Molecular Plant Pathology (2019) 20, 3-7
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The need for speed: compartmentalized genome evolution in filamentous phytopathogens
Molecular Plant Pathology 20 (1), 3-7
Abstract: More than 10 years of extensive efforts since the dawn of high-throughput sequencing have resulted in a wealth of genome data for filamentous plant pathogens and have led to several key concepts in the research areas of genomics and plant-microbe interactions. Most recently, utilization of portable high-throughput sequencing devices for long-read sequencing has opened the door to new opportunities in pathogen population genomics and even for on-field pathogenomic investigations. We are, however, at a critical point where current genome evolution models are difficult to be reconciled with the plethora of different genome architectures and their supplementary characteristics. Initial pathogenomic analyses provided key insights on how the rapid evolution of some pathogens could be supported by plastic genomes (N.B.: In the context of this article, 'rapid' or 'fast' evolution is meant to indicate collectively all types of mutational events, i.e. nucleotide substitutions, insertions/deletions, rearrangements and copy number variation, that occur at a higher rate than 'normal', i.e. for example in housekeeping genes). Such plastic genomes are typically characterized by only moderately preserved synteny (gene collinearity) and frequent chromosomal and gene polymorphisms between isolates of the same species. One of the most widespread models in this respect is the 'two-speed' hypothesis, according to which large-scale genome compartmentalization is thought to accelerate, or at least be critical, for the evolution of genomic loci that include virulence-related genes (Dong et al., 2015). The two-speed concept is based on the idea that genomes of filamentous plant pathogens are compartmentalized and exhibit a mosaic genome architecture, comprising gene-dense/repeat-poor regions harboring essential and widely conserved housekeeping genes and gene-sparse/repeat-rich regions containing fast-evolving virulence-associated genes (e.g. effector genes) (Dong et al., 2015). Additional characteristics of two-speed genomes can be AT-rich isochores and accessory chromosomes, which altogether sustain genomic compartmentalization and are believed to allow for the rapid evolution of these genomes. Thus, the original two-speed hypothesis embraces two different aspects—(1) the presence of physical genomic compartmentalization and (2) the more rapid evolution of genes residing in one of these compartments. While the latter feature is clearly related to speed (i.e. the rate of mutational events per time unit), the former facet is a description of large-scale genomic organization and thus essentially unrelated to speed. In this sense, the phrase two-speed genome might be considered a misleading term, since the genome of every pathogen is assumed to have slowly evolving housekeeping and more rapidly evolving virulence-associated genes, i.e. having two speeds, regardless of its large-scale genomic organization. Since nevertheless this expression has been firmly established in scientific literature, we use it in the context of this article, but also propose an in our view more appropriate alternative (see below).
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Database assignments for author(s): Ralph Panstruga
Research topic(s) for pests/diseases/weeds:
molecular biology - genes
general biology - morphology - evolution
Pest and/or beneficial records: