Genome evolution in filamentous plant pathogens: why bigger can be better

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.

A fungal avirulence factor encoded in a highly plastic genomic region triggers partial resistance to septoria tritici blotch

“…The mechanisms underlying effector diversification remain largely unexplored. Many pathogen genomes are compartmentalised into highly conserved or rapidly evolving regions, often described as the ‘two‐speed genome’ (Raffaele & Kamoun, 2012). Effector genes are frequently localised in the highly variable compartments, which are often rich in transposable elements (Ma et al ., 2010; Soyer et al ., 2014; Plissonneau et al ., 2018).…”

“…Effector genes are frequently localised in the highly variable compartments, which are often rich in transposable elements (Ma et al ., 2010; Soyer et al ., 2014; Plissonneau et al ., 2018). Transposable elements are thought to contribute to genome evolution and the diversification of effector genes (Raffaele & Kamoun, 2012). They translocate within a genome, causing gene disruption, duplication or deletion of genomic sequences.…”

Evidence for intragenic recombination and selective sweep in an effector gene of Phytophthora infestans

“…Effector genes commonly lie in gene‐sparse, transposon‐rich regions of the pathogen genome (Haas et al., 2009; Raffaele & Kamoun, 2012). This physical location provides effector genes a unique opportunity to generate sequence duplication.…”

“…Functional redundancy encoded by multiple copies of effector genes relaxes selective pressure on one or more of the gene copies, which in turn allows more frequent and abrupt mutations to occur without severe impact on the fitness of the pathogen. Indeed, multiple mutation mechanisms including base substitution, deletion, pseudogenization, and transcriptional silencing have been documented in effector genes (Cooke et al., 2012; Raffaele & Kamoun, 2012). Interaction of these mutation events results in higher genetic variation in effector genes than in the rest of pathogen genome (Karasov, Horton, & Bergelson, 2014; Raffaele & Kamoun, 2012) and enhances response to selection driven by the change in host defense systems.…”

“…The pathogen genome contains at least 550 effectors all earmarked with a conserved N‐terminal motif of Arginine–X–Leucine–Arginine (RXLR), where X can be one of any 20 amino acids (Haas et al., 2009). However, this RXLR effector repertoire is likely expanding, contributing to the enormous size of the P. infestans genome (Haas et al., 2009; Raffaele & Kamoun, 2012). Biochemical and virulent functions of some RXLR effectors in P. infestans have been characterized recently (Bozkurt et al., 2011; King et al., 2014; McLellan et al., 2013; Wang et al., 2015; Yang, McLellan, et al., 2016).…”