Fungi are a diverse group of organisms with a huge variation in reproductive strategy. While almost all species can reproduce sexually, many reproduce asexually most of the time. When sexual reproduction does occur, large variation exists in the amount of in- and out-breeding. While budding yeast is expected to outcross only once every 10 000 generations, other fungi are obligate outcrossers with well-mixed panmictic populations. In this review, we give an overview of the costs and benefits of sexual and asexual reproduction in fungi, and the mechanisms that evolved in fungi to reduce the costs of either mode. The proximate molecular mechanisms potentiating outcrossing and meiosis appear to be present in nearly all fungi, making them of little use for predicting outcrossing rates, but also suggesting the absence of true ancient asexual lineages. We review how population genetic methods can be used to estimate the frequency of sex in fungi and provide empirical data that support a mixed mode of reproduction in many species with rare to frequent sex in between rounds of mitotic reproduction. Finally, we highlight how these estimates might be affected by the fungus-specific mechanisms that evolved to reduce the costs of sexual and asexual reproduction.
Although congruence between host and pathogen phylogenies has been extensively investigated, the congruence between host and pathogen genetic structures at the within-species level has received little attention. Using an unprecedented and comprehensive collection of associated plant–pathogen samples, we investigated the degree of congruence between the genetic structures across Europe of two evolutionary and ecological model organisms, the anther-smut pathogen Microbotryum lychnidis-dioicae and its host plant Silene latifolia. We demonstrated a significant and particularly strong level of host–pathogen co-structure, with three main genetic clusters displaying highly similar spatial ranges in Western Europe, Eastern Europe and Italy, respectively. Correcting for the geographical component of genetic variation, significant correlations were still found between the genetic distances of anther-smut and host populations. Inoculation experiments suggested plant local adaptation, at the cluster level, for resistance to pathogens. These findings indicate that the pathogen remained isolated in the same fragmented southern refugia as its host plant during the last glaciation, and that little long-distance dispersal has occurred since the recolonization of Europe for either the plant or the pathogen, despite their known ability to travel across continents. This, together with the inoculation results, suggests that coevolutionary and competitive processes may be drivers of host–pathogen co-structure.
Bacterial-fungal interactions are widespread in nature and there is a growing number of studies reporting distinct fungus-associated bacteria. However, little is known so far about how shifts in the fungus-associated bacteriome will affect the fungal host’s lifestyle. In the present study, we describe for the first time the bacterial community associated with the saprotrophic fungus Mucor hiemalis, commonly found in soil and rhizosphere. Two broad-spectrum antibiotics that strongly altered the bacterial community associated with the fungus were applied. Our results revealed that the antibiotic treatment did not significantly reduce the amount of bacteria associated to the fungus but rather changed the community composition by shifting from initially dominating Alpha-Proteobacteria to dominance of Gamma-Proteobacteria. A novel approach was applied for the isolation of fungal-associated bacteria which also revealed differences between bacterial isolates obtained from the original and the antibiotic-treated M. hiemalis. The shift in the composition of the fungal-associated bacterial community led to significantly reduced fungal growth, changes in fungal morphology, behavior and secondary-metabolites production. Furthermore, our results showed that the antibiotic-treated isolate was more attractive and susceptible to mycophagous bacteria as compared to the original isolate. Overall, our study highlights the importance of the fungus-associated bacteriome for the host’s lifestyle and interactions and indicate that isolation with antibacterials is not sufficient to eradicate the associated bacteria.
