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Burbano, H. A.

Publications and source records attributed to Burbano, H. A..

17 recordsLinked to original sources

Persistent trade-offs balance competition and colonization across centuries

Microbial competition drives rapid adaptation, often forcing organisms to specialize in new ecological niches. Adaptations that improve competitive ability can reduce performance in other environments creating trade-offs. Whether such trade-offs persist in nature--or are eroded as lineages adapt through compensatory changes--remains largely unknown. Here we show that a trade-off between competitive ability and host colonization has been stably maintained in natural Pseudomonas populations for centuries. Wild plant-pathogenic Pseudomonas compete using tailocins--phage-derived molecular weapons that bind to specific cell-surface receptors. Genomic surveys and functional assays reveal that the most broadly lethal tailocins remain rare--while the tailocins production increases competitive killing, it also compromises plant colonization. We determine that the polymorphisms behind this trade-off are not transient -- historical genomes spanning two centuries show that the trade-off has been maintained for at least 10-10 generations. Our results demonstrate that, in natural populations, a trade-off between competition and pathogenicity is fundamental and not easily overcome. SignificanceWhen a microbe colonizes a host, it must both establish infection and outcompete other organisms. Short-term experiments show that gains in competitive ability can reduce colonization, creating trade-offs, but whether microbes resolve these conflicts over long evolutionary timescales is unknown. We show that a trade-off between competitive killing and host colonization has been stably maintained for centuries in natural Pseudomonas populations infecting Arabidopsis thaliana. Tailocins--phage-derived weapons--provide strong competitive advantages, yet their production reduces colonization success, explaining why the most broadly lethal variants remain rare. Genomic surveys and historical genomes spanning two centuries reveal that the polymorphisms underlying this trade-off have persisted across 10-10 generations. Understanding such long-lived constraints can inform antimicrobial strategies that exploit evolutionary trade-offs.

evolutionary biology↗

Museum genomics reveals temporal genetic stasis and global genetic diversity in Arabidopsis thaliana

Global patterns of population genetic variation through time offer a window into evolutionary processes that maintain diversity. Over time, lineages may expand or contract their distribution, causing turnover in population genetic composition. At individual loci, migration, drift, and selection (among other processes) may affect allele frequencies. Museum specimens of widely distributed species offer a unique window into the genetics of understudied populations and changes over time. Here, we sequenced genomes of 130 herbarium specimens and 91 new field collections of Arabidopsis thaliana and combined these with published genomes. We sought a broader view of genomic diversity across the species, and to test if population genomic composition is changing through time. We documented extensive and previously uncharacterized diversity in a range of populations in Africa, populations that are under threat from anthropogenic climate change. Through time, we did not find dramatic changes in genomic composition of populations. Instead, we found a pattern of genetic change every 100 years of the same magnitude seen when comparing Eurasian populations that are 185 km apart, potentially due to a combination of drift and changing selection. We found only mixed signals of polygenic adaptation at phenology and physiology QTL. We did find that genes conserved across eudicots show altered levels of directional allele frequency change, potentially due to variable purifying and background selection. Our study highlights how museum specimens can reveal new dimensions of population diversity and show how wild populations are evolving in recent history.

evolutionary biology↗

Multiple horizontal mini-chromosome transfers drive genome evolution of clonal blast fungus lineages

Crop disease pandemics are often driven by clonal lineages of plant pathogens that reproduce asexually. How these clonal pathogens continuously adapt to their hosts despite harboring limited genetic variation, and in absence of sexual recombination remains elusive. Here, we reveal multiple instances of horizontal chromosome transfer within pandemic clonal lineages of the blast fungus Magnaporthe (Syn. Pyricularia) oryzae. We identified a horizontally transferred 1.2Mb supernumerary mini-chromosome which is remarkably conserved between M. oryzae isolates from both the rice blast fungus lineage and the lineage infecting Indian goosegrass (Eleusine indica), a wild grass that often grows in the proximity of cultivated cereal crops. Furthermore, we show that this mini-chromosome was horizontally acquired by clonal rice blast isolates through at least nine distinct transfer events over the past three centuries. These findings establish horizontal mini-chromosome transfer as a mechanism facilitating genetic exchange among different host-associated blast fungus lineages. We propose that blast fungus populations infecting wild grasses act as genetic reservoirs that drive genome evolution of pandemic clonal lineages that afflict cereal crops.

evolutionary biology↗

A weaponized phage suppresses competitors in historical and modern metapopulations of pathogenic bacteria

