Hybridization speeds up the emergence and evolution of a new pathogen species

Plant pathogens can evolve new host specificities and overcome host resistances over surprisingly few generations, a process that is greatly accelerated by agricultural practices. A new study provides a striking example in which the rapid emergence of a new pathogen via introgressive hybridization mirrors the evolution of a hybrid cereal crop

Non-Mendelian transmission of accessory chromosomes in fungi

Non-Mendelian transmission has been reported for various genetic elements, ranging from small transposons to entire chromosomes. One prime example of such a transmission pattern are B chromosomes in plants and animals. Accessory chromosomes in fungi are similar to B chromosomes in showing presence/absence polymorphism and being non-essential. How these chromosomes are transmitted during meiosis is however poorly understood-despite their often high impact on the fitness of the host. For several fungal organisms, a non-Mendelian transmission or a mechanistically unique meiotic drive of accessory chromosomes have been reported. In this review, we provide an overview of the possible mechanisms that can cause the non-Mendelian transmission or meiotic drives of fungal accessory chromosomes. We compare processes responsible for the non-Mendelian transmission of accessory chromosomes for different fungal eukaryotes and discuss the structural traits of fungal accessory chromosomes affecting their meiotic transmission. We conclude that research on fungal accessory chromosomes, due to their small size, ease of sequencing, and epigenetic profiling, can complement the study of B chromosomes in deciphering factors that influence and regulate the non-Mendelian transmission of entire chromosomes

Local adaptation drives the diversification of effectors in the fungal wheat pathogen Parastagonospora nodorum in the United States

Filamentous fungi rapidly evolve in response to environmental selection pressures in part due to their genomic plasticity. Parastagonospora nodorum, a fungal pathogen of wheat and causal agent of septoria nodorum blotch, responds to selection pressure exerted by its host, influencing the gain, loss, or functional diversification of virulence determinants, known as effector genes. Whole genome resequencing of 197 P. nodorum isolates collected from spring, durum, and winter wheat production regions of the United States enabled the examination of effector diversity and genomic regions under selection specific to geographically discrete populations. 1,026,859 SNPs/InDels were used to identify novel loci, as well as SnToxA and SnTox3 as factors in disease. Genes displaying presence/absence variation, predicted effector genes, and genes localized on an accessory chromosome had significantly higher pN/pS ratios, indicating a higher rate of sequence evolution. Population structure analyses indicated two P. nodorum populations corresponding to the Upper Midwest (Population 1) and Southern/Eastern United States (Population 2). Prevalence of SnToxA varied greatly between the two populations which correlated with presence of the host sensitivity gene Tsn1 in the most prevalent cultivars in the corresponding regions. Additionally, 12 and 5 candidate effector genes were observed to be under diversifying selection among isolates from Population 1 and 2, respectively, but under purifying selection or neutrally evolving in the opposite population. Selective sweep analysis revealed 10 and 19 regions that had recently undergone positive selection in Population 1 and 2, respectively, involving 92 genes in total. When comparing genes with and without presence/absence variation, those genes exhibiting this variation were significantly closer to transposable elements. Taken together, these results indicate that P. nodorum is rapidly adapting to distinct selection pressures unique to spring and winter wheat production regions by rapid adaptive evolution and various routes of genomic diversification, potentially facilitated through transposable element activity

On variant discovery in genomes of fungal plant pathogens

Comparative genome analyses of eukaryotic pathogens including fungi and oomycetes have revealed extensive variability in genome composition and structure. The genomes of individuals from the same population can exhibit different numbers of chromosomes and different organization of chromosomal segments, defining so-called accessory compartments that have been shown to be crucial to pathogenicity in plant-infecting fungi. This high level of structural variation confers a methodological challenge for population genomic analyses. Variant discovery from population sequencing data is typically achieved using established pipelines based on the mapping of short reads to a reference genome. These pipelines have been developed, and extensively used, for eukaryote genomes of both plants and animals, to retrieve single nucleotide polymorphisms and short insertions and deletions. However, they do not permit the inference of large-scale genomic structural variation, as this task typically requires the alignment of complete genome sequences. Here, we compare traditional variant discovery approaches to a pipeline based on de novo genome assembly of short read data followed by whole genome alignment, using simulated data sets with properties mimicking that of fungal pathogen genomes. We show that the latter approach exhibits levels of performance comparable to that of read-mapping based methodologies, when used on sequence data with sufficient coverage. We argue that this approach further allows additional types of genomic diversity to be explored, in particular as long-read third-generation sequencing technologies are becoming increasingly available to generate population genomic data