Author Summary Some fungi are capable of sexual reproduction without the need for a sexually compatible partner, a behavior called homothallism. For some of these fungi, it was observed that they carried in a single individual all the genes normally determining sexual identity in two distinct sexually compatible individuals, but in most cases the role of these genes is still unclear. Here we examined in detail the homothallic sexual cycle of the yeast Phaffia rhodozyma that belongs to the Basidiomycota, which is the fungal lineage that also includes the mushrooms. Phaffia rhodozyma produces astaxanthin, a pigment with antioxidant properties used in the food and cosmetic industries and is accessible to genetic modifications, so far aimed mainly at improving astaxanthin production. Here we harnessed these genetic tools to dissect the self-fertile life cycle of this yeast and found that all genes normally involved in two-partner sexual reproduction are also required for self-fertile sex in P. rhodozyma and propose a model describing molecular interactions required to trigger sexual development. We also generated preferably outcrossing strains, which are potentially useful for further improvement of P. rhodozyma as an industrial organism.
Plant-associated microorganisms have been shown to critically affect host physiology and performance, suggesting that evolution and ecology of plants and animals can only be understood in a holobiont (host and its associated organisms) context. Host-associated microbial community structures are affected by abiotic and host factors, and increased attention is given to the role of the microbiome in interactions such as pathogen inhibition. However, little is known about how these factors act on the microbial community, and especially what role microbe–microbe interaction dynamics play. We have begun to address this knowledge gap for phyllosphere microbiomes of plants by simultaneously studying three major groups of Arabidopsis thaliana symbionts (bacteria, fungi and oomycetes) using a systems biology approach. We evaluated multiple potential factors of microbial community control: we sampled various wild A. thaliana populations at different times, performed field plantings with different host genotypes, and implemented successive host colonization experiments under lab conditions where abiotic factors, host genotype, and pathogen colonization was manipulated. Our results indicate that both abiotic factors and host genotype interact to affect plant colonization by all three groups of microbes. Considering microbe–microbe interactions, however, uncovered a network of interkingdom interactions with significant contributions to community structure. As in other scale-free networks, a small number of taxa, which we call microbial “hubs,” are strongly interconnected and have a severe effect on communities. By documenting these microbe–microbe interactions, we uncover an important mechanism explaining how abiotic factors and host genotypic signatures control microbial communities. In short, they act directly on “hub” microbes, which, via microbe–microbe interactions, transmit the effects to the microbial community. We analyzed two “hub” microbes (the obligate biotrophic oomycete pathogen Albugo and the basidiomycete yeast fungus Dioszegia) more closely. Albugo had strong effects on epiphytic and endophytic bacterial colonization. Specifically, alpha diversity decreased and beta diversity stabilized in the presence of Albugo infection, whereas they otherwise varied between plants. Dioszegia, on the other hand, provided evidence for direct hub interaction with phyllosphere bacteria. The identification of microbial “hubs” and their importance in phyllosphere microbiome structuring has crucial implications for plant–pathogen and microbe–microbe research and opens new entry points for ecosystem management and future targeted biocontrol. The revelation that effects can cascade through communities via “hub” microbes is important to understand community structure perturbations in parallel fields including human microbiomes and bioprocesses. In particular, parallels to human microbiome “keystone” pathogens and microbes open new avenues of interdisciplinary research that promise to better our understanding of functions of host-associated microbiomes.
Fungi represent a large proportion of the genetic diversity on Earth and fungal activity influences the structure of plant and animal communities, as well as rates of ecosystem processes. Large-scale DNA-sequencing datasets are beginning to reveal the dimensions of fungal biodiversity, which seem to be fundamentally different to bacteria, plants and animals. In this Review, we describe the patterns of fungal biodiversity that have been revealed by molecular-based studies. Furthermore, we consider the evidence that supports the roles of different candidate drivers of fungal diversity at a range of spatial scales, as well as the role of dispersal limitation in maintaining regional endemism and influencing local community assembly. Finally, we discuss the ecological mechanisms that are likely to be responsible for the high heterogeneity that is observed in fungal communities at local scales.
Habitat fragmentation is well known to affect plant and animal diversity as a result of reduced habitat area and connectivity, but its effects on microorganisms are poorly understood. Using high-throughput sequencing of two regions of the rRNA gene, we studied the effects of forest area and connectivity on the diversity and composition of fungi associated with the roots of the dominant tree, Metrosideros polymorpha, in a lava-fragmented landscape on the Island of Hawaii. We found that local fungal diversity increased with forest area, whereas fungal species composition was correlated with fragment connectivity.
When news of xylella hit in 2013, I immediately thought: Scam. In Puglia, ancient olive trees are protected by law from being cut down or otherwise removed. As you can imagine, this law has been unpopular with certain businesses, like real estate developers and road-builders. The areas affected by xylella were, by strange chance, extraordinarily beautiful landscapes – ripe for posh new hotels. The emergency plan which a handful of authorities drew up shortly after the announcement of the xylella epidemic in Puglia was trenchant: cut down all the infected trees, along with a goodly number of their neighbors in case they too had been blighted. Ecco fatto: suddenly there would be more elbow (or hotel) room in several lovely seaside locales in Puglia.
Which of course is only one interpretation of the facts. On the other hand, I'm no agronomist, and as reports of the seriousness of the xylella infection echoed in the press, I began to think I'd jumped to a hasty and cynical conclusion. (For more views on the xylella story, see this independent blog.) Developments over the last few months, however, suggest I may have been right all along. A 2015 report on mafia infiltration of Italian agriculture, written by a team led by the renowned anti-mafia prosecutor Gian Carlo Caselli, dedicated a 9-page sub-chapter to what it called “The Strange Case of Xylella Fastidiosa,” echoing Robert Louis Stevenson’s novella of Jekyll and Hyde. The report noted that xylella broke out shortly after an international agronomy conference had been held in Bari in 2010, though the infection appeared not in olive trees near Bari, but in the Gallipoli area – precisely where hordes of troublesome grandfather trees were holding up plans for a perfectly lovely new mega-resort. Cue yet another criminal investigation: in mid-December, prosecutors led by Cataldo Motta, chief magistrate in Lecce, charged ten agronomists and other public “experts” who’d launched the xylella jihad with a range of misdeeds, among which are spreading plant disease, making false official statements, and destroying and disfiguring natural landscapes. (Italian and English.) The Lecce prosecutors also blocked further eradication of ancient olive trees, at least for the time being.
Pyricularia oryzae is a species complex that causes blast disease on more than 50 species of poaceous plants. Pyricularia oryzae has a worldwide distribution as a rice (Oryza) pathogen and in the last century emerged as an important wheat (Triticum) pathogen in southern Brazil. Presently, P. oryzae pathotype Oryza is considered the rice blast pathogen, whereas P. oryzae pathotype Triticum is the wheat blast pathogen. In this study we investigated whether the Oryza and Triticum pathotypes of P. oryzae were distinct at the species level. We also describe a new Pyricularia species causing blast on several other poaceous hosts in Brazil, including wheat. We conducted phylogenetic analyses using 10 housekeeping loci from an extensive sample (N = 128) of sympatric populations of P. oryzae adapted to rice, wheat and other poaceous hosts found in or near wheat fields. The Bayesian phylogenetic analysis grouped the isolates into two major monophyletic clusters (I and II) with high Bayesian probabilities (P = 0.99). Cluster I contained isolates obtained from wheat as well as other Poaceae hosts (P = 0.98). Cluster II was divided into three host-associated clades (Clades 1, 2 and 3; P > 0.75). Clade 1 contained isolates obtained from wheat and other poaceous hosts, Clade 2 contained exclusively wheat-derived isolates, and Clade 3 comprised isolates associated only with rice. Our interpretation was that cluster I and cluster II correspond to two distinct species: Pyricularia graminis-tritici sp. nov. (Pgt), newly described in this study, and Pyricularia oryzae (Po). The host-associated clades found in P. oryzae Cluster II correspond to P. oryzae pathotype Triticum (PoT; Clades 1 and 2), and P. oryzae pathotype Oryza (PoO; Clade 3). No morphological or cultural differences were observed among these species, but a distinctive pathogenicity spectrum was observed. Pgt and PoT were pathogenic and highly aggressive on Triticum aestivum (wheat), Hordeum vulgare (barley), Urochloa brizantha (signal grass) and Avena sativa (oats). PoO was highly virulent on the original rice host (Oryza sativa), and also on wheat, barley, and oats, but not on signal grass. We concluded that blast disease on wheat and its associated Poaceae hosts in Brazil is caused by multiple Pyricularia species: the newly described Pyricularia graminis-tritici sp. nov., and the known P. oryzae pathotypes Triticum and Oryza. To our knowledge, P. graminis-tritici sp. nov. is still restricted to Brazil, but obviously represents a serious threat to wheat cultivation globally.