Bacteriophages, the viruses of bacteria, are proposed to drive bacterial population dynamics, yet direct evidence of their impact on natural populations is limited. Here we identified viral sequences in a metapopulation of wild plant-associated Pseudomonas spp. genomes. We discovered that the most abundant viral cluster does not encode an intact phage but instead encodes a tailocin - a phage-derived element that bacteria use to kill competitors for interbacterial warfare. Each pathogenic Pseudomonas sp. strain carries one of a few distinct tailocin variants, which target variable polysaccharides in the outer membrane of co-occurring pathogenic strains. Analysis of historic herbarium samples from the last 170 years revealed that the same tailocin and receptor variants have persisted in the Pseudomonas populations for at least two centuries, suggesting the continued use of a defined set of tailocin haplotypes and receptors. These results indicate that tailocin genetic diversity can be mined to develop targeted "tailocin cocktails" for microbial control. One-Sentence SummaryBacterial pathogens in a host-associated metapopulation use a repurposed prophage to kill their competitors.

microbiology↗

Century-long timelines of herbarium genomes predict plant stomatal response to climate change

Dissecting plant responses to the environment is key to understanding if and how plants adapt to anthropogenic climate change. Stomata, plants pores for gas exchange, are expected to decrease in density following increased CO2 concentrations, a trend already observed in multiple plant species. However, it is unclear if such responses are based on genetic changes and evolutionary adaptation. Here we make use of extensive knowledge of 43 genes in the stomatal development pathway and newly generated genome information of 191 A. thaliana historical herbarium specimens collected over the last 193 years to directly link genetic variation with climate change. While we find that the essential transcription factors SPCH, MUTE and FAMA, central to stomatal development, are under strong evolutionary constraints, several regulators of stomatal development show signs of local adaptation in contemporary samples from different geographic regions. We then develop a polygenic score based on known effects of gene knock-out on stomatal development that recovers a classic pattern of stomatal density decrease over the last centuries without requiring direct phenotype observation of historical samples. This approach combining historical genomics with functional experimental knowledge could allow further investigations of how different, even in historical samples unmeasurable, cellular plant phenotypes have already responded to climate change through adaptive evolution. One sentence summaryUsing a molecular-knowledge based genetic phenotype proxy, historical whole-genome A. thaliana timelines compared with contemporary data indicate a shift of stomatal density following climate-associated predictions.

plant biology↗

Wild grass isolates of Magnaporthe (Syn. Pyricularia) spp. from Germany can cause blast disease on cereal crops

Pathogens that cause destructive crop diseases often infect wild host plants. However, surveys of major plant pathogens tend to be skewed towards cultivated crops and often neglect the wild hosts. Here, we report an emerging disease threat generated by the blast fungus Magnaporthe (Syn. Pyricularia) spp. in central Europe. We found that this notoriously devastating plant pathogen infects the wild grasses foxtail millet (Setaria spp.) and crabgrass (Digitaria spp.) in south-western Germany, a region previously deemed unfavorable for blast disease. Using phenotypic characterization and genomic analyses, we determined that the observed disease symptoms are associated with the Setaria spp.-infecting lineage of M. oryzae and its sister species Magnaporthe grisea. We showed that M. oryzae isolates can infect barley and wheat, thus highlighting the risk of pathogen spread to crops. In addition, M. oryzae isolates which co-occur in natural populations display compatible mating types and variable candidate effector gene content, which may enhance the pathogens adaptive potential. Our findings stress the risk of blast fungus infections expanding into European cereal crops through migration and host jumps. This underlines the importance for pathogen surveillance not only on cultivated crops, but also on wild host plants. Author SummaryWild plant species are often overlooked during pathogen virulence surveys. However, many of the diseases we observe in crops are a consequence of host jumps from wild to cultivated plant species. This is reminiscent of zoonotic diseases, where host jumps from wild animals to humans result in new disease outbreaks. Here, we report that the notoriously devastating blast fungus Magnaporthe (Syn. Pyricularia) spp. occurs on wild grasses in south-western Germany. This region, which is at the center of the European cereal belt, has so far been viewed as having unfavorable climatic conditions for the blast disease. The newly identified blast fungus isolates have the capacity to infect wheat and barley cultivars, highlighting the risk of the disease spreading to staple cereal crops. In addition, there is potential for sexual recombination in local populations, which may increase the evolutionary potential of the fungus and might facilitate host jumps to cereal crops. Our findings emphasize the urgent need for surveillance of plant diseases on both wild hosts and crops.

