlier signatures were related to abiotic and biotic stress responses, and the monoterpenoid biosynthesis and ubiquitin-mediated proteolysis KEGG pathways were significantly enriched in certain populations and deserve further attention in other long-lived trees.ConclusionsDespite the strong population structure in P. chienii, genomic data revealed signatures of divergent selection associated with environmental variables. Our research provides SNPs, candidate unigenes, and biological pathways related to environmental variables to facilitate elucidation of the genetic variation in P. chienii in relation to environmental adaptation. Our study provides a promising tool for population genomic analyses and insights into the molecular basis of local adaptation.

Project description:Pathogen introductions have led to numerous disease outbreaks in naive regions of the globe. The plant pathogen Xylella fastidiosa has been associated with various recent epidemics in Europe affecting agricultural crops, such as almond, grapevine, and olive, but also endemic species occurring in natural forest landscapes and ornamental plants. We compared whole-genome sequences of X. fastidiosa subspecies multiplex from America and strains associated with recent outbreaks in southern Europe to infer their likely origins and paths of introduction within and between the two continents. Phylogenetic analyses indicated multiple introductions of X. fastidiosa subspecies multiplex into Italy, Spain, and France, most of which emerged from a clade with limited genetic diversity with a likely origin in California, USA. The limited genetic diversity observed in X. fastidiosa subspecies multiplex strains originating from California is likely due to the clade itself being an introduction from X. fastidiosa subspecies multiplex populations in the southeastern United States, where this subspecies is most likely endemic. Despite the genetic diversity found in some areas in Europe, there was no clear evidence of recombination occurring among introduced X. fastidiosa strains in Europe. Sequence type taxonomy, based on multilocus sequence typing (MLST), was shown, at least in one case, to not lead to monophyletic clades of this pathogen; whole-genome sequence data were more informative in resolving the history of introductions than MLST data. Although additional data are necessary to carefully tease out the paths of these recent dispersal events, our results indicate that whole-genome sequence data should be considered when developing management strategies for X. fastidiosa outbreaks.IMPORTANCEXylella fastidiosa is an economically important plant-pathogenic bacterium that has emerged as a pathogen of global importance associated with a devastating epidemic in olive trees in Italy associated with X. fastidiosa subspecies pauca and other outbreaks in Europe, such as X. fastidiosa subspecies fastidiosa and X. fastidiosa subspecies multiplex in Spain and X. fastidiosa subspecies multiplex in France. We present evidence of multiple introductions of X. fastidiosa subspecies multiplex, likely from the United States, into Spain, Italy, and France. These introductions illustrate the risks associated with the commercial trade of plant material at global scales and the need to develop effective policy to limit the likelihood of pathogen pollution into naive regions. Our study demonstrates the need to utilize whole-genome sequence data to study X. fastidiosa introductions at outbreak stages, since a limited number of genetic markers does not provide sufficient phylogenetic resolution to determine dispersal paths or relationships among strains that are of biological and quarantine relevance.

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Allopatric Plant Pathogen Population Divergence following Disease Emergence.

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