Dynamics of transposable elements in recently diverged fungal pathogens: lineage-specific transposable element content and efficiency of genome defences

Transposable elements (TEs) impact genome plasticity, architecture and evolution in fungal plant pathogens. The wide range of TE content observed in fungal genomes reflects diverse efficacy of host-genome defence mechanisms that can counter-balance TE expansion and spread. Closely related species can harbour drastically different TE repertoires, suggesting variation in the efficacy of genome defences. The evolution of fungal effectors, which are crucial determinants of pathogenicity, has been linked to the activity of TEs in pathogen genomes. Here we describe how TEs have shaped genome evolution of the fungal wheat pathogen Zymoseptoria tritici and four closely related species. We compared de novo TE annotations and Repeat-Induced Point mutation signatures in thirteen genomes from the Zymoseptoria species-complex. Then, we assessed the relative insertion ages of TEs using a comparative genomics approach. Finally, we explored the impact of TE insertions on genome architecture and plasticity. The thirteen genomes of Zymoseptoria species reflect different TE dynamics with a majority of recent insertions. TEs associate with distinct genome compartments in all Zymoseptoria species, including chromosomal rearrangements, genes showing presence/absence variation and effectors. European Z. tritici isolates have reduced signatures of Repeat-Induced Point mutations compared to Iranian isolates and closely related species. Our study supports the hypothesis that ongoing but moderate TE mobility in Zymoseptoria species shapes pathogen genome evolution.Competing Interest StatementThe authors have declared no competing interest

Forest Saccharomyces paradoxus are robust to seasonal biotic and abiotic changes

Microorganisms are famous for adapting quickly to new environments. However, most evidence for rapid microbial adaptation comes from laboratory experiments or domesticated environments, and it is unclear how rates of adaptation scale from human-influenced environments to the great diversity of wild microorganisms. We examined potential monthly-scale selective pressures in the model forest yeast Saccharomyces paradoxus. Contrary to expectations of seasonal adaptation, the S. paradoxus population was stable over four seasons in the face of abiotic and biotic environmental changes. While the S. paradoxus population was diverse, including 41 unique genotypes among 192 sampled isolates, there was no correlation between S. paradoxus genotypes and seasonal environments. Consistent with observations from other S. paradoxus populations, the forest population was highly clonal and inbred. This lack of recombination, paired with population stability, implies that S. paradoxus evolved the phenotypic plasticity needed to resist seasonal environmental fluctuations long ago, and that individual S. paradoxus are generalists with regard to seasonal environments. Similarly, while the forest population included diversity among phenotypes related to intraspecific interference competition, there was no evidence for active coevolution among these phenotypes. At least ten percent of the forest S. paradoxus individuals produced “}killer toxins{”, which kill sensitive Saccharomyces cells, but the presence of a toxin-producing isolate did not predict resistance to the toxin among nearby isolates. How forest yeasts acclimate to changing environments remains an open question, and future studies should investigate the physiological responses that allow microbial cells to cope with environmental fluctuations in their native habitats.Competing Interest StatementThe authors have declared no competing interest

Plant pathogens provide clues to the potential origin of bat white-nose syndromePseudogymnoascus destructans