Sphaerulina musiva (Peck) Verkley, Quaedvlieg and Crous (syn = Septoria musiva Peck, Mycosphaerella populorum Thompson) is a pathogen of poplar that causes two distinct diseases, leaf spots and cankers. This pathogen co-evolved with Populus deltoides but recent reports have linked it to infections in planted stands of P. trichocarpa, P. balsamifera and their hybrids. Reports of S. musiva have mainly come from central and eastern US and eastern Canada, the assumed endemic range of the pathogen. S. musiva was detected for the first time in the Canadian provinces of British Columbia in 2006 and in Alberta in 2009. Our objectives were to determine the source of S. musiva in British Columbia and Alberta and examine the dispersal pathways of this pathogen across North America. For this task we sequenced eight genes and extracted single nucleotide polymorphisms on a geographically diverse set of 73 strains of S. musiva. Population structure and Approximate Bayesian Computation (ABC) analyses eliminated eastern Canada as a source for these introductions. Genetic diversity estimates and ABC analyses support an eastern US centre of origin for S. musiva and two waves of dispersal into Canada. The recently detected west Canadian populations appear to have received contributions from Saskatchewan (a western Canadian population) and also, in the case of British Columbia from the mid-west US populations. These results also reveal distinct eastern and western Canadian populations. Our analyses suggest that dissemination of the pathogen appears to be associated with the natural distribution of wild P. deltoides and more recently linked to anthropogenic activities. The most parsimonious explanation for the contemporary spread of S. musiva across the landscape is via infected plant material. Our analysis of the tree disease caused by S. musiva demonstrates that a population genetics approach is essential to reveal potential sources and patterns of spread of a pathogen.
Experimental evolution allows us to observe evolution in real time. New advances in genome sequencing make it trivial to discover the mutations that have arisen in evolved cultures; however, linking those mutations to particular adaptive traits remains difficult. We evaluated the fitness impacts of thousands of single-gene losses and amplifications in yeast. We discovered that only a fraction of the hundreds of possible beneficial mutations were actually detected in evolution experiments performed previously. Our results provide evidence that 35% of the mutations identified in experimentally evolved populations are advantageous and that the distribution of beneficial fitness effects depends on the genetic background and the selective conditions. Furthermore, we show that it is possible to select for alternative mutations that improve fitness by blocking particularly high-fitness routes to adaptation.
We used a population genomics approach to test the hypothesis of clonal expansion of a highly fit genotype in populations of Verticillium dahliae. This fungal pathogen has a broad host range and can be dispersed in contaminated seed or other plant material. It has a highly clonal population structure, with several lineages having nearly worldwide distributions in agricultural crops. Isolates in lineage 1A are highly virulent and cause defoliation in cotton, okra, and olive (denoted 1A/D), whereas those in other lineages cause wilting but not defoliation (ND). We tested whether the highly virulent lineage 1A/D could have spread from the southwestern United States to the Mediterranean basin, as predicted from historical records. We found 187 single-nucleotide polymorphisms (SNPs), determined by genotyping by sequencing, among 91 isolates of lineage 1A/D and 5 isolates in the closely related lineage 1B/ND. Neighbor-joining and maximum-likelihood analyses on the 187 SNPs showed a clear divergence between 1A/D and 1B/ND haplotypes. Data for only 77 SNPs were obtained for all 96 isolates (no missing data); lineages 1A/D and 1B/ND differed by 27 of these 77 SNPs, confirming a clear divergence between the two lineages. No evidence of recombination was detected within or between these two lineages. Phylogenetic and genealogical analyses resulted in five distinct subclades of 1A/D isolates that correlated closely with geographic origins in the Mediterranean basin, consistent with the hypothesis that the D pathotype was introduced at least five times in independent founder events into this region from a relatively diverse source population. The inferred ancestral haplotype was found in two isolates sampled before 1983 from the southwestern United States, which is consistent with historical records that 1A/D originated in North America. The five subclades coalesce with the ancestral haplotype at the same time, consistent with a hypothesis of rapid population expansion in the source population during the emergence of 1A/D as a severe pathogen of cotton in the United States.
The co-occurrence of diseases can inform the underlying network biology of shared and multifunctional genes and pathways. In addition, comorbidities help to elucidate the effects of external exposures, such as diet, lifestyle and patient care. With worldwide health transaction data now often being collected electronically, disease co-occurrences are starting to be quantitatively characterized. Linking network dynamics to the real-life, non-ideal patient in whom diseases co-occur and interact provides a valuable basis for generating hypotheses on molecular disease mechanisms, and provides knowledge that can facilitate drug repurposing and the development of targeted therapeutic strategies.
The widespread distribution and relapsing nature of Plasmodium vivax infection present major challenges for the elimination of malaria. To characterize the genetic diversity of this parasite in individual infections and across the population, we performed deep genome sequencing of >200 clinical samples collected across the Asia-Pacific region and analyzed data on >300,000 SNPs and nine regions of the genome with large copy number variations. Individual infections showed complex patterns of genetic structure, with variation not only in the number of dominant clones but also in their level of relatedness and inbreeding. At the population level, we observed strong signals of recent evolutionary selection both in known drug resistance genes and at new loci, and these varied markedly between geographical locations. These findings demonstrate a dynamic landscape of local evolutionary adaptation in the parasite population and provide a foundation for genomic surveillance to guide effective strategies for control and elimination of P. vivax.
Soil microorganisms are central to the provision of food, feed, fiber, and medicine. Engineering of soil microbiomes may promote plant growth and plant health, thus contributing to food security and agricultural sustainability ( 1 , 2 ). However, little is known about most soil microorganisms and their impact on plant health. Disease-suppressive soils offer microbiome-mediated protection of crop plants against infections by soil-borne pathogens. Understanding of the microbial consortia and mechanisms involved in disease suppression may help to better manage plants while reducing fertilizer and pesticide inputs.
Plants are able to recognize conserved features of potential microbial invaders and mount an active defense in most cases. Over the course of evolution, a number of these microbes including plant pathogenic fungi and oomycetes have evolved means through the secretion of small molecules (effectors) to block these defenses and promote virulence. In recent years, research has uncovered a wealth of knowledge regarding how effectors function within the plant cell to promote disease. Function of effectors ranges from altering plant cellular metabolic pathways and signaling cascades, RNA silencing, anti-microbial inhibition, and interfering with recognition machinery. The importance of understanding effector function has given rise to a new area of research termed effectoromics, which in this review refers to high-throughput studies to elucidate the function of a large number of candidate effector genes. Effectoromics research has led to the identification of a number of effectors with redundant function, indicating that pathogenic fungi and oomycetes contain effectors that are individually dispensable but functionally redundant that act synergistically to promote disease.
