The need for speed: compartmentalized genome evolution in filamentous phytopathogens

Frantzeskakis, Lamprinos; Kusch, Stefan; Panstruga, Ralph

doi:10.1111/mpp.12738

Cited by 89 publications

(117 citation statements)

References 18 publications

Supporting

Mentioning

106

Contrasting

Order By: Relevance

“…The reason for this separation of effectors and housekeeping genes is probably that regulatory changes necessary to optimise the expression of the effectors are easier to achieve if there are no housekeeping genes nearby, as co‐regulation effects that could bring the cell metabolism out of balance are less likely to occur. This means that effectors often localise to ‘compartments’ in the genome distinct from conserved genes (Frantzeskakis et al ., ). In Phytophthora and powdery mildew, this is realised by the location of effectors in gene‐sparse regions (Raffaele et al ., ; Spanu et al ., ; Raffaele & Kamoun, ; Hacquard et al ., ); in for example Colletotrichum , Fusarium and Leptosphaeria , this is enabled by physiologically dispensible chromosomes (Balesdent et al ., ; Vlaardingerbroek et al ., ; Plaumann et al ., ), and in Neofusicoccum and Ustilago this is made possible by clustering of virulence factors (Lanver et al ., ; Massonnet et al ., ).…”

Section: Pathogens Maintain Effector Reservoirs That Are Crucial For mentioning

confidence: 99%

An evolutionary framework for host shifts – jumping ships for survival

Thines

2019

New Phytologist

126

View full text Add to dashboard Cite

Summary Host jumping is a process by which pathogens settle in new host groups. It is a cornerstone in the evolution of pathogens, as it leads to pathogen diversification. It is unsurprising that host jumping is observed in facultative pathogens, as they can reproduce even if they kill their hosts. However, host jumps were thought to be rare in obligate biotrophic pathogens, but molecular phylogenetics has revealed that the opposite is true. Here, I review some concepts and recent findings and present several hypotheses on the matter. In short, pathogens evolve and diversify via host jumps, followed by radiation, specialisation and speciation. Host jumps are facilitated by, for example, effector innovations, stress, compatible pathogens and physiological similarities. Host jumping, subsequent establishment, and speciation takes place rapidly – within centuries and millennia rather than over millions of years. If pathogens are unable to evolve into neutral or mutualistic interactions with their hosts, they will eventually be removed from the host population, despite balancing trade‐offs. Thus, generally, plant pathogens only survive in the course of evolution if they jump hosts. This is also reflected by the diversity patterns observed in many genera of plant pathogens, where it leads to a mosaic pattern of host groups over time, in which the original host group becomes increasingly obscure.

show abstract

Section: Pathogens Maintain Effector Reservoirs That Are Crucial For mentioning

confidence: 99%

An evolutionary framework for host shifts – jumping ships for survival

Thines

2019

New Phytologist

126

View full text Add to dashboard Cite

show abstract

“…However, in some cases meiotic gene drives have been observed increasing their potential to be inherited and potentially explaining their abundance in pathogen populations [22]. Supernumerary chromosomes are usually gene poor and repeat rich compared to the corechromosomes, and form one illustration of the two-speed genome concept [12,23]. However, a clear association with adaptive evolution is not always evident as they do not necessarily carry virulence-related genes [9,24].…”

Section: Introductionmentioning

confidence: 99%

Genomic rearrangements generate hypervariable mini-chromosomes in host-specific lineages of the blast fungus

Langner

Harant

Gómez-Luciano

et al. 2020

Preprint

View full text Add to dashboard Cite

Supernumerary mini-chromosomes-a unique type of genomic structural variation-have been implicated in the emergence of virulence traits in plant pathogenic fungi. However, the mechanisms that facilitate the emergence and maintenance of mini-chromosomes across fungi remain poorly understood. In the blast fungus Magnaporthe oryzae, mini-chromosomes have been first described in the early 1990s but, until very recently, have been overlooked in genomic studies. Here we investigated structural variation in four isolates of the blast fungus M. oryzae from different grass hosts and analyzed the sequences of mini-chromosomes in the rice, foxtail millet and goosegrass isolates. The mini-chromosomes of these isolates turned out to be highly diverse with distinct sequence composition. They are enriched in repetitive elements and have lower gene density than core-chromosomes. We identified several virulence-related genes in the mini-chromosome of the rice isolate, including the polyketide synthase Ace1 and the effector gene AVR-Pik. Macrosynteny analyses around these loci revealed structural rearrangements, including inter-chromosomal translocations between core-and mini-chromosomes. Our findings provide evidence that mini-chromosomes independently emerge from structural rearrangements of core-chromosomes and might contribute to adaptive evolution of the blast fungus. Author summaryThe genomes of plant pathogens often exhibit an architecture that facilitates high rates of dynamic rearrangements and genetic diversification in virulence associated regions. These regions, which tend to be gene sparse and repeat rich, are thought to serve as a cradle for adaptive evolution. Supernumerary chromosomes, i.e. chromosomes that are only present in some but not all individuals of a species, are a special type of structural variation that have been observed in plants, animals, and fungi. Here we identified and studied supernumerary mini-chromosomes in the blast fungus Magnaporthe oryzae, a pathogen that causes some of the most destructive plant diseases. We found that rice, foxtail millet and goosegrass isolates of this pathogen contain mini-chromosomes with distinct sequence composition. All minichromosomes are rich in repetitive genetic elements and have lower gene densities than core-chromosomes. Further, we identified virulence-related genes on the mini-chromosome of the rice isolate. We observed large-scale genomic rearrangements around these loci, indicative of a role of mini-chromosomes in facilitating genome dynamics. Taken together, our results indicate that mini-chromosomes facilitate genome rearrangements and possibly adaptive evolution of the blast fungus.