plant biology↗

Polymorphic Inverted Repeats near coding genes impact chromatin topology and phenotypic traits in Arabidopsis thaliana

Transposons are mobile elements that are commonly silenced to protect eukaryotic genome integrity. In plants, transposable elements (TEs) can be activated during stress conditions and subsequently insert into gene-rich regions. TE-derived inverted repeats (IRs) are commonly found near plant genes, where they affect host gene expression with potentially positive effects on adaptation. However, the molecular mechanisms by which these IRs control gene expression is unclear in most cases. Here, we identify in the Arabidopsis thaliana genome hundreds of IRs located near genes that are transcribed by RNA Polymerase II, resulting in the production of 24-nt small RNAs that trigger methylation of the IRs. The expression of these IRs is associated with drastic changes in the local 3D chromatin organization, which alter the expression pattern of the hosting genes. Notably, the presence and structure of many IRs differ between A. thaliana accessions. Capture-C sequencing experiments revealed that such variation changes short-range chromatin interactions, which translates into changes in gene expression patterns. CRISPR/Cas9-mediated disruption of two of such IRs leads to a switch in genome topology and gene expression, with phenotypic consequences. Our data demonstrate that the insertion of an IR near a gene provides an anchor point for chromatin interactions that can profoundly impact the activity of neighboring loci. This turns IRs into powerful evolutionary agents that can contribute to rapid adaptation.

plant biology↗

A pandemic clonal lineage of the wheat blast fungus

Wheat, the most important food crop, is threatened by a blast disease pandemic. Here, we show that a clonal lineage of the wheat blast fungus recently spread to Asia and Africa following two independent introductions from South America. Through a combination of genome analyses and laboratory experiments, we show that the decade-old blast pandemic lineage can be controlled by the Rmg8 disease resistance gene and is sensitive to strobilurin fungicides. However, we also highlight the potential of the pandemic clone to evolve fungicide-insensitive variants and sexually recombine with African lineages. This underscores the urgent need for genomic surveillance to track and mitigate the spread of wheat blast outside of South America, and to guide pre-emptive wheat breeding for blast resistance.

evolutionary biology↗

SNP calling parameters have minimal impact on population structure and divergence time estimates for the rice blast fungus

ObjectivesAccurate single-nucleotide polymorphisms (SNP) calls are crucial for robust evolutionary and population genetic inferences in genomic analyses. Such inferences can reveal the time-scales and processes associated with the emergence and spread of pandemic plant pathogens, such as the rice blast fungus Magnaporthe oryzae (Syn. Pyricularia oryzae). However, the specificity and sensitivity of SNP calls depend on the filtering parameters applied to the data. Here, we used a benchmarking approach to evaluate the impact of SNP calling on different population genetic analyses of the rice blast fungus, namely genetic clustering, topology of phylogenetic reconstructions and estimation of evolutionary rates. ResultsTo benchmark SNP calling parameters, we generated a gold standard set of validated SNPs by sequencing nine M. oryzae genomes with both Illumina short-reads and Oxford Nanopore Technologies (ONT). We used the gold standard set of SNPs to identify the SNP calling parameter configuration that maximizes sensitivity and specificity. We found that the choice of parameter configurations can substantially change the number of ascertained SNPs, preferentially affecting SNPs segregating at low population frequency. However, SNP calling parameter configurations did not significantly affect the clustering of isolates in clonal lineages, the monophyly of each clonal lineage, and the estimation of evolutionary rates. We leverage the evolutionary rates obtained from each SNP calling parameter configuration to generate divergence time estimates that take into account the uncertainty associated with both the estimation of evolutionary rates and SNP calling. Our analysis indicates that M. oryzae clonal lineage expansions took place ~300 years ago.

genomics↗

Rapid adaptation and range expansion in response to agriculture over the last two centuries

North America has seen a massive increase in cropland use since 1800, accompanied more recently by the intensification of agricultural practices. Through genome analysis of present-day and historical samples spanning environments over the last two centuries, we studied the impact of these changes in farming on the extent and tempo of evolution across the native range of common waterhemp (Amaranthus tuberculatus), a now pervasive agricultural weed. Modern agriculture has imposed strengths of selection rarely observed in the wild, with striking shifts in allele frequency trajectories since agricultural intensification in the 1960s. An evolutionary response to this extreme selection was facilitated by a concurrent human-mediated range shift. By reshaping genome-wide diversity across the landscape, agriculture has driven the success of this weed in the 21st-century. One Sentence SummaryModern agriculture has shaped the evolution of a native plant into a weed by driving range shifts and strengths of selection rarely observed in the wild.

