Abstract

The interaction of pathogens with their hosts creates strong reciprocal selection pressures. Pathogens often deploy an arsenal of small proteins called effectors that manipulate the plant immune system and promote disease. In the post-genomics era, a major interest has been to understand what shapes the localization of effector genes in pathogen genomes. The two-speed genome model originated with the discovery of repeat-rich and gene-sparse genome compartments with an over-representation of effector-like genes in a subset of plant pathogens. These highly polymorphic genome compartments are thought to create unique niches for effector genes and facilitate rapid adaptation. Research over the past decade has revealed a number of twists to the two-speed genome model and raised questions about the universality among plant pathogens. Here, we critically review the foundations of the two-speed model by presenting recent work on epigenetics, transposable element dynamics, and population genetics. Numerous examples have demonstrated that the location of effector genes in rapidly evolving compartments has created key adaptations. However, recent evidence suggests that the two-speed genome is unlikely to have evolved to specifically benefit the plant pathogen lifestyle. We propose that fundamental drivers of eukaryotic genome evolution have shaped both pathogen and non-pathogen genomes alike. An evolutionary genomics perspective on the two-speed genome model will open up fruitful new research avenues.

Highlights

  • Eukaryotic microorganisms are crucial components of worldwide ecosystems

  • In the fungal pathogens Fusarium oxysporum, Leptosphaeria maculans, and Zymoseptoria tritici, accessory chromosomes or accessory compartments are generally characterized by low gene density, low gene expression, facultative heterochromatin, and enrichment of species-specific genes (Feurtey et al, 2019; Fokkens et al, 2018; Plissonneau et al, 2018; Soyer et al, 2014)

  • Plant pathogenic fungi provide some of the most fascinating examples of how genome evolution is linked to phenotypic trait evolution

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Summary

Introduction

Eukaryotic microorganisms are crucial components of worldwide ecosystems. Many eukaryotic microorganisms engage in symbiotic relationships that can range from mutualistic to pathogenic. Recent genomic analyses of diverse plant pathogens have revealed that effectors do not always cluster, that effectors and TEs do not necessarily co-localize (Frantzeskakis et al, 2018; Schwessinger et al, 2018, 2020; Stam et al, 2018; Wyka et al, 2020), and that more than two discrete types of genomic regions can occur (Fokkens et al, 2018). Irrespective in which species genome compartmentalization has been observed, this phenomenon has nearly always been linked to the occurrence of repetitive genomic elements

Do transposable element insertion dynamics create compartmentalized genomes?
Dynamic chromatin for dynamic compartments
Conclusions
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