Key Points
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Evolution of symbiosis and parasitism is typically associated with genome reduction. Surprisingly, the recent sequencing of the genomes of several filamentous plant pathogens revealed multiple examples of large genomes shaped by repeat-driven expansions.
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The expanded genomes of filamentous plant pathogens show a clear heterogeneity in repeat and gene content. Repeat-rich regions frequently contain genes encoding proteins involved in host–pathogen interactions.
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Repeat-rich regions vary in size and distribution in filamentous plant pathogen genomes from different lineages. A range of mechanisms contribute to the high polymorphism, including mutations, recombination, transposon activity, epigenetic processes and horizontal gene and chromosome transfer.
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The plasticity of the repeat-rich regions affects the emergence of virulence, notably by gene inactivation, altered gene sequence or structure, and the birth of new genes.
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In the co-evolutionary conflict between filamentous pathogens and their hosts, large, flexible genomes are likely to provide a macroevolutionary advantage by reducing the risk of pathogen extinction when resistance emerges in the host or when the host population disappears.
Abstract
Many species of fungi and oomycetes are plant pathogens of great economic importance. Over the past 7 years, the genomes of more than 30 of these filamentous plant pathogens have been sequenced, revealing remarkable diversity in genome size and architecture. Whereas the genomes of many parasites and bacterial symbionts have been reduced over time, the genomes of several lineages of filamentous plant pathogens have been shaped by repeat-driven expansions. In these lineages, the genes encoding proteins involved in host interactions are frequently polymorphic and reside within repeat-rich regions of the genome. Here, we review the properties of these adaptable genome regions and the mechanisms underlying their plasticity, and we illustrate cases in which genome plasticity has contributed to the emergence of new virulence traits. We also discuss how genome expansions may have had an impact on the co-evolutionary conflict between these filamentous plant pathogens and their hosts.
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Acknowledgements
This work was funded by the Gatsby Charitable Foundation and a Marie Curie Intra-European Fellowship (contract 255104) to S.R. We thank our colleagues and members of the Kamoun laboratory for discussions, and E. Kemen for comments on drafts of the manuscript.
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Glossary
- Effector
-
A pathogenic molecule that alters host cell structure and function, thereby facilitating infection and/or triggering defence responses.
- Clade
-
A group of organisms that has evolved from a common ancestor.
- Biotrophic
-
A pathogen that requires living host cells to complete its life cycle.
- Necrotrophic
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A pathogen that kills host cells and colonizes the dead tissue.
- Host-selective toxins
-
Molecules produced by necrotrophic plant pathogens that trigger cell death in particular plant genotypes.
- Isochore
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A genome block of homogeneous GC content that differs from the remainder of the genome.
- Heterochromatin
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A tightly packed form of DNA that affects gene expression and can be modulated by epigenetic imprinting.
- Conditionally dispensable chromosomes
-
(CDCs). Accessory chromosomes that are not required for basic growth but can confer advantages under certain conditions.
- Single-nucleotide polymorphisms
-
(SNPs). DNA sequence polymorphisms involving the replacement of one nucleotide by another.
- Mesosynteny
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Conservation of gene content but not gene order or orientation.
- Pseudogenization
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A process through which genes lose their ability to code for proteins, either by mutation or by loss of expression.
- Copy number variation
-
(CNV). A form of genetic polymorphism in which the number of copies of a gene is modified within a genome.
- Clade selection
-
A macroevolutionary concept that proposes that a clade carrying a certain set of genes can survive over a longer time relative to another clade. Also known as species selection.
- Macroevolutionary
-
The evolution of a group of organisms (clade) over long periods of time.
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Raffaele, S., Kamoun, S. Genome evolution in filamentous plant pathogens: why bigger can be better. Nat Rev Microbiol 10, 417–430 (2012). https://doi.org/10.1038/nrmicro2790
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DOI: https://doi.org/10.1038/nrmicro2790
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