evolutionary biology↗

Fine-scale Population Structure of North American Arabidopsis thaliana Reveals Multiple Sources of Introduction from Across Eurasia

Large-scale movement of organisms across their habitable range, or migration, is an important evolutionary process that can contribute to observed patterns of genetic diversity and our understanding of the adaptive spread of alleles. While human migrations have been studied in great detail with modern and ancient genomes, recent anthropogenic influence on reducing the biogeographical constraints on the migration of non-native species has presented opportunities in several study systems to ask the questions about how repeated introductions shape genetic diversity in the introduced range. We present here the most comprehensive view of population structure of North American Arabidopsis thaliana by studying a set of 500 (whole-genome sequenced) and over 2800 (RAD-seq genotyped) individuals in the context of global diversity represented by Afro-Eurasian genomes. We use haplotype-sharing, phylogenetic modeling and rare-allele sharing based methods to identify putative sources of introductions of extant N. American A. thaliana from the native range of Afro-Eurasia. We find evidence of admixture among the introduced lineages that has resulted in the increased haplotype diversity and reduced mutational load. Further, we also present signals of selection in the immune-system related genes that impart qualitative disease resistance to pathogens of bacterial and oomycete origins. Thus, multiple introductions to a non-native range can quickly increase adaptive potential of a colonizing species by increasing haplotypic diversity through admixture. The results presented here lay the foundation for further investigations into the functional significance of admixture.

evolutionary biology↗

Museum phylogenomics of extinct Oryctes beetles from the Mascarene Islands

The evolution of island systems is characterized by processes that result in extreme morphological diversity, high endemism and high extinction rates. These dynamics can make phylogenetic reconstruction difficult, i.e. the extinct flightless Dodo from Mauritius was assigned to the family of doves only through DNA analysis of subfossils. Many insect species on islands have gone extinct through habitat loss, and face similar challenges to decipher their evolutionary history, however historical specimens have not yet been harnessed for phylogenomic reconstructions. Here, we employed historical museum specimens from the Mascarene Islands to generate the first whole-genome based phylogeny of three presumably extinct species of the rhinoceros beetle genus Oryctes. We compared their genomes with those of an extant Oryctes species from the island of Reunion, as well as a flightless Reunion-based species previously placed into the supposedly unrelated genus Marronus. We found that Marronus borbonicus belongs instead to the genus Oryctes and that the two Reunion-based species (O. borbonicus and M. borbonicus) are not sister taxa, suggesting two independent colonizations. The divergence time between them (<3Myr) overlaps with the volcanic formation of Reunion, likely indicating that M. borbonicus became flightless in situ. Our study showcases the power of genomes from insect museum specimens to address evolutionary questions in light of increasing extinction rates.

evolutionary biology↗

Recently expanded clonal lineages of the rice blast fungus display distinct patterns of presence/absence of effector genes

BackgroundUnderstanding the mechanisms and timescales of plant pathogen outbreaks requires a detailed genome-scale analysis of their population history. The fungus Magnaporthe (Syn. Pyricularia) oryzae --the causal agent of blast disease of cereals-- is among the most destructive plant pathogens to world agriculture and a major threat to the production of rice, wheat and other cereals. Although M. oryzae is a multihost pathogen that infects more than 50 species of cereals and grasses, all rice-infecting isolates belong to a single genetically defined lineage. Here, we combined multiple genomics datasets to reconstruct the genetic history of the rice-infecting lineage of M. oryzae based on 131 isolates from 21 countries. ResultsThe global population of the rice blast fungus consists of a diverse set of individuals and three well-defined genetic groups. Multiple population genetic tests revealed that the rice-infecting lineage of the blast fungus probably originated from a recombining diverse group in South East Asia followed by three independent clonal expansions that took place over the last [~]200 years. Patterns of allele sharing identified a subpopulation from the recombining diverse group that introgressed with one of the clonal lineages before its global expansion. Remarkably, the four genetic lineages of the rice blast fungus vary in the number and patterns of presence/absence of candidate effector genes. In particular, clonal lineages carry a reduced repertoire of effector genes compared with the diverse group, and specific combinations of effector presence/absence define each of the pandemic clonal lineages. ConclusionsOur analyses reconstruct the genetic history of the rice-infecting lineage of M. oryzae revealing three clonal lineages associated with rice blast pandemics. Each of these lineages displays a specific pattern of presence/absence of effector genes that may have shaped their adaptation to the rice host and their evolutionary history.

evolutionary biology↗

Mining ancient microbiomes using selective enrichment of damaged DNA molecules

BackgroundThe identification of bona fide microbial taxa in microbiomes derived from ancient and historical samples is complicated by the unavoidable mixture between DNA from ante- and post-mortem microbial colonizers. One possibility to distinguish between these sources of microbial DNA is querying for the presence of age-associated degradation patterns typical of ancient DNA (aDNA). The presence of uracils, resulting from cytosine deamination, has been detected ubiquitously in aDNA retrieved from diverse sources, and used as an authentication criterion. Here, we employ a library preparation method that separates molecules that carry uracils from those that do not for a set of samples that includes Neandertal remains, herbarium specimens and archaeological plant remains. ResultsWe show that sequencing DNA libraries enriched in molecules carrying uracils effectively amplifies age associated degradation patterns in microbial mixtures of ancient and historical origin. This facilitates the discovery of authentic ancient microbial taxa in cases where degradation patterns are difficult to detect due to large sequence divergence in microbial mixtures. Additionally, the relative enrichment of taxa in the uracil enriched fraction can help to identify bona fide ancient microbial taxa that could be missed using a more targeted approach. ConclusionsOur experiments show, that in addition to its use in enriching authentic endogenous DNA of organisms of interest, the selective enrichment of damaged DNA molecules can be a valuable tool in the discovery of ancient microbial taxa.

genomics↗

A map of climate change-driven natural selection in Arabidopsis thaliana

Through the lens of evolution, climate change is an agent of directional selection that forces populations to change and adapt, or face extinction. Current assessments of the risks associated with climate change1,2, however, do not typically take into account that natural selection can dramatically impact the genetic makeup of populations3. We made use of extensive genome information in Arabidopsis thaliana and measured how rainfall-manipulation affected the fitness of 517 natural lines grown in Spain and Germany. This allowed us to directly infer selection at the genetic level4. Natural selection was particularly strong in the hot-dry Spanish location, killing 63% of lines and significantly changing the frequency of [~]5% of all genome-wide variants. A significant proportion of this selection over variants could be predicted from climate (mis)match between experimental sites and the geographic areas of where variants are found (R2=29-52%). Field-validated predictions across the species range indicated that Mediterranean and Western Siberia populations -- at the edges of the species environmental limits -- currently experience the strongest climate-driven selection, and Central Europeans the weakest. With rapidly increasing droughts and rising temperatures in Europe5, we forecast a wave of directional selection moving North, putting many native A thaliana populations at evolutionary risk.

evolutionary biology↗

A rainfall-manipulation experiment with 517 Arabidopsis thaliana accessions

The gold standard for studying natural selection and adaptation in the wild is to quantify lifetime fitness of individuals from natural populations that have been grown together in a common garden, or that have been reciprocally transplanted. By combining fitness values with species traits and genome sequences, one can infer selection coefficients at the genetic level. Here we present a rainfall-manipulation experiment with 517 whole-genome sequenced natural accessions of the plant Arabidopsis thaliana spanning the global distribution of the species. The experiments were conducted in two field stations in contrasting climates, in the Mediterranean and in Central Europe, where we built rainout shelters and simulated high and low rainfall. Using custom image analysis we quantified fitness- and phenology-related traits for 23,154 pots, which contained about 14,500 plants growing independently, and over 310,000 plants growing in small populations (max. 30 plants). This large field experiment dataset, which associates fitness and ecologically-relevant traits with genomes, will provide an important resource to test eco-evolutionary genetic theories and to understand the potential evolutionary impacts of future climates on an important plant model species.

evolutionary biology↗

nQuire: A Statistical Framework For Ploidy Estimation Using Next Generation Sequencing

SummarynQuire is a statistical framework that distinguishes between diploids, triploids and tetraploids using next generation sequencing. The command-line tool models the distribution of base frequencies at variable sites using a Gaussian Mixture Model, and uses maximum likelihood to select the most plausible ploidy model.\n\nAvailability and ImplementationThe model is implemented as a stand-alone Linux command line tool in the C programming language and is available at github under the MIT licence. Please also refer to github.com/clwgg/nQuire for usage instructions. Contact: clemens.weiss@tuebingen.mpg.de or hernan.burbano@tuebingen.mpg.de

bioinformatics↗