ABSTRACT
When a pathogen invades a plant, it encounters a diverse microbiota with some members contributing to the health and growth of the plant host. So far, the relevance of interactions between pathogens and the plant microbiota are poorly understood; however, new lines of evidence suggest that pathogens play an important role in shaping the microbiome of their host during invasion. This review aims to summarize recent findings that document changes in microbial community composition during the invasion of filamentous pathogens in plant tissues. We explore the known mechanisms of interaction between plant pathogens and the host microbiota that underlie these changes, particularly the pathogen-encoded traits that are produced to target specific microbes. Moreover, we discuss the limitations of current strategies and shed light on new perspectives to study the complex interaction networks between filamentous pathogens and the plant microbiome.
Subject(s)
Host-Pathogen Interactions , Microbiota , Plant Diseases , Plants , Microbiota/physiology , Plant Diseases/microbiology , Plants/microbiology , Fungi/physiology , Fungi/genetics , Fungi/pathogenicityABSTRACT
How organisms respond to environmental stress is a key topic in evolutionary biology. This study focused on the genomic evolution of Laburnicola rhizohalophila, a dark-septate endophytic fungus from roots of a halophyte. Chromosome-level assemblies were generated from five representative isolates from structured subpopulations. The data revealed significant genomic plasticity resulting from chromosomal polymorphisms created by fusion and fission events, known as dysploidy. Analyses of genomic features, phylogenomics, and macrosynteny have provided clear evidence for the origin of intraspecific diploid-like hybrids. Notably, one diploid phenotype stood out as an outlier and exhibited a conditional fitness advantage when exposed to a range of abiotic stresses compared with its parents. By comparing the gene expression patterns in each hybrid parent triad under the four growth conditions, the mechanisms underlying growth vigor were corroborated through an analysis of transgressively upregulated genes enriched in membrane glycerolipid biosynthesis and transmembrane transporter activity. In vitro assays suggested increased membrane integrity and lipid accumulation, as well as decreased malondialdehyde production under optimal salt conditions (0.3 M NaCl) in the hybrid. These attributes have been implicated in salinity tolerance. This study supports the notion that hybridization-induced genome doubling leads to the emergence of phenotypic innovations in an extremophilic endophyte.
Subject(s)
Diploidy , Plant Roots , Salt-Tolerant Plants , Plant Roots/microbiology , Salt-Tolerant Plants/microbiology , Salt-Tolerant Plants/genetics , Hybrid Vigor/genetics , Phylogeny , Genome, Fungal , Ascomycota/genetics , Ascomycota/metabolism , Gene Expression Regulation, Fungal , Endophytes/genetics , Endophytes/metabolism , Stress, Physiological/genetics , Phenotype , Salt Tolerance/genetics , Hybridization, GeneticABSTRACT
Invasive fungal pathogens pose a substantial threat to widely cultivated crop species, owing to their capacity to adapt to new hosts and new environmental conditions. Gaining insights into the demographic history of these pathogens and unravelling the mechanisms driving coevolutionary processes are crucial for developing durably effective disease management programmes. Pyrenophora teres is a significant fungal pathogen of barley, consisting of two lineages, Ptt and Ptm, with global distributions and demographic histories reflecting barley domestication and spread. However, the factors influencing the population structure of P. teres remain poorly understood, despite the varietal and environmental heterogeneity of barley agrosystems. Here, we report on the population genomic structure of P. teres in France and globally. We used genotyping-by-sequencing to show that Ptt and Ptm can coexist in the same area in France, with Ptt predominating. Furthermore, we showed that differences in the vernalization requirement of barley varieties were associated with population differentiation within Ptt in France and at a global scale, with one population cluster found on spring barley and another population cluster found on winter barley. Our results demonstrate how cultivation conditions, possibly associated with genetic differences between host populations, can be associated with the maintenance of divergent invasive pathogen populations coexisting over large geographic areas. This study not only advances our understanding of the coevolutionary dynamics of the Pt-barley pathosystem but also prompts further research on the relative contributions of adaptation to the host versus adaptation to abiotic conditions in shaping Ptt populations.
Subject(s)
Ascomycota , Hordeum , Plant Diseases , Hordeum/microbiology , Plant Diseases/microbiology , France , Ascomycota/genetics , Host-Pathogen Interactions/genetics , Phylogeny , VernalizationABSTRACT
Metaorganism research contributes substantially to our understanding of the interaction between microbes and their hosts, as well as their co-evolution. Most research is currently focused on the bacterial community, while archaea often remain at the sidelines of metaorganism-related research. Here, we describe the archaeome of a total of eleven classical and emerging multicellular model organisms across the phylogenetic tree of life. To determine the microbial community composition of each host, we utilized a combination of archaea and bacteria-specific 16S rRNA gene amplicons. Members of the two prokaryotic domains were described regarding their community composition, diversity, and richness in each multicellular host. Moreover, association with specific hosts and possible interaction partners between the bacterial and archaeal communities were determined for the marine models. Our data show that the archaeome in marine hosts predominantly consists of Nitrosopumilaceae and Nanoarchaeota, which represent keystone taxa among the porifera. The presence of an archaeome in the terrestrial hosts varies substantially. With respect to abundant archaeal taxa, they harbor a higher proportion of methanoarchaea over the aquatic environment. We find that the archaeal community is much less diverse than its bacterial counterpart. Archaeal amplicon sequence variants are usually host-specific, suggesting adaptation through co-evolution with the host. While bacterial richness was higher in the aquatic than the terrestrial hosts, a significant difference in diversity and richness between these groups could not be observed in the archaeal dataset. Our data show a large proportion of unclassifiable archaeal taxa, highlighting the need for improved cultivation efforts and expanded databases.
ABSTRACT
Entire chromosomes are typically only transmitted vertically from one generation to the next. The horizontal transfer of such chromosomes has long been considered improbable, yet gained recent support in several pathogenic fungi where it may affect the fitness or host specificity. To date, it is unknown how these transfers occur, how common they are, and whether they can occur between different species. In this study, we show multiple independent instances of horizontal transfers of the same accessory chromosome between two distinct strains of the asexual entomopathogenic fungus Metarhizium robertsii during experimental co-infection of its insect host, the Argentine ant. Notably, only the one chromosome-but no other-was transferred from the donor to the recipient strain. The recipient strain, now harboring the accessory chromosome, exhibited a competitive advantage under certain host conditions. By phylogenetic analysis, we further demonstrate that the same accessory chromosome was horizontally transferred in a natural environment between M. robertsii and another congeneric insect pathogen, Metarhizium guizhouense. Hence, horizontal chromosome transfer is not limited to the observed frequent events within species during experimental infections but also occurs naturally across species. The accessory chromosome that was transferred contains genes that may be involved in its preferential horizontal transfer or support its establishment. These genes encode putative histones and histone-modifying enzymes, as well as putative virulence factors. Our study reveals that both intra- and interspecies horizontal transfer of entire chromosomes is more frequent than previously assumed, likely representing a not uncommon mechanism for gene exchange.
Subject(s)
Ants , Animals , Phylogeny , Histones , Insecta , ChromosomesABSTRACT
Many pathogens evolved compartmentalized genomes with conserved core and variable accessory regions (ARs) that carry effector genes mediating virulence. The fungal plant pathogen Fusarium oxysporum has such ARs, often spanning entire chromosomes. The presence of specific ARs influences the host range, and horizontal transfer of ARs can modify the pathogenicity of the receiving strain. However, how these ARs evolve in strains that infect the same host remains largely unknown. We defined the pan-genome of 69 diverse F. oxysporum strains that cause Fusarium wilt of banana, a significant constraint to global banana production, and analyzed the diversity and evolution of the ARs. Accessory regions in F. oxysporum strains infecting the same banana cultivar are highly diverse, and we could not identify any shared genomic regions and in planta-induced effectors. We demonstrate that segmental duplications drive the evolution of ARs. Furthermore, we show that recent segmental duplications specifically in accessory chromosomes cause the expansion of ARs in F. oxysporum. Taken together, we conclude that extensive recent duplications drive the evolution of ARs in F. oxysporum, which contribute to the evolution of virulence.
Subject(s)
Fusarium , Genome, Fungal , Segmental Duplications, Genomic , Fusarium/genetics , Host Specificity , Genomics , Plant Diseases/genetics , Plant Diseases/microbiologyABSTRACT
Fungal pathogens cause devastating disease in crops. Understanding the evolutionary origin of pathogens is essential to the prediction of future disease emergence and the potential of pathogens to disperse. The fungus Pyrenophora teres f. teres causes net form net blotch (NFNB), an economically significant disease of barley. In this study, we have used 104 P. teres f. teres genomes from four continents to explore the population structure and demographic history of the fungal pathogen. We showed that P. teres f. teres is structured into populations that tend to be geographically restricted to different regions. Using Multiple Sequentially Markovian Coalescent and machine learning approaches we demonstrated that the demographic history of the pathogen correlates with the history of barley, highlighting the importance of human migration and trade in spreading the pathogen. Exploring signatures of natural selection, we identified several population-specific selective sweeps that colocalized with genomic regions enriched in putative virulence genes, and loci previously identified as determinants of virulence specificities by quantitative trait locus analyses. This reflects rapid adaptation to local hosts and environmental conditions of P. teres f. teres as it spread with barley. Our research highlights how human activities can contribute to the spread of pathogens that significantly impact the productivity of field crops.
Subject(s)
Ascomycota , Hordeum , Humans , Hordeum/genetics , Hordeum/microbiology , Domestication , Ascomycota/genetics , Plant Diseases/genetics , Plant Diseases/microbiology , Quantitative Trait Loci/geneticsABSTRACT
Some fungal accessory chromosomes (ACs) may contribute to virulence in plants. However, the mechanisms by which ACs determine specific traits associated with lifestyle transitions along a symbiotic continuum are not clear. Here we delineated the genetic divergence in two sympatric but considerably variable isolates (16B and 16W) of the poplar-associated fungus Stagonosporopsis rhizophilae. We identified a â¼0.6-Mb horizontally acquired AC in 16W that resulted in a mildly parasitic lifestyle in plants. Complete deletion of the AC (Δ16W) significantly altered the fungal phenotype. Specifically, Δ16W was morphologically more similar to 16B, showed enhanced melanization, and established beneficial interactions with poplar plants, thereby acting as a dark septate endophyte. RNA sequencing (RNA-seq) analysis showed that AC loss induced the upregulation of genes related to root colonization and biosynthesis of indole acetic acid and melanin. We observed that the AC maintained a more open status of chromatin across the genome, indicating an impressive remodeling of cis-regulatory elements upon AC loss, which potentially enhanced symbiotic effectiveness. We demonstrated that the symbiotic capacities were non-host-specific through comparable experiments on Triticum- and Arabidopsis-fungus associations. Furthermore, the three isolates generated symbiotic interactions with a nonvascular liverwort. In summary, our study suggests that the AC is a suppressor of symbiosis and provides insights into the underlying mechanisms of mutualism with vascular plants in the absence of traits encoded by the AC. We speculate that AC-situated effectors and other potential secreted molecules may have evolved to specifically target vascular plants and promote mild virulence.
Subject(s)
Ascomycota , Symbiosis , Symbiosis/genetics , Endophytes/genetics , Trees/genetics , Ascomycota/genetics , Plants/genetics , ChromosomesABSTRACT
Puccinia coronata f. sp. avenae (Pca) is an important fungal pathogen causing crown rust that impacts oat production worldwide. Genetic resistance for crop protection against Pca is often overcome by the rapid virulence evolution of the pathogen. This study investigated the factors shaping adaptive evolution of Pca using pathogen populations from distinct geographic regions within the United States and South Africa. Phenotypic and genome-wide sequencing data of these diverse Pca collections, including 217 isolates, uncovered phylogenetic relationships and established distinct genetic composition between populations from northern and southern regions from the United States and South Africa. The population dynamics of Pca involve a bidirectional movement of inoculum between northern and southern regions of the United States and contributions from clonality and sexuality. The population from South Africa is solely clonal. A genome-wide association study (GWAS) employing a haplotype-resolved Pca reference genome was used to define 11 virulence-associated loci corresponding to 25 oat differential lines. These regions were screened to determine candidate Avr effector genes. Overall, the GWAS results allowed us to identify the underlying genetic factors controlling pathogen recognition in an oat differential set used in the United States to assign pathogen races (pathotypes). Key GWAS findings support complex genetic interactions in several oat lines, suggesting allelism among resistance genes or redundancy of genes included in the differential set, multiple resistance genes recognizing genetically linked Avr effector genes, or potentially epistatic relationships. A careful evaluation of the composition of the oat differential set accompanied by the development or implementation of molecular markers is recommended. [Formula: see text] Copyright © 2024 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.
