Key Points
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During crop production, fungal plant pathogens cause severe yield losses. Uniform agricultural ecosystems are conducive for the rapid evolution and dissemination of pathogens.
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The genomes of fungal plant pathogens can vary in size and composition, even between closely related species. Differences in the content of transposable elements cause variation in genome architecture.
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Variation in genome architecture results from differences in population genetic factors, including effective population size and the strength of genetic drift.
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During periods of low effective population size, non-adaptive mutations, such as transposable elements, can invade genomes and shape their architecture.
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Transposable elements contribute to the establishment and maintenance of rapidly evolving genome compartments that can comprise virulence genes. High mutation rates in these compartments support the evolution of new virulence phenotypes.
Abstract
The fungal kingdom comprises some of the most devastating plant pathogens. Sequencing the genomes of fungal pathogens has shown a remarkable variability in genome size and architecture. Population genomic data enable us to understand the mechanisms and the history of changes in genome size and adaptive evolution in plant pathogens. Although transposable elements predominantly have negative effects on their host, fungal pathogens provide prominent examples of advantageous associations between rapidly evolving transposable elements and virulence genes that cause variation in virulence phenotypes. By providing homogeneous environments at large regional scales, managed ecosystems, such as modern agriculture, can be conducive for the rapid evolution and dispersal of pathogens. In this Review, we summarize key examples from fungal plant pathogen genomics and discuss evolutionary processes in pathogenic fungi in the context of molecular evolution, population genomics and agriculture.
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Change history
31 August 2017
In Table 1 of this article, the species-specific hosts for both Leptosphaeria species should be crucifers (currently it is written as conifers). The mistakes have been corrected in the PDF and online. The authors apologize to the readers for any confusion caused.
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Acknowledgements
The authors thank B. McDonald, M. Freitag, J. Haueisen and J. Dutheil for helpful discussions and comments in regard to a previous version of this Review. Research carried out in the group of E.H.S. is funded by the Max Planck Society, Germany, and a personal grant from the State of Schleswig-Holstein, Germany, to E.H.S.
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FURTHER INFORMATION
Glossary
- Biotrophs
-
Pathogens that manipulate host defences and obtain their nutrients from living plant cells through specialized 'feeding' structures or hyphae formed intracellularly in the host.
- Necrotrophs
-
Pathogens that kill host cells by secreting toxins and enzymes to obtain nutrients for growth and reproduction.
- Hemibiotrophs
-
Pathogens that undergo a longer latent or biotrophic phase followed by a switch to necrotrophic growth.
- Effectors
-
Pathogen-produced molecules that are secreted during infection to manipulate host defences and facilitate pathogen invasion.
- Apoplastic space
-
Space outside of the plant plasma membrane.
- Symplastic space
-
Space on the inner side of the plant plasma membrane.
- Cultivars
-
Varieties of crop plants of the same species that have distinct phenotypes and genotypes. Distinct cultivars are obtained by plant breeding, whereby desired traits are selected and propagated.
- Transposable elements
-
Genetic elements that move from one location in the genome of their host to another. Transposable elements are also known as transposons.
- Metapopulation dynamics
-
Local fluctuations in the (actual as well as effective) population size of spatially separated populations that belong to the same species.
- Non-synonymous mutations
-
Nucleotide changes in coding sequences that alter the amino acid sequence in the translated proteins.
- Synonymous mutations
-
Nucleotide changes in coding sequences that alter the codons, but not the amino acid sequence, in translated proteins.
- Trench warfare
-
A model that predicts constant diversity in a host–pathogen system, due to the maintenance of multiple alleles at a co-evolving locus by positive diversifying selection or balancing selection.
- 'Arms race' evolution
-
The co-evolution of host and pathogen alleles, which results in the recurrent fixation of advantageous alleles at a co-evolving locus. The fixation of advantageous alleles is mediated by positive directional selection.
- Tajimas D
-
A statistical test parameter that is used in population genetics and DNA sequence analyses. Tajima's test is used to identify sequences that do not fit the neutral theory model, by which the fate of any mutation is determined by genetic drift.
- Divergence patterns
-
The distribution of substitutions varies along the genome, as different parts of the genome evolve by processes and by different rates. The underlying pattern of divergence can be investigated to unravel the history of mutational events and the effect of selection versus neutral processes on the sequence evolution.
- Selective sweep
-
An increase in the frequency of an advantageous allele (and closely linked chromosomal segments) that is caused by positive selection. Sweeps initially decrease genetic variation and subsequently lead to a local excess of rare alleles (homozygosity excess) as new unique mutations accumulate.
- Linkage disequilibrium
-
The non-random association of alleles at different loci.
- Accessory chromosomes
-
Chromosomes that are not present in all isolates of the same pathogenic species. Such chromosomes often encode determinants of host specificity.
- Heterothallic
-
In heterothallic species, two individuals that have opposite mating types are required for sexual reproduction. By contrast, homothallic organisms have both mating types in one thallus.
- Mesosynteny
-
A term that refers to the conservation of gene content on chromosomes, but a variation in the gene order and orientation. This is a phenomenon that is, thus far, particularly described in dothideomycete fungi.
- Effective population size
-
(Ne). The approximate number of breeding individuals that produce offspring that live to reproductive age. This number influences the rate of loss of genetic variation, the efficiency of natural selection, and the accumulation of beneficial and deleterious mutations. It is frequently much smaller than the number of individuals in a population.
- Sexual spores
-
Spores that originate from sexual crossings that differ morphologically from asexual spores.
- Muller's ratchet
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The irreversible accumulation of deleterious mutations in organisms that reproduce asexually.
- Parasexual
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A process whereby genetic material is exchanged between fused hyphae or cells without meiosis. Parasexuality enables the organism to recombine its genome and generate new genotypes in the absence of sexual mating.
- Selection coefficient
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The average proportional reduction in fitness of one genotype relative to another owing to selection (designated by 's').
- Heterokaryons
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Cells that contain two or more genetically distinct nuclei.
- Introgressive hybridization
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The transfer of genes from one species to another through hybridization followed by backcrossing with the parental species.
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Möller, M., Stukenbrock, E. Evolution and genome architecture in fungal plant pathogens. Nat Rev Microbiol 15, 756–771 (2017). https://doi.org/10.1038/nrmicro.2017.76
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DOI: https://doi.org/10.1038/nrmicro.2017.76
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