White-nose syndrome has killed millions of bats, yet both the origins and infection strategy of the causative fungus, Pseudogymnoascus destructans, remain elusive. We provide evidence for a novel hypothesis that P. destructans emerged from plant-associated fungi and retained invasion strategies affiliated with fungal pathogens of plants. We demonstrate that P. destructans invades bat skin in successive biotrophic and necrotrophic stages (hemibiotrophic infection), a mechanism previously only described in plant fungal pathogens. Further, the convergence of hyphae at hair follicles suggests nutrient tropism. Tropism, biotrophy, and necrotrophy are often associated with structures termed appressoria in plant fungal pathogens; the penetrating hyphae produced by P. destructans resemble appressoria. Finally, we conducted a phylogenomic analysis of a taxonomically diverse collection of fungi. Despite gaps in genetic sampling of prehistoric and contemporary fungal species, we estimate an 88% probability the ancestral state of the clade containing P. destructans was a plant-associated fungus

Colonization dynamics of Pantoea agglomeransin the wheat root habitat

Plants are colonized by microbial communities that have diverse implications for plant development and health. The establishment of a stable plant–bacteria interaction depends on a continuous coexistence over generations. Transmission via the seed is considered as the main route for vertical inheritance of plant-associated bacteria. Nonetheless, the ecological principles that govern the plant colonization by seed endophytes remain understudied. Here we quantify the contribution of arrival time and colonization history to bacterial colonization of the wheat root. Establishing a common seed endophyte, Pantoea agglomerans, and wheat as a model system enabled us to document bacterial colonization of the plant roots during the early stages of germination. Using our system, we estimate the carrying capacity of the wheat roots as 108 cells g−1, which is robust among individual plants and over time. Competitions in planta reveal a significant advantage of early incoming colonizers over late-incoming colonizers. Priming for the wheat environment had little effect on the colonizer success. Our experiments thus provide empirical data on the root colonization dynamics of a seed endophyte. The persistence of seed endophyte bacteria with the plant population over generations may contribute to the stable transmission that is one route for the evolution of a stable host-associated lifestyle

Seed-derived microbial colonization of Wild Emmer and domesticated bread wheat (Triticum dicoccoides and T. aestivum) seedlings shows pronounced differences in overall diversity and composition

The composition of the plant microbiota may be altered by ecological and evolutionary changes in the host population. Seed-associated microbiota, expected to be largely vertically transferred, have the potential to coadapt with their host over generations. Strong directional selection and changes in the genetic composition of plants during domestication and cultivation may have impacted the assembly and transmission of seed-associated microbiota. Nonetheless, the effect of plant speciation and domestication on the composition of these microbes is poorly understood. Here, we have investigated the composition of bacteria and fungi associated with the wild emmer wheat (Triticum dicoccoides) and domesticated bread wheat (Triticum aestivum). We show that vertically transmitted bacteria, but not fungi, of domesticated bread wheat species T. aestivum are less diverse and more inconsistent among individual plants compared to those of the wild emmer wheat species T. dicoccoides. We propagated wheat seeds under sterile conditions to characterize the colonization of seedlings by seed-associated microbes. Hereby, we show markedly different community compositions and diversities of leaf and root colonizers of the domesticated bread wheat compared to the wild emmer wheat. By propagating the wild emmer wheat and domesticated bread wheat in two different soils, we furthermore reveal a small effect of plant genotype on microbiota assembly. Our results suggest that domestication and prolonged breeding have impacted the vertically transferred bacteria, but only to a lesser extent have affected the soil-derived microbiota of bread wheat.IMPORTANCE Genetic and physiological changes associated with plant domestication have been studied for many crop species. Still little is known about the impact of domestication on the plant-associated microbiota. In this study, we analyze the seed-associated and soil-derived bacterial and fungal microbiota of domesticated bread wheat and wild emmer wheat. We show a significant difference in the seed-associated, but not soil-derived, bacterial communities of the wheat species. Interestingly, we find less pronounced effects on the fungal communities. Overall, this study provides novel insight into the diversity of vertically transmitted microbiota of wheat and thereby contributes to our understanding of wheat as a “}metaorganism.{” Insight into the wheat microbiota is of fundamental importance for the development of improved crops