Subject(s)
Basidiomycota , Disease Resistance , Puccinia , Disease Resistance/genetics , Avena/genetics , Avena/microbiology , Virulence/genetics , Genome-Wide Association Study , Phylogeny , Plant Diseases/microbiology , Basidiomycota/genetics , Population DynamicsABSTRACT
A serious factor hampering global maize production is gray leaf spot disease. Cercospora zeina is one of the causative pathogens, but population genomics analysis of C. zeina is lacking. We conducted whole-genome Illumina sequencing of a representative set of 30 C. zeina isolates from Kenya and Uganda (East Africa) and Zambia, Zimbabwe, and South Africa (Southern Africa). Selection of the diverse set was based on microsatellite data from a larger collection of the pathogen. Pangenome analysis of the C. zeina isolates was done by (1) de novo assembly of the reads with SPAdes, (2) annotation with BRAKER, and (3) protein clustering with OrthoFinder. A published long-read assembly of C. zeina (CMW25467) from Zambia was included and annotated using the same pipeline. This analysis revealed 790 non-shared accessory and 10,677 shared core orthogroups (genes) between the 31 isolates. Accessory gene content was largely shared between isolates from all countries, with a few genes unique to populations from Southern Africa (32) or East Africa (6). There was a significantly higher proportion of effector genes in the accessory secretome (44%) compared to the core secretome (24%). PCA, ADMIXTURE, and phylogenetic analysis using a neighbor-net network indicated a population structure with a geographical subdivision between the East African isolates and the Southern African isolates, although gene flow was also evident. The small pangenome and partial population differentiation indicated recent dispersal of C. zeina into Africa, possibly from 2 regional founder populations, followed by recurrent gene flow owing to widespread maize production across sub-Saharan Africa.
Subject(s)
Metagenomics , Zea mays , Zea mays/genetics , Phylogeny , South AfricaABSTRACT
Meiosis is associated with genetic changes in the genome-via recombination, gene conversion, and mutations. The occurrence of gene conversion and mutations during meiosis may further be influenced by the chromatin conformation, similar to the effect of the chromatin conformation on the mitotic mutation rate. To date, however, the exact distribution and type of meiosis-associated changes and the role of the chromatin conformation in this context are largely unexplored. Here, we determine recombination, gene conversion, and de novo mutations using whole-genome sequencing of all meiotic products of 23 individual meioses in Zymoseptoria tritici, an important pathogen of wheat. We confirm a high genome-wide recombination rate of 65 centimorgan (cM)/Mb and see higher recombination rates on the accessory compared to core chromosomes. A substantial fraction of 0.16% of all polymorphic markers was affected by gene conversions, showing a weak GC-bias and occurring at higher frequency in regions of constitutive heterochromatin, indicated by the histone modification H3K9me3. The de novo mutation rate associated with meiosis was approximately three orders of magnitude higher than the corresponding mitotic mutation rate. Importantly, repeat-induced point mutation (RIP), a fungal defense mechanism against duplicated sequences, is active in Z. tritici and responsible for the majority of these de novo meiotic mutations. Our results indicate that the genetic changes associated with meiosis are a major source of variability in the genome of an important plant pathogen and shape its evolutionary trajectory. IMPORTANCE The impact of meiosis on the genome composition via gene conversion and mutations is mostly poorly understood, in particular, for non-model species. Here, we sequenced all four meiotic products for 23 individual meioses and determined the genetic changes caused by meiosis for the important fungal wheat pathogen Zymoseptoria tritici. We found a high rate of gene conversions and an effect of the chromatin conformation on gene conversion rates. Higher conversion rates were found in regions enriched with the H3K9me3-a mark for constitutive heterochromatin. Most importantly, meiosis was associated with a much higher frequency of de novo mutations than mitosis; 78% of the meiotic mutations were caused by repeat-induced point mutations-a fungal defense mechanism against duplicated sequences. In conclusion, the genetic changes associated with meiosis are therefore a major factor shaping the genome of this fungal pathogen.
Subject(s)
Ascomycota , Gene Conversion , Point Mutation , Heterochromatin/genetics , Ascomycota/genetics , Mutation , Meiosis/geneticsABSTRACT
Identifying traits involved in plant-pathogen interactions is one of the major objectives in molecular plant pathology. Evolutionary analyses may assist in the identification of genes encoding traits that are involved in virulence and local adaptation, including adaptation to agricultural intervention strategies. In the past decades, the number of available genome sequences of fungal plant pathogens has rapidly increased, providing a rich source for the discovery of functionally important genes as well as inference of species histories. Positive selection in the form of diversifying or directional selection leaves particular signatures in genome alignments and can be identified with statistical genetics methods. This review summarises the concepts and approaches used in evolutionary genomics and lists major discoveries related to plant-pathogen adaptative evolution. We underline the significant contribution of evolutionary genomics in discovering virulence-related traits and the study of plant-pathogen ecology and adaptive evolution.