show abstract

“…; Frantzeskakis et al. ). Repetitive DNA may locally increase the mutation rate and contribute to gene duplications and structural variation among alleles (Ohta ).…”

mentioning

confidence: 99%

“…Pathogens constitute model species for addressing this issue, as their antagonistic interaction with the host drives a co-evolutionary dynamics where positive selection recurrently replaces existing alleles in response to allelic changes in the host, a scenario termed arms race evolution (Tellier et al 2014). Based on the finding of high variability in specific genome compartments of several species, it has been proposed that plant pathogens represent exceptional outliers regarding evolutionary rates (Raffaele and Kamoun 2012;Upson et al 2018;Frantzeskakis et al 2019). Furthermore, their life cycles typically combine both asexual and sexual reproduction, raising the question of the importance of meiotic recombination on the rate of adaptation, as it has been evidenced in plant and animal species (Seidl and Thomma 2014).…”

mentioning

confidence: 99%

“…Fungal effector genes, which are encoding proteins that interfere with host defenses and may determine the host range of the pathogen, have been found in several species to associate with repetitive DNA. It has been proposed that repeat-rich genome compartments provide particularly favorable environments for the rapid evolution of new virulence specificities (e.g., Ma et al 2010;Spanu et al 2010;Klosterman et al 2011;Daverdin et al 2012;Frantzeskakis et al 2019). Repetitive DNA may locally increase the mutation rate and contribute to gene duplications and structural variation among alleles (Ohta 2000).…”

mentioning

confidence: 99%

See 1 more Smart Citation

The genomic determinants of adaptive evolution in a fungal pathogen

2019

View full text Add to dashboard Cite

Unravelling the strength, frequency, and distribution of selective variants along the genome as well as the underlying factors shaping this distribution are fundamental goals of evolutionary biology. Antagonistic host‐pathogen coevolution is thought to be a major driver of genome evolution between interacting species. While rapid evolution of pathogens has been documented in several model organisms, the genetic mechanisms of their adaptation are still poorly understood and debated, particularly the role of sexual reproduction. Here, we apply a population genomic approach to infer genome‐wide patterns of selection among 13 isolates of Zymoseptoria tritici , a fungal pathogen characterized by extremely high genetic diversity, gene density, and recombination rates. We report that the genome of Z. tritici undergoes a high rate of adaptive substitutions, with 44% of nonsynonymous substitutions being adaptive on average. This fraction reaches 68% in so‐called effector genes encoding determinants of pathogenicity, and the distribution of fitness effects differs in this class of genes as they undergo adaptive mutations with stronger positive fitness effects, but also more slightly deleterious mutations. Besides the globally high rate of adaptive substitutions, we report a negative relationship between pN/pS and the fine‐scale recombination rate and a strong positive correlation between the rate of adaptive nonsynonymous substitutions (ω a ) and recombination rate. This result suggests a pervasive role of both background selection and Hill‐Robertson interference even in a species with an exceptionally high recombination rate (60 cM/Mb on average). While transposable elements (TEs) have been suggested to contribute to adaptation by creating compartments of fast‐evolving genomic regions, we do not find a significant effect of TEs on the rate of adaptive mutations. Overall our study suggests that sexual recombination is a significant driver of genome evolution, even in rapidly evolving organisms subject to recurrent mutations with large positive effects.

show abstract

The need for speed: compartmentalized genome evolution in filamentous phytopathogens

Cited by 89 publications

References 18 publications

An evolutionary framework for host shifts – jumping ships for survival

An evolutionary framework for host shifts – jumping ships for survival

Genomic rearrangements generate hypervariable mini-chromosomes in host-specific lineages of the blast fungus

The genomic determinants of adaptive evolution in a fungal pathogen

Contact Info

Product

Resources

About