Fig. 5 Highly polymorphic in the effector genes between and within the host-specific subgroups of M. oryzae. a The percentage of genes showing loss, outlier values of dN/dS when dN/dS was included or excluded for each functional category. The black and gray bars indicate the percentage of genes showing loss or outlier values of dN/dS and the others, respectively. These percentages were calculated when we used 70-15 strain genome as the reference. b Distribution of presence and absence of genes encoding the known effectors in M. oryzae and M. grisea. Heat map shows breadth coverage of genes. The blue and yellow panels indicate absence and presence polymorphisms, respectively. The tree indicates the relationship among the tested pathogens based on Fig. 1b
Background Magnaporthe oryzae (anamorph Pyricularia oryzae) is the causal agent of blast disease of Poaceae crops and their wild relatives. To understand the genetic mechanisms that drive host specialization of M. oryzae, we carried out whole genome resequencing of four M. oryzae isolates from rice (Oryza sativa), one from foxtail millet (Setaria italica), three from wild foxtail millet S. viridis, and one isolate each from finger millet (Eleusine coracana), wheat (Triticum aestivum) and oat (Avena sativa), in addition to an isolate of a sister species M. grisea, that infects the wild grass Digitaria sanguinalis.
Results Whole genome sequence comparison confirmed that M. oryzae Oryza and Setaria isolates form a monophyletic and close to another monophyletic group consisting of isolates from Triticum and Avena. This supports previous phylogenetic analysis based on a small number of genes and molecular markers. When comparing the host specific subgroups, 1.2–3.5 % of genes showed presence/absence polymorphisms and 0–6.5 % showed an excess of non-synonymous substitutions. Most of these genes encoded proteins whose functional domains are present in multiple copies in each genome. Therefore, the deleterious effects of these mutations could potentially be compensated by functional redundancy. Unlike the accumulation of nonsynonymous nucleotide substitutions, gene loss appeared to be independent of divergence time. Interestingly, the loss and gain of genes in pathogens from the Oryza and Setaria infecting lineages occurred more frequently when compared to those infecting Triticum and Avena even though the genetic distance between Oryza and Setaria lineages was smaller than that between Triticum and Avena lineages. In addition, genes showing gain/loss and nucleotide polymorphisms are linked to transposable elements highlighting the relationship between genome position and gene evolution in this pathogen species.
Conclusion Our comparative genomics analyses of host-specific M. oryzae isolates revealed gain and loss of genes as a major evolutionary mechanism driving specialization to Oryza and Setaria. Transposable elements appear to facilitate gene evolution possibly by enhancing chromosomal rearrangements and other forms of genetic variation.
Enzymatic effectors targeting nucleic acids, proteins and other cellular components are the mainstay of conflicts across life forms. Using comparative genomics we identify a large class of eukaryotic proteins, which include effectors from oomycetes, fungi and other parasites. The majority of these proteins have a characteristic domain architecture with one of several N-terminal ‘Header’ domains, which are predicted to play a role in trafficking of these effectors, including a novel version of the Ubiquitin fold. The Headers are followed by one or more diverse C-terminal domains, such as restriction endonuclease (REase), protein kinase, HNH endonuclease, LK-nuclease (a RNase) and multiple distinct peptidase domains, which are predicted to carry their toxicity determinants. The most common types of these proteins appear to have originated from prokaryotic transposases (e.g. TN7 and Mu) and combine a CDC6/ORC1-STAND clade NTPase domain with a C-terminal REase domain. Other than the so-called Crinkler effectors of oomycetes and fungi, these effectors are encoded by other eukaryotic parasites such as trypanosomatids (the RHS proteins) and the rhizarian Plasmodiophora, and symbionts like Capsaspora. Remarkably, we also find these proteins in free-living eukaryotes, including several viridiplantae, fungi, amoebozoans and animals. These versions might either still be transposons or function in other poorly understood eukaryote-specific inter-organismal and inter-genomic conflicts. These include the Medea1 selfish element of Tribolium that spreads via post-zygotic killing. We present a unified mechanism for the recombination-dependent diversification and action of this widespread class of molecular weaponry deployed across diverse conflicts ranging from parasitic to free-living forms.
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