Subject(s)
Adaptation, Physiological , Genome, Fungal , Adaptation, Physiological/genetics , Virulence/genetics , Phenotype , Plant Diseases/microbiologyABSTRACT
Agro-ecosystems provide environments that are conducive for rapid evolution and dispersal of plant pathogens. Previous studies have demonstrated that hybridization of crop pathogens can give rise to new lineages with altered virulence profiles. Currently, little is known about either the genetics of fungal pathogen hybridization or the mechanisms that may prevent hybridization between related species. The fungus Pyrenophora teres is a global pathogen of barley. The pathogenic fungus P. teres exists as two distinct lineages P. teres f. teres and P. teres f. maculata (Ptt and Ptm, respectively), which both infect barley but produce very distinct lesions and rarely interbreed. Interestingly, Ptt and Ptm can, by experimental mating, produce viable progenies. Here, we addressed the underlying genetics of reproductive barriers of P. teres. We hypothesize that Ptt and Ptm diverged in the past, possibly by adapting to distinct hosts, and only more recently colonized the same host in agricultural fields. Using experimental mating and in planta phenotyping in barley cultivars susceptible to both P. teres forms, we demonstrate that hybrids produce mixed infection phenotypes but overall show inferior pathogenic fitness relative to the pure parents. Based on analyses of 104 hybrid genomes, we identify signatures of negative epistasis between parental alleles at distinct loci (Dobzhansky-Müller incompatibilities). Most DMI regions are not involved in virulence but certain genes are predicted or known to play a role in virulence. These results potentially suggest that divergent niche adaptation-albeit in the same host plant-contributes to speciation in P. teres.
Subject(s)
Ecosystem , Hordeum , Phenotype , Hordeum/genetics , Hordeum/microbiology , Virulence/genetics , Plant Diseases/genetics , Plant Diseases/microbiologyABSTRACT
Human activity impacts the evolutionary trajectories of many species worldwide. Global trade of agricultural goods contributes to the dispersal of pathogens reshaping their genetic makeup and providing opportunities for virulence gains. Understanding how pathogens surmount control strategies and cope with new climates is crucial to predicting the future impact of crop pathogens. Here, we address this by assembling a global thousand-genome panel of Zymoseptoria tritici, a major fungal pathogen of wheat reported in all production areas worldwide. We identify the global invasion routes and ongoing genetic exchange of the pathogen among wheat-growing regions. We find that the global expansion was accompanied by increased activity of transposable elements and weakened genomic defenses. Finally, we find significant standing variation for adaptation to new climates encountered during the global spread. Our work shows how large population genomic panels enable deep insights into the evolutionary trajectory of a major crop pathogen.
Subject(s)
Acclimatization , Adaptation, Physiological , Humans , Virulence/genetics , Genomics , Plant Diseases/microbiologyABSTRACT
The fungal kingdom represents an extraordinary diversity of organisms with profound impacts across animal, plant, and ecosystem health. Fungi simultaneously support life, by forming beneficial symbioses with plants and producing life-saving medicines, and bring death, by causing devastating diseases in humans, plants, and animals. With climate change, increased antimicrobial resistance, global trade, environmental degradation, and novel viruses altering the impact of fungi on health and disease, developing new approaches is now more crucial than ever to combat the threats posed by fungi and to harness their extraordinary potential for applications in human health, food supply, and environmental remediation. To address this aim, the Canadian Institute for Advanced Research (CIFAR) and the Burroughs Wellcome Fund convened a workshop to unite leading experts on fungal biology from academia and industry to strategize innovative solutions to global challenges and fungal threats. This report provides recommendations to accelerate fungal research and highlights the major research advances and ideas discussed at the meeting pertaining to 5 major topics: (1) Connections between fungi and climate change and ways to avert climate catastrophe; (2) Fungal threats to humans and ways to mitigate them; (3) Fungal threats to agriculture and food security and approaches to ensure a robust global food supply; (4) Fungal threats to animals and approaches to avoid species collapse and extinction; and (5) Opportunities presented by the fungal kingdom, including novel medicines